Accepted Manuscript The FLOWERING LOCUS T / TERMINAL FLOWER 1 Gene Family: Functional Evolution and MolecularMechanisms Daniel P. Wickland, Yoshie Hanzawa PII:
S1674-2052(15)00094-5
DOI:
10.1016/j.molp.2015.01.007
Reference:
MOLP 70
To appear in:
MOLECULAR PLANT
Received Date: 21 October 2014 Revised Date:
19 December 2014
Accepted Date: 9 January 2015
Please cite this article as: Wickland D.P., and Hanzawa Y. (2015). The FLOWERING LOCUS T / TERMINAL FLOWER 1 Gene Family: Functional Evolution and MolecularMechanisms. Mol. Plant. doi: 10.1016/j.molp.2015.01.007. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT FT/TFL1: Functional Evolution and Mechanisms
Title:
The FLOWERING LOCUS T / TERMINAL FLOWER 1 Gene Family: Functional Evolution
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and MolecularMechanisms
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Authors:
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Daniel P. Wickland and Yoshie Hanzawa1
Department of Crop Sciences, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA. Tel:+1 (217) 333-4685
To whom correspondence should be addressed:[email protected]
Running title:
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FT/TFL1: Functional Evolution and Mechanisms
Short Summary:
The key flowering regulators FLOWERING LOCUS T (FT) and TERMINAL FLOWER 1 (TFL1) are homologous, but their functions in flowering control are opposite. Here we summarize the recent progress in diverse roles and unique evolution of the FT/TFL1 gene family,and highlight recent work to elucidate the molecular mechanisms of these proteins.
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ACCEPTED MANUSCRIPT FT/TFL1: Functional Evolution and Mechanisms ABSTRACT
In plant development, the flowering transition and inflorescence architecture are modulated by two homologous proteins, FLOWERING LOCUS T (FT) and TERMINAL
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FLOWER 1 (TFL1). The florigen FTpromotes the transition to reproductive development and flowering, while TFL1represses this transition. Despite these proteins’ importance to plant adaptation and crop improvement and their intense study by the plant community, the molecular mechanisms controlling the opposing actions of FT and TFL1 have remained mysterious. Recent
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studies in multiple species have unveiled diverse roles of the FT/TFL1gene family in developmental process other than flowering regulation. In addition, the striking evolution of FT
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homologs into flowering repressorshas occurred independently in several species during the evolution of flowering plants. These reports indicate that the FT/TFL1 gene family is a major target of evolution in nature.Here we comprehensively survey the conserved and diverse functions of the FT/TFL1 gene familythroughut the plant kingdom, summarize new findings regarding the unique evolution of FT in multiple species, and highlight recent work to elucidate
Keywords:
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the molecular mechanisms of theseproteins.
FT; TFL1; PEBP; flowering; evolution; photoperiod; development; inflorescence
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architecture
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ACCEPTED MANUSCRIPT FT/TFL1: Functional Evolution and Mechanisms
INTRODUCTION Several interconnected pathways coordinate flowering time with environmental input to optimize plant adaptation and reproductive success: the photoperiodic, vernalization, ambient
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temperature, plant hormone and autonomous flowering pathways(Blázquez et al., 2003; MutasaGöttgens and Hedden, 2009; Amasino, 2010; Andrés and Coupland, 2012). Two important genes downstream of these flowering pathways are FLOWERING LOCUS T (FT)and TERMINAL FLOWER 1(TFL1). FT and TFL1 encode a pair of flowering regulators with homology to
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phosphatidylethanolamine-binding proteins (PEBPs), which function in diverse signaling pathways involved in growth and differentiation in bacteria, animals and plants (Kardailsky et
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al., 1999; Kobayashi et al., 1999; Yeung et al., 1999; Chautard et al., 2004; Hanzawa et al., 2005; Ahn et al., 2006; Karlgren et al., 2011). FT and TFL1 share ~60% amino acid sequence identity but function in an opposite manner (Hanzawa et al., 2005; Ahn et al., 2006). FTpromotes the transition
to
reproductive
development
and
flowering,
while
TFL1represses
this
transition(Shannon and Meeks-Wagner, 1991; Bradley et al., 1997; Kardailsky et al., 1999; Kobayashi et al., 1999). The flowering inductive function of the universal florigen FT has been
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documented in all angiospermspecies examined (Turck et al., 2008), and the flowering repressive function of TFL1 has been reported in many species as well. Despite the widespread conservation of these flowering regulators across flowering plants, recent studies have unveiled several examples of evolution of FT homologs into flowering repressors. In addition, diverse
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roles of the FT/TFL1 gene family in various developmental processes other than flowering regulation have been reported in multiple species. Although much remains unknown about FT
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and TFL1 function at the molecular level, ongoing approaches are beginning to elucidate the molecular mechanisms underlying FT and TFL1 action. This review summarizes newly accumulated knowledge about the FT/TFL1 gene family,
with a strong emphasis onevolution. We begin by surveying both the conserved and diverse roles of these genes in Arabidopsis and other plant species. Next, the unique evolution of FT and TFL1 homologs in multiple species is covered. The remainder of the review summarizes recent work exploring the molecular actions of these proteins.
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ACCEPTED MANUSCRIPT FT/TFL1: Functional Evolution and Mechanisms
FUNCTIONS IN FLOWERING IN ARABIDOPSIS Photoperiodic input is a primary trigger of FT expression in the facultative long-day plant Arabidopsis thaliana (Arabidopsis). FT facilitates the transition to flowering in response to its
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induction by the transcription factor CONSTANS (CO) (Putterill et al., 1995; Suárez-López et al., 2001). Regulated by the circadian clock and tightly controlled at the transcriptional and posttranscriptional levels by the interplay of multiple transcription factors and photoreceptors (Valverde, 2011; Andrés and Coupland, 2012), CO peaks under long photoperiods at the end of
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the day, when it reaches levels sufficient to promote FT expression in the leaves (Suárez-López et al., 2001; Valverde, 2011). Environmental factors other than photoperiod modulate FT
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expression as well. Temperature-responsive FT regulators, which target the FT promoter or noncoding regions, include SHORT VEGETATIVE PHASE (SVP) (Hartmann et al., 2000; Lee et al., 2007), PHYTOCHROME INTERACTING FACTOR4 (PIF4) (Kumar et al., 2012), LIKE HETEROCHROMATIN PROTEIN1 (LHP1) (Kotake et al., 2003; Adrian et al., 2010) and FLOWERING LOCUS C (FLC) (Michaels and Amasino, 1999; Searle et al., 2006). Upon induction by CO, FT protein has been suggested to move from the leaves through
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the phloem to the shoot apical meristem (SAM) (Corbesier et al., 2007). In the meristem, FT binds to the bZIPtranscription factor FD to form a complex that regulates meristem identity genes, resulting in flowering induction (Abe et al., 2005; Wigge et al., 2005). The meristem identity genes induced by the FT/FD complex, which include APETALA1 (AP1)and
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FRUITFULL (FUL), reprogram the primordia to produce reproductive organs instead of vegetative ones (Abe et al., 2005; Teper-Bamnolker and Samach, 2005; Wigge et al., 2005;
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Amasino, 2010). In addition to inducing FT, CO is suggested to induce—directly or indirectly— expression of TERMINAL FLOWER 1 (TFL1), which controls inflorescence meristem identity and delays the transition to the reproductive phase at the SAM(Simon et al., 1996). TFL1 represses the expression of several genes downstream of FT such as LEAFY (LFY)and AP1, perhaps by partnering with FD, with which it weakly interacts (Bradley et al., 1997; Ratcliffe et al., 1998; Ratcliffe et al., 1999; Hanano and Goto, 2011). The high sequence homology of TFL1 to FT suggests conserved biochemical action, but the action and regulation of these proteins at the molecular level remain unclear(Hanzawa et al., 2005; Ahn et al., 2006), as discussed later in this review.
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ACCEPTED MANUSCRIPT FT/TFL1: Functional Evolution and Mechanisms The six-member PEBP gene family in Arabidopsis also includes TWIN SISTER OF FT (TSF),
BROTHER
OF
FT
(BFT),
ARABIDOPSIS
THALIANA
CENTRORADIALIS
HOMOLOGUE (ATC) and MOTHER OF FT AND TFL1 (MFT) (Kardailsky et al., 1999; Kobayashi et al., 1999; Yoo et al., 2004; Yamaguchi et al., 2005). The conserved roles of these
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genes in flowering regulation have been reported. TSF, the closest FT homolog, resembles FT in terms of protein sequence, induction by CO, diurnal expression, binding to FD, and promotion of flowering when overexpressed (Yamaguchi et al., 2005; Jang et al., 2009). BFT also shares high sequence similarity and diurnal expression with FT but functions in a TFL1-like manner as a
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repressor of flowering genes and flowering (Yoo et al., 2010). ATC represses flowering under short photoperiods, and evidence suggests that this graft-transmissible protein, like FT, moves
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systemically from the vasculature to the shoot apex(Huang et al., 2012a). In addition, ATC interacts with FD and downregulates the meristem identity gene AP1. Finally, MFT shares high homology with both FT and TFL1 and participates in flowering induction, perhaps acting redundantly with FT (Yoo et al., 2004).
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CONSERVED FUNCTIONS IN DIVERSE SPECIES
FT and TFL1 homologs control flowering
Amongangiosperms, FT homologs induce flowering and TFL1 homologs repress flowering. Species possessing flowering inductive FT genes include woody perennials (Endo et
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al., 2005; Böhlenius et al., 2006; Carmona et al., 2007; Matsuda et al., 2009; Kotoda et al., 2010; Hsu et al., 2011; Song et al., 2013), grasses (Kojima et al., 2002; Hayama et al., 2003; Yan et al.,
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2006; Li and Dubcovsky, 2008; Kikuchi et al., 2009; Lazakis et al., 2011; Meng et al., 2011; Wu et al., 2013a; Coelho et al., 2014), legumes (Hecht et al., 2005; Kong et al., 2010; Ono et al., 2010; Laurie et al., 2011; Nan et al., 2014) and ornamentals(Hayama et al., 2007; Hou and Yang, 2009; Imamura et al., 2011; Oda et al., 2012; Xiang et al., 2012; Li et al., 2013; Nakano et al., 2013), among others (Table 1; Figure 1). Likewise, flowering repressive TFL1homologs exist in woody perennials (Pillitteri et al., 2004; Kotoda and Wada, 2005; Boss et al., 2006; Esumi et al., 2010; Chen and Jiang, 2013; Randoux et al., 2014), grasses (Nakagawa et al., 2002; Danilevskaya et al., 2008) and ornamentals(Hou and Yang, 2009; Imamura et al., 2011), among others.
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ACCEPTED MANUSCRIPT FT/TFL1: Functional Evolution and Mechanisms The interaction between FT/TFL1 and FD has been demonstrated in several species. FT homologs from rice (Oryza sativa) (Taoka et al., 2011), soybean (Glycine max) (Nan et al., 2014), maize (Zea mays)(Muszynski et al., 2006; Danilevskaya et al., 2008), rose (Rosa spp.) (Randoux et al., 2014), wheat (Triticumaestivum) (Li and Dubcovsky, 2008), kiwifruit
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(Actinidiaspp.) (Varkonyi-Gasic et al., 2013)and chrysanthemum (Chrysanthemum spp.) (Higuchi et al., 2013) have been shown to interact with their respective species-specific FD homologs.Similarly, TFL1 homologs from rose (Randoux et al., 2014) and kiwifruit (Varkonyi-
TFL1 homologs control inflorescence architecture
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Gasic et al., 2013) interact with their respective FD homologs.
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In Arabidopsis, TFL1 delays the flowering transition and promotes indeterminacy of the inflorescence shoot by repressing progressive changes in the developmental phases of the SAM(Bradley et al., 1997). The role of TFL1 in inflorescence architecture is conserved in a number of species. In tomato (Solanumlycopersicum), the TFL1 homolog SELF-PRUNING (SP) influences stem growth habit. Tomato carrying the dominant SP allele exhibits indeterminate growth characterized by the continuous production of inflorescences and fruit, while tomato
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carrying the recessive allele exhibits determinate growth characterized by earlier cessation of inflorescence production and smaller stature (Pnueli et al., 1998; Jiang et al., 2013). In both rose and strawberry (Fragariavesca), non-functional recessive homologs of TFL1 (RoKSN and FvKSN, respectively) establish the horticulturally desirable trait of continuous flowering habit
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(Iwata et al., 2012). In soybean (Glycine max), the TFL1 homolog Dt1 controls stem growth habit (Bernard, 1972; Liu et al., 2010; Tian et al., 2010); the dominant Dt1 allele establishes
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indeterminate habit, in which growth continues after flowering, and the recessive allele establishes determinate habit, in which growth ceases after the onset of flowering. Finally, the common bean (Phaseolus vulgaris) TFL1 homolog PvTFL1y also controls growth habit (Kwak et al., 2012; Repinski et al., 2012), and the pea (Pisumsativum) TFL1 homolog PsTFL1a maintains indeterminate growth (Foucher et al., 2003).
DIVERSE FUNCTIONS OF THE FT/TFL1 GENE FAMILY
Diverse roles of FT and TFL1 homologs in Arabidopsis
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ACCEPTED MANUSCRIPT FT/TFL1: Functional Evolution and Mechanisms Members of the FT/TFL1 gene family in Arabidopsis encompass several functions beyond regulation of flowering time, including light-induced stomatal opening, stress-induced flowering and seed germination. FT and TSF regulate stomatalopening by activating H+ATPases in guard cells in response to blue light (Kinoshita et al., 2011; Ando et al., 2013). FT
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and TSF also control lateral shoot development under long and short photoperiods, respectively (Hiraoka et al., 2013). In addition to its activation by photoperiod, FT is induced under stress conditions by salicylic acid to promote flowering (Martínez et al., 2004). BFT also functions in a stress-responsive flowering pathway; under conditions of high salinity, BFT delays the flowering
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transition by competing with FT for the same binding site on FD (Ryu et al., 2011; Ryu et al., 2014). However, it remains unclear whether the delayed flowering results from the BFT-FD
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complex acting as a transcriptional repressor or from the prevention of FT-FD complex formation due to BFT binding to FD. Finally, MFT promotes seed germination by interacting with the gibberellin and abscisic acid signaling pathways, which control the breakdown of seed dormancy (Xi et al., 2010).
Diverse roles of FT and TFL1 homologs in other plant species in
Arabidopsis,
diversedevelopmental
theFT/TFL1
gene
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As
processes.
For
instance,
family
some
in
other
speciesfunctions
FThomologsregulate
aspects
in of
development in response to temperature. The two FT genes in sugar beet (Beta vulgaris) are involved in flowering response to the extended cold winter temperatures associated with
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vernalization(Pin et al., 2010). Similarly, poplar (Populustrichocarpa) relies on two FT homologs to coordinate its recurrent, seasonal flowering cycle in response to temperature(Hsu et
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al., 2011). PtFT2, which supports vegetative growth and inhibition of bud set during autumn, is upregulatedboth by high temperatures and long photoperiods during the spring and summer. Conversely, PtFT1, which initiates reproductive growth, is repressed by high temperatures but induced by low temperatures during winter. Low temperatures also promote expression of FT genes in Satsuma mandarin (Citrus unshiu) (Nishikawa et al., 2007) and kiwifruit (VarkonyiGasic et al., 2013). Finally, some members of this gene family modulate growth of underground storage organs. The potato (Solanumtuberosum) FT homolog StSP6A functions as a mobile “tuberigen” that induces the photoperiod-sensitive process of tuberization(Navarro et al., 2011),
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ACCEPTED MANUSCRIPT FT/TFL1: Functional Evolution and Mechanisms and the onion (Allium cepa) FT homologs AcFT1 and AcFT4 play roles in bulb formation, as described later in this review(Lee et al., 2013).
