ARTICLE ADDENDUM Plant Signaling & Behavior 10:9, e1062195; September 2015; © 2015 Taylor & Francis Group, LLC
Involvement of cotton gene GhFPF1 in the regulation of shade avoidance responses in Arabidopsis thaliana Xiaoyan Wang1,2, Chaoyou Pang1, Hengling Wei1, and Shuxun Yu1,* 1
State Key Laboratory of Cotton Biology; Institute of Cotton Research of CAAS; Anyang, Henan, China; 2Anyang Institute of Technology; College of Biology
and Food Engineering; Anyang, Henan, China
P
hytochrome system perceives the reduction in the ratio of red to farred light when plants are grown under dense canopy. This signal, regarded as a warning of competition, will trigger a series of phenotypic changes to avoid shade. Progress has been made for several phytochrome signaling intermediates acting as positive regulators of accelerated elongation growth and promotion of flowering in shade-avoidance has been identified. Recently, a FPF1 homolog GhFPF1 was identified in upland cotton. Our data supported that transgenic Arabidopsis of over-expressing GhFPF1 displayed a constitutive shade-avoiding phenotype resembling phyB mutants in several respects such as accelerated elongation of hypocotyl and petioles, upward of leaf movement, and promoted flowering. In this addendum, by dissection of GhFPF1 acting as a component of shadeavoidance responses we suppose that GhFPF1 might influence the timing of the floral transition independently of shade-mediated early flowering. Furthermore, the opposite changes of IAA content in transgenic leaves and stems suggested that alteration of IAA storage and release took place during shadeavoidance responses. Keywords: Arabidopsis, auxin, cotton, FLOWERING PROMOTING FACTOR 1 (FPF1), flowering time, Phytochrome B, shade-avoidance syndrome (SAS) *Correspondence to: Shuxun Yu; Email: yu@cricaas. com.cn Submitted: 06/01/2015 Accepted: 06/10/2015 http://dx.doi.org/10.1080/15592324.2015.1062195 www.tandfonline.com
In response to competion for light, angiosperms own well capacity to avoid shade. Select absorption of red light (R) by photosynthetic pigments reduced the ratio of red light (R) to far-red light (FR) within a dense vegetation community. Perception of such light signals by phytochrome will trigger rapid changes of gene expression and a suit of physiological processes termed as shade-avoidance Plant Signaling & Behavior
syndrome (SAS). Several developmental adjustments will take place during SAS, including accelerated elongation growth of internode, petioles and hypocotyl, increased apical dominance, promoted flowering and upward of leaf movement.1 Among the 5 kinds of phytochrome (phyA-phyE) identified in Arabidopsis thaliana, phyB plays a key role in shade avoidance. Even under high R/FR light, phyB mutants of Arabidopsis constitutively display typical phenotypic traits of SAS.2 phyD and phyE also contribute to shade-avoidance responses.3,4 Much progress has been made in understanding the molecular basis of shade avoidance over the past 2 decades. Under high R/FR, a subfamily of basic helixloop-helix (bHLH) proteins PHYTOCHROME-INTERACTING FACTOR3 (PIF3), PIF4, PIF5 and PIF7 have been uncovered to interact physically with active form of phyB, causing PIF proteins phosphorylated and degraded via the ubiquitinproteasome system. When exposed to low R/FR, PIF proteins accumulate because of reduced active phyB.5,6 Shade-induced elongation growth is significantly attenuated in pif4, pif5 and pif7 mutants, demonstrating the positive regulation of PIFs in SAS.5,6 In response to different light cues, dynamic destiny of PIFs suggested that a protein phosphatase and a protein kinase whose activities or availability are dependent on variations of light quality could participate in this.7 Coincidentally, a leucine-rich repeat (LRR) receptor-like kinase gene ERECTA, identified by QTL analysis of a Ler £ Cvi recombinant inbred line (RIL) population has been confirmed to regulate leaf hyponasty, petiole elongation during shade avoidance.8-11 e1062195-1
Our study revealed that GhFPF1 involved in floral promotion previously could trigger shade-avoidance syndrome (SAS) in Arabidopsis.12 The reports that genes related to flowering regulation were found to be involved in SAS was not unusual. EARLY FLOWERING 3 (ELF3) gene, modulating the circadian rhythm and flowering time generally has been confirmed to act as a component of a PHYB signaling complex in early morphogenesis but both genes control floral transition via independent signal transduction pathways.13,14 Our study demonstrated that GhFPF1 over-expression lines generated elongated appearance, rapid flowering and suppressed PHYB expression compared with wild-type.12 Microarrays and genetic screens helped to figure out that florigen gene FLOWERING LOCUS T (FT) was up-regulated during far-red exposure.15,16 At the same time, evidences showed that a low R:FR ratio would bypass the floral repressor FLOWERING LOCUS C (FLC)-mediated late flowering rather than inactivate its expression to accelerate flowering.17 Significantly suppressed FLC expression was found in the transgenic Arabidopsis,12 indicating that GhFPF1 might influence the timing of floral transition independently of shademediated early flowering.
