Letters
Origin of plant auxin biosynthesis in charophyte algae Chunyang Wang1,2*, Yang Liu2*, Si-Shen Li2, and Guan-Zhu Han1,3 1
Jiangsu Key Laboratory for Microbes and Functional Genomics, Jiangsu Engineering and Technology Research Center for Microbiology, College of Life Sciences, Nanjing Normal University, Nanjing, Jiangsu 210023, China 2 State Key Laboratory of Crop Biology, Shandong Agricultural University, Tai’an, Shandong 271018, China 3 Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ 85721, USA
The TRYPTOPHAN AMINOTRANSFERASE OF ARABIDOPSIS (TAA)/YUCCA flavin monooxygenase (YUC) pathway is the main auxin biosynthesis pathway in plants [1]. The origin of plant auxin biosynthesis remains unclear and controversial. Recently Yue et al. addressed this issue by performing phylogenetic analysis of TAA and YUC proteins [2]. They found that land plant TAA proteins are most closely related to proteins from non-plant eukaryotes (such as Choanoflagellida and Haptophyta). Moreover, by searching against expressed sequence tag (EST) database, Yue et al. claimed that no TAA and YUC protein homologs were found in Charophyta, a group of freshwater green algae from which land plants originated [3,4]. Therefore, they concluded that there is ‘little phylogenetic evidence for the presence of the TAA/YUC pathway in any algal group’ and thus suggest the TAA/YUC pathway originated in the most recent common ancestor (MRCA) of land plants [2]. However, EST data only represent a fraction of the genomic information of an organism. When one searches against EST data to identify protein homologs, the presence of significant hits indicates the presence of homologs, but the absence of significant hits does not necessarily indicate the absence of homologs. Recently the genome sequence of one charophyte (Klebsormidium flaccidum) and transcriptome data of four charophytes (Nitella hyalina, Nitella mirabilis, Penium margaritaceum, and Spirogyra pratensis) have been published [3,5]; we have made use of these data to revisit the question of the origin of the TAA/YUC pathway in plants. To obtain a more complete picture, the genome sequences of three representative chlorophytes (Coccomyxa subellipsoidea, Ostreococcus lucimarinus, and Ostreococcus tauri) were also included in our study. We found significant homologs (using the BLAST algorithm with Arabidopsis thaliana proteins as queries and an e value threshold of 10 5) of both TAA and YUC proteins in the K. flaccidum genome, and significant homologs of YUC proteins in the N. hyaline and N. mirabilis transcriptome data and in the three chlorophyte genomes. It is worth noting that, similarly to using EST data, the absence of significant hits in transcriptome data (especially when the coverage is low) does not necessarily indicate the absence of homologs. One might argue that these algal proteins are distantly Corresponding authors: Li, S.-S. ([email protected]); Han, G.-Z. ([email protected]) * These authors contributed equally to this work. 1360-1385/ ß 2014 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tplants.2014.10.004
related homologs of TAA and YUC proteins in land plants. To assess this possibility, we conducted phylogenetic analysis of TAA and YUC homologs of bacteria, archaea, and eukaryotes (including land plants, charophytes, and other eukaryotes). Our phylogenetic analysis (Figure 1) shows that the K. flaccidum TAA homolog (kfl00051_0080) groups with land plant TAA proteins, and the K. flaccidum YUC homolog (kfl00109_0340) and the N. hyaline YUC homolog (JO301227) group with land plant YUC proteins. Therefore, our results provide clear evidence that the TAA/YUC pathway is already present in Charophyta. We found that plant TAA proteins nest within the diversity of TAA homologs of non-plant eukaryotic origin; the most parsimonious explanation is a horizontal gene transfer (HGT) event of TAA proteins from non-plant eukaryotes to plants. Yue et al. suggest that