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EVOLUTION OF THE FT/TFL1 GENE FAMILY
The origin of the FT/TFL1 gene family
Recent reports indicate thatMFT genes are ancestral to FT and TFL1 genes, as basal plant species such as mosses possesshomologs of MFT but not ofFT or TFL1(Hedman et al., 2009;
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Karlgren et al., 2011). It is thought that duplication of an ancestral MFT-like gene during evolution spawned an MFT-like clade and anFT/TFL1-like clade, which led to further
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diversification of function, duplication and, with the emergence of angiosperms, eventual divergence into separate FT-like and TFL1-like clades (Hedman et al., 2009; Karlgren et al., 2011; Klintenäs et al., 2012). Data from gymnosperms suggest that the ancestor of FT and TFL1 functioned in a TFL1-like manner and that FT and TFL1 function diverged after the evolutionary separation of gymnosperms and angiosperms (Karlgren et al., 2011; Klintenäs et al., 2012) (Table 1).In the gymnosperm Norway spruce (Piceaabies), for instance, PaFTL1 and PaFTL2
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possess sequence homology to both FT and TFL1 but appear to function more similarly to TFL1 interms of growth repression in a general sense; PaFTL2functions in initiation of early bud set and cessation of growth in late summer to achieve full cold hardiness (Karlgren et al., 2013). Both PaFTL1 and PaFTL2 delay flowering in transgenic Arabidopsis (Karlgren et al., 2011;
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Recentevolution of FT homologs intoflowering repressors Intriguingly,some FT homologs apparently have acquired a repressor function during
recent evolution (Figure 2). In multiplespecies, arepressor FT antagonizes the function of aparalogousinducer FT. Sunflower (Helianthus annuus) contains four FT homologs, one of which resulted from a mutation that yielded a novel repressor function (Blackman et al., 2010). Wild sunflower carries an in-frame allele of HaFT1, an FT homolog that stimulates flowering in transgenic Arabidopsis. Domesticated sunflower, however, carries a frame-shifted HaFT1 allele, which encodes a protein that represses flowering. In transgenic Arabidopsis, the domesticated HaFT1 allele delays flowering by interfering with another sunflower FT homolog, the flowering
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ACCEPTED MANUSCRIPT FT/TFL1: Functional Evolution and Mechanisms inductive and long-day expressed HaFT4, in a dominant-negative fashion. The widespread prevalence of the HaFT1frameshift allele among domesticated sunflower varieties suggests that selection played a role in its retention. Likewise, sugar beet contains two FT homologs, BvFT1 and BvFT2, with opposite functions (Pin et al., 2010). BvFT1, which apparently gaineda
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repressor function during sugar beet evolution, inhibits flowering by repressing the flowering inducer BvFT2 before the onset of vernalization. Vernalization then reduces BvFT1 expression and upregulatesBvFT2 expression, triggering flowering. In onion, the FT homolog AcFT4 acts as a repressor of bulb formation. During early development, AcFT4 inhibits bulb formation by
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repressing AcFT1 expression (Lee et al., 2013). After an onion plant reaches maturity under the appropriate daylength, downregulation of AcFT4 allows upregulation of AcFT1, which formation.
Finally,
three
of
the
four
FT
homologs
in
tobacco
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inducesbulb
(Nicotianatabacum)repress flowering in tobacco (Harig et al., 2012), and FT homologs from sugarcane (Saccharumspp.) (Coelho et al., 2014), longan (Dimocarpuslongan) (Winterhagen et al., 2013) and soybean (Zhai et al., 2014) have been shown to repress flowering in transgenic Arabidopsis.
Sequence alignment of these proteins reveals two conserved sites that distinguish inducer
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and repressor function in FT homologs (Figure2). In species that possess repressor FTs, all inducer FTs (except GmFT5a in soybean) contain tyrosine at position 134 based on alignment with Arabidopsis FT protein sequence, and all repressor FTs (except FT-/TFL1-like PaFTL1 and PaFTL2 in Norway spruce) contain non-tyrosine amino acids, possibly indicating a contribution
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of this site to FT inductive function. In support of this notion, Arabidopsis FT gains repressor activity in response to substitution at position 134 (Ho and Weigel, 2014), and this residue
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contributes to the antagonistic roles of BvFT1 and BvFT2 in sugar beet as well(Pin et al., 2010). The conserved tyrosine at this position in the repressors PaFTL1 and PaFTL2 from the gymnosperm Norway spruce implies the ancestral TFL1-like function of FT and TFL1. The second conserved residue lies at position 138. In species that possess repressor FTs,
all inducer FTs contain tryptophan at this siteand all repressor FTs (except DlFT2 in longan and GmFT4 in soybean) contain non-tryptophan amino acids at this site, suggesting the importance of this residue to FT inductive function. Indeed, mutation at residue Trp-138 as well as residues Glu-109, Gln-140 and Asn-152 in Arabidopsis converts FT into a TFL1-like repressor by affecting protein surface charge (Ho and Weigel, 2014); furthermore,residue 138partly
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ACCEPTED MANUSCRIPT FT/TFL1: Functional Evolution and Mechanisms determines the antagonistic functions of BvFT1 and BvFT2 in sugar beet (Pin et al., 2010). Tyr85 (His-88in TFL1) and Gln-140 (Asp-144 in TFL1) contribute to the functional specificity of FT and TFL1 in Arabidopsis (Hanzawa et al., 2005; Ahn et al., 2006). Amongthese repressor FT proteins, position 85 is invariant and contains the characteristic tyrosine residue, indicating that
after the divergence of FT-like and TFL1-like genes.
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mutation at Tyr-134 and Trp-138 occurred multiple times during the evolution of the FT clade
MOLECULARMECHANISMS OF FT AND TFL1 FUNCTION
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Although much remains unknown about the molecular mechanisms underlying FT and TFL1 function in Arabidopsis, recent work has identified several FT- and TFL1-interacting
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molecules and continues gradually to uncover the molecular and biochemical nature of FT and TFL1 action. In addition to the established interactions of FT and TFL1 with FD to modulate flowering gene expression, novel molecules involved in FT transport andthe role of TFL1 in trafficking to protein storage vesicles have been reported, as detailed below.
FT and TFL1 function as transcriptional regulators
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It is thought that FT and TFL1 do not bind directly to DNA but act as transcriptional coregulators by interacting with the transcription factor FD, as described earlier. The complex of FD with either FT or TFL1 likely contains other protein components. In rice, the FT ortholog Hd3a is generated in the leaves and moves to the SAM, where it forms a complex with 14-3-3
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proteins that mediate its interaction withOsFD1, an FD homolog(Tamaki et al., 2007; Komiya et al., 2008). Once in the nucleus, the Hd3a/14-3-3/OsFD1 complex (known as the “florigen
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activation complex”) promotes expression of OsMADS15, anAP1homolog(Komiya et al., 2008; Taoka et al., 2011).Likewise, the tomato TFL1 homolog SP binds to 14-3-3 proteins (Pnueli et al., 2001). In Arabidopsis, interactions between 14-3-3 proteins and FT, TFL1 and FD suggest that a similar mechanism operates in this species (Pnueli et al., 2001; Taoka et al., 2011; Ho and Weigel, 2014). These observations in multiple species support the molecular models proposed previously, in which interacting proteins or protein complexes recruited by FT and/or TFL1 define the opposing actions of FT and TFL1 (Hanzawa et al., 2005; Ho and Weigel, 2014). In contrast tothe interaction between FT andBRANCHED1 (BRC1) described below, direct interaction between FT and TFL1 has not been reported, potentially indicating that TFL1
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ACCEPTED MANUSCRIPT FT/TFL1: Functional Evolution and Mechanisms replaces FT in the florigen activation complex and altersaction of the complex through recruitment of uncharacterized factors and/or protein modifications.
BRC1 interacts with FT to repress axillary bud flowering
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In addition to moving from the leaves to the SAM, FT moves to axillary buds, where it interacts with the TCP transcription factor BRC1 (Aguilar-Martínez et al., 2007; Niwa et al., 2013). BRC1 regulates axillary bud development and differentiation, a process tightly linked to the shoot apex floral transition in Arabidopsis. A repressor of axillary bud development, BRC1
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inhibits FT function to delay flowering in axillary meristems. BRC1 interacts directly with FT withoutinvolvement of 14-3-3 proteins (Niwa et al., 2013). BRC1 also interacts with TSF but not
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with TFL1. Overexpression of BRC1 in the shoot apex retards flowering, while loss-of-function elevates expression of the meristem identity genesAP1 and FUL,which suggests that BRC1 represses FT’s induction of these genes.Whether BRC1 comprises part of the florigen activation complex or prevents FT from forming the florigen activation complex remains unclear. Nevertheless, the role of FT and BRC1 in axillary bud development indicates FT’s involvement not only in flowering control but also in regulation of shoot architecture. Supporting FT function
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in inflorescence development, ectopic expression of FT in Arabidopsis results in determinate stem growth characterized by the SAM producing a terminal flower similar to that ofTFL1lossof-function mutants.
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FTIP1 and PC are implicated in movement of FT FT-INTERACTING PROTEIN 1 (FTIP1) is thoughtto facilitate FT movement from
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phloem companion cells to sieve elements (Liu et al., 2012). Loss of FTIP1 delays flowering time and disrupts FT movement to sieve elements, resulting in FT accumulation in phloem companion cells. Therefore, FTIP1-mediated transport is required for FT to induce flowering at the shoot apex. Experiments using FT-transformed Cucurbitamoschatasuggest that FT enters the phloem translocation stream by diffusing through plasmodesmata(Yoo et al., 2013). A selective mechanism is then thought to regulate delivery of FT from the phloem translocation stream into the SAM. FT also binds to the phospholipid phosphatidylcholine (PC), a component of cellular membranes (Nakamura et al., 2014). High levels of PC at the shoot apex cause both early
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ACCEPTED MANUSCRIPT FT/TFL1: Functional Evolution and Mechanisms flowering—especially in combination with high levels of FT—and elevated expression of the FT targets SOC1 and AP1, while low levels of PC cause late flowering. Therefore, PC may promote flowering through the action of FT. Different molecular species of PC oscillate throughout the day, and FT preferentially binds to those PC species abundant during the light period, suggesting
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a mechanism by which FT induces flowering at the appropriate time of day. Two models have been proposed to account for the effect of PC on flowering phenotype(Nakamura et al., 2014). A constituent of the nuclear membrane, PC may import FT into the nucleus from the cytosol to
FT to FD. Further study would clarify these scenarios.
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Mobile TFL1 plays a role in vesicle trafficking
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promote flowering. Another possibility is that vesicles containing PC function in trafficking of
Like FT, TFL1 functions as a mobile signal but only within the SAM (Conti and Bradley, 2007). While TFL1 mRNA remains confined tothe central region of the shoot apex, TFL1 protein spreads throughout the shoot apex (but does not reach floral meristems). This TFL1 movement throughout the SAM may ensure indeterminacy of the region by preventing the local expression of flowering genes. No such TFL1 movement in the shoot apex is observed in the
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LFY loss-of-function mutant, which indicates that LFY indirectly promotes TFL1 movement to outer cells of the meristem. TFL1 function in endomembrane trafficking to protein storage vesicles—cell components that store assorted proteins and minerals—has also been reported (Sohn et al., 2007). TFL1loss-of-function mutants exhibit disrupted trafficking to protein storage
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vesicles, implicating TFL1 involvement in endomembrane trafficking. This finding, in addition to the fact that TFL1 protein is found in both the nucleus and cytoplasm,may suggest that TFL1
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blocks FD-dependent transcription by shuttling FD from the nucleus to protein storage vesicles(Hanano and Goto, 2011). However, more research is needed to investigate this possibility.
CONCLUSION
Photoperiodic regulation of flowering time facilitates the regional adaptation of plants and influences agricultural growing seasons.Central components of the photoperiodic flowering response, genes belonging to the FT/TFL1 family show conserved functions among angiosperms, with FT homologs acting as flowering inducers and TFL1 homologs acting as flowering
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ACCEPTED MANUSCRIPT FT/TFL1: Functional Evolution and Mechanisms repressors.In addition to operating in diverse developmental processes, FT and TFL1 have evolved dynamically over the course of plant evolution. Recent evolution of FT homologs has resulted in their acquisition of a repressor function in multiple species. Current research is gradually revealing the molecular mechanisms of FT and TFL1 action and uncovering the
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significance of FT- and TFL1-interacting proteins in controlling the opposing functions of FT and TFL1.Futureapproaches will address the tantalizing questions that remain.What molecules comprise theflorigen activation complex, and what molecular mechanisms control the activity of this complex? Is there any link between phospholipids and TFL1-regulated vesicle trafficking?
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Does FT, in addition to TFL1, participate in vesicle trafficking, and what mechanisms govern this process? Our burgeoning knowledge of the FT/TFL1 gene family will allow modification of
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florigen and anti-florigenaction in the near future, thereby supporting efforts to breed superior crop varieties highly adaptive to a wide range of environments in order to meet the agricultural demands of the rapidly expandingglobal population.
FUNDING
This work was supported by the Agriculture and Food Research Initiative Competitive Grants
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Program from the USDA National Institute of Food and Agriculture (USDA-NIFA2011-00078) and the Plant Genome Research Program from the National Science Foundation (NSF-PGRPIOS-1339388). No conflict of interest declared.
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FIGURE LEGENDS
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Figure 1. Phylogenetic tree of the FT/TFL1 protein family Maximum likelihood phylogenetic tree of the FT/TFL1 protein family in 50 plant species characterized by transgenic approaches. The tree was constructed using the Maximum Likelihood method in MEGA6 software(Tamura et al., 2013). Bootstrap values >30% for 1,000 resamplings are shown on branches. Blue and red branches indicate FT-like and TFL1-like proteins, respectively. Protein names in brown indicate FT-like proteins with repressor function. Arabidopsis proteins are shown in bold.
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ACCEPTED MANUSCRIPT FT/TFL1: Functional Evolution and Mechanisms Figure 2. Amino acid alignment of inducer FTs and repressor FTs at the conserved external loop in exon 4 Alignment of amino acid sequences of FT homologs at the conserved position 85 (exon 2) and segment B (positions 128-141, exon 4) from Arabidopsis(Kardailsky et al., 1999; Kobayashi et
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al., 1999), onion (Lee et al., 2013), sugar beet (Pin et al., 2010), longan(Winterhagen et al., 2013), soybean (Kong et al., 2010; Nan et al., 2014; Zhai et al., 2014), sunflower (Blackman et al., 2010), tobacco (Harig et al., 2012)and sugarcane (Coelho et al., 2014). FT-/TFL1-like proteins from Norway spruce are also included (Karlgren et al., 2011). Red asterisks
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indicaterepressor function characterized in a gene’s native species and blue asterisks indicate repressor function characterized in transgenic Arabidopsis. Amino acid positions indicated are
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based on the Arabidopsis FT protein sequence. All inducer FTs (except GmFT5a) contain tyrosine at position 134, while repressor FTs (except FT-/TFL1-like PaFTL1 and PaFTL2) contain non-tyrosine amino acids. Additionally, all inducer FTs contain tryptophan at position 138, while repressor FTs (except DlFT2 and GmFT4) contain non-tryptophan amino acids.
Protein sequences with the following IDs were obtained from The Arabidopsis Information
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Resource (TAIR), Genbank and Phytozome: AT1G65480.1 (AtFT), AT5G03840.1 (AtTFL1), AGZ20207.1 (AcFT1), AGZ20210.1 (AcFT4), ADM92608.1 (BvFT1), ADM92610.1 (BvFT2), AEZ63949.1 (DlFT1), AEZ63950.1 (DlFT2), BAJ33491.1 (GmFT2a), Glyma08g47810.1 (GmFT4), BAJ33494.1 (GmFT5a), ADF32943.1 (HaFT1), ADF32945.1 (HaFT4), AFS17369.1
ABQ85553.1
(PaFTL2),
AC C
(PaFTL1),
EP
(NtFT1), AFS17370.1 (NtFT2), AFS17371.1 (NtFT3), AFS17372.1 (NtFT4), AEH59567.1
14
AHZ46121.1
(ScFT1).
ACCEPTED MANUSCRIPT
FT/TFL1: Functional Evolution and Mechanisms Table 1. Diverse functions of the FT/TFL1 gene family in 49 plant species characterized by transgenic approaches.
Clustered gentian (Gentianatriflora) Common bean (Phaseolus vulgaris) Dancing lady orchid (Oncidiumgowerramsey) Fig (Ficuscarica)
HvFT1
• InductionB
HvFT2
• InductionB
HvFT3
• InductionB
PsTFL1
• RepressionA
RI PT
REGULATORY INPUT
• Promotion of polycarpy
• VernalizationD
SC
• Induction • RepressionA • Repression
M AN U
Black cherry (Prunusserotina) Chinese narcissus (Narcissus tazettavar. chinensis) Chrysanthemum (Chrysanthemum spp.)