As documented earlier, phytochrome B will migrate to the nucleus after activation by R light, where it can interact with PIFs.5,6 Data shown that PIFs can also interact with DELLA proteins whose stability is mainly regulated by gibberellin (GA).18 Regarding SAS, plant hormones auxin, gibberellin and ethylene play important roles in this.19,20 In young Arabidopsis seedlings, low R:FR increased the abundance of 3-indoleacetic acid (IAA),21 but this was not the case in the petiole and lamina of Arabidopsis leaves22 or in the leaves of tomato.23 In response to low R:FR ratio signals, many plants display a rapid and pronounced increase in the elongation growth rate of stems and petioles, often at the cost of leaf and storage organ development. Thus content of free IAA in cauline leaves and infancy stems was measured using Liquid chromatography–electrospray tandem mass spectrometry (LC– ESI–MS/MS) method. Compared with wild-type, transgenic leaves contain only an half of free IAA but it is just opposite for the stems (Fig. 1). That is in agreement with the notion that faster growth of stems induced by shade requires intact auxin signaling and involves accumulation of free IAA in stems but adjustments in auxin distribution may be also implicated in the inhibition of leaf expansion by shade.
Figure 1. Free IAA content was changed in transgenic leaves and stems compared with wild-type Arabidopsis. Transgenic Arabidopsis (Line 3, Line 4) and wild-type (WT) plants were grown under long-day conditions with high red to far red light (R/FR ratio: 4.5) provided by fluorescent lamps. Before flowering, the infancy stems and cauline leaves were taken for determination of auxin by liquid chromatography–electrospray tandem mass spectrometry (LC–ESI–MS/MS) method. Data are means §SE of 3 replicates, and significant effects of IAA in transgenic leaves and stems compared with wild-type are indicated (One-Way ANOVA, *** P < 0.001).
e1062195-2
Plant Signaling & Behavior
Disclosure of Potential Conflicts of Interest
No potential conflicts of interest were disclosed. Funding
The work described in this addendum was supported by the National High-tech Research and Development Projects of China (2013AA102601) and funded by the Major Projects of Anyang City Science and Technology Plan (ANKE20140208). References 1. Franklin KA. Shade avoidance. New Phytol 2008; 179:930-44; PMID:18537892; http://dx.doi.org/ 10.1111/j.1469-8137.2008.02507.x 2. Reed JW, Nagpal P, Poole DS, Furuya M, Chory J. Mutations in the gene for the red/far-red light receptor phytochrome B alter cell elongation and physiological responses throughout Arabidopsis development. Plant Cell 1993; 5:147-157; PMID:8453299; http://dx.doi. org/10.1105/tpc.5.2.147 3. Devlin PF, Patel SR, Whitelam GC. Phytochrome E influences internode elongation and flowering time in Arabidopsis. Plant Cell 1998; 10:1479-1487; PMID:9724694; http://dx.doi.org/10.1105/ tpc.10.9.1479 4. Devlin PF, Robson PRH, Patel SR, Goosey L, Sharrock RA, Whitelam GC. Phytochrome D acts in the shadeavoidance syndrome in Arabidopsis by controlling elongation growth and flowering time. PlantPhysiol 1999; 119:909-915. 