YUCs in land plants are derived from an HGT event from bacteria to the MRCA of land plants [2]. However, we believe that the evolutionary scenario might be complex and involve multiple HGT events. Three equally probable explanations for the phylogenetic topology of YUC-related proteins could be conceived: (i) an HGT event from bacteria to plants, (ii) an HGT from bacteria to plants and a subsequent HGT from plants to bacteria, and (iii) independent HGT events from bacteria to land plants and Charophyta. Sequencing of additional charophyte and basal land plant genomes might reveal which is the most likely explanation. Nevertheless, our results show that the TAA/YUC pathway is present in Charophyta, and this is consistent with the finding that endogenous auxins have been detected in K. flaccidum [6]. Our results illustrate the limitations of proving the absence of particular proteins in an organism from EST data alone. Based on the limited information available, we are not sure whether Charophyta acquired TAA and YUC proteins synchronously or asynchronously. The possibility that the earlier-branching charophytes (such as Mesostigma and Chlorokybus) only have one of the proteins cannot be formally excluded. Given that our analyses pinpoint the presence of the TAA/YUC pathway in Charophyta, Yue et al. seem to overstate the role of the origin of TAA/YUC auxin biosynthesis pathway in the emergence of land plants [2]. Because microbes exist everywhere, regulating and counteracting the microbial activity proposed by Yu et al. [2] might be still a potential mechanism for auxin biosynthesis initially evolving in algae. However, the microbes may not be those encountered in the terrestrial environment as proposed by Yu et al. [2], and are more likely to be those encountered in the aquatic environment. Interestingly, the presence Trends in Plant Science, December 2014, Vol. 19, No. 12
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Letters (A)
Trends in Plant Science December 2014, Vol. 19, No. 12
Arabidopsis thaliana_AT1G70560_TAA1 Arabidopsis thaliana_AT1G23320_TAR1 Arabidopsis thaliana_AT4G24670_TAR2 Oryza sava_NP_001054761 Oryza sava_BAD68317 Marchana polymorpha_AAN74743 Selaginealla moellendorffii_XP_002970176 Physcomitrella patens_XP_001773769 Physcomitrella patens_XP_001752157 Plants Physcomitrella patens_XP_001757187 Oryza sava_NP_001044075 Oryza sava_NP_001044074 Arabidopsis thaliana_AT1G34040_TAR4 Selaginealla moellendorffii_XP_002960756 Selaginealla moellendorffii_XP_002965434 Physcomitrella patens_XP_001766876 Physcomitrella patens_XP_001756693 Klebsormidium flaccidum_00051_0080 Charophyta Salpingoeca sp._XP_004988548 Choanoflagellida Monosiga brevicollis_XP_001746485 Ichthyosporea Capsaspora owczarzaki_XP_004346719 Thecamonas trahens_ADVD01000853 Apusozoa Haptophytes Emiliania huxleyi_EOD27665 Guillardia theta_EKX38867 Cryptophytes Sulfurovum sp._YP_001359354 Epsilon-proteobacteria Wolinella succinogenes_NP_908102 Clostridium ultunense_WP_005584467 Firmicutes Clostridium pasteurianum_WP_015617191 Bacillus sp._WP_006836268 Corynebacterium ammoniagenes_WP_003846958 High GC Gram+ Klebsormidium flaccidum_00096_0120 Charophyta Ktedonobacter racemifer_WP_007912997 GNS bacteria Sphaerobacter thermophilus_WP_012870920 Thermosediminibacter oceani_WP_013276200 Firmicutes Tepidanaerobacter acetatoxydans_WP_013777772 Uncultured bacterium_EKE15292 Bacteria Clostridium sp._CDB16244 Firmicutes Natrialba hulunbeirensis_WP_006652091 Archaea Natrialba chahannaoensis_WP_006167735