MdFT1, MdFT2 MdCENa, MdCENb AaTFL1
OTHER FUNCTION
• LD photoperiod D • HvCO1 D • HvFT3 D • SD photoperiod D • SD photoperiod D
REFERENCES Esumi et al., 2005; Kotoda and Wada, 2005; Mimida et al., 2009 Kotoda et al., 2010 Mimida et al., 2009 Wang et al., 2011 Faure et al., 2007; Kikuchi et al., 2009; Campoli et al., 2012 Faure et al., 2007; Kikuchi et al., 2009 Faure et al., 2007; Kikuchi et al., 2009 Wang and Pijut, 2013
NtFT
• InductionA
• Warm temperature D
Li et al., 2013; Noy-Porat et al., 2013
CsFTL3
• Induction
• SD photoperiod D • Heat E • CsAFTE • LD photoperiod D
Oda et al., 2012; Nakano et al., 2013
TE D
Alpine rock-cress (Arabisalpina) Barley (Hordeumvulgare)
MdTFL1-1, MdTFL1-2
FLOWERING FUNCTION • RepressionA
EP
Apple (Malusdomestica)
HOMOLOG
CsAFT GtF1, GtF2 GtTFL1 PvTFL1y
• Repression • InductionA • RepressionA • RepressionA
OnFT OnTFL1 FcFT1
• InductionA • RepressionA • InductionC
AC C
SPECIES
• Promotion of indeterminacy • Photoperiod D
15
Higuchi et al., 2013 Imamura et al., 2011 Imamura et al., 2011 Kwak et al., 2008; Repinski et al., 2012 Hou and Yang, 2009 Hou and Yang, 2009 Ikegami et al., 2013
ACCEPTED MANUSCRIPT
FT/TFL1: Functional Evolution and Mechanisms
Maize (Zea mays)
Medicago (Medicagotruncatula)
• RepressionA • InductionA
PnTFL1 PnFT1, PnFT2 PaFT
• RepressionA • InductionA • InductionA
DlFT1
• InductionA
DlFT2
• RepressionA
Ljcen1 LjFT ZCN8
• RepressionA • Induction A • Induction
ZCN2
• Repression
MtFTa1
• Growth regulation
• InductionA
MtFTc
• InductionA
• Cool temperature D
• SD photoperiod D
• LD photoperiod D • SD photoperiod D • Autonomous pathwayD
• LD photoperiod D
16
Boss et al., 2006; Carmona et al., 2007; Fernandez et al., 2010; Crane et al., 2012 Carmona et al., 2007 Esumi et al., 2009 Esumi et al., 2010 Varkonyi-Gasic et al., 2013 Varkonyi-Gasic et al., 2013 Fukuda et al., 2011 Igasaki et al., 2008 Igasaki et al., 2008 Zhang et al., 2011 Winterhagen et al., 2013 Winterhagen et al., 2013
• LD photoperiod D • VernalizationD
• Induction
MtFTb1
RI PT
Kiwifruit CEN LsFT
• Dormancy release
• CytokininsD
SC
• InductionA • InductionA • RepressionA • InductionA
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Lotus japonicus
VvFT PmFT PmTFL1 Kiwifruit FT
• Control ofbranching and fruit density
TE D
Lettuce (Lactuca sativa) Lombardy poplar (Populusnigra) London plane (Platanusacerifolia) Longan (Dimocarpuslongan)
• RepressionA
EP
Japanese apricot (Prunusmume) Kiwifruit (Actinidiaspp.)
VvTFL1A
AC C
Grapevine (Vitisvinifera)
Guo et al., 2006 Ono et al., 2010 Muszynski et al., 2006; Danilevskaya et al., 2008; Lazakis et al., 2011; Meng et al., 2011 Danilevskaya et al., 2008; Danilevskaya et al., 2010 Hecht et al., 2005; Laurie et al., 2011; Putterill et al., 2013 Hecht et al., 2005; Laurie et al., 2011; Putterill et al., 2013 Hecht et al., 2005; Laurie et al., 2011; Putterill et al., 2013
ACCEPTED MANUSCRIPT
FT/TFL1: Functional Evolution and Mechanisms • Induction • RepressionA
PaFTL2
• RepressionA
AcFT1 AcFT2
• Induction of bulb formation • InductionA
AcFT4
Phalaenopsis orchid (Phalaenopsis hybrid Fortune Saltzman)
Pharbitis (Ipomoea nil)
• Repression • InductionA
PsFTa2 PsFTb1 PsFTb2 PsFTc PsTFL1a
• InductionA • InductionA • InductionA • InductionA
PsTFL1c
• Repression
PpTFL1
• InductionA
PpTFL1-1, PpTFL1-2, PcTFL1-1, PcTFL1-2 PhFT
• Repression
PnFT1
• AcFT4 E
Karlgren et al., 2011; Klintenäs et al., 2012; Karlgren et al., 2013 Karlgren et al., 2011; Klintenäs et al., 2012; Karlgren et al., 2013 Lee et al., 2013
• VernalizationD
Lee et al., 2013
• LD photoperiod E
Lee et al., 2013 Pillitteri et al., 2004 Hecht et al., 2011
• Promotion of inflorescence identity
Hecht et al., 2011 Hecht et al., 2011 Hecht et al., 2011 Hecht et al., 2011 Singer et al., 1990; Foucher et al., 2003 Singer et al., 1990; Foucher et al., 2003 Liang et al., 2010; Chen and Jiang, 2013 Esumi et al., 2005; Freiman et al., 2012
TE D
CsTFL PsFTa1
• SD photoperiod D
• Maintenance of indeterminacy
EP
Peach (Prunuspersica) Pear (Pyrusspp.)
• Inhibition of bulb formation
AC C
Orange (Citrus sinensis) Pea (Pisumsativum)
• Cone development, meristem inhibition and needle formation • Bud set/burst • Growth repression
RI PT
PaFTL1
Song et al., 2013
SC
Onion (Allium cepa)
VcFT
M AN U
Northern Highbush Blueberry (Vacciniumcorymbosum) Norway Spruce (Piceaabies)
• InductionA
• Warm temperature (day) D • Cool temperature (night) D
Li et al., 2014b
• Induction
• SD photoperiod D
Hayama et al., 2007
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ACCEPTED MANUSCRIPT
FT/TFL1: Functional Evolution and Mechanisms
AcFT
• InductionA
• Fruit development
PtFT1
• Induction
PtFT2
• Induction
• Growth cessation and bud set • Promotion ofvegetative growth • Regulation of meristem identity
• Repression • InductionA
• Cool temperature D • PtCO2 D • LD photoperiodD • Warm temperature D
SC
PopCEN1, PopCEN2 PopMFT StTFL1
RI PT
• Induction
• Regulation oftuberization
StSP3D StSP6A
• Induction
Cm-FTL1, Cm-FTL2 FTL1, FTL2
• InductionA
Hd3a
• Induction
• Induction oftuberization
• Induction
• SD photoperiod D • StCOE
• LD photoperiod D • miR5200E • SD photoperiod D • DTH2 D • EHD1 D • EHD2 D • HD1 D
AC C
EP
Pumpkin (Cucurbita maxima) Purple false brome (Brachypodiumdistachyon) Rice (Oryza sativa)
JcFT
M AN U
Potato (Solanumtuberosum)
• Induction
TE D
Physic nut (Jatrophacurcas) Pineapple (Ananascomosus) Poplar (Populusspp.)
• SD photoperiod D • Salicylic acid D • Nutrient stress D
PnFT2
Rice
RFT1
• LD photoperiod D
• Induction
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Hayama et al., 2007; Wada et al., 2010; Yamada and Takeno, 2014 Li et al., 2014a; Ye et al., 2014 Lv et al., 2012 Böhlenius et al., 2006; Hsu et al., 2011 Böhlenius et al., 2006; Hsu et al., 2011 Mohamed et al., 2010 Mohamed et al., 2010 Guo et al., 2010 Navarro et al., 2011 Navarro et al., 2011; González-Schain et al., 2012 Lin et al., 2007 Wu et al., 2013a Izawa et al., 2002; Kojima et al., 2002; Hayama et al., 2003; Doi et al., 2004; Matsubara et al., 2008; Park et al., 2008; Wu et al., 2008; Komiya et al., 2009; Wu et al., 2013b; Cai et al., 2014
Izawa et al., 2002; Kojima et
ACCEPTED MANUSCRIPT
FT/TFL1: Functional Evolution and Mechanisms • DTH2 D • EHD1 D • EHD2 D
• Repression • Repression
RoFT
• InductionA • RepressionA
Ryegrass (Loliumperenne) Satsuma mandarin (Citrus unshiu)
LpTFL1 CiFT
• InductionA
Snapdragon (Antirrhinum spp.) Soybean (Glycine max)
CEN
• RepressionC
Sugar beet
• Cool temperature D
• Maintenance of inflorescence identity • Control of stem growth habit • Inhibition of seed germination
• Induction
GmFT4 GmFT5a
• RepressionA • Induction
• E1 D
• InductionA
• SD photoperiod D
CgFT
al., 2002; Hayama et al., 2003; Doi et al., 2004; Matsubara et al., 2008; Park et al., 2008; Wu et al., 2008; Komiya et al., 2009; Cai et al., 2014; Wu et al., 2013b Nakagawa et al., 2002 Iwata et al., 2012; Koskela et al., 2012; Randoux et al., 2014 Remay et al., 2009; Randoux et al., 2014 Jensen et al., 2001 Endo et al., 2005; Nishikawa et al., 2007; Matsuda et al., 2009 Bradley et al., 1996; Amaya et al., 1999 Bernard, 1972; Liu et al., 2010; Tian et al., 2010 Li et al., 2014c
• LD photoperiod D • SD photoperiod E
Kong et al., 2010; Sun et al., 2011; Nan et al., 2014 Zhai et al., 2014 Kong et al., 2010; Nan et al., 2014 Huang et al., 2012b; Xiang et al., 2012 Iwata et al., 2012; Koskela et al., 2012
• Induction
• LD photoperiod D • Far-red and blue light D
Koskela et al., 2012; Rantanen et al., 2014
• Repression
• SD photoperiod D
Pin et al., 2010; Pin et al.,
EP
GmFT2a
AC C
Spring orchid (Cymbidium spp.) Strawberry (Fragariavesca)
• VernalizationE
TE D
Dt1 GmMFT
• Establishment of continuous flowering habit (recessive allele)
SC
RCN1, RCN2 RoKSN
M AN U
Rose (Rosa spp.)
RI PT
(Oryza sativa)
FvKSN / FvTFL1
• Repression
FvFT1
BvFT1
• Establishment of continuous flowering habit (recessive allele)
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ACCEPTED MANUSCRIPT
FT/TFL1: Functional Evolution and Mechanisms • Cold E • BvBTC1 E • BvBTC1 D
(Beta vulgaris)
Tomato (Solanumlycopersicum)
SFT Wheat (Triticumaestivum)
• RepressionA • RepressionA • Repression A • Induction A • Repression
• SD photoperiod D • LD photoperiod D • SD photoperiod D
• Induction
TaMFT
• Regulation of germination
TE D
• Induction
Pin et al., 2010; Pin et al., 2012 Coelho et al., 2014 Coelho et al., 2014 Blackman et al., 2010 Blackman et al., 2010 Harig et al., 2012
• SD photoperiod D
Harig et al., 2012 Pnueli et al., 1998; Jiang et al., 2013
• SP E
Lifschitz et al., 2006; Shalit et al., 2009 Nakamura et al., 2011
• Maintenance of indeterminate growth • Regulation of growth cycles
• Induction
TaFT / TaFT1
RI PT
ScTFL1 ScFT1 HaFT1 HaFT4 NtFT1, NtFT2, NtFT3 NtFT4 SP
SC
Sugarcane (Saccharumspp.) Sunflower (Helianthus annuus) Tobacco (Nicotianatabacum)
• Induction
M AN U
BvFT2
2012
• Cool temperature D
Yan et al., 2006; Li and Dubcovsky, 2008; Lv et al., 2014
A: function assessed in transgenic Arabidopsis; B: function assessed in transgenic rice; C: function assessed in transgenic tobacco;
AC C
EP
D: input that induces expression of a particular FT/TFL1 homolog;E: input that represses expression of a particular FT/TFL1 homolog.
20
ACCEPTED MANUSCRIPT FT/TFL1: Functional Evolution and Mechanisms LITERATURE CITED Abe, M., Kobayashi, Y., Yamamoto, S., Daimon, Y., Yamaguchi, A., Ikeda, Y., Ichinoki, H., Notaguchi, M., Goto, K. and Araki, T. (2005). FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex. Science. 309, 1052–1056.
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ACCEPTED MANUSCRIPT FT/TFL1: Functional Evolution and Mechanisms Boss, P.K., Sreekantan, L. and Thomas, M.R. (2006). A grapevine TFL1 homologue can delay flowering and alter floral development when overexpressed in heterologous species. Funct. Plant Biol. 33, 31–41.
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Coelho, C.P., Minow, M.A.A., Chalfun-Júnior, A. and Colasanti, J. (2014). Putative sugarcane FT/TFL1 genes delay flowering time and alter reproductive architecture in Arabidopsis. Front. Plant Sci. 5, doi: 10.3389/fpls.2014.00221.
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ACCEPTED MANUSCRIPT FT/TFL1: Functional Evolution and Mechanisms Danilevskaya, O.N., Meng, X., Hou, Z., Ananiev, E. V and Simmons, C.R. (2008). A genomic and expression compendium of the expanded PEBP gene family from maize. Plant Physiol. 146, 250–264.
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Endo, T., Shimada, T., Fujii, H., Kobayashi, Y., Araki, T. and Omura, M. (2005). Ectopic expression of an FT homolog from Citrus confers an early flowering phenotype on trifoliate orange (Poncirus trifoliata L. Raf.). Transgenic Res. 14, 703–712. Esumi, T., Tao, R. and Yonemori, K. (2005). Isolation of LEAFY and TERMINAL FLOWER 1 homologues from six fruit tree species in the subfamily Maloideae of the Rosaceae. Sex. Plant Reprod. 17, 277–287. Esumi, T., Hagihara, C., Kitamura, Y., Yamane, H. and Tao, R. (2009). Identification of an FT ortholog in Japanese apricot (Prunus mume Sieb. et Zucc.). J. Hortic. Sci. Biotechnol. 84, 149–154.
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Esumi, T., Kitamura, Y., Hagihara, C., Yamane, H. and Tao, R. (2010). Identification of a TFL1 ortholog in Japanese apricot (Prunus mume Sieb. et Zucc.). Sci. Hortic. 125, 608–616.
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Faure, S., Higgins, J., Turner, A. and Laurie, D.A. (2007). The FLOWERING LOCUS T-like gene family in barley (Hordeum vulgare). Genetics. 176, 599–609.
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ACCEPTED MANUSCRIPT FT/TFL1: Functional Evolution and Mechanisms Fukuda, M., Matsuo, S., Kikuchi, K., Kawazu, Y., Fujiyama, R. and Honda, I. (2011). Isolation and functional characterization of the FLOWERING LOCUS T homolog, the LsFT gene, in lettuce. J. Plant Physiol. 168, 1602–1607.
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González-Schain, N.D., Díaz-Mendoza, M., Zurczak, M. and Suárez-López, P. (2012). Potato CONSTANS is involved in photoperiodic tuberization in a graft-transmissible manner. Plant J. 70, 678–690. Guo, X., Zhao, Z., Chen, J., Hu, X. and Luo, D. (2006). A putative CENTRORADIALIS/TERMINAL FLOWER1-like gene, Ljcen1, plays a role in phase transition in Lotus japonicus. J. Plant Physiol. 163, 436–444.
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Guo, J.L., Yu, C.L., Fan, C.Y., Lu, Q.-N., Yin, J.M., Zhang, Y.F. and Yang, Q. (2010). Cloning and characterization of a potato TFL1 gene involved in tuberization regulation. Plant Cell, Tissue Organ Cult. 103, 103–109.
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Hanano, S. and Goto, K. (2011). Arabidopsis TERMINAL FLOWER1 is involved in the regulation of flowering time and inflorescence development through transcriptional repression. Plant Cell. 23, 3172–3184. Hanzawa, Y., Money, T. and Bradley, D. (2005). A single amino acid converts a repressor to an activator of flowering. Proc. Natl. Acad. Sci. 102, 7748–7753.
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Harig, L., Beinecke, F.A., Oltmanns, J., Muth, J., Müller, O., Rüping, B., Twyman, R.M., Fischer, R., Prüfer, D. and Noll, G.A. (2012). Proteins from the FLOWERING LOCUS T-like subclade of the PEBP family act antagonistically to regulate floral initiation in tobacco. Plant J. 72, 908–921.
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ACCEPTED MANUSCRIPT FT/TFL1: Functional Evolution and Mechanisms Hecht, V., Laurie, R.E., Schoor, J.K. Vander, Ridge, S., Knowles, C.L., Liew, L.C., Sussmilch, F.C., Murfet, I.C., Macknight, R.C. and Weller, J.L. (2011). The pea GIGAS gene is a FLOWERING LOCUS T homolog necessary for graft-transmissible specification of flowering but not for responsiveness to photoperiod. Plant Cell. 23, 147–161.