5. Lorrain S, Allen T, Duek PD, Whitelam GC, Fankhauser C. Phytochrome-mediated inhibition of shade avoidance involves degradation of growth-promoting bHLH transcription factors. Plant J 2008; 53:312-323; PMID:18047474; http://dx.doi.org/10.1111/j.1365313X.2007.03341.x 6. Leivar P, Tepperman JM, Cohn MM, Monte E, AlSady B, Erickson E, Quail PH. Dynamic antagonism between phytochromes and PIF family basic helix-loophelix factors induces selective reciprocal responses to light and shade in a rapidly responsive transcriptional net-work in Arabidopsis. Plant Cell 2012; 24:13981419; PMID:22517317; http://dx.doi.org/10.1105/ tpc.112.095711 7. Li L, Ljung K, Breton G, Schmitz RJ, Pruneda-Paz J, Cowing-Zitron C, Cole BJ, Ivans LJ, Pedmale UV, Jung H-S, Ecker JR, Kay SA, Chory J. Linking photoreceptor excitation to changes in plant architecture. Genes Dev 2012; 26:785-790; PMID:22508725; http://dx. doi.org/10.1101/gad.187849.112 8. Swarup K, Alonso-Blanco C, Lynn JR, Michaels SD, Amasino RM, Koornneef M, Millar AJ. Natural allelic variation identifies new genes in the Arabidopsis circadian system. Plant J 1999; 20:67-77; PMID:10571866; http://dx.doi.org/10.1046/j.1365-313X.1999.00577.x 9. van Zanten M, Snoek LB, Van Eck-Stouten E, Proveniers MCG, Torii KU, Voesenek LACJ, Peeters AJM, Millenaar FF. Ethylene-induced hyponastic growth in Arabidopsis thaliana is controlled by ERECTA. Plant J 2010; 61:83-95; PMID:19796369; http://dx.doi.org/ 10.1111/j.1365-313X.2009.04035.x 10. van Zanten M, Snoek LB, Van Eck-Stouten E, Proveniers MCG, Torii KU, Voesenek LACJ, Millenaar FF, Peeters AJM. ERECTA controls low light intensityinduced differential petiole growth independent of Phytochrome B and Crytochrome 2 action in Arabidopsis thaliana. Plant Signal Behav 2010; 5:284-286; PMID:20037477; http://dx.doi.org/10.4161/ psb.5.3.10706
Volume 10 Issue 9
11. Patel D, Basu M, Hayes S, Majlath I, Hetherington FM, Tschaplinski TJ. and Franklin KA. Temperaturedependent shade avoidance involves the receptor-like kinase ERECTA. Plant J 2013; 73:980-992; PMID:23199031; http://dx.doi.org/10.1111/tpj.12088 12. Wang X, Fan S, Song M, Pang C, Wei H, Yu J, Ma Q, Yu S. Upland Cotton Gene GhFPF1 Confers Promotion of Flowering Time and Shade-Avoidance Responses in Arabidopsis thaliana. PloS One 2014; 9: e91869; PMID:24626476; http://dx.doi.org/10.1371/ journal.pone.0091869 13. Liu XL, Covington MF, Frankhauser C, Chory J, Wagner DR. ELF3 encodes a circadian clock-regulated nuclear protein that functions in Arabidopsis PHYB signal transduction pathway. Plant Cell 2001; 13:12931304; PMID:11402161; http://dx.doi.org/10.1105/ tpc.13.6.1293 14. Coluccio MP, Sanchez SE, Kasulin L, Yanovsky MJ, Botto JF. Genetic mapping of natural variation in a shade avoidance response: ELF3 is the candidate gene for a QTL in hypocotyl growth regulation. J Exp Botany 2011; 62:167-176; PMID:20713464; http://dx. doi.org/10.1093/jxb/erq253 15. Devlin PF, Yanovsky MJ, Kay SA. A genomic analysis of the shade avoidance response in Arabidopsis. Plant
www.tandfonline.com
16.
17.
18.
19.