Arabidopsis thaliana_AT1G04180_YUC9 Arabidopsis thaliana_AT5G43890_YUC5 Arabidopsis thaliana_AT4G28720_YUC8 Arabidopsis thaliana_AT2G33230_YUC7 Arabidopsis thaliana_AT1G04610_YUC3 Oryza sava_NP_001052088 Oryza sava_NP_001059508 Arabidopsis thaliana_AT4G32540_YUC1 Arabidopsis thaliana_AT5G11320_YUC4 Arabidopsis thaliana_AT4G13260_YUC2 Arabidopsis thaliana_AT5G25620_YUC6 Oryza sava_NP_001042455 Oryza sava_NP_001066871 Arabidopsis thaliana_AT1G48910_YUC10 Arabidopsis thaliana_AT1G21430_YUC11 Oryza sava_NP_001066335 Oryza sava_NP_001042717 Plants Oryza sava_NP_001042716 Oryza sava_NP_001049048 Physcomitrella patens_XP_001776377 Physcomitrella patens_XP_001759473 Physcomitrella patens_XP_001756351 Physcomitrella patens_XP_001771611 Physcomitrella patens_XP_001753831 Selaginella moellendorffii_XP_002961029 Selaginella moellendorffii_XP_002974880 Selaginella moellendorffii_XP_002965620 Physcomitrella patens_XP_001781831 Klebsormidium flaccidum_00109_0340 Charophyta Nitella hyalina_JO301227 Mesorhizobium amorphae_ZP_09091806 Alpha-proteobacteria Sinorhizobium fredii_YP_005190010 CFB group bacteria Spirosoma linguale_YP_003386696 Beutenbergia cavernae_YP_002880946 High GC Gram+ Mycobacterium_sp._YP_640097 Mycobacterium amorphae_ZP_09087212 Alpha-proteobacteria Mycobacterium_sp._YP_642359 High GC Gram+ Streptomyces sviceus_ZP_06917824 Archaea Haloterrigena turkmenica_YP_003405537 Alpha-proteobacteria Mesorhizobium amorphae_ZP_09090301 Paenibacillus mucilaginosus_YP_005311360 Firmicutes Bacillus cereus_ZP_04244770 Alpha-proteobacteria Caulobacter segnis_YP_003594633 Nitella mirabilis_JV798146 Charophyta Pusillimonas_sp._YP_004417986 Beta-proteobacteria GNS bacteria Sphaerobacter thermophilus_YP_003321561 Chlorella vulgaris_70408 Green Algae Coccomyxa subellipsoidea_C169_39236 CFB group bacteria Rhodothermus marinus_YP_003290739 Cyanothece_sp._YP_003887096 Cyanobacteria Arthrospira platensis_ZP_06385236 Heterolobosea Naegleria gruberi_XP_002672151 Planctomycetes Pirellula staleyi_YP_003369057 High GC Gram+ Streptomyces sviceus_ZP_06914541 Gamma-proteobacteria Pseudomonas syringae_ZP_06480076 Spirochetes Leptospira noguchii_ZP_09262867 Gamma-proteobacteria Legionella pneumophila_YP_005185215 Beta-proteobacteria Nitrosomonas europaea_NP_842204 Xenopus tropicalis_NP_001025595 Metazoa Homo sapiens_NP_001451 Saccoglossus kowalevskii_XP_002740302 Ajellomyces capsulatus_EEH06281 Fungi Ostreococcus tauri_XP_003084158 Green Algae Ostreococcus lucimarinus_XP_001422130 Klebsormidium flaccidum_00117_0190 Charophyta Oryza sava_NP_001063857 Oryza sava_NP_001063855 Oryza sava_NP_001052272 S.moellendorffii_XP_002967925 Plants S.moellendorffii_XP_002964000 Arabidopsis thaliana_NP_173359 Arabidopsis thaliana_NP_199331 Charophyta Klebsormidium flaccidum_00283_0240 Ruegeria pomeroyi_YP_168154 Alpha-proteobacteria Labrenzia alexandrii_EEE43794 Bradyrhizobium_sp._YP_001242107 Ectocarpus siliculosus_CBJ27809 Brown Algae Ectocarpus siliculosus_CBJ32621 Fungi Uslago maydis_XP_759576 High GC Gram+ Nocardia farcinica_YP_119941
(B)
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0.3 TRENDS in Plant Science
Figure 1. Phylogenetic analyses of TAA-related proteins (A) and YUC-related proteins (B). Protein sequences were aligned using MUSCLE (multiple sequence comparison by log-expectation [9]) and manually refined. The phylogenetic trees were reconstructed using both the Bayesian method implemented in MrBayes [10] and the neighborjoining method implemented in MEGA5 (molecular evolutionary genetics analysis [11]) with 1000 bootstrap replicates. Numbers around the selected nodes are support values (Bayesian posterior probabilities/bootstrap values). The scale bar indicates the genetic distance.
of TAA/YUC auxin biosynthesis pathway coincides with the presence of the PIN-FORMED (PIN) family (auxin transporters) and other auxin-response components in Charophyta, raising the possibility that potentially a functional auxin signaling pathway is present in charophyte lineages [5,7,8]. Therefore, other possible mechanisms related to cell expansion and division, which are directly modulated by auxin in plants, should not be neglected for the initial acquisition of TAA/YUC pathway in algae. 742
Acknowledgments We thank two anonymous reviewers for extremely constructive comments. This research was supported by the National Key Technologies R&D Program of China (Grant No. 2011BAD35B03).
