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Evolutionary history of the GH3 family of acyl adenylases in rosids

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Abstract

GH3 amino acid conjugases have been identified in many plant and bacterial species. The evolution of GH3 genes in plant species is explored using the sequenced rosids Arabidopsis, papaya, poplar, and grape. Analysis of the sequenced non-rosid eudicots monkey flower and columbine, the monocots maize and rice, as well as spikemoss and moss is included to provide further insight into the origin of GH3 clades. Comparison of co-linear genes in regions surrounding GH3 genes between species helps reconstruct the evolutionary history of the family. Combining analysis of synteny with phylogenetics, gene expression and functional data redefines the Group III GH3 genes, of which AtGH3.12/PBS3, a regulator of stress-induced salicylic acid metabolism and plant defense, is a member. Contrary to previous reports that restrict PBS3 to Arabidopsis and its close relatives, PBS3 syntelogs are identified in poplar, grape, columbine, maize and rice suggesting descent from a common ancestral chromosome dating to before the eudicot/monocot split. In addition, the clade containing PBS3 has undergone a unique expansion in Arabidopsis, with expression patterns for these genes consistent with specialized and evolving stress-responsive functions.

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Abbreviations

BTH:

1,2,3-benzothiodiazole-7-carbothioic acid S-methyl ester

IAA:

Indole-3-acetic acid

JA:

Jasmonic acid

SA:

Salicylic acid

bZIP:

Basic-domain leucine-zipper

ERF :

Ethylene response factor

GDG1 :

GH3-like defense gene 1

GH3 :

Gretchen Hagen 3

ICS1 :

Isochorismate synthase 1

JAR1 :

Jasmonic acid resistant 1

PBS3 :

avrPphB susceptible 3

WIN3 :

HopW1-1-interacting 3

Ac:

Aquilegia coerulea (columbine)

At:

Arabidopsis thaliana

Cp:

Carica papaya (papaya)

Mg:

Mimulus guttatus (monkey flower)

Os:

Oryza sativa (rice)

Pp:

Physcomitrella patens (moss)

Pt:

Populus trichocarpa (poplar)

Sm:

Selaginella moellendorffii (spikemoss)

Vv:

Vitis vinifera (grape)

Zm:

Zea mays (maize)

ML:

Maximum likelihood

MP:

Maximum parsimony

NJ:

Neighbor joining

PID:

Percent identity

WGD:

Whole genome duplication

References

  • Albertazzi G, Milc J, Caffagni A, Francia E, Roncaglia E et al (2009) Gene expression in grapevine cultivars in response to Bois noir phytoplasma infection. Plant Sci 176:792–804

    Article  CAS  Google Scholar 

  • Ariizumi T, Hatakeyama K, Hinata K, Inatsugi R, Nishida I, Sata S, Kato T, Tabata S, Toriyama K (2004) Disruption of the novel plant protein NEF1 affects lipid accumulation in the plastids of the tapetum and exine formation of pollen, resulting in male sterility in Arabidopsis thaliana. Plant J 39:170–181

    Article  PubMed  CAS  Google Scholar 

  • Bierfreund NM, Tintelnot S, Reski R, Decker EL (2004) Loss of GH3 function does not affect phytochrome-mediated development in a moss, Physcomitrella patens. J Plant Physiol 161:823–835

    Article  PubMed  CAS  Google Scholar 

  • Blanc G, Hokamp K, Wolfe KH (2003) A recent polyploidy superimposed on older large-scale duplications in the Arabidopsis genome. Genome Res 13:137–144

    Article  PubMed  CAS  Google Scholar 

  • Bourne DJ, Barrow KD, Milborrow BV (1991) Salicyloylaspartate as an endogenous component of the leaves of Phaseolus vulgaris. Phytochemistry 30:4041–4044

    Article  CAS  Google Scholar 

  • Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552

    PubMed  CAS  Google Scholar 

  • Chang K-H, Xiang H, Dunaway-Mariano D (1997) Acyl-adenylate motif of the acyl-adenylate/thioester-forming enzyme superfamily: a site directed mutagenesis study with the Pseudomonas sp. Strain CBS3 4-chlorobenzoate:Coenzyme A ligase. Biochemistry 36:15650–15659

    Article  PubMed  CAS  Google Scholar 

  • Chini A, Fonseca S, Fernandez G, Adie B, Chico JM et al (2007) The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448:666

    Article  PubMed  CAS  Google Scholar 

  • Conti E, Franks NP, Brick P (1996) Crystal structure of firefly luciferase throws light on a superfamily of adenylate-forming enzymes. Structure 4:287–298