Physiol 2003; 133:1617-1629; PMID:14645734; http://dx.doi.org/10.1104/pp.103.034397 Endo M, Nakamura S, Araki T, Mochizuki N, Nagatani A. Phytochrome B in the mesophyll delays flowering by suppressing FLOWERING LOCUS T expression in Arabidopsis vascular bundles. Plant Cell 2005; 17:1941-1952; PMID:15965119; http://dx.doi. org/10.1105/tpc.105.032342 Wollenberg A C, Strasser B, Cerdan P D, Amasino RM. Acceleration of flowering during shade avoidance in Arabidopsis alters the balance between FLOWERING LOCUS C-mediated repression and photoperiodic induction of flowering. Plant Physiol 2008; 148:1681-1694; PMID:18790998; http://dx.doi.org/ 10.1104/pp.108.125468 de Lucas M, Daviere JM, Rodriguez-Falcon M, Pontin M, Iglesias-Pedraz JM, Lorrain S, Fankhauser C, Blazquez MA, Titarenko E, Prat S. Molecular framework for light and gibberellin control of cell elongation. Nature 2008; 451:480-6; PMID:18216857; http://dx. doi.org/10.1038/nature06520 Morelli G, Ruberti I. Shade avoidance responses. Driving auxin along lateral routes. Plant Physiol 2000; 122:621-6; PMID:10712524; http://dx.doi.org/ 10.1104/pp.122.3.621
Plant Signaling & Behavior
20. Pierik R, Cuppens MLC, Voesenek LACJ, Visser EJW. Interactions between ethylene and gibberellins in phytochrome-mediated shade avoidance responses in tobacco. Plant Physiol 2004; 136:2928-2936; PMID:15448197; http://dx.doi.org/10.1104/ pp.104.045120 21. Tao Y, Ferrer JL, Ljung K, Pojer F, Hong FX, Long JA, Li L, Moreno JE, Bowman ME, Ivans LJ, et al. Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants. Cell 2008; 133:164-176; PMID:18394996; http://dx.doi. org/10.1016/j.cell.2008.01.049 22. Kozuka T, Kobayashi J, Horiguchi G, Demura T, Sakakibara H, Tsukaya H, Nagatani A. Involvement of auxin and brassinosteroid in the regulation of petiole elongation under the shade. Plant Physiol 2010; 153:1608-1618; PMID:20538889; http://dx.doi.org/ 10.1104/pp.110.156802 23. Cagnola JI, Ploschuk E, Benech-Arnold T, Finlayson SA, Casal JJ. Stem transcriptome reveals mechanisms to reduce the energetic cost of shade-avoidance responses in tomato. Plant Physiol 2012; 160:1110-1119; PMID:22872775; http://dx.doi.org/10.1104/ pp.112.201921
e1062195-3
Involvement of cotton gene GhFPF1 in the regulation of shade avoidance responses in Arabidopsis thaliana Xiaoyan Wang1,2, Chaoyou Pang1, Hengling Wei1, and Shuxun Yu1,* 1
State Key Laboratory of Cotton Biology; Institute of Cotton Research of CAAS; Anyang, Henan, China; 2Anyang Institute of Technology; College of Biology
and Food Engineering; Anyang, Henan, China
P
hytochrome system perceives the reduction in the ratio of red to farred light when plants are grown under dense canopy. This signal, regarded as a warning of competition, will trigger a series of phenotypic changes to avoid shade. Progress has been made for several phytochrome signaling intermediates acting as positive regulators of accelerated elongation growth and promotion of flowering in shade-avoidance has been identified. Recently, a FPF1 homolog GhFPF1 was identified in upland cotton. Our data supported that transgenic Arabidopsis of over-expressing GhFPF1 displayed a constitutive shade-avoiding phenotype resembling phyB mutants in several respects such as accelerated elongation of hypocotyl and petioles, upward of leaf movement, and promoted flowering. In this addendum, by dissection of GhFPF1 acting as a component of shadeavoidance responses we suppose that GhFPF1 might influence the timing of the floral transition independently of shade-mediated early flowering. Furthermore, the opposite changes of IAA content in transgenic leaves and stems suggested that alteration of IAA storage and release took place during shadeavoidance responses. Keywords: Arabidopsis, auxin, cotton, FLOWERING PROMOTING FACTOR 1 (FPF1), flowering time, Phytochrome B, shade-avoidance syndrome (SAS) *Correspondence to: Shuxun Yu; Email: yu@cricaas. com.cn Submitted: 06/01/2015 Accepted: 06/10/2015 http://dx.doi.org/10.1080/15592324.2015.1062195 www.tandfonline.com
In response to competion for light, angiosperms own well capacity to avoid shade. Select absorption of red light (R) by photosynthetic pigments reduced the ratio of red light (R) to far-red light (FR) within a dense vegetation community. Perception of such light signals by phytochrome will trigger rapid changes of gene expression and a suit of physiological processes termed as shade-avoidance Plant Signaling & Behavior