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Hiraoka, K., Yamaguchi, A., Abe, M. and Araki, T. (2013). The florigen genes FT and TSF modulate lateral shoot outgrowth in Arabidopsis thaliana. Plant Cell Physiol. 54, 352–368.
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ACCEPTED MANUSCRIPT FT/TFL1: Functional Evolution and Mechanisms Iwata, H., Gaston, A., Remay, A., Thouroude, T., Jeauffre, J., Kawamura, K., Oyant, L.H. S., Araki, T., Denoyes, B. and Foucher, F. (2012). The TFL1 homologue KSN is a regulator of continuous flowering in rose and strawberry. Plant J. 69, 116–125.
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Karlgren, A., Gyllenstrand, N., Clapham, D. and Lagercrantz, U. (2013). FLOWERING LOCUS T/TERMINAL FLOWER1-like genes affect growth rhythm and bud set in Norway spruce. Plant Physiol. 163, 792–803.
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ACCEPTED MANUSCRIPT FT/TFL1: Functional Evolution and Mechanisms Kobayashi, Y., Kaya, H., Goto, K., Iwabuchi, M. and Araki, T. (1999). A pair of related genes with antagonistic roles in mediating flowering signals. Science. 286, 1960–1962.
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ACCEPTED MANUSCRIPT FT/TFL1: Functional Evolution and Mechanisms Laurie, R.E., Diwadkar, P., Jaudal, M., Zhang, L., Hecht, V., Wen, J., Tadege, M., Mysore, K.S., Putterill, J., Weller, J.L. and Macknight, R.C. (2011). The Medicago FLOWERING LOCUS T homolog, MtFTa1, is a key regulator of flowering time. Plant Physiol. 156, 2207–2224.
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ACCEPTED MANUSCRIPT FT/TFL1: Functional Evolution and Mechanisms Mohamed, R., Wang, C.T., Ma, C., Shevchenko, O., Dye, S.J., Puzey, J.R., Etherington, E., Sheng, X., Meilan, R., Strauss, S.H. and Brunner, A.M. (2010). Populus CEN/TFL1 regulates first onset of flowering, axillary meristem identity and dormancy release in Populus. Plant J. 62, 674–688.
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ACCEPTED MANUSCRIPT FT/TFL1: Functional Evolution and Mechanisms Niwa, M., Daimon, Y., Kurotani, K., Higo, A., Pruneda-Paz, J.L., Breton, G., Mitsuda, N., Kay, S.A., Ohme-Takagi, M., Endo, M. and Araki, T. (2013). BRANCHED1 interacts with FLOWERING LOCUS T to repress the floral transition of the axillary meristems in Arabidopsis. Plant Cell. 25, 1228–1242.
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ACCEPTED MANUSCRIPT FT/TFL1: Functional Evolution and Mechanisms Putterill, J., Robson, F., Lee, K., Simon, R. and Coupland, G. (1995). The CONSTANS gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors. Cell. 80, 847–857.
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Varkonyi-Gasic, E., Moss, S.M.A., Voogd, C., Wang, T., Putterill, J. and Hellens, R.P. (2013). Homologs of FT, CEN and FD respond to developmental and environmental signals affecting growth and flowering in the perennial vine kiwifruit. New Phytol. 198, 732–746.
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Wada, K.C., Yamada, M., Shiraya, T. and Takeno, K. (2010). Salicylic acid and the flowering gene FLOWERING LOCUS T homolog are involved in poor-nutrition stressinduced flowering of Pharbitis nil. J. Plant Physiol. 167, 447–452. Wang, R., Albani, M.C., Vincent, C., Bergonzi, S., Luan, M., Bai, Y., Kiefer, C., Castillo, R. and Coupland, G. (2011). Aa TFL1 confers an age-dependent response to vernalization in perennial Arabis alpina. Plant Cell. 23, 1307–1321. Wang, Y. and Pijut, P.M. (2013). Isolation and characterization of a TERMINAL FLOWER 1 homolog from Prunus serotina Ehrh. Tree Physiol. 33, 855–865.
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Wigge, P.A., Kim, M.C., Jaeger, K.E., Busch, W., Schmid, M., Lohmann, J.U. and Weigel, D. (2005). Integration of spatial and temporal information during floral induction in Arabidopsis. Science. 309, 1056–1059.
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Winterhagen, P., Tiyayon, P., Samach, A., Hegele, M. and Wünsche, J.N. (2013). Isolation and characterization of FLOWERING LOCUS T subforms and APETALA1 of the subtropical fruit tree Dimocarpus longan. Plant Physiol. Biochem. 71, 184–190.
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Wu, C., You, C., Li, C., Long, T., Chen, G., Byrne, M.E. and Zhang, Q. (2008). RID1, encoding a Cys2/His2-type zinc finger transcription factor, acts as a master switch from vegetative to floral development in rice. Proc. Natl. Acad. Sci. 105, 12915–12920. Wu, L., Liu, D., Wu, J., Zhang, R., Qin, Z., Liu, D., Li, A., Fu, D., Zhai, W. and Mao, L. (2013a). Regulation of FLOWERING LOCUS T by a microRNA in Brachypodium distachyon. Plant Cell. 25, 4363–4377. Wu, W., Zheng, X.M., Lu, G., Zhong, Z., Gao, H.H., Chen, L., Wu, C., Wang, H.-J.H., Wang, Q., Zhou, K., et al. (2013b). Association of functional nucleotide polymorphisms at DTH2 with the northward expansion of rice cultivation in Asia. Proc. Natl. Acad. Sci. 11025, 2775–2780.
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ACCEPTED MANUSCRIPT FT/TFL1: Functional Evolution and Mechanisms Xi, W., Liu, C., Hou, X. and Yu, H. (2010). MOTHER OF FT AND TFL1 regulates seed germination through a negative feedback loop modulating ABA signaling in Arabidopsis. Plant Cell. 22, 1733–1748.
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Xiang, L., Li, X., Qin, D., Guo, F., Wu, C., Miao, L. and Sun, C. (2012). Functional analysis of FLOWERING LOCUS T orthologs from spring orchid (Cymbidium goeringii Rchb. f.) that regulates the vegetative to reproductive transition. Plant Physiol. Biochem. 58, 98–105. Yamada, M. and Takeno, K. (2014). Stress and salicylic acid induce the expression of PnFT2 in the regulation of the stress-induced flowering of Pharbitis nil. J. Plant Physiol. 171, 205– 212.
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Yamaguchi, A., Kobayashi, Y., Goto, K., Abe, M. and Araki, T. (2005). TWIN SISTER OF FT (TSF) acts as a floral pathway integrator redundantly with FT. Plant Cell Physiol. 46, 1175–1189.
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Yan, L., Fu, D., Li, C., Blechl, A., Tranquilli, G., Bonafede, M., Sanchez, A., Valarik, M., Yasuda, S. and Dubcovsky, J. (2006). The wheat and barley vernalization gene VRN3 is an orthologue of FT. Proc. Natl. Acad. Sci. 103, 19581–19586. Ye, J., Geng, Y., Zhang, B., Mao, H., Qu, J. and Chua, N.-H. (2014). The Jatropha FT ortholog is a systemic signal regulating growth and flowering time. Biotechnol. Biofuels. 7, 10.1186/1754–6834–7–91.
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Yeung, K., Seitz, T., Li, S., Janosch, P., McFerran, B., Kaiser, C., Fee, F., Katsanakis, K.D., Rose, D.W., Mischak, H., Sedivy, J.M. and Kolch, W. (1999). Suppression of Raf-1 kinase activity and MAP kinase signalling by RKIP. Nature. 401, 173–177.
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Yoo, S., Kardailsky, I., Lee, J.S., Weigel, D. and Ahn, J.H. (2004). Acceleration of flowering by overexpression of MFT (MOTHER OF FT AND TFL1). Mol. Cells. 17, 95–101.
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Yoo, S.J., Chung, K.S., Jung, S.H., Yoo, S.Y., Lee, J.S. and Ahn, J.H. (2010). BROTHER OF FT AND TFL1 (BFT) has TFL1-like activity and functions redundantly with TFL1 in inflorescence meristem development in Arabidopsis. Plant J. 63, 241–253. Yoo, S.C., Chen, C., Rojas, M., Daimon, Y., Ham, B.K., Araki, T. and Lucas, W.J. (2013). Phloem long-distance delivery of FLOWERING LOCUS T (FT) to the apex. Plant J. 75, 456–468. Zhai, H., Lü, S., Liang, S., Wu, H., Zhang, X., Liu, B., Kong, F., Yuan, X., Li, J. and Xia, Z. (2014). GmFT4, a homolog of FLOWERING LOCUS T, is positively regulated by E1 and functions as a flowering repressor in soybean. PLoS One. 9, e89030. Zhang, J., Liu, G., Guo, C., He, Y., Li, Z., Ning, G., Shi, X. and Bao, M. (2011). The FLOWERING LOCUS T orthologous gene of Platanus acerifolia is expressed as
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alternatively spliced forms with distinct spatial and temporal patterns. Plant Biol. (Stuttg). 13, 809–820.
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S1674-2052(15)00094-5
DOI:
10.1016/j.molp.2015.01.007
Reference:
MOLP 70
To appear in:
MOLECULAR PLANT
Received Date: 21 October 2014 Revised Date:
19 December 2014
Accepted Date: 9 January 2015
Please cite this article as: Wickland D.P., and Hanzawa Y. (2015). The FLOWERING LOCUS T / TERMINAL FLOWER 1 Gene Family: Functional Evolution and MolecularMechanisms. Mol. Plant. doi: 10.1016/j.molp.2015.01.007. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT FT/TFL1: Functional Evolution and Mechanisms
Title:
The FLOWERING LOCUS T / TERMINAL FLOWER 1 Gene Family: Functional Evolution
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and MolecularMechanisms
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Authors:
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Daniel P. Wickland and Yoshie Hanzawa1
Department of Crop Sciences, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA. Tel:+1 (217) 333-4685
To whom correspondence should be addressed:[email protected]
Running title:
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FT/TFL1: Functional Evolution and Mechanisms
Short Summary:
The key flowering regulators FLOWERING LOCUS T (FT) and TERMINAL FLOWER 1 (TFL1) are homologous, but their functions in flowering control are opposite. Here we summarize the recent progress in diverse roles and unique evolution of the FT/TFL1 gene family,and highlight recent work to elucidate the molecular mechanisms of these proteins.
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ACCEPTED MANUSCRIPT FT/TFL1: Functional Evolution and Mechanisms ABSTRACT
In plant development, the flowering transition and inflorescence architecture are modulated by two homologous proteins, FLOWERING LOCUS T (FT) and TERMINAL
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FLOWER 1 (TFL1). The florigen FTpromotes the transition to reproductive development and flowering, while TFL1represses this transition. Despite these proteins’ importance to plant adaptation and crop improvement and their intense study by the plant community, the molecular mechanisms controlling the opposing actions of FT and TFL1 have remained mysterious. Recent
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studies in multiple species have unveiled diverse roles of the FT/TFL1gene family in developmental process other than flowering regulation. In addition, the striking evolution of FT
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homologs into flowering repressorshas occurred independently in several species during the evolution of flowering plants. These reports indicate that the FT/TFL1 gene family is a major target of evolution in nature.Here we comprehensively survey the conserved and diverse functions of the FT/TFL1 gene familythroughut the plant kingdom, summarize new findings regarding the unique evolution of FT in multiple species, and highlight recent work to elucidate
Keywords:
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the molecular mechanisms of theseproteins.
FT; TFL1; PEBP; flowering; evolution; photoperiod; development; inflorescence
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architecture
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ACCEPTED MANUSCRIPT FT/TFL1: Functional Evolution and Mechanisms
INTRODUCTION Several interconnected pathways coordinate flowering time with environmental input to optimize plant adaptation and reproductive success: the photoperiodic, vernalization, ambient
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temperature, plant hormone and autonomous flowering pathways(Blázquez et al., 2003; MutasaGöttgens and Hedden, 2009; Amasino, 2010; Andrés and Coupland, 2012). Two important genes downstream of these flowering pathways are FLOWERING LOCUS T (FT)and TERMINAL FLOWER 1(TFL1). FT and TFL1 encode a pair of flowering regulators with homology to
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phosphatidylethanolamine-binding proteins (PEBPs), which function in diverse signaling pathways involved in growth and differentiation in bacteria, animals and plants (Kardailsky et
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al., 1999; Kobayashi et al., 1999; Yeung et al., 1999; Chautard et al., 2004; Hanzawa et al., 2005; Ahn et al., 2006; Karlgren et al., 2011). FT and TFL1 share ~60% amino acid sequence identity but function in an opposite manner (Hanzawa et al., 2005; Ahn et al., 2006). FTpromotes the transition
to
reproductive
development
and
flowering,
while
TFL1represses
this
transition(Shannon and Meeks-Wagner, 1991; Bradley et al., 1997; Kardailsky et al., 1999; Kobayashi et al., 1999). The flowering inductive function of the universal florigen FT has been
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documented in all angiospermspecies examined (Turck et al., 2008), and the flowering repressive function of TFL1 has been reported in many species as well. Despite the widespread conservation of these flowering regulators across flowering plants, recent studies have unveiled several examples of evolution of FT homologs into flowering repressors. In addition, diverse
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roles of the FT/TFL1 gene family in various developmental processes other than flowering regulation have been reported in multiple species. Although much remains unknown about FT
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and TFL1 function at the molecular level, ongoing approaches are beginning to elucidate the molecular mechanisms underlying FT and TFL1 action. This review summarizes newly accumulated knowledge about the FT/TFL1 gene family,
with a strong emphasis onevolution. We begin by surveying both the conserved and diverse roles of these genes in Arabidopsis and other plant species. Next, the unique evolution of FT and TFL1 homologs in multiple species is covered. The remainder of the review summarizes recent work exploring the molecular actions of these proteins.
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FUNCTIONS IN FLOWERING IN ARABIDOPSIS Photoperiodic input is a primary trigger of FT expression in the facultative long-day plant Arabidopsis thaliana (Arabidopsis). FT facilitates the transition to flowering in response to its
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induction by the transcription factor CONSTANS (CO) (Putterill et al., 1995; Suárez-López et al., 2001). Regulated by the circadian clock and tightly controlled at the transcriptional and posttranscriptional levels by the interplay of multiple transcription factors and photoreceptors (Valverde, 2011; Andrés and Coupland, 2012), CO peaks under long photoperiods at the end of
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the day, when it reaches levels sufficient to promote FT expression in the leaves (Suárez-López et al., 2001; Valverde, 2011). Environmental factors other than photoperiod modulate FT
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expression as well. Temperature-responsive FT regulators, which target the FT promoter or noncoding regions, include SHORT VEGETATIVE PHASE (SVP) (Hartmann et al., 2000; Lee et al., 2007), PHYTOCHROME INTERACTING FACTOR4 (PIF4) (Kumar et al., 2012), LIKE HETEROCHROMATIN PROTEIN1 (LHP1) (Kotake et al., 2003; Adrian et al., 2010) and FLOWERING LOCUS C (FLC) (Michaels and Amasino, 1999; Searle et al., 2006). Upon induction by CO, FT protein has been suggested to move from the leaves through
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the phloem to the shoot apical meristem (SAM) (Corbesier et al., 2007). In the meristem, FT binds to the bZIPtranscription factor FD to form a complex that regulates meristem identity genes, resulting in flowering induction (Abe et al., 2005; Wigge et al., 2005). The meristem identity genes induced by the FT/FD complex, which include APETALA1 (AP1)and
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FRUITFULL (FUL), reprogram the primordia to produce reproductive organs instead of vegetative ones (Abe et al., 2005; Teper-Bamnolker and Samach, 2005; Wigge et al., 2005;
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Amasino, 2010). In addition to inducing FT, CO is suggested to induce—directly or indirectly— expression of TERMINAL FLOWER 1 (TFL1), which controls inflorescence meristem identity and delays the transition to the reproductive phase at the SAM(Simon et al., 1996). TFL1 represses the expression of several genes downstream of FT such as LEAFY (LFY)and AP1, perhaps by partnering with FD, with which it weakly interacts (Bradley et al., 1997; Ratcliffe et al., 1998; Ratcliffe et al., 1999; Hanano and Goto, 2011). The high sequence homology of TFL1 to FT suggests conserved biochemical action, but the action and regulation of these proteins at the molecular level remain unclear(Hanzawa et al., 2005; Ahn et al., 2006), as discussed later in this review.