    Article  PubMed  CAS  Google Scholar 

  • Craigon DJ, James N, Okyere J, Higgins J, Jotham J et al (2004) Nascarrays: a repository for microarray data generated by NASC’s transcriptomics service. Nucleic Acids Res 32:D575–D577

    Article  PubMed  CAS  Google Scholar 

  • Dereeper A, Guignon V, Blanc G, Audic S, Buffet S et al (2008) Phylogeny.Fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36:W465–W469

    Article  PubMed  CAS  Google Scholar 

  • Ding X, Cao Y, Huang L, Zhao J, Xu C et al (2008) Activation of the indole-3-acetic acid-amido synthetase GH3–8 suppresses expansin expression and promotes salicylate- and jasmonate-independent basal immunity in rice. Plant Cell 20:228–240

    Article  PubMed  CAS  Google Scholar 

  • Dombrecht B, Xue GP, Sprague SJ, Kirkegaard JA, Ross JJ et al (2007) MYC2 differentially modulates diverse jasmonate-dependent functions in Arabidopsis. Plant Cell 19:2225–2245

    Article  PubMed  CAS  Google Scholar 

  • Domingo C, Andres F, Tharreau D, Iglesias DJ, Talon M (2009) Constitutive expression of OsGH3.1 reduces auxin content and enhances defense response and resistance to a fungal pathogen in rice. Mol Plant-Micro Interact 22:201–210

    Article  CAS  Google Scholar 

  • Dudareva N, Pichersky E (2000) Biochemical and molecular genetic aspects of floral scents. Plant Physiol 122:627–634

    Article  PubMed  CAS  Google Scholar 

  • Edgar RC (2004) Muscle: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  PubMed  CAS  Google Scholar 

  • Felten J, Kohler A, Morin E, Bhalerao RP, Palme K et al (2009) The ectomycorrhizal fungus Laccaria bicolor stimulates lateral root formation in poplar and Arabidopsis through auxin transport and signaling. Plant Physiol 151:1991–2005

    Article  PubMed  CAS  Google Scholar 

  • Ferrari S, Plotnikova JM, De Lorenzo G, Ausubel FM (2003) Arabidopsis local resistance to Botrytis cinerea involves salicylic acid and camalexin and requires EDS4 and PAD2, but not SID2, EDS5, or PAD4. Plant J 35:193–205

    Article  PubMed  CAS  Google Scholar 

  • Freeling M (2009) Bias in plant gene content following different sorts of duplication: Tandem, whole-genome, segmental, or by transposition. Annu Rev Plant Biol 60:433–453

    Article  PubMed  CAS  Google Scholar 

  • Goda H, Sasaki E, Akiyama K, Maruyama-Nakashita A, Nakabayashi K et al (2008) The AtGenExpress hormone and chemical treatment data set: experimental design, data evaluation, model data analysis and data access. Plant J 55:526–542

    Article  PubMed  CAS  Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  • Gutterson N, Reuber TL (2004) Regulation of disease resistance pathways by AP2/ERF transcription factors. Curr Opin Plant Biol 7:465–471

    Article  PubMed  CAS  Google Scholar 

  • Haberer G, Hindemitt T, Meyers BC, Mayer KFX (2004) Transcriptional similarities, dissimilarities, and conservation of cis-elements in duplicated genes of Arabidopsis. Plant Physiol 136:3009–3022

    Article  PubMed  CAS  Google Scholar 

  • Hagen G, Kleinschmidt A, Guilfoyle T (1984) Auxin-regulated gene expression in intact soybean Glycine max cultivar Wayne hypocotyl and excised hypocotyl sections. Planta 162:147–153

    Article  CAS  Google Scholar 

  • Hall BG (2005) Comparison of the accuracies of several phylogenetic methods using protein and DNA sequences. Mol Biol Evol 22:792–802

    Article  PubMed  CAS  Google Scholar 

  • Hanada K, Zou C, Lehti-Shiu MD, Shinozaki K, Shiu SH (2008) Importance of lineage-specific expansion of plant tandem duplicates in the adaptive response to environmental stimuli. Plant Physiol 148:993–1003

    Article  PubMed  CAS  Google Scholar 

  • Hsieh H-L, Okamoto H, Wang M, Ang L-H, Matsui M et al (2000) FIN219, an auxin-regulated gene, defines a link between phytochrome A and the downstream regulator COP1 in light control of Arabidopsis development. Genes Dev 14:1958–1970

    PubMed  CAS  Google Scholar 

  • Huelsenbeck JP, Hillis DM (1993) Success of phylogenetic methods in the four-taxon case. Syst Biol 42:247–264