References 1 Mashiguchi, K. et al. (2011) The main auxin biosynthesis pathway in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 108, 18512–18517 2 Yue, J. et al. (2014) Origin of plant auxin biosynthesis. Trends Plant Sci. 19, 764–770 3 Timme, R.E. et al. (2012) Broad phylogenomic sampling and the sister lineage of land plants. PLoS ONE 7, e29696
Letters 4 Finet, C. et al. (2010) Multigene phylogeny of the green lineage reveals the origin and diversification of land plants. Curr. Biol. 20, 2217–2222 5 Hori, K. et al. (2014) Klebsormidium flaccidum genome reveals primary factors for plant terrestrial adaptation. Nat. Commun. 5, 3978 6 Stirk, W. et al. (2013) Auxin and cytokinin relationships in 24 microalgal strains. J. Phycol. 49, 459–467 7 Viaene, T. et al. (2013) Origin and evolution of PIN auxin transporters in the green lineage. Trends Plant Sci. 18, 5–10
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8 De Smet, I. et al. (2011) Unraveling the evolution of auxin signaling. Plant Physiol. 155, 209–221 9 Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797 10 Ronquist, F. and Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574 11 Tamura, K. et al. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731–2739
Origin of plant auxin biosynthesis in charophyte algae: a reply to Wang et al.§ Jinling Huang1, Jipei Yue2, and Xiangyang Hu2 1 2
Department of Biology, East Carolina University, Greenville, NC 27858, USA Kunming Institute of Botany, Chinese Academy of Science, Kunming, China
The origin of plant auxin biosynthesis has long been controversial [1]. In our analyses of the TAA/YUC indole-3acetic acid (IAA) biosynthetic pathway we suggested that this pathway evolved in land plants [2]. With the availability of Klebsormidium genome and other charophyte sequence data, Wang et al. performed additional phylogenetic analyses [3]. It was concluded by Wang et al. that clear evidence exists for the origin of the TAA/YUC pathway at least in charophytes. In our opinion, such a conclusion is contingent on two assumptions: (i) Klebsormidium or any other charophyte TAA and YUC homologs are functionally involved in IAA biosynthesis, and (ii) both of the two gene families (TAAs and YUCs) in charophytes and land plants share a common ancestry. At present, sufficient functional information for charophyte TAA and YUC homologs is still lacking. In the analyses of the TAA gene family by Wang et al. [3], land plant and charophyte sequences indeed form a clade, but they are also affiliated with homologs from miscellaneous eukaryotes. Although the green plant TAA clade (charophytes and land plants) was interpreted by Wang et al. as being horizontally transferred from a non-plant eukaryote [3], it can be easily explained by other scenarios (e.g., vertical inheritance followed by differential losses or gene transfer in the reverse direction). Given the affinity of plant TAAs to homologs from other eukaryotes that are not known to produce IAA, it is likely that TAAs also participate in activities other than IAA biosynthesis [2]. In this respect, the finding of TAA homologs should by no means be
considered as clear evidence for the existence of IAA production in charophytes. In the molecular phylogeny of the YUC family, relationships between charophyte and land plant sequences are unresolved, and it is uncertain whether land plant and charophyte YUCs derive from a common origin. Nevertheless, two of the three scenarios invoked by Wang et al. [scenarios (ii) and (iii)] suggest that charophyte and land plant YUCs likely do not form a monophyletic group. Furthermore, scenario (iii), which involves independent acquisitions by land plants and charophytes, is consistent with a land plant origin of the TAA/ YUC pathway or, at best, points to independent origins of IAA production in land plants and charophytes. Therefore, the data presented by Wang et al. are ambiguous and neither support nor reject the available hypotheses (algal origin vs land plant origin of IAA biosynthesis). It is likely that the origin of plant auxin biosynthesis will continue to be debated. Further functional investigations and phylogenetic analyses with additional samplings are necessary to better understand this important topic of plant biology. References 1 Lau, S. et al. (2009) Auxin signaling in algal lineages: fact or myth? Trends Plant Sci. 14, 182–188 2 Yue, J. et al. (2014) Origin of plant auxin biosynthesis. Trends Plant Sci. 19, 764–770 3 Wang, C. et al. (2014) Origin of plant auxin biosynthesis in charophyte algae. Trends Plant Sci. 19, 741–743