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ACCEPTED MANUSCRIPT FT/TFL1: Functional Evolution and Mechanisms The six-member PEBP gene family in Arabidopsis also includes TWIN SISTER OF FT (TSF),
BROTHER
OF
FT
(BFT),
ARABIDOPSIS
THALIANA
CENTRORADIALIS
HOMOLOGUE (ATC) and MOTHER OF FT AND TFL1 (MFT) (Kardailsky et al., 1999; Kobayashi et al., 1999; Yoo et al., 2004; Yamaguchi et al., 2005). The conserved roles of these
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genes in flowering regulation have been reported. TSF, the closest FT homolog, resembles FT in terms of protein sequence, induction by CO, diurnal expression, binding to FD, and promotion of flowering when overexpressed (Yamaguchi et al., 2005; Jang et al., 2009). BFT also shares high sequence similarity and diurnal expression with FT but functions in a TFL1-like manner as a
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repressor of flowering genes and flowering (Yoo et al., 2010). ATC represses flowering under short photoperiods, and evidence suggests that this graft-transmissible protein, like FT, moves
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systemically from the vasculature to the shoot apex(Huang et al., 2012a). In addition, ATC interacts with FD and downregulates the meristem identity gene AP1. Finally, MFT shares high homology with both FT and TFL1 and participates in flowering induction, perhaps acting redundantly with FT (Yoo et al., 2004).
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CONSERVED FUNCTIONS IN DIVERSE SPECIES
FT and TFL1 homologs control flowering
Amongangiosperms, FT homologs induce flowering and TFL1 homologs repress flowering. Species possessing flowering inductive FT genes include woody perennials (Endo et
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al., 2005; Böhlenius et al., 2006; Carmona et al., 2007; Matsuda et al., 2009; Kotoda et al., 2010; Hsu et al., 2011; Song et al., 2013), grasses (Kojima et al., 2002; Hayama et al., 2003; Yan et al.,
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2006; Li and Dubcovsky, 2008; Kikuchi et al., 2009; Lazakis et al., 2011; Meng et al., 2011; Wu et al., 2013a; Coelho et al., 2014), legumes (Hecht et al., 2005; Kong et al., 2010; Ono et al., 2010; Laurie et al., 2011; Nan et al., 2014) and ornamentals(Hayama et al., 2007; Hou and Yang, 2009; Imamura et al., 2011; Oda et al., 2012; Xiang et al., 2012; Li et al., 2013; Nakano et al., 2013), among others (Table 1; Figure 1). Likewise, flowering repressive TFL1homologs exist in woody perennials (Pillitteri et al., 2004; Kotoda and Wada, 2005; Boss et al., 2006; Esumi et al., 2010; Chen and Jiang, 2013; Randoux et al., 2014), grasses (Nakagawa et al., 2002; Danilevskaya et al., 2008) and ornamentals(Hou and Yang, 2009; Imamura et al., 2011), among others.
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(Actinidiaspp.) (Varkonyi-Gasic et al., 2013)and chrysanthemum (Chrysanthemum spp.) (Higuchi et al., 2013) have been shown to interact with their respective species-specific FD homologs.Similarly, TFL1 homologs from rose (Randoux et al., 2014) and kiwifruit (Varkonyi-
TFL1 homologs control inflorescence architecture
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Gasic et al., 2013) interact with their respective FD homologs.
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In Arabidopsis, TFL1 delays the flowering transition and promotes indeterminacy of the inflorescence shoot by repressing progressive changes in the developmental phases of the SAM(Bradley et al., 1997). The role of TFL1 in inflorescence architecture is conserved in a number of species. In tomato (Solanumlycopersicum), the TFL1 homolog SELF-PRUNING (SP) influences stem growth habit. Tomato carrying the dominant SP allele exhibits indeterminate growth characterized by the continuous production of inflorescences and fruit, while tomato
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carrying the recessive allele exhibits determinate growth characterized by earlier cessation of inflorescence production and smaller stature (Pnueli et al., 1998; Jiang et al., 2013). In both rose and strawberry (Fragariavesca), non-functional recessive homologs of TFL1 (RoKSN and FvKSN, respectively) establish the horticulturally desirable trait of continuous flowering habit
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(Iwata et al., 2012). In soybean (Glycine max), the TFL1 homolog Dt1 controls stem growth habit (Bernard, 1972; Liu et al., 2010; Tian et al., 2010); the dominant Dt1 allele establishes
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indeterminate habit, in which growth continues after flowering, and the recessive allele establishes determinate habit, in which growth ceases after the onset of flowering. Finally, the common bean (Phaseolus vulgaris) TFL1 homolog PvTFL1y also controls growth habit (Kwak et al., 2012; Repinski et al., 2012), and the pea (Pisumsativum) TFL1 homolog PsTFL1a maintains indeterminate growth (Foucher et al., 2003).
DIVERSE FUNCTIONS OF THE FT/TFL1 GENE FAMILY
Diverse roles of FT and TFL1 homologs in Arabidopsis
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and TSF also control lateral shoot development under long and short photoperiods, respectively (Hiraoka et al., 2013). In addition to its activation by photoperiod, FT is induced under stress conditions by salicylic acid to promote flowering (Martínez et al., 2004). BFT also functions in a stress-responsive flowering pathway; under conditions of high salinity, BFT delays the flowering
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transition by competing with FT for the same binding site on FD (Ryu et al., 2011; Ryu et al., 2014). However, it remains unclear whether the delayed flowering results from the BFT-FD
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complex acting as a transcriptional repressor or from the prevention of FT-FD complex formation due to BFT binding to FD. Finally, MFT promotes seed germination by interacting with the gibberellin and abscisic acid signaling pathways, which control the breakdown of seed dormancy (Xi et al., 2010).
Diverse roles of FT and TFL1 homologs in other plant species in
Arabidopsis,
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processes.
For
instance,
family
some
in
other
speciesfunctions
FThomologsregulate
aspects
in of
development in response to temperature. The two FT genes in sugar beet (Beta vulgaris) are involved in flowering response to the extended cold winter temperatures associated with
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vernalization(Pin et al., 2010). Similarly, poplar (Populustrichocarpa) relies on two FT homologs to coordinate its recurrent, seasonal flowering cycle in response to temperature(Hsu et
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al., 2011). PtFT2, which supports vegetative growth and inhibition of bud set during autumn, is upregulatedboth by high temperatures and long photoperiods during the spring and summer. Conversely, PtFT1, which initiates reproductive growth, is repressed by high temperatures but induced by low temperatures during winter. Low temperatures also promote expression of FT genes in Satsuma mandarin (Citrus unshiu) (Nishikawa et al., 2007) and kiwifruit (VarkonyiGasic et al., 2013). Finally, some members of this gene family modulate growth of underground storage organs. The potato (Solanumtuberosum) FT homolog StSP6A functions as a mobile “tuberigen” that induces the photoperiod-sensitive process of tuberization(Navarro et al., 2011),
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EVOLUTION OF THE FT/TFL1 GENE FAMILY
The origin of the FT/TFL1 gene family
Recent reports indicate thatMFT genes are ancestral to FT and TFL1 genes, as basal plant species such as mosses possesshomologs of MFT but not ofFT or TFL1(Hedman et al., 2009;
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Karlgren et al., 2011). It is thought that duplication of an ancestral MFT-like gene during evolution spawned an MFT-like clade and anFT/TFL1-like clade, which led to further
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diversification of function, duplication and, with the emergence of angiosperms, eventual divergence into separate FT-like and TFL1-like clades (Hedman et al., 2009; Karlgren et al., 2011; Klintenäs et al., 2012). Data from gymnosperms suggest that the ancestor of FT and TFL1 functioned in a TFL1-like manner and that FT and TFL1 function diverged after the evolutionary separation of gymnosperms and angiosperms (Karlgren et al., 2011; Klintenäs et al., 2012) (Table 1).In the gymnosperm Norway spruce (Piceaabies), for instance, PaFTL1 and PaFTL2
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possess sequence homology to both FT and TFL1 but appear to function more similarly to TFL1 interms of growth repression in a general sense; PaFTL2functions in initiation of early bud set and cessation of growth in late summer to achieve full cold hardiness (Karlgren et al., 2013). Both PaFTL1 and PaFTL2 delay flowering in transgenic Arabidopsis (Karlgren et al., 2011;
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Recentevolution of FT homologs intoflowering repressors Intriguingly,some FT homologs apparently have acquired a repressor function during
recent evolution (Figure 2). In multiplespecies, arepressor FT antagonizes the function of aparalogousinducer FT. Sunflower (Helianthus annuus) contains four FT homologs, one of which resulted from a mutation that yielded a novel repressor function (Blackman et al., 2010). Wild sunflower carries an in-frame allele of HaFT1, an FT homolog that stimulates flowering in transgenic Arabidopsis. Domesticated sunflower, however, carries a frame-shifted HaFT1 allele, which encodes a protein that represses flowering. In transgenic Arabidopsis, the domesticated HaFT1 allele delays flowering by interfering with another sunflower FT homolog, the flowering
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repressor function during sugar beet evolution, inhibits flowering by repressing the flowering inducer BvFT2 before the onset of vernalization. Vernalization then reduces BvFT1 expression and upregulatesBvFT2 expression, triggering flowering. In onion, the FT homolog AcFT4 acts as a repressor of bulb formation. During early development, AcFT4 inhibits bulb formation by
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repressing AcFT1 expression (Lee et al., 2013). After an onion plant reaches maturity under the appropriate daylength, downregulation of AcFT4 allows upregulation of AcFT1, which formation.
Finally,
three
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the
four
FT
homologs
in
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(Nicotianatabacum)repress flowering in tobacco (Harig et al., 2012), and FT homologs from sugarcane (Saccharumspp.) (Coelho et al., 2014), longan (Dimocarpuslongan) (Winterhagen et al., 2013) and soybean (Zhai et al., 2014) have been shown to repress flowering in transgenic Arabidopsis.
Sequence alignment of these proteins reveals two conserved sites that distinguish inducer
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and repressor function in FT homologs (Figure2). In species that possess repressor FTs, all inducer FTs (except GmFT5a in soybean) contain tyrosine at position 134 based on alignment with Arabidopsis FT protein sequence, and all repressor FTs (except FT-/TFL1-like PaFTL1 and PaFTL2 in Norway spruce) contain non-tyrosine amino acids, possibly indicating a contribution
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of this site to FT inductive function. In support of this notion, Arabidopsis FT gains repressor activity in response to substitution at position 134 (Ho and Weigel, 2014), and this residue
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contributes to the antagonistic roles of BvFT1 and BvFT2 in sugar beet as well(Pin et al., 2010). The conserved tyrosine at this position in the repressors PaFTL1 and PaFTL2 from the gymnosperm Norway spruce implies the ancestral TFL1-like function of FT and TFL1. The second conserved residue lies at position 138. In species that possess repressor FTs,
all inducer FTs contain tryptophan at this siteand all repressor FTs (except DlFT2 in longan and GmFT4 in soybean) contain non-tryptophan amino acids at this site, suggesting the importance of this residue to FT inductive function. Indeed, mutation at residue Trp-138 as well as residues Glu-109, Gln-140 and Asn-152 in Arabidopsis converts FT into a TFL1-like repressor by affecting protein surface charge (Ho and Weigel, 2014); furthermore,residue 138partly
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after the divergence of FT-like and TFL1-like genes.
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mutation at Tyr-134 and Trp-138 occurred multiple times during the evolution of the FT clade
MOLECULARMECHANISMS OF FT AND TFL1 FUNCTION
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Although much remains unknown about the molecular mechanisms underlying FT and TFL1 function in Arabidopsis, recent work has identified several FT- and TFL1-interacting
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molecules and continues gradually to uncover the molecular and biochemical nature of FT and TFL1 action. In addition to the established interactions of FT and TFL1 with FD to modulate flowering gene expression, novel molecules involved in FT transport andthe role of TFL1 in trafficking to protein storage vesicles have been reported, as detailed below.
FT and TFL1 function as transcriptional regulators
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It is thought that FT and TFL1 do not bind directly to DNA but act as transcriptional coregulators by interacting with the transcription factor FD, as described earlier. The complex of FD with either FT or TFL1 likely contains other protein components. In rice, the FT ortholog Hd3a is generated in the leaves and moves to the SAM, where it forms a complex with 14-3-3
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proteins that mediate its interaction withOsFD1, an FD homolog(Tamaki et al., 2007; Komiya et al., 2008). Once in the nucleus, the Hd3a/14-3-3/OsFD1 complex (known as the “florigen
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activation complex”) promotes expression of OsMADS15, anAP1homolog(Komiya et al., 2008; Taoka et al., 2011).Likewise, the tomato TFL1 homolog SP binds to 14-3-3 proteins (Pnueli et al., 2001). In Arabidopsis, interactions between 14-3-3 proteins and FT, TFL1 and FD suggest that a similar mechanism operates in this species (Pnueli et al., 2001; Taoka et al., 2011; Ho and Weigel, 2014). These observations in multiple species support the molecular models proposed previously, in which interacting proteins or protein complexes recruited by FT and/or TFL1 define the opposing actions of FT and TFL1 (Hanzawa et al., 2005; Ho and Weigel, 2014). In contrast tothe interaction between FT andBRANCHED1 (BRC1) described below, direct interaction between FT and TFL1 has not been reported, potentially indicating that TFL1
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ACCEPTED MANUSCRIPT FT/TFL1: Functional Evolution and Mechanisms replaces FT in the florigen activation complex and altersaction of the complex through recruitment of uncharacterized factors and/or protein modifications.
BRC1 interacts with FT to repress axillary bud flowering
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In addition to moving from the leaves to the SAM, FT moves to axillary buds, where it interacts with the TCP transcription factor BRC1 (Aguilar-Martínez et al., 2007; Niwa et al., 2013). BRC1 regulates axillary bud development and differentiation, a process tightly linked to the shoot apex floral transition in Arabidopsis. A repressor of axillary bud development, BRC1
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inhibits FT function to delay flowering in axillary meristems. BRC1 interacts directly with FT withoutinvolvement of 14-3-3 proteins (Niwa et al., 2013). BRC1 also interacts with TSF but not
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with TFL1. Overexpression of BRC1 in the shoot apex retards flowering, while loss-of-function elevates expression of the meristem identity genesAP1 and FUL,which suggests that BRC1 represses FT’s induction of these genes.Whether BRC1 comprises part of the florigen activation complex or prevents FT from forming the florigen activation complex remains unclear. Nevertheless, the role of FT and BRC1 in axillary bud development indicates FT’s involvement not only in flowering control but also in regulation of shoot architecture. Supporting FT function
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in inflorescence development, ectopic expression of FT in Arabidopsis results in determinate stem growth characterized by the SAM producing a terminal flower similar to that ofTFL1lossof-function mutants.
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FTIP1 and PC are implicated in movement of FT FT-INTERACTING PROTEIN 1 (FTIP1) is thoughtto facilitate FT movement from
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phloem companion cells to sieve elements (Liu et al., 2012). Loss of FTIP1 delays flowering time and disrupts FT movement to sieve elements, resulting in FT accumulation in phloem companion cells. Therefore, FTIP1-mediated transport is required for FT to induce flowering at the shoot apex. Experiments using FT-transformed Cucurbitamoschatasuggest that FT enters the phloem translocation stream by diffusing through plasmodesmata(Yoo et al., 2013). A selective mechanism is then thought to regulate delivery of FT from the phloem translocation stream into the SAM. FT also binds to the phospholipid phosphatidylcholine (PC), a component of cellular membranes (Nakamura et al., 2014). High levels of PC at the shoot apex cause both early
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ACCEPTED MANUSCRIPT FT/TFL1: Functional Evolution and Mechanisms flowering—especially in combination with high levels of FT—and elevated expression of the FT targets SOC1 and AP1, while low levels of PC cause late flowering. Therefore, PC may promote flowering through the action of FT. Different molecular species of PC oscillate throughout the day, and FT preferentially binds to those PC species abundant during the light period, suggesting
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a mechanism by which FT induces flowering at the appropriate time of day. Two models have been proposed to account for the effect of PC on flowering phenotype(Nakamura et al., 2014). A constituent of the nuclear membrane, PC may import FT into the nucleus from the cytosol to
FT to FD. Further study would clarify these scenarios.