syndrome (SAS). Several developmental adjustments will take place during SAS, including accelerated elongation growth of internode, petioles and hypocotyl, increased apical dominance, promoted flowering and upward of leaf movement.1 Among the 5 kinds of phytochrome (phyA-phyE) identified in Arabidopsis thaliana, phyB plays a key role in shade avoidance. Even under high R/FR light, phyB mutants of Arabidopsis constitutively display typical phenotypic traits of SAS.2 phyD and phyE also contribute to shade-avoidance responses.3,4 Much progress has been made in understanding the molecular basis of shade avoidance over the past 2 decades. Under high R/FR, a subfamily of basic helixloop-helix (bHLH) proteins PHYTOCHROME-INTERACTING FACTOR3 (PIF3), PIF4, PIF5 and PIF7 have been uncovered to interact physically with active form of phyB, causing PIF proteins phosphorylated and degraded via the ubiquitinproteasome system. When exposed to low R/FR, PIF proteins accumulate because of reduced active phyB.5,6 Shade-induced elongation growth is significantly attenuated in pif4, pif5 and pif7 mutants, demonstrating the positive regulation of PIFs in SAS.5,6 In response to different light cues, dynamic destiny of PIFs suggested that a protein phosphatase and a protein kinase whose activities or availability are dependent on variations of light quality could participate in this.7 Coincidentally, a leucine-rich repeat (LRR) receptor-like kinase gene ERECTA, identified by QTL analysis of a Ler £ Cvi recombinant inbred line (RIL) population has been confirmed to regulate leaf hyponasty, petiole elongation during shade avoidance.8-11 e1062195-1
Our study revealed that GhFPF1 involved in floral promotion previously could trigger shade-avoidance syndrome (SAS) in Arabidopsis.12 The reports that genes related to flowering regulation were found to be involved in SAS was not unusual. EARLY FLOWERING 3 (ELF3) gene, modulating the circadian rhythm and flowering time generally has been confirmed to act as a component of a PHYB signaling complex in early morphogenesis but both genes control floral transition via independent signal transduction pathways.13,14 Our study demonstrated that GhFPF1 over-expression lines generated elongated appearance, rapid flowering and suppressed PHYB expression compared with wild-type.12 Microarrays and genetic screens helped to figure out that florigen gene FLOWERING LOCUS T (FT) was up-regulated during far-red exposure.15,16 At the same time, evidences showed that a low R:FR ratio would bypass the floral repressor FLOWERING LOCUS C (FLC)-mediated late flowering rather than inactivate its expression to accelerate flowering.17 Significantly suppressed FLC expression was found in the transgenic Arabidopsis,12 indicating that GhFPF1 might influence the timing of floral transition independently of shademediated early flowering.
As documented earlier, phytochrome B will migrate to the nucleus after activation by R light, where it can interact with PIFs.5,6 Data shown that PIFs can also interact with DELLA proteins whose stability is mainly regulated by gibberellin (GA).18 Regarding SAS, plant hormones auxin, gibberellin and ethylene play important roles in this.19,20 In young Arabidopsis seedlings, low R:FR increased the abundance of 3-indoleacetic acid (IAA),21 but this was not the case in the petiole and lamina of Arabidopsis leaves22 or in the leaves of tomato.23 In response to low R:FR ratio signals, many plants display a rapid and pronounced increase in the elongation growth rate of stems and petioles, often at the cost of leaf and storage organ development. Thus content of free IAA in cauline leaves and infancy stems was measured using Liquid chromatography–electrospray tandem mass spectrometry (LC– ESI–MS/MS) method. Compared with wild-type, transgenic leaves contain only an half of free IAA but it is just opposite for the stems (Fig. 1). That is in agreement with the notion that faster growth of stems induced by shade requires intact auxin signaling and involves accumulation of free IAA in stems but adjustments in auxin distribution may be also implicated in the inhibition of leaf expansion by shade.