Corresponding author: Huang, J. ([email protected]) 1360-1385/ ß 2014 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tplants.2014.10.005
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Origin of plant auxin biosynthesis in charophyte algae Chunyang Wang1,2*, Yang Liu2*, Si-Shen Li2, and Guan-Zhu Han1,3 1
Jiangsu Key Laboratory for Microbes and Functional Genomics, Jiangsu Engineering and Technology Research Center for Microbiology, College of Life Sciences, Nanjing Normal University, Nanjing, Jiangsu 210023, China 2 State Key Laboratory of Crop Biology, Shandong Agricultural University, Tai’an, Shandong 271018, China 3 Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ 85721, USA
The TRYPTOPHAN AMINOTRANSFERASE OF ARABIDOPSIS (TAA)/YUCCA flavin monooxygenase (YUC) pathway is the main auxin biosynthesis pathway in plants [1]. The origin of plant auxin biosynthesis remains unclear and controversial. Recently Yue et al. addressed this issue by performing phylogenetic analysis of TAA and YUC proteins [2]. They found that land plant TAA proteins are most closely related to proteins from non-plant eukaryotes (such as Choanoflagellida and Haptophyta). Moreover, by searching against expressed sequence tag (EST) database, Yue et al. claimed that no TAA and YUC protein homologs were found in Charophyta, a group of freshwater green algae from which land plants originated [3,4]. Therefore, they concluded that there is ‘little phylogenetic evidence for the presence of the TAA/YUC pathway in any algal group’ and thus suggest the TAA/YUC pathway originated in the most recent common ancestor (MRCA) of land plants [2]. However, EST data only represent a fraction of the genomic information of an organism. When one searches against EST data to identify protein homologs, the presence of significant hits indicates the presence of homologs, but the absence of significant hits does not necessarily indicate the absence of homologs. Recently the genome sequence of one charophyte (Klebsormidium flaccidum) and transcriptome data of four charophytes (Nitella hyalina, Nitella mirabilis, Penium margaritaceum, and Spirogyra pratensis) have been published [3,5]; we have made use of these data to revisit the question of the origin of the TAA/YUC pathway in plants. To obtain a more complete picture, the genome sequences of three representative chlorophytes (Coccomyxa subellipsoidea, Ostreococcus lucimarinus, and Ostreococcus tauri) were also included in our study. We found significant homologs (using the BLAST algorithm with Arabidopsis thaliana proteins as queries and an e value threshold of 10 5) of both TAA and YUC proteins in the K. flaccidum genome, and significant homologs of YUC proteins in the N. hyaline and N. mirabilis transcriptome data and in the three chlorophyte genomes. It is worth noting that, similarly to using EST data, the absence of significant hits in transcriptome data (especially when the coverage is low) does not necessarily indicate the absence of homologs. One might argue that these algal proteins are distantly Corresponding authors: Li, S.-S. ([email protected]); Han, G.-Z. ([email protected]) * These authors contributed equally to this work. 1360-1385/ ß 2014 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tplants.2014.10.004