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Mobile TFL1 plays a role in vesicle trafficking
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promote flowering. Another possibility is that vesicles containing PC function in trafficking of
Like FT, TFL1 functions as a mobile signal but only within the SAM (Conti and Bradley, 2007). While TFL1 mRNA remains confined tothe central region of the shoot apex, TFL1 protein spreads throughout the shoot apex (but does not reach floral meristems). This TFL1 movement throughout the SAM may ensure indeterminacy of the region by preventing the local expression of flowering genes. No such TFL1 movement in the shoot apex is observed in the
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LFY loss-of-function mutant, which indicates that LFY indirectly promotes TFL1 movement to outer cells of the meristem. TFL1 function in endomembrane trafficking to protein storage vesicles—cell components that store assorted proteins and minerals—has also been reported (Sohn et al., 2007). TFL1loss-of-function mutants exhibit disrupted trafficking to protein storage
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vesicles, implicating TFL1 involvement in endomembrane trafficking. This finding, in addition to the fact that TFL1 protein is found in both the nucleus and cytoplasm,may suggest that TFL1
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blocks FD-dependent transcription by shuttling FD from the nucleus to protein storage vesicles(Hanano and Goto, 2011). However, more research is needed to investigate this possibility.
CONCLUSION
Photoperiodic regulation of flowering time facilitates the regional adaptation of plants and influences agricultural growing seasons.Central components of the photoperiodic flowering response, genes belonging to the FT/TFL1 family show conserved functions among angiosperms, with FT homologs acting as flowering inducers and TFL1 homologs acting as flowering
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ACCEPTED MANUSCRIPT FT/TFL1: Functional Evolution and Mechanisms repressors.In addition to operating in diverse developmental processes, FT and TFL1 have evolved dynamically over the course of plant evolution. Recent evolution of FT homologs has resulted in their acquisition of a repressor function in multiple species. Current research is gradually revealing the molecular mechanisms of FT and TFL1 action and uncovering the
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significance of FT- and TFL1-interacting proteins in controlling the opposing functions of FT and TFL1.Futureapproaches will address the tantalizing questions that remain.What molecules comprise theflorigen activation complex, and what molecular mechanisms control the activity of this complex? Is there any link between phospholipids and TFL1-regulated vesicle trafficking?
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Does FT, in addition to TFL1, participate in vesicle trafficking, and what mechanisms govern this process? Our burgeoning knowledge of the FT/TFL1 gene family will allow modification of
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florigen and anti-florigenaction in the near future, thereby supporting efforts to breed superior crop varieties highly adaptive to a wide range of environments in order to meet the agricultural demands of the rapidly expandingglobal population.
FUNDING
This work was supported by the Agriculture and Food Research Initiative Competitive Grants
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Program from the USDA National Institute of Food and Agriculture (USDA-NIFA2011-00078) and the Plant Genome Research Program from the National Science Foundation (NSF-PGRPIOS-1339388). No conflict of interest declared.
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FIGURE LEGENDS
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Figure 1. Phylogenetic tree of the FT/TFL1 protein family Maximum likelihood phylogenetic tree of the FT/TFL1 protein family in 50 plant species characterized by transgenic approaches. The tree was constructed using the Maximum Likelihood method in MEGA6 software(Tamura et al., 2013). Bootstrap values >30% for 1,000 resamplings are shown on branches. Blue and red branches indicate FT-like and TFL1-like proteins, respectively. Protein names in brown indicate FT-like proteins with repressor function. Arabidopsis proteins are shown in bold.
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ACCEPTED MANUSCRIPT FT/TFL1: Functional Evolution and Mechanisms Figure 2. Amino acid alignment of inducer FTs and repressor FTs at the conserved external loop in exon 4 Alignment of amino acid sequences of FT homologs at the conserved position 85 (exon 2) and segment B (positions 128-141, exon 4) from Arabidopsis(Kardailsky et al., 1999; Kobayashi et
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al., 1999), onion (Lee et al., 2013), sugar beet (Pin et al., 2010), longan(Winterhagen et al., 2013), soybean (Kong et al., 2010; Nan et al., 2014; Zhai et al., 2014), sunflower (Blackman et al., 2010), tobacco (Harig et al., 2012)and sugarcane (Coelho et al., 2014). FT-/TFL1-like proteins from Norway spruce are also included (Karlgren et al., 2011). Red asterisks
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indicaterepressor function characterized in a gene’s native species and blue asterisks indicate repressor function characterized in transgenic Arabidopsis. Amino acid positions indicated are
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based on the Arabidopsis FT protein sequence. All inducer FTs (except GmFT5a) contain tyrosine at position 134, while repressor FTs (except FT-/TFL1-like PaFTL1 and PaFTL2) contain non-tyrosine amino acids. Additionally, all inducer FTs contain tryptophan at position 138, while repressor FTs (except DlFT2 and GmFT4) contain non-tryptophan amino acids.
Protein sequences with the following IDs were obtained from The Arabidopsis Information
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Resource (TAIR), Genbank and Phytozome: AT1G65480.1 (AtFT), AT5G03840.1 (AtTFL1), AGZ20207.1 (AcFT1), AGZ20210.1 (AcFT4), ADM92608.1 (BvFT1), ADM92610.1 (BvFT2), AEZ63949.1 (DlFT1), AEZ63950.1 (DlFT2), BAJ33491.1 (GmFT2a), Glyma08g47810.1 (GmFT4), BAJ33494.1 (GmFT5a), ADF32943.1 (HaFT1), ADF32945.1 (HaFT4), AFS17369.1
ABQ85553.1
(PaFTL2),
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(PaFTL1),
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(NtFT1), AFS17370.1 (NtFT2), AFS17371.1 (NtFT3), AFS17372.1 (NtFT4), AEH59567.1
14
AHZ46121.1
(ScFT1).
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FT/TFL1: Functional Evolution and Mechanisms Table 1. Diverse functions of the FT/TFL1 gene family in 49 plant species characterized by transgenic approaches.
Clustered gentian (Gentianatriflora) Common bean (Phaseolus vulgaris) Dancing lady orchid (Oncidiumgowerramsey) Fig (Ficuscarica)
HvFT1
• InductionB
HvFT2
• InductionB
HvFT3
• InductionB
PsTFL1
• RepressionA
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REGULATORY INPUT
• Promotion of polycarpy
• VernalizationD
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• Induction • RepressionA • Repression
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Black cherry (Prunusserotina) Chinese narcissus (Narcissus tazettavar. chinensis) Chrysanthemum (Chrysanthemum spp.)
MdFT1, MdFT2 MdCENa, MdCENb AaTFL1
OTHER FUNCTION
• LD photoperiod D • HvCO1 D • HvFT3 D • SD photoperiod D • SD photoperiod D
REFERENCES Esumi et al., 2005; Kotoda and Wada, 2005; Mimida et al., 2009 Kotoda et al., 2010 Mimida et al., 2009 Wang et al., 2011 Faure et al., 2007; Kikuchi et al., 2009; Campoli et al., 2012 Faure et al., 2007; Kikuchi et al., 2009 Faure et al., 2007; Kikuchi et al., 2009 Wang and Pijut, 2013
NtFT
• InductionA
• Warm temperature D
Li et al., 2013; Noy-Porat et al., 2013
CsFTL3
• Induction
• SD photoperiod D • Heat E • CsAFTE • LD photoperiod D
Oda et al., 2012; Nakano et al., 2013
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Alpine rock-cress (Arabisalpina) Barley (Hordeumvulgare)
MdTFL1-1, MdTFL1-2
FLOWERING FUNCTION • RepressionA
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Apple (Malusdomestica)
HOMOLOG
CsAFT GtF1, GtF2 GtTFL1 PvTFL1y
• Repression • InductionA • RepressionA • RepressionA
OnFT OnTFL1 FcFT1
• InductionA • RepressionA • InductionC
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SPECIES
• Promotion of indeterminacy • Photoperiod D
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Higuchi et al., 2013 Imamura et al., 2011 Imamura et al., 2011 Kwak et al., 2008; Repinski et al., 2012 Hou and Yang, 2009 Hou and Yang, 2009 Ikegami et al., 2013
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FT/TFL1: Functional Evolution and Mechanisms
Maize (Zea mays)
Medicago (Medicagotruncatula)
• RepressionA • InductionA
PnTFL1 PnFT1, PnFT2 PaFT
• RepressionA • InductionA • InductionA
DlFT1
• InductionA
DlFT2
• RepressionA
Ljcen1 LjFT ZCN8
• RepressionA • Induction A • Induction
ZCN2
• Repression
MtFTa1
• Growth regulation
• InductionA
MtFTc
• InductionA
• Cool temperature D
• SD photoperiod D
• LD photoperiod D • SD photoperiod D • Autonomous pathwayD
• LD photoperiod D
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Boss et al., 2006; Carmona et al., 2007; Fernandez et al., 2010; Crane et al., 2012 Carmona et al., 2007 Esumi et al., 2009 Esumi et al., 2010 Varkonyi-Gasic et al., 2013 Varkonyi-Gasic et al., 2013 Fukuda et al., 2011 Igasaki et al., 2008 Igasaki et al., 2008 Zhang et al., 2011 Winterhagen et al., 2013 Winterhagen et al., 2013
• LD photoperiod D • VernalizationD
• Induction
MtFTb1
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Kiwifruit CEN LsFT
• Dormancy release
• CytokininsD
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• InductionA • InductionA • RepressionA • InductionA
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Lotus japonicus
VvFT PmFT PmTFL1 Kiwifruit FT
• Control ofbranching and fruit density
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Lettuce (Lactuca sativa) Lombardy poplar (Populusnigra) London plane (Platanusacerifolia) Longan (Dimocarpuslongan)
• RepressionA
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Japanese apricot (Prunusmume) Kiwifruit (Actinidiaspp.)
VvTFL1A
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Grapevine (Vitisvinifera)
Guo et al., 2006 Ono et al., 2010 Muszynski et al., 2006; Danilevskaya et al., 2008; Lazakis et al., 2011; Meng et al., 2011 Danilevskaya et al., 2008; Danilevskaya et al., 2010 Hecht et al., 2005; Laurie et al., 2011; Putterill et al., 2013 Hecht et al., 2005; Laurie et al., 2011; Putterill et al., 2013 Hecht et al., 2005; Laurie et al., 2011; Putterill et al., 2013
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FT/TFL1: Functional Evolution and Mechanisms • Induction • RepressionA
PaFTL2
• RepressionA
AcFT1 AcFT2
• Induction of bulb formation • InductionA
AcFT4
Phalaenopsis orchid (Phalaenopsis hybrid Fortune Saltzman)
Pharbitis (Ipomoea nil)
• Repression • InductionA
PsFTa2 PsFTb1 PsFTb2 PsFTc PsTFL1a
• InductionA • InductionA • InductionA • InductionA
PsTFL1c
• Repression
PpTFL1
• InductionA
PpTFL1-1, PpTFL1-2, PcTFL1-1, PcTFL1-2 PhFT
• Repression
PnFT1
• AcFT4 E
Karlgren et al., 2011; Klintenäs et al., 2012; Karlgren et al., 2013 Karlgren et al., 2011; Klintenäs et al., 2012; Karlgren et al., 2013 Lee et al., 2013
• VernalizationD
Lee et al., 2013
• LD photoperiod E
Lee et al., 2013 Pillitteri et al., 2004 Hecht et al., 2011
• Promotion of inflorescence identity
Hecht et al., 2011 Hecht et al., 2011 Hecht et al., 2011 Hecht et al., 2011 Singer et al., 1990; Foucher et al., 2003 Singer et al., 1990; Foucher et al., 2003 Liang et al., 2010; Chen and Jiang, 2013 Esumi et al., 2005; Freiman et al., 2012
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CsTFL PsFTa1
• SD photoperiod D
• Maintenance of indeterminacy
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Peach (Prunuspersica) Pear (Pyrusspp.)
• Inhibition of bulb formation
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Orange (Citrus sinensis) Pea (Pisumsativum)
• Cone development, meristem inhibition and needle formation • Bud set/burst • Growth repression
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PaFTL1
Song et al., 2013
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Onion (Allium cepa)
VcFT
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Northern Highbush Blueberry (Vacciniumcorymbosum) Norway Spruce (Piceaabies)
• InductionA
• Warm temperature (day) D • Cool temperature (night) D
Li et al., 2014b
• Induction
• SD photoperiod D
Hayama et al., 2007
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FT/TFL1: Functional Evolution and Mechanisms
AcFT
• InductionA
• Fruit development
PtFT1
• Induction
PtFT2
• Induction
• Growth cessation and bud set • Promotion ofvegetative growth • Regulation of meristem identity
• Repression • InductionA
• Cool temperature D • PtCO2 D • LD photoperiodD • Warm temperature D
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PopCEN1, PopCEN2 PopMFT StTFL1
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• Induction
• Regulation oftuberization
StSP3D StSP6A
• Induction
Cm-FTL1, Cm-FTL2 FTL1, FTL2
• InductionA
Hd3a
• Induction
• Induction oftuberization
• Induction
• SD photoperiod D • StCOE
• LD photoperiod D • miR5200E • SD photoperiod D • DTH2 D • EHD1 D • EHD2 D • HD1 D
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Pumpkin (Cucurbita maxima) Purple false brome (Brachypodiumdistachyon) Rice (Oryza sativa)
JcFT
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Potato (Solanumtuberosum)
• Induction
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Physic nut (Jatrophacurcas) Pineapple (Ananascomosus) Poplar (Populusspp.)
• SD photoperiod D • Salicylic acid D • Nutrient stress D
PnFT2
Rice
RFT1
• LD photoperiod D
• Induction
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Hayama et al., 2007; Wada et al., 2010; Yamada and Takeno, 2014 Li et al., 2014a; Ye et al., 2014 Lv et al., 2012 Böhlenius et al., 2006; Hsu et al., 2011 Böhlenius et al., 2006; Hsu et al., 2011 Mohamed et al., 2010 Mohamed et al., 2010 Guo et al., 2010 Navarro et al., 2011 Navarro et al., 2011; González-Schain et al., 2012 Lin et al., 2007 Wu et al., 2013a Izawa et al., 2002; Kojima et al., 2002; Hayama et al., 2003; Doi et al., 2004; Matsubara et al., 2008; Park et al., 2008; Wu et al., 2008; Komiya et al., 2009; Wu et al., 2013b; Cai et al., 2014
Izawa et al., 2002; Kojima et
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FT/TFL1: Functional Evolution and Mechanisms • DTH2 D • EHD1 D • EHD2 D
• Repression • Repression
RoFT
• InductionA • RepressionA
Ryegrass (Loliumperenne) Satsuma mandarin (Citrus unshiu)
LpTFL1 CiFT
• InductionA
Snapdragon (Antirrhinum spp.) Soybean (Glycine max)
CEN
• RepressionC
Sugar beet
• Cool temperature D
• Maintenance of inflorescence identity • Control of stem growth habit • Inhibition of seed germination
• Induction
GmFT4 GmFT5a
• RepressionA • Induction
• E1 D
• InductionA
• SD photoperiod D
CgFT
al., 2002; Hayama et al., 2003; Doi et al., 2004; Matsubara et al., 2008; Park et al., 2008; Wu et al., 2008; Komiya et al., 2009; Cai et al., 2014; Wu et al., 2013b Nakagawa et al., 2002 Iwata et al., 2012; Koskela et al., 2012; Randoux et al., 2014 Remay et al., 2009; Randoux et al., 2014 Jensen et al., 2001 Endo et al., 2005; Nishikawa et al., 2007; Matsuda et al., 2009 Bradley et al., 1996; Amaya et al., 1999 Bernard, 1972; Liu et al., 2010; Tian et al., 2010 Li et al., 2014c
• LD photoperiod D • SD photoperiod E
Kong et al., 2010; Sun et al., 2011; Nan et al., 2014 Zhai et al., 2014 Kong et al., 2010; Nan et al., 2014 Huang et al., 2012b; Xiang et al., 2012 Iwata et al., 2012; Koskela et al., 2012
• Induction
• LD photoperiod D • Far-red and blue light D
Koskela et al., 2012; Rantanen et al., 2014
• Repression
• SD photoperiod D
Pin et al., 2010; Pin et al.,
EP
GmFT2a
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Spring orchid (Cymbidium spp.) Strawberry (Fragariavesca)
• VernalizationE
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Dt1 GmMFT
• Establishment of continuous flowering habit (recessive allele)
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RCN1, RCN2 RoKSN
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Rose (Rosa spp.)