Figure 1. Free IAA content was changed in transgenic leaves and stems compared with wild-type Arabidopsis. Transgenic Arabidopsis (Line 3, Line 4) and wild-type (WT) plants were grown under long-day conditions with high red to far red light (R/FR ratio: 4.5) provided by fluorescent lamps. Before flowering, the infancy stems and cauline leaves were taken for determination of auxin by liquid chromatography–electrospray tandem mass spectrometry (LC–ESI–MS/MS) method. Data are means §SE of 3 replicates, and significant effects of IAA in transgenic leaves and stems compared with wild-type are indicated (One-Way ANOVA, *** P < 0.001).
e1062195-2
Plant Signaling & Behavior
Disclosure of Potential Conflicts of Interest
No potential conflicts of interest were disclosed. Funding
The work described in this addendum was supported by the National High-tech Research and Development Projects of China (2013AA102601) and funded by the Major Projects of Anyang City Science and Technology Plan (ANKE20140208). References 1. Franklin KA. Shade avoidance. New Phytol 2008; 179:930-44; PMID:18537892; http://dx.doi.org/ 10.1111/j.1469-8137.2008.02507.x 2. Reed JW, Nagpal P, Poole DS, Furuya M, Chory J. Mutations in the gene for the red/far-red light receptor phytochrome B alter cell elongation and physiological responses throughout Arabidopsis development. Plant Cell 1993; 5:147-157; PMID:8453299; http://dx.doi. org/10.1105/tpc.5.2.147 3. Devlin PF, Patel SR, Whitelam GC. Phytochrome E influences internode elongation and flowering time in Arabidopsis. Plant Cell 1998; 10:1479-1487; PMID:9724694; http://dx.doi.org/10.1105/ tpc.10.9.1479 4. Devlin PF, Robson PRH, Patel SR, Goosey L, Sharrock RA, Whitelam GC. Phytochrome D acts in the shadeavoidance syndrome in Arabidopsis by controlling elongation growth and flowering time. PlantPhysiol 1999; 119:909-915. 5. Lorrain S, Allen T, Duek PD, Whitelam GC, Fankhauser C. Phytochrome-mediated inhibition of shade avoidance involves degradation of growth-promoting bHLH transcription factors. Plant J 2008; 53:312-323; PMID:18047474; http://dx.doi.org/10.1111/j.1365313X.2007.03341.x 6. Leivar P, Tepperman JM, Cohn MM, Monte E, AlSady B, Erickson E, Quail PH. Dynamic antagonism between phytochromes and PIF family basic helix-loophelix factors induces selective reciprocal responses to light and shade in a rapidly responsive transcriptional net-work in Arabidopsis. Plant Cell 2012; 24:13981419; PMID:22517317; http://dx.doi.org/10.1105/ tpc.112.095711 7. Li L, Ljung K, Breton G, Schmitz RJ, Pruneda-Paz J, Cowing-Zitron C, Cole BJ, Ivans LJ, Pedmale UV, Jung H-S, Ecker JR, Kay SA, Chory J. Linking photoreceptor excitation to changes in plant architecture. Genes Dev 2012; 26:785-790; PMID:22508725; http://dx. doi.org/10.1101/gad.187849.112 8. Swarup K, Alonso-Blanco C, Lynn JR, Michaels SD, Amasino RM, Koornneef M, Millar AJ. Natural allelic variation identifies new genes in the Arabidopsis circadian system. Plant J 1999; 20:67-77; PMID:10571866; http://dx.doi.org/10.1046/j.1365-313X.1999.00577.x 9. van Zanten M, Snoek LB, Van Eck-Stouten E, Proveniers MCG, Torii KU, Voesenek LACJ, Peeters AJM, Millenaar FF. Ethylene-induced hyponastic growth in Arabidopsis thaliana is controlled by ERECTA. Plant J 2010; 61:83-95; PMID:19796369; http://dx.doi.org/ 10.1111/j.1365-313X.2009.04035.x 10. van Zanten M, Snoek LB, Van Eck-Stouten E, Proveniers MCG, Torii KU, Voesenek LACJ, Millenaar FF, Peeters AJM. ERECTA controls low light intensityinduced differential petiole growth independent of Phytochrome B and Crytochrome 2 action in Arabidopsis thaliana. Plant Signal Behav 2010; 5:284-286; PMID:20037477; http://dx.doi.org/10.4161/ psb.5.3.10706