related homologs of TAA and YUC proteins in land plants. To assess this possibility, we conducted phylogenetic analysis of TAA and YUC homologs of bacteria, archaea, and eukaryotes (including land plants, charophytes, and other eukaryotes). Our phylogenetic analysis (Figure 1) shows that the K. flaccidum TAA homolog (kfl00051_0080) groups with land plant TAA proteins, and the K. flaccidum YUC homolog (kfl00109_0340) and the N. hyaline YUC homolog (JO301227) group with land plant YUC proteins. Therefore, our results provide clear evidence that the TAA/YUC pathway is already present in Charophyta. We found that plant TAA proteins nest within the diversity of TAA homologs of non-plant eukaryotic origin; the most parsimonious explanation is a horizontal gene transfer (HGT) event of TAA proteins from non-plant eukaryotes to plants. Yue et al. suggest that YUCs in land plants are derived from an HGT event from bacteria to the MRCA of land plants [2]. However, we believe that the evolutionary scenario might be complex and involve multiple HGT events. Three equally probable explanations for the phylogenetic topology of YUC-related proteins could be conceived: (i) an HGT event from bacteria to plants, (ii) an HGT from bacteria to plants and a subsequent HGT from plants to bacteria, and (iii) independent HGT events from bacteria to land plants and Charophyta. Sequencing of additional charophyte and basal land plant genomes might reveal which is the most likely explanation. Nevertheless, our results show that the TAA/YUC pathway is present in Charophyta, and this is consistent with the finding that endogenous auxins have been detected in K. flaccidum [6]. Our results illustrate the limitations of proving the absence of particular proteins in an organism from EST data alone. Based on the limited information available, we are not sure whether Charophyta acquired TAA and YUC proteins synchronously or asynchronously. The possibility that the earlier-branching charophytes (such as Mesostigma and Chlorokybus) only have one of the proteins cannot be formally excluded. Given that our analyses pinpoint the presence of the TAA/YUC pathway in Charophyta, Yue et al. seem to overstate the role of the origin of TAA/YUC auxin biosynthesis pathway in the emergence of land plants [2]. Because microbes exist everywhere, regulating and counteracting the microbial activity proposed by Yu et al. [2] might be still a potential mechanism for auxin biosynthesis initially evolving in algae. However, the microbes may not be those encountered in the terrestrial environment as proposed by Yu et al. [2], and are more likely to be those encountered in the aquatic environment. Interestingly, the presence Trends in Plant Science, December 2014, Vol. 19, No. 12
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Letters (A)
Trends in Plant Science December 2014, Vol. 19, No. 12
Arabidopsis thaliana_AT1G70560_TAA1 Arabidopsis thaliana_AT1G23320_TAR1 Arabidopsis thaliana_AT4G24670_TAR2 Oryza sava_NP_001054761 Oryza sava_BAD68317 Marchana polymorpha_AAN74743 Selaginealla moellendorffii_XP_002970176 Physcomitrella patens_XP_001773769 Physcomitrella patens_XP_001752157 Plants Physcomitrella patens_XP_001757187 Oryza sava_NP_001044075 Oryza sava_NP_001044074 Arabidopsis thaliana_AT1G34040_TAR4 Selaginealla moellendorffii_XP_002960756 Selaginealla moellendorffii_XP_002965434 Physcomitrella patens_XP_001766876 Physcomitrella patens_XP_001756693 Klebsormidium flaccidum_00051_0080 Charophyta Salpingoeca sp._XP_004988548 Choanoflagellida Monosiga brevicollis_XP_001746485 Ichthyosporea Capsaspora owczarzaki_XP_004346719 Thecamonas trahens_ADVD01000853 Apusozoa Haptophytes Emiliania huxleyi_EOD27665 Guillardia theta_EKX38867 Cryptophytes Sulfurovum sp._YP_001359354 Epsilon-proteobacteria Wolinella succinogenes_NP_908102 Clostridium ultunense_WP_005584467 Firmicutes Clostridium pasteurianum_WP_015617191 Bacillus sp._WP_006836268 Corynebacterium ammoniagenes_WP_003846958 High GC Gram+ Klebsormidium flaccidum_00096_0120 Charophyta Ktedonobacter racemifer_WP_007912997 GNS bacteria Sphaerobacter thermophilus_WP_012870920 Thermosediminibacter oceani_WP_013276200 Firmicutes Tepidanaerobacter acetatoxydans_WP_013777772 Uncultured bacterium_EKE15292 Bacteria Clostridium sp._CDB16244 Firmicutes Natrialba hulunbeirensis_WP_006652091 Archaea Natrialba chahannaoensis_WP_006167735