    Google Scholar 

  • Jagadeeswaran G, Raina S, Acharya BR, Maqbool SB, Mosher SL et al (2007) Arabidopsis GH3-like Defense Gene 1 is required for accumulation of salicylic acid, activation of defense responses and resistance to Pseudomonas syringae. Plant J 51:234–246

    Article  PubMed  CAS  Google Scholar 

  • Jaillon O, Aury JM, Noel B, Policriti A, Clepet C et al (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463–467

    Article  PubMed  CAS  Google Scholar 

  • Jain M, Kaur N, Tyagi AK, Khurana JP (2006) The auxin-responsive GH3 gene family in rice (oryza sativa). Funct Integr Genomics 6:36–46

    Article  PubMed  CAS  Google Scholar 

  • Jansen R, Kaittanis C, Saski C, Lee S-B, Tomkins J et al (2006) Phylogenetic analyses of Vitis (Vitaceae) based on complete chloroplast genome sequences: effects of taxon sampling and phylogenetic methods on resolving relationships among rosids. BMC Evol Biol 6:32

    Article  PubMed  Google Scholar 

  • Jun J, Mandoiu I, Nelson C (2009) Identification of mammalian orthologs using local synteny. BMC Genomics 10:630

    Article  PubMed  Google Scholar 

  • Kessler D, Diezel C, Baldwin IT (2010) Changing pollinators as a means of escaping herbivores. Curr Biol 20:237–242

    Article  PubMed  CAS  Google Scholar 

  • Khan S, Stone JM (2007) Arabidopsis thaliana GH3.9 influences primary root growth. Planta 226:21–34

    Article  PubMed  CAS  Google Scholar 

  • Krishnaswamy S, Verma S, Rahman MH, Kav NNV (2011) Functional characterization of four APETALA2-family genes (RAP2.6, RAP2.6L, DREB19 and DREB26) in Arabidopsis. Plant Mol Biol 75:107–127

    Article  PubMed  CAS  Google Scholar 

  • Lee MW, Lu H, Jung HW, Greenberg JT (2007) A key role for the Arabidopsis WIN3 protein in disease resistance triggered by Pseudomonas syringae that secrete AvrRpt2. MPMI 20:1192–1200

    Article  PubMed  CAS  Google Scholar 

  • Lee MW, Jelenska J, Greenberg JT (2008) Arabidopsis proteins important for modulating defense responses to Pseudomonas syringae that secrete HopW1–1. Plant J 54:452–465

    Article  PubMed  CAS  Google Scholar 

  • Liu Kl, Kang B-C, Jiang H, Moore SL, Li H et al (2005) A GH3-like gene, CcGH3, isolated from Capsicum chinense l. Fruit is regulated by auxin and ethylene. Plant Mol Biol 58:447–464

    Article  PubMed  CAS  Google Scholar 

  • Ludwig-Muller J, Julke S, Bierfreund NM, Decker EL, Reski R (2009) Moss (Physcomitrella patens) GH3 proteins act in auxin homeostasis. New Phytol 181:323–338

    Article  PubMed  Google Scholar 

  • Lyons E, Freeling M (2008) How to usefully compare homologous plant genes and chromosomes as DNA sequences. Plant J 53:661–673

    Article  PubMed  CAS  Google Scholar 

  • Lyons E, Pedersen B, Kane J, Alam M, Ming R et al (2008) Finding and comparing syntenic regions among Arabidopsis and the outgroups papaya, poplar, and grape: CoGe with rosids. Plant Physiol 148:1772–1781

    Article  PubMed  CAS  Google Scholar 

  • Martinez C, Pons E, Prats G, Leon J (2004) Salicylic acid regulates flowering time and links defence responses and reproductive development. Plant J 37:209–217

    Article  PubMed  CAS  Google Scholar 

  • Ming R, Hou S, Feng Y, Yu Q, Dionne-Laporte A et al (2008) The draft genome of the transgenic tropical fruit tree papaya (Carica papaya linnaeus). Nature 452:991–996

    Article  PubMed  CAS  Google Scholar 

  • Molina C, Grotewold E (2005) Genome wide analysis of Arabidopsis core promoters. BMC Genomics 6:25

    Article  PubMed  Google Scholar 

  • Mount DW (2004) Bioinformatics: sequence and genome analysis. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Nakazawa M, Yabe N, Ichikawa T, Yamamoto YY, Yoshizumi T et al (2001) DFL1, an auxin-responsive GH3 gene homologue, negatively regulates shoot cell elongation and lateral root formation, and positively regulates the light response of hypocotyl length. Plant J 25:213–221

    Article  PubMed  CAS  Google Scholar 

  • Nobuta K, Okrent RA, Stoutemyer M, Rodibaugh N, Kempema L et al (2007) The GH3 acyl adenylase family member PBS3 regulates salicylic acid-dependent defense responses in Arabidopsis. Plant Physiol 144:1144–1156