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(Oryza sativa)
FvKSN / FvTFL1
• Repression
FvFT1
BvFT1
• Establishment of continuous flowering habit (recessive allele)
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FT/TFL1: Functional Evolution and Mechanisms • Cold E • BvBTC1 E • BvBTC1 D
(Beta vulgaris)
Tomato (Solanumlycopersicum)
SFT Wheat (Triticumaestivum)
• RepressionA • RepressionA • Repression A • Induction A • Repression
• SD photoperiod D • LD photoperiod D • SD photoperiod D
• Induction
TaMFT
• Regulation of germination
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• Induction
Pin et al., 2010; Pin et al., 2012 Coelho et al., 2014 Coelho et al., 2014 Blackman et al., 2010 Blackman et al., 2010 Harig et al., 2012
• SD photoperiod D
Harig et al., 2012 Pnueli et al., 1998; Jiang et al., 2013
• SP E
Lifschitz et al., 2006; Shalit et al., 2009 Nakamura et al., 2011
• Maintenance of indeterminate growth • Regulation of growth cycles
• Induction
TaFT / TaFT1
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ScTFL1 ScFT1 HaFT1 HaFT4 NtFT1, NtFT2, NtFT3 NtFT4 SP
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Sugarcane (Saccharumspp.) Sunflower (Helianthus annuus) Tobacco (Nicotianatabacum)
• Induction
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BvFT2
2012
• Cool temperature D
Yan et al., 2006; Li and Dubcovsky, 2008; Lv et al., 2014
A: function assessed in transgenic Arabidopsis; B: function assessed in transgenic rice; C: function assessed in transgenic tobacco;
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D: input that induces expression of a particular FT/TFL1 homolog;E: input that represses expression of a particular FT/TFL1 homolog.
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ACCEPTED MANUSCRIPT FT/TFL1: Functional Evolution and Mechanisms LITERATURE CITED Abe, M., Kobayashi, Y., Yamamoto, S., Daimon, Y., Yamaguchi, A., Ikeda, Y., Ichinoki, H., Notaguchi, M., Goto, K. and Araki, T. (2005). FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex. Science. 309, 1052–1056.
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ACCEPTED MANUSCRIPT FT/TFL1: Functional Evolution and Mechanisms Boss, P.K., Sreekantan, L. and Thomas, M.R. (2006). A grapevine TFL1 homologue can delay flowering and alter floral development when overexpressed in heterologous species. Funct. Plant Biol. 33, 31–41.
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Cai, Y., Chen, X., Xie, K., Xing, Q., Wu, Y., Li, J., Du, C., Sun, Z. and Guo, Z. (2014). Dlf1, a WRKY transcription factor, is involved in the control of flowering time and plant height in rice. PLoS One. 9, e102529.
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Campoli, C., Drosse, B., Searle, I., Coupland, G. and VonKorff, M. (2012). Functional characterisation of HvCO1, the barley (Hordeum vulgare) flowering time ortholog of CONSTANS. Plant J. 69, 868–880. Carmona, M.J., Calonje, M. and Martínez-Zapater, J.M. (2007). The FT/TFL1 gene family in grapevine. Plant Mol. Biol. 63, 637–650. Chautard, H., Jacquet, M., Schoentgen, F., Bureaud, N. and Bénédetti, H. (2004). Tfs1p, a member of the PEBP family, inhibits the Ira2p but not the Ira1p Ras GTPase-activating protein in Saccharomyces cerevisiae. Eukaryot. Cell. 3, 459–470.
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Chen, Y. and Jiang, P. (2013). Characterization of peach TFL1 and comparison with FT/TFL1 gene families of the Rosaceae. J. Am. Soc. Hortic. Sci. 138, 12–17.
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Coelho, C.P., Minow, M.A.A., Chalfun-Júnior, A. and Colasanti, J. (2014). Putative sugarcane FT/TFL1 genes delay flowering time and alter reproductive architecture in Arabidopsis. Front. Plant Sci. 5, doi: 10.3389/fpls.2014.00221.
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Conti, L. and Bradley, D. (2007). TERMINAL FLOWER1 is a mobile signal controlling Arabidopsis architecture. Plant Cell. 19, 767–778. Corbesier, L., Vincent, C., Jang, S., Fornara, F., Fan, Q., Searle, I., Giakountis, A., Farrona, S., Gissot, L., Turnbull, C. and Coupland, G. (2007). FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science. 316, 1030–1033. Crane, O., Halaly, T., Pang, X., Lavee, S., Perl, A., Vankova, R. and Or, E. (2012). Cytokinin-induced VvTFL1A expression may be involved in the control of grapevine fruitfulness. Planta. 235, 181–192.
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ACCEPTED MANUSCRIPT FT/TFL1: Functional Evolution and Mechanisms Danilevskaya, O.N., Meng, X., Hou, Z., Ananiev, E. V and Simmons, C.R. (2008). A genomic and expression compendium of the expanded PEBP gene family from maize. Plant Physiol. 146, 250–264.
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Danilevskaya, O.N., Meng, X. and Ananiev, E. V (2010). Concerted modification of flowering time and inflorescence architecture by ectopic expression of TFL1-like genes in maize. Plant Physiol. 153, 238–251.
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Doi, K., Izawa, T., Fuse, T., Yamanouchi, U., Kubo, T., Shimatani, Z., Yano, M. and Yoshimura, A. (2004). Ehd1, a B-type response regulator in rice, confers short-day promotion of flowering and controls FT-like gene expression independently of Hd1. Genes Dev. 18, 926–936.
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Endo, T., Shimada, T., Fujii, H., Kobayashi, Y., Araki, T. and Omura, M. (2005). Ectopic expression of an FT homolog from Citrus confers an early flowering phenotype on trifoliate orange (Poncirus trifoliata L. Raf.). Transgenic Res. 14, 703–712. Esumi, T., Tao, R. and Yonemori, K. (2005). Isolation of LEAFY and TERMINAL FLOWER 1 homologues from six fruit tree species in the subfamily Maloideae of the Rosaceae. Sex. Plant Reprod. 17, 277–287. Esumi, T., Hagihara, C., Kitamura, Y., Yamane, H. and Tao, R. (2009). Identification of an FT ortholog in Japanese apricot (Prunus mume Sieb. et Zucc.). J. Hortic. Sci. Biotechnol. 84, 149–154.
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Esumi, T., Kitamura, Y., Hagihara, C., Yamane, H. and Tao, R. (2010). Identification of a TFL1 ortholog in Japanese apricot (Prunus mume Sieb. et Zucc.). Sci. Hortic. 125, 608–616.
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Faure, S., Higgins, J., Turner, A. and Laurie, D.A. (2007). The FLOWERING LOCUS T-like gene family in barley (Hordeum vulgare). Genetics. 176, 599–609.
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Fernandez, L., Torregrosa, L., Segura, V., Bouquet, A. and Martinez-Zapater, J.M. (2010). Transposon-induced gene activation as a mechanism generating cluster shape somatic variation in grapevine. Plant J. 61, 545–457. Foucher, F., Morin, J., Courtiade, J., Cadioux, S., Ellis, N., Banfield, M.J. and Rameau, C. (2003). DETERMINATE and LATE FLOWERING are two TERMINAL FLOWER1/CENTRORADIALIS homologs that control two distinct phases of flowering initiation and development in pea. Plant Cell. 15, 2742–2754. Freiman, A., Shlizerman, L., Golobovitch, S., Yablovitz, Z., Korchinsky, R., Cohen, Y., Samach, A., Chevreau, E., LeRoux, P.M., Patocchi, A. and Flaishman, M.A. (2012). Development of a transgenic early flowering pear (Pyrus communis L.) genotype by RNAi silencing of PcTFL1-1 and PcTFL1-2. Planta. 235, 1239–1251.
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ACCEPTED MANUSCRIPT FT/TFL1: Functional Evolution and Mechanisms Fukuda, M., Matsuo, S., Kikuchi, K., Kawazu, Y., Fujiyama, R. and Honda, I. (2011). Isolation and functional characterization of the FLOWERING LOCUS T homolog, the LsFT gene, in lettuce. J. Plant Physiol. 168, 1602–1607.
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González-Schain, N.D., Díaz-Mendoza, M., Zurczak, M. and Suárez-López, P. (2012). Potato CONSTANS is involved in photoperiodic tuberization in a graft-transmissible manner. Plant J. 70, 678–690. Guo, X., Zhao, Z., Chen, J., Hu, X. and Luo, D. (2006). A putative CENTRORADIALIS/TERMINAL FLOWER1-like gene, Ljcen1, plays a role in phase transition in Lotus japonicus. J. Plant Physiol. 163, 436–444.
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Guo, J.L., Yu, C.L., Fan, C.Y., Lu, Q.-N., Yin, J.M., Zhang, Y.F. and Yang, Q. (2010). Cloning and characterization of a potato TFL1 gene involved in tuberization regulation. Plant Cell, Tissue Organ Cult. 103, 103–109.
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Hanano, S. and Goto, K. (2011). Arabidopsis TERMINAL FLOWER1 is involved in the regulation of flowering time and inflorescence development through transcriptional repression. Plant Cell. 23, 3172–3184. Hanzawa, Y., Money, T. and Bradley, D. (2005). A single amino acid converts a repressor to an activator of flowering. Proc. Natl. Acad. Sci. 102, 7748–7753.
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Harig, L., Beinecke, F.A., Oltmanns, J., Muth, J., Müller, O., Rüping, B., Twyman, R.M., Fischer, R., Prüfer, D. and Noll, G.A. (2012). Proteins from the FLOWERING LOCUS T-like subclade of the PEBP family act antagonistically to regulate floral initiation in tobacco. Plant J. 72, 908–921.
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Hartmann, U., Höhmann, S., Nettesheim, K., Wisman, E., Saedler, H. and Huijser, P. (2000). Molecular cloning of SVP: a negative regulator of the floral transition in Arabidopsis. Plant J. 21, 351–360.
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Hayama, R., Yokoi, S., Tamaki, S., Yano, M. and Shimamoto, K. (2003). Adaptation of photoperiodic control pathways produces short-day flowering in rice. Nature. 422, 719–722. Hayama, R., Agashe, B., Luley, E., King, R. and Coupland, G. (2007). A circadian rhythm set by dusk determines the expression of FT homologs and the short-day photoperiodic flowering response in Pharbitis. Plant Cell. 19, 2988–3000. Hecht, V., Foucher, F., Ferrándiz, C., Macknight, R., Navarro, C., Morin, J., Vardy, M.E., Ellis, N., Beltrán, J.P., Rameau, C. and Weller, J.L. (2005). Conservation of Arabidopsis flowering genes in model legumes. Plant Physiol. 137, 1420–1434.
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ACCEPTED MANUSCRIPT FT/TFL1: Functional Evolution and Mechanisms Hecht, V., Laurie, R.E., Schoor, J.K. Vander, Ridge, S., Knowles, C.L., Liew, L.C., Sussmilch, F.C., Murfet, I.C., Macknight, R.C. and Weller, J.L. (2011). The pea GIGAS gene is a FLOWERING LOCUS T homolog necessary for graft-transmissible specification of flowering but not for responsiveness to photoperiod. Plant Cell. 23, 147–161.
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Hedman, H., Källman, T. and Lagercrantz, U. (2009). Early evolution of the MFT-like gene family in plants. Plant Mol. Biol. 70, 359–369. Higuchi, Y., Narumi, T., Oda, A., Nakano, Y., Sumitomo, K., Fukai, S. and Hisamatsu, T. (2013). The gated induction system of a systemic floral inhibitor, antiflorigen, determines obligate short-day flowering in chrysanthemums. Proc. Natl. Acad. Sci. 110, 17137–17142.
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Hiraoka, K., Yamaguchi, A., Abe, M. and Araki, T. (2013). The florigen genes FT and TSF modulate lateral shoot outgrowth in Arabidopsis thaliana. Plant Cell Physiol. 54, 352–368.
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Ho, W.W.H. and Weigel, D. (2014). Structural features determining flower-promoting activity of Arabidopsis FLOWERING LOCUS T. Plant Cell. 26, 552–564. Hou, C.J. and Yang, C.H. (2009). Functional analysis of FT and TFL1 orthologs from orchid (Oncidium Gower Ramsey) that regulate the vegetative to reproductive transition. Plant Cell Physiol. 50, 1544–1557.
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Hsu, C.Y., Adams, J.P., Kim, H., No, K., Ma, C., Strauss, S.H., Drnevich, J., Vandervelde, L., Ellis, J.D., Rice, B.M., et al. (2011). FLOWERING LOCUS T duplication coordinates reproductive and vegetative growth in perennial poplar. Proc. Natl. Acad. Sci. 108, 10756– 10761.
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Huang, N., Jane, W., Chen, J. and Yu, T. (2012a). Arabidopsis thaliana CENTRORADIALIS homologue (ATC) acts systemically to inhibit floral initiation in Arabidopsis. Plant J. 72, 175–184.
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Huang, W., Fang, Z., Zeng, S., Zhang, J., Wu, K., Chen, Z., Teixeira da Silva, J. and Duan, J. (2012b). Molecular cloning and functional analysis of three FLOWERING LOCUS T (FT) homologous genes from Chinese Cymbidium. Int. J. Mol. Sci. 13, 11385–11398. Igasaki, T., Watanabe, Y., Nishiguchi, M. and Kotoda, N. (2008). The FLOWERING LOCUS T/TERMINAL FLOWER 1 family in Lombardy poplar. Plant Cell Physiol. 49, 291–300. Ikegami, H., Nogata, H., Inoue, Y., Himeno, S., Yakushiji, H. and Hirata, C. (2013). Expression of FcFT1, a FLOWERING LOCUS T-like gene, is regulated by light and associated with inflorescence differentiation in fig (Ficus carica L.). BMC Plant Biol. 13, doi: 10.1186/1471–2229–13–216. Imamura, T., Nakatsuka, T., Higuchi, A., Nishihara, M. and Takahashi, H. (2011). The gentian orthologs of the FT/TFL1 gene family control floral initiation in Gentiana. Plant Cell Physiol. 52, 1031–1041.
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ACCEPTED MANUSCRIPT FT/TFL1: Functional Evolution and Mechanisms Iwata, H., Gaston, A., Remay, A., Thouroude, T., Jeauffre, J., Kawamura, K., Oyant, L.H. S., Araki, T., Denoyes, B. and Foucher, F. (2012). The TFL1 homologue KSN is a regulator of continuous flowering in rose and strawberry. Plant J. 69, 116–125.
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Izawa, T., Oikawa, T., Sugiyama, N., Tanisaka, T., Yano, M. and Shimamoto, K. (2002). Phytochrome mediates the external light signal to repress FT orthologs in photoperiodic flowering of rice. Genes Dev. 16, 2006–2020. Jang, S., Torti, S. and Coupland, G. (2009). Genetic and spatial interactions between FT, TSF and SVP during the early stages of floral induction in Arabidopsis. Plant J. 60, 614–625.
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Jensen, C.S., Salchert, K. and Nielsen, K.K. (2001). A TERMINAL FLOWER1-like gene from perennial ryegrass involved in floral transition and axillary meristem identity. Plant Physiol. 125, 1517–1528.
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Jiang, K., Liberatore, K.L., Park, S.J., Alvarez, J.P. and Lippman, Z.B. (2013). Tomato yield heterosis is triggered by a dosage sensitivity of the florigen pathway that fine-tunes shoot architecture. PLoS Genet. 9, e1004043. Kardailsky, I., Shukla, V.K., Ahn, J.H., Dagenais, N., Christensen, S.K., Nguyen, J.T., Chory, J., Harrison, M.J. and Weigel, D. (1999). Activation tagging of the floral inducer FT. Science. 286, 1962–1965.
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Karlgren, A., Gyllenstrand, N., Källman, T., Sundström, J.F., Moore, D., Lascoux, M. and Lagercrantz, U. (2011). Evolution of the PEBP gene family in plants: functional diversification in seed plant evolution. Plant Physiol. 156, 1967–1677.
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Karlgren, A., Gyllenstrand, N., Clapham, D. and Lagercrantz, U. (2013). FLOWERING LOCUS T/TERMINAL FLOWER1-like genes affect growth rhythm and bud set in Norway spruce. Plant Physiol. 163, 792–803.
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Kikuchi, R., Kawahigashi, H., Ando, T., Tonooka, T. and Handa, H. (2009). Molecular and functional characterization of PEBP genes in barley reveal the diversification of their roles in flowering. Plant Physiol. 149, 1341–1353. Kinoshita, T., Ono, N., Hayashi, Y., Morimoto, S., Nakamura, S., Soda, M., Kato, Y., Ohnishi, M., Nakano, T., Inoue, S. and Shimazaki, K. (2011). FLOWERING LOCUS T regulates stomatal opening. Curr. Biol. 21, 1232–1238. Klintenäs, M., Pin, P.A., Benlloch, R., Ingvarsson, P.K. and Nilsson, O. (2012). Analysis of conifer FLOWERING LOCUS T/TERMINAL FLOWER1-like genes provides evidence for dramatic biochemical evolution in the angiosperm FT lineage. New Phytol. 196, 1260– 1273.