Arabidopsis thaliana_AT1G04180_YUC9 Arabidopsis thaliana_AT5G43890_YUC5 Arabidopsis thaliana_AT4G28720_YUC8 Arabidopsis thaliana_AT2G33230_YUC7 Arabidopsis thaliana_AT1G04610_YUC3 Oryza sava_NP_001052088 Oryza sava_NP_001059508 Arabidopsis thaliana_AT4G32540_YUC1 Arabidopsis thaliana_AT5G11320_YUC4 Arabidopsis thaliana_AT4G13260_YUC2 Arabidopsis thaliana_AT5G25620_YUC6 Oryza sava_NP_001042455 Oryza sava_NP_001066871 Arabidopsis thaliana_AT1G48910_YUC10 Arabidopsis thaliana_AT1G21430_YUC11 Oryza sava_NP_001066335 Oryza sava_NP_001042717 Plants Oryza sava_NP_001042716 Oryza sava_NP_001049048 Physcomitrella patens_XP_001776377 Physcomitrella patens_XP_001759473 Physcomitrella patens_XP_001756351 Physcomitrella patens_XP_001771611 Physcomitrella patens_XP_001753831 Selaginella moellendorffii_XP_002961029 Selaginella moellendorffii_XP_002974880 Selaginella moellendorffii_XP_002965620 Physcomitrella patens_XP_001781831 Klebsormidium flaccidum_00109_0340 Charophyta Nitella hyalina_JO301227 Mesorhizobium amorphae_ZP_09091806 Alpha-proteobacteria Sinorhizobium fredii_YP_005190010 CFB group bacteria Spirosoma linguale_YP_003386696 Beutenbergia cavernae_YP_002880946 High GC Gram+ Mycobacterium_sp._YP_640097 Mycobacterium amorphae_ZP_09087212 Alpha-proteobacteria Mycobacterium_sp._YP_642359 High GC Gram+ Streptomyces sviceus_ZP_06917824 Archaea Haloterrigena turkmenica_YP_003405537 Alpha-proteobacteria Mesorhizobium amorphae_ZP_09090301 Paenibacillus mucilaginosus_YP_005311360 Firmicutes Bacillus cereus_ZP_04244770 Alpha-proteobacteria Caulobacter segnis_YP_003594633 Nitella mirabilis_JV798146 Charophyta Pusillimonas_sp._YP_004417986 Beta-proteobacteria GNS bacteria Sphaerobacter thermophilus_YP_003321561 Chlorella vulgaris_70408 Green Algae Coccomyxa subellipsoidea_C169_39236 CFB group bacteria Rhodothermus marinus_YP_003290739 Cyanothece_sp._YP_003887096 Cyanobacteria Arthrospira platensis_ZP_06385236 Heterolobosea Naegleria gruberi_XP_002672151 Planctomycetes Pirellula staleyi_YP_003369057 High GC Gram+ Streptomyces sviceus_ZP_06914541 Gamma-proteobacteria Pseudomonas syringae_ZP_06480076 Spirochetes Leptospira noguchii_ZP_09262867 Gamma-proteobacteria Legionella pneumophila_YP_005185215 Beta-proteobacteria Nitrosomonas europaea_NP_842204 Xenopus tropicalis_NP_001025595 Metazoa Homo sapiens_NP_001451 Saccoglossus kowalevskii_XP_002740302 Ajellomyces capsulatus_EEH06281 Fungi Ostreococcus tauri_XP_003084158 Green Algae Ostreococcus lucimarinus_XP_001422130 Klebsormidium flaccidum_00117_0190 Charophyta Oryza sava_NP_001063857 Oryza sava_NP_001063855 Oryza sava_NP_001052272 S.moellendorffii_XP_002967925 Plants S.moellendorffii_XP_002964000 Arabidopsis thaliana_NP_173359 Arabidopsis thaliana_NP_199331 Charophyta Klebsormidium flaccidum_00283_0240 Ruegeria pomeroyi_YP_168154 Alpha-proteobacteria Labrenzia alexandrii_EEE43794 Bradyrhizobium_sp._YP_001242107 Ectocarpus siliculosus_CBJ27809 Brown Algae Ectocarpus siliculosus_CBJ32621 Fungi Uslago maydis_XP_759576 High GC Gram+ Nocardia farcinica_YP_119941
(B)
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0.3 TRENDS in Plant Science
Figure 1. Phylogenetic analyses of TAA-related proteins (A) and YUC-related proteins (B). Protein sequences were aligned using MUSCLE (multiple sequence comparison by log-expectation [9]) and manually refined. The phylogenetic trees were reconstructed using both the Bayesian method implemented in MrBayes [10] and the neighborjoining method implemented in MEGA5 (molecular evolutionary genetics analysis [11]) with 1000 bootstrap replicates. Numbers around the selected nodes are support values (Bayesian posterior probabilities/bootstrap values). The scale bar indicates the genetic distance.