Volume 10 Issue 9
11. Patel D, Basu M, Hayes S, Majlath I, Hetherington FM, Tschaplinski TJ. and Franklin KA. Temperaturedependent shade avoidance involves the receptor-like kinase ERECTA. Plant J 2013; 73:980-992; PMID:23199031; http://dx.doi.org/10.1111/tpj.12088 12. Wang X, Fan S, Song M, Pang C, Wei H, Yu J, Ma Q, Yu S. Upland Cotton Gene GhFPF1 Confers Promotion of Flowering Time and Shade-Avoidance Responses in Arabidopsis thaliana. PloS One 2014; 9: e91869; PMID:24626476; http://dx.doi.org/10.1371/ journal.pone.0091869 13. Liu XL, Covington MF, Frankhauser C, Chory J, Wagner DR. ELF3 encodes a circadian clock-regulated nuclear protein that functions in Arabidopsis PHYB signal transduction pathway. Plant Cell 2001; 13:12931304; PMID:11402161; http://dx.doi.org/10.1105/ tpc.13.6.1293 14. Coluccio MP, Sanchez SE, Kasulin L, Yanovsky MJ, Botto JF. Genetic mapping of natural variation in a shade avoidance response: ELF3 is the candidate gene for a QTL in hypocotyl growth regulation. J Exp Botany 2011; 62:167-176; PMID:20713464; http://dx. doi.org/10.1093/jxb/erq253 15. Devlin PF, Yanovsky MJ, Kay SA. A genomic analysis of the shade avoidance response in Arabidopsis. Plant
www.tandfonline.com
16.
17.
18.
19.
Physiol 2003; 133:1617-1629; PMID:14645734; http://dx.doi.org/10.1104/pp.103.034397 Endo M, Nakamura S, Araki T, Mochizuki N, Nagatani A. Phytochrome B in the mesophyll delays flowering by suppressing FLOWERING LOCUS T expression in Arabidopsis vascular bundles. Plant Cell 2005; 17:1941-1952; PMID:15965119; http://dx.doi. org/10.1105/tpc.105.032342 Wollenberg A C, Strasser B, Cerdan P D, Amasino RM. Acceleration of flowering during shade avoidance in Arabidopsis alters the balance between FLOWERING LOCUS C-mediated repression and photoperiodic induction of flowering. Plant Physiol 2008; 148:1681-1694; PMID:18790998; http://dx.doi.org/ 10.1104/pp.108.125468 de Lucas M, Daviere JM, Rodriguez-Falcon M, Pontin M, Iglesias-Pedraz JM, Lorrain S, Fankhauser C, Blazquez MA, Titarenko E, Prat S. Molecular framework for light and gibberellin control of cell elongation. Nature 2008; 451:480-6; PMID:18216857; http://dx. doi.org/10.1038/nature06520 Morelli G, Ruberti I. Shade avoidance responses. Driving auxin along lateral routes. Plant Physiol 2000; 122:621-6; PMID:10712524; http://dx.doi.org/ 10.1104/pp.122.3.621
Plant Signaling & Behavior
20. Pierik R, Cuppens MLC, Voesenek LACJ, Visser EJW. Interactions between ethylene and gibberellins in phytochrome-mediated shade avoidance responses in tobacco. Plant Physiol 2004; 136:2928-2936; PMID:15448197; http://dx.doi.org/10.1104/ pp.104.045120 21. Tao Y, Ferrer JL, Ljung K, Pojer F, Hong FX, Long JA, Li L, Moreno JE, Bowman ME, Ivans LJ, et al. Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants. Cell 2008; 133:164-176; PMID:18394996; http://dx.doi. org/10.1016/j.cell.2008.01.049 22. Kozuka T, Kobayashi J, Horiguchi G, Demura T, Sakakibara H, Tsukaya H, Nagatani A. Involvement of auxin and brassinosteroid in the regulation of petiole elongation under the shade. Plant Physiol 2010; 153:1608-1618; PMID:20538889; http://dx.doi.org/ 10.1104/pp.110.156802 23. Cagnola JI, Ploschuk E, Benech-Arnold T, Finlayson SA, Casal JJ. Stem transcriptome reveals mechanisms to reduce the energetic cost of shade-avoidance responses in tomato. Plant Physiol 2012; 160:1110-1119; PMID:22872775; http://dx.doi.org/10.1104/ pp.112.201921
e1062195-3