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ACCEPTED MANUSCRIPT FT/TFL1: Functional Evolution and Mechanisms Kobayashi, Y., Kaya, H., Goto, K., Iwabuchi, M. and Araki, T. (1999). A pair of related genes with antagonistic roles in mediating flowering signals. Science. 286, 1960–1962.
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Kojima, S., Takahashi, Y., Kobayashi, Y., Monna, L., Sasaki, T., Araki, T. and Yano, M. (2002). Hd3a, a rice ortholog of the Arabidopsis FT gene, promotes transition to flowering downstream of Hd1 under short-day conditions. Plant Cell Physiol. 43, 1096–1105. Komiya, R., Ikegami, A., Tamaki, S., Yokoi, S. and Shimamoto, K. (2008). Hd3a and RFT1 are essential for flowering in rice. Development. 135, 767–774.
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Komiya, R., Yokoi, S. and Shimamoto, K. (2009). A gene network for long-day flowering activates RFT1 encoding a mobile flowering signal in rice. Development. 136, 3443–3450.
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Kong, F., Liu, B., Xia, Z., Sato, S., Kim, B.M., Watanabe, S., Yamada, T., Tabata, S., Kanazawa, A., Harada, K. and Abe, J. (2010). Two coordinately regulated homologs of FLOWERING LOCUS T are involved in the control of photoperiodic flowering in soybean. Plant Physiol. 154, 1220–1231. Koskela, E.A., Mouhu, K., Albani, M.C., Kurokura, T., Rantanen, M., Sargent, D.J., Battey, N.H., Coupland, G., Elomaa, P. and Hytönen, T. (2012). Mutation in TERMINAL FLOWER1 reverses the photoperiodic requirement for flowering in the wild strawberry Fragaria vesca. Plant Physiol. 159, 1043–1054.
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Kotake, T., Takada, S., Nakahigashi, K., Ohto, M. and Goto, K. (2003). ArabidopsisTERMINAL FLOWER 2 gene encodes a heterochromatin protein 1 homolog and represses both FLOWERING LOCUS T to regulate flowering time and several floral homeotic genes. Plant Cell Physiol. 44, 555–564.
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Kotoda, N. and Wada, M. (2005). MdTFL1, a TFL1-like gene of apple, retards the transition from the vegetative to reproductive phase in transgenic Arabidopsis. Plant Sci. 168, 95–104.
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Kotoda, N., Hayashi, H., Suzuki, M., Igarashi, M., Hatsuyama, Y., Kidou, S.I., Igasaki, T., Nishiguchi, M., Yano, K., Shimizu, T., Takahashi, S., Iwanami, H., Moriya, S. and Abe, K. (2010). Molecular characterization of FLOWERING LOCUS T-like genes of apple (Malus x domestica Borkh.). Plant Cell Physiol. 51, 561–575. Kumar, S.V., Lucyshyn, D., Jaeger, K.E., Alós, E., Alvey, E., Harberd, N.P. and Wigge, P.A. (2012). Transcription factor PIF4 controls the thermosensory activation of flowering. Nature. 484, 242–245. Kwak, M., Velasco, D. and Gepts, P. (2008). Mapping homologous sequences for determinacy and photoperiod sensitivity in common bean (Phaseolus vulgaris). J. Hered. 99, 283–291. Kwak, M., Toro, O., Debouck, D.G. and Gepts, P. (2012). Multiple origins of the determinate growth habit in domesticated common bean (Phaseolus vulgaris). Ann. Bot. 110, 1573– 1580.
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ACCEPTED MANUSCRIPT FT/TFL1: Functional Evolution and Mechanisms Laurie, R.E., Diwadkar, P., Jaudal, M., Zhang, L., Hecht, V., Wen, J., Tadege, M., Mysore, K.S., Putterill, J., Weller, J.L. and Macknight, R.C. (2011). The Medicago FLOWERING LOCUS T homolog, MtFTa1, is a key regulator of flowering time. Plant Physiol. 156, 2207–2224.
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Lazakis, C.M., Coneva, V. and Colasanti, J. (2011). ZCN8 encodes a potential orthologue of Arabidopsis FT florigen that integrates both endogenous and photoperiod flowering signals in maize. J. Exp. Bot. 62, 4833–4842. Lee, J.H., Yoo, S.J., Park, S.H., Hwang, I., Lee, J.S. and Ahn, J.H. (2007). Role of SVP in the control of flowering time by ambient temperature in Arabidopsis. Genes Dev. 21, 397–402.
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Lee, R., Baldwin, S., Kenel, F., McCallum, J. and Macknight, R. (2013). FLOWERING LOCUS T genes control onion bulb formation and flowering. Nat. Commun. 4, doi: 10.1038/ncomms3884.
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Li, C. and Dubcovsky, J. (2008). Wheat FT protein regulates VRN1 transcription through interactions with FDL2. Plant J. 55, 543–554. Li, X.F., Jia, L.Y., Xu, J., Deng, X.J., Wang, Y., Zhang, W., Zhang, X.P., Fang, Q., Zhang, D.M., Sun, Y. and Xu, L. (2013). FT-like NFT1 gene may play a role in flower transition induced by heat accumulation in Narcissus tazetta var.chinensis. Plant Cell Physiol. 54, 270–281.
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Li, C., Luo, L., Fu, Q., Niu, L. and Xu, Z. (2014a). Isolation and functional characterization of JcFT, a FLOWERING LOCUS T (FT) homologous gene from the biofuel plant Jatropha curcas. BMC Plant Biol. 14, doi: 10.1186/1471–2229–14–125.
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Li, D.M., Lu, F.B., Zhu, G.F., Sun, Y.B., Liu, H.L., Liu, J.W. and Wang, Z. (2014b). Molecular characterization and functional analysis of a Flowering locus T homolog gene from a Phalaenopsis orchid. Genet. Mol. Res. 13, 5982–5994.
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Li, Q., Fan, C., Zhang, X., Wang, X., Wu, F., Hu, R. and Fu, Y. (2014c). Identification of a soybean MOTHER OF FT AND TFL1 homolog involved in regulation of seed germination. PLoS One. 9, e99642. Liang, H., Zhebentyayeva, T., Olukolu, B., Wilde, D., Reighard, G.L. and Abbott, A. (2010). Comparison of gene order in the chromosome region containing a TERMINALFLOWER 1 homolog in apricot and peach reveals microsynteny across angiosperms. Plant Sci. 179, 390–398. Lifschitz, E., Eviatar, T., Rozman, A., Shalit, A., Goldshmidt, A., Amsellem, Z., Alvarez, J.P. and Eshed, Y. (2006). The tomato FT ortholog triggers systemic signals that regulate growth and flowering and substitute for diverse environmental stimuli. Proc. Natl. Acad. Sci. 103, 6398–6403.
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ACCEPTED MANUSCRIPT FT/TFL1: Functional Evolution and Mechanisms Lin, M.K., Belanger, H., Lee, Y.J., Varkonyi-Gasic, E., Taoka, K.I., Miura, E., XoconostleCázares, B., Gendler, K., Jorgensen, R.A., Phinney, B., Lough, T.J. and Lucas, W.J. (2007). FLOWERING LOCUS T protein may act as the long-distance florigenic signal in the cucurbits. Plant Cell. 19, 1488–1506.
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Liu, B., Watanabe, S., Uchiyama, T., Kong, F., Kanazawa, A., Xia, Z., Nagamatsu, A., Arai, M., Yamada, T., Kitamura, K., Masuta, C., Harada, K. and Abe, J. (2010). The soybean stem growth habit gene Dt1 is an ortholog of Arabidopsis TERMINAL FLOWER1. Plant Physiol. 153, 198–210.
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Liu, L., Liu, C., Hou, X., Xi, W., Shen, L., Tao, Z., Wang, Y. and Yu, H. (2012). FTIP1 is an essential regulator required for florigen transport. PLoS Biol. 10, e1001313.
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Lv, L., Duan, J., Xie, J., Wei, C., Liu, Y., Liu, S. and Sun, G. (2012). Isolation and characterization of a FLOWERING LOCUS T homolog from pineapple (Ananas comosus (L.) Merr). Gene. 505, 368–73. Lv, B., Nitcher, R., Han, X., Wang, S., Ni, F., Li, K., Pearce, S., Wu, J., Dubcovsky, J. and Fu, D. (2014). Characterization of FLOWERING LOCUS T1 (FT1) gene in Brachypodium and wheat. PLoS One. 9, e94171. Martínez, C., Pons, E., Prats, G. and León, J. (2004). Salicylic acid regulates flowering time and links defence responses and reproductive development. Plant J. 37, 209–217.
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Matsubara, K., Yamanouchi, U., Wang, Z.X., Minobe, Y., Izawa, T. and Yano, M. (2008). Ehd2, a rice ortholog of the maize INDETERMINATE1 gene, promotes flowering by upregulating Ehd1. Plant Physiol. 148, 1425–1435.
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Matsuda, N., Ikeda, K., Kurosaka, M., Takashina, T., Isuzugawa, K., Endo, T. and Omura, M. (2009). Early flowering phenotype in transgenic pears (Pyrus communis L.) expressing the CiFT gene. J. Japanese Soc. Hortic. Sci. 78, 410–416.
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Meng, X., Muszynski, M.G. and Danilevskaya, O.N. (2011). The FT-like ZCN8 gene functions as a floral activator and is involved in photoperiod sensitivity in maize. Plant Cell. 23, 942–960. Michaels, S.D. and Amasino, R.M. (1999). FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell. 11, 949–956. Mimida, N., Kotoda, N., Ueda, T., Igarashi, M., Hatsuyama, Y., Iwanami, H., Moriya, S. and Abe, K. (2009). Four TFL1/CEN-like genes on distinct linkage groups show different expression patterns to regulate vegetative and reproductive development in apple (Malus x domestica Borkh.). Plant Cell Physiol. 50, 394–412.
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ACCEPTED MANUSCRIPT FT/TFL1: Functional Evolution and Mechanisms Mohamed, R., Wang, C.T., Ma, C., Shevchenko, O., Dye, S.J., Puzey, J.R., Etherington, E., Sheng, X., Meilan, R., Strauss, S.H. and Brunner, A.M. (2010). Populus CEN/TFL1 regulates first onset of flowering, axillary meristem identity and dormancy release in Populus. Plant J. 62, 674–688.
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Muszynski, M.G., Dam, T., Li, B., Shirbroun, D.M., Hou, Z., Bruggemann, E., Archibald, R., Ananiev, E. V and Danilevskaya, O.N. (2006). delayed flowering1 encodes a basic leucine zipper protein that mediates floral inductive signals at the shoot apex in maize. Plant Physiol. 142, 1523–1536.
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Mutasa-Göttgens, E. and Hedden, P. (2009). Gibberellin as a factor in floral regulatory networks. J. Exp. Bot. 60, 1979–1989.
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Nakagawa, M., Shimamoto, K. and Kyozuka, J. (2002). Overexpression of RCN1 and RCN2, rice TERMINAL FLOWER 1/CENTRORADIALIS homologs, confers delay of phase transition and altered panicle morphology in rice. Plant J. 29, 743–750. Nakamura, S., Abe, F., Kawahigashi, H., Nakazono, K., Tagiri, A., Matsumoto, T., Utsugi, S., Ogawa, T., Handa, H., Ishida, H., Mori, M., Kawaura, K., Ogihara, Y. and Miura, H. (2011). A wheat homolog of MOTHER OF FT AND TFL1 acts in the regulation of germination. Plant Cell. 23, 3215–3229.
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Nakamura, Y., Andrés, F., Kanehara, K., Liu, Y., Dörmann, P. and Coupland, G. (2014). Arabidopsis florigen FT binds to diurnally oscillating phospholipids that accelerate flowering. Nat. Commun. 5, doi: 10.1038/ncomms4553. Nakano, Y., Higuchi, Y., Sumitomo, K. and Hisamatsu, T. (2013). Flowering retardation by high temperature in chrysanthemums: involvement of FLOWERING LOCUS T-like 3 gene repression. J. Exp. Bot. 64, 909–920.
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Nan, H., Cao, D., Zhang, D., Li, Y., Lu, S., Tang, L., Yuan, X., Liu, B. and Kong, F. (2014). GmFT2a and GmFT5a redundantly and differentially regulate flowering through interaction with and upregulation of the bZIP transcription factor GmFDL19 in soybean. PLoS One. 9, e97669. Navarro, C., Abelenda, J.A., Cruz-Oró, E., Cuéllar, C.A., Tamaki, S., Silva, J., Shimamoto, K. and Prat, S. (2011). Control of flowering and storage organ formation in potato by FLOWERING LOCUS T. Nature. 478, 119–122. Nishikawa, F., Endo, T., Shimada, T., Fujii, H., Shimizu, T., Omura, M. and Ikoma, Y. (2007). Increased CiFT abundance in the stem correlates with floral induction by low temperature in Satsuma mandarin (Citrus unshiu Marc.). J. Exp. Bot. 58, 3915–3927.
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ACCEPTED MANUSCRIPT FT/TFL1: Functional Evolution and Mechanisms Niwa, M., Daimon, Y., Kurotani, K., Higo, A., Pruneda-Paz, J.L., Breton, G., Mitsuda, N., Kay, S.A., Ohme-Takagi, M., Endo, M. and Araki, T. (2013). BRANCHED1 interacts with FLOWERING LOCUS T to repress the floral transition of the axillary meristems in Arabidopsis. Plant Cell. 25, 1228–1242.
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Noy-Porat, T., Cohen, D., Mathew, D., Eshel, A., Kamenetsky, R. and Flaishman, M.A. (2013). Turned on by heat: differential expression of FT and LFY-like genes in Narcissus tazetta during floral transition. J. Exp. Bot. 64, 3273–3284.
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Oda, A., Narumi, T., Li, T., Kando, T., Higuchi, Y., Sumitomo, K., Fukai, S. and Hisamatsu, T. (2012). CsFTL3, a chrysanthemum FLOWERING LOCUS T-like gene, is a key regulator of photoperiodic flowering in chrysanthemums. J. Exp. Bot. 63, 1461–1477.
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Ono, N., Ishida, K., Yamashino, T., Nakanishi, H., Sato, S., Tabata, S. and Mizuno, T. (2010). Genomewide characterization of the light-responsive and clock-controlled output pathways in Lotus japonicus with special emphasis of its uniqueness. Plant Cell Physiol. 51, 1800–1814. Park, S.J., Kim, S.L., Lee, S., Je, B. Il, Piao, H.L., Park, S.H., Kim, C.M., Ryu, C.H., Park, S.H., Xuan, Y., Colasanti, J., An, G. and Han, C. (2008). Rice Indeterminate 1 (OsId1) is necessary for the expression of Ehd1 (Early heading date 1) regardless of photoperiod. Plant J. 56, 1018–1029.
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Pillitteri, L.J., Lovatt, C.J. and Walling, L.L. (2004). Isolation and characterization of a TERMINAL FLOWER homolog and its correlation with juvenility in citrus. Plant Physiol. 135, 1540–1551.
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Pin, P.A., Benlloch, R., Bonnet, D., Wremerth-Weich, E., Kraft, T., Gielen, J.J.L. and Nilsson, O. (2010). An antagonistic pair of FT homologs mediates the control of flowering time in sugar beet. Science. 330, 1397–1400.
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Pin, P.A., Zhang, W., Vogt, S.H., Dally, N., Büttner, B., Schulze-Buxloh, G., Jelly, N.S., Chia, T.Y.P., Mutasa-Göttgens, E.S., Dohm, J.C., et al. (2012). The role of a pseudoresponse regulator gene in life cycle adaptation and domestication of beet. Curr. Biol. 22, 1095–1101. Pnueli, L., Carmel-Goren, L., Hareven, D., Gutfinger, T., Alvarez, J., Ganal, M., Zamir, D. and Lifschitz, E. (1998). The SELF-PRUNING gene of tomato regulates vegetative to reproductive switching of sympodial meristems and is the ortholog of CEN and TFL1. Development. 125, 1979–1989. Pnueli, L., Gutfinger, T., Hareven, D., Ben-Naim, O., Ron, N., Adir, N. and Lifschitz, E. (2001). Tomato SP-interacting proteins define a conserved signaling system that regulates shoot architecture and flowering. Plant Cell. 13, 2687–2702.
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ACCEPTED MANUSCRIPT FT/TFL1: Functional Evolution and Mechanisms Putterill, J., Robson, F., Lee, K., Simon, R. and Coupland, G. (1995). The CONSTANS gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors. Cell. 80, 847–857.
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