of TAA/YUC auxin biosynthesis pathway coincides with the presence of the PIN-FORMED (PIN) family (auxin transporters) and other auxin-response components in Charophyta, raising the possibility that potentially a functional auxin signaling pathway is present in charophyte lineages [5,7,8]. Therefore, other possible mechanisms related to cell expansion and division, which are directly modulated by auxin in plants, should not be neglected for the initial acquisition of TAA/YUC pathway in algae. 742
Acknowledgments We thank two anonymous reviewers for extremely constructive comments. This research was supported by the National Key Technologies R&D Program of China (Grant No. 2011BAD35B03).
References 1 Mashiguchi, K. et al. (2011) The main auxin biosynthesis pathway in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 108, 18512–18517 2 Yue, J. et al. (2014) Origin of plant auxin biosynthesis. Trends Plant Sci. 19, 764–770 3 Timme, R.E. et al. (2012) Broad phylogenomic sampling and the sister lineage of land plants. PLoS ONE 7, e29696
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Origin of plant auxin biosynthesis in charophyte algae: a reply to Wang et al.§ Jinling Huang1, Jipei Yue2, and Xiangyang Hu2 1 2
Department of Biology, East Carolina University, Greenville, NC 27858, USA Kunming Institute of Botany, Chinese Academy of Science, Kunming, China
The origin of plant auxin biosynthesis has long been controversial [1]. In our analyses of the TAA/YUC indole-3acetic acid (IAA) biosynthetic pathway we suggested that this pathway evolved in land plants [2]. With the availability of Klebsormidium genome and other charophyte sequence data, Wang et al. performed additional phylogenetic analyses [3]. It was concluded by Wang et al. that clear evidence exists for the origin of the TAA/YUC pathway at least in charophytes. In our opinion, such a conclusion is contingent on two assumptions: (i) Klebsormidium or any other charophyte TAA and YUC homologs are functionally involved in IAA biosynthesis, and (ii) both of the two gene families (TAAs and YUCs) in charophytes and land plants share a common ancestry. At present, sufficient functional information for charophyte TAA and YUC homologs is still lacking. In the analyses of the TAA gene family by Wang et al. [3], land plant and charophyte sequences indeed form a clade, but they are also affiliated with homologs from miscellaneous eukaryotes. Although the green plant TAA clade (charophytes and land plants) was interpreted by Wang et al. as being horizontally transferred from a non-plant eukaryote [3], it can be easily explained by other scenarios (e.g., vertical inheritance followed by differential losses or gene transfer in the reverse direction). Given the affinity of plant TAAs to homologs from other eukaryotes that are not known to produce IAA, it is likely that TAAs also participate in activities other than IAA biosynthesis [2]. In this respect, the finding of TAA homologs should by no means be
considered as clear evidence for the existence of IAA production in charophytes. In the molecular phylogeny of the YUC family, relationships between charophyte and land plant sequences are unresolved, and it is uncertain whether land plant and charophyte YUCs derive from a common origin. Nevertheless, two of the three scenarios invoked by Wang et al. [scenarios (ii) and (iii)] suggest that charophyte and land plant YUCs likely do not form a monophyletic group. Furthermore, scenario (iii), which involves independent acquisitions by land plants and charophytes, is consistent with a land plant origin of the TAA/ YUC pathway or, at best, points to independent origins of IAA production in land plants and charophytes. Therefore, the data presented by Wang et al. are ambiguous and neither support nor reject the available hypotheses (algal origin vs land plant origin of IAA biosynthesis). It is likely that the origin of plant auxin biosynthesis will continue to be debated. Further functional investigations and phylogenetic analyses with additional samplings are necessary to better understand this important topic of plant biology. References 1 Lau, S. et al. (2009) Auxin signaling in algal lineages: fact or myth? Trends Plant Sci. 14, 182–188 2 Yue, J. et al. (2014) Origin of plant auxin biosynthesis. Trends Plant Sci. 19, 764–770 3 Wang, C. et al. (2014) Origin of plant auxin biosynthesis in charophyte algae. Trends Plant Sci. 19, 741–743
Corresponding author: Huang, J. ([email protected]) 1360-1385/ ß 2014 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tplants.2014.10.005
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