    Article  PubMed  CAS  Google Scholar 

  • Okrent RA, Brooks MD, Wildermuth MC (2009) Arabidopsis GH3.12 (PBS3) conjugates amino acids to 4-substituted benzoates and is inhibited by salicylate. J Biol Chem 284:9742–9754

    Article  PubMed  CAS  Google Scholar 

  • Ouyang S, Zhu W, Hamilton J, Lin H, Campbell M et al (2006) The TIGR rice genome annotation resource: improvements and new features. Nucleic Acids Res 35:D883–D887

    Article  PubMed  Google Scholar 

  • Park J-E, Seo PJ, Lee A-K, Jung J-H, Kim Y-S et al (2007a) An Arabidopsis GH3 gene, encoding an auxin-conjugating enzyme, mediates phytochrome B-regulated light signals in hypocotyl growth. Plant Cell Physiol 48:1236–1241

    Article  PubMed  CAS  Google Scholar 

  • Park J-E, Park J-Y, Kim Y-S, Staswick PE, Jeon J, Yun J, Kim S-Y, Kim J, Lee Y-H, Park C-M (2007b) GH3-mediated auxin homeostasis links growth regulation with stress adaptation response in Arabidopsis. J Biol Chem 282:10036–10046

    Article  PubMed  CAS  Google Scholar 

  • Rensing SA, Lang D, Zimmer AD, Terry A, Salamov A et al (2008) The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319:64–69

    Article  PubMed  CAS  Google Scholar 

  • Rizzon C, Ponger L, Gaut BS (2006) Striking similarities in the genomic distribution of tandemly arrayed genes in Arabidopsis and rice. PLoS Comput Biol 2:e115

    Google Scholar 

  • Schnable PS, Ware D, Fulton RS, Stein JC, Wei F et al (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326:1112–1115

    Article  PubMed  CAS  Google Scholar 

  • Semon M, Wolfe KH (2007) Consequences of genome duplication. Curr Opin Genet Dev 17:505–512

    Article  PubMed  CAS  Google Scholar 

  • Singh KB, Foley RC, Onate-Sanchez L (2002) Transcription factors in plant defense and stress responses. Curr Opin Plant Biol 5:430–436

    Article  PubMed  CAS  Google Scholar 

  • Staswick PE, Tiryaki I (2004) The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in Arabidopsis. Plant Cell 16:2117–2127

    Article  PubMed  CAS  Google Scholar 

  • Staswick PE, Su W, Howell SH (1992) Methyl jasmonate inhibition of root growth and induction of a leaf protein are decreased in an Arabidopsis thaliana mutant. Proc Natl Acad Sci USA 89:6837–6840

    Article  PubMed  CAS  Google Scholar 

  • Staswick PE, Tiryaki I, Rowe ML (2002) Jasmonate response locus JAR1 and several related Arabidopsis genes encode enzymes of the firefly luciferase superfamily that show activity on jasmonic, salicylic, and indole-3-acetic acids in an assay for adenylation. Plant Cell 14:1405–1415

    Article  PubMed  CAS  Google Scholar 

  • Staswick PE, Serban B, Rowe M, Tiryaki I, Maldonado MT et al (2005) Characterization of an Arabidopsis enzyme family that conjugates amino acids to indole-3-acetic acid. Plant Cell 17:616–627

    Article  PubMed  CAS  Google Scholar 

  • Steel M (2005) Should phylogenetic models be trying to “Fit an elephant”? Trends Genet 21:307–309

    Article  PubMed  CAS  Google Scholar 

  • Sun F, Liu P, Xu J, Dong H (2010) Mutation in RAP2.6L, a transactivator of the ERF transcription factor family enhances resistance to Pseudomonas syringae. Physiol Mol Plant Pathol 74:295–301

    Article  CAS  Google Scholar 

  • Suzuki Y, Yanaguchi I, Murofushi N, Takahasi N (1988) Biological conversion of benzoic acid in Lemna paucicostata 151 and its relation to flower induction. Plant Cell Physiol 29:439–444

    CAS  Google Scholar 

  • Takase T, Nakazawa M, Ishikawa A, Manabe K, Matsui M (2003) DFL2, a new member of the Arabidopsis GH3 family is involved in red light-specific hypocotyl elongation. Plant Cell Physiol 44:1071–1080

    Article  PubMed  CAS  Google Scholar 

  • Takase T, Nakazawa M, Ishikawa A, Kawashima M, Ichikawa T, Takahashi N, Shimada H, Manabe K, Matsui M (2004) ydk1-D, an auxin-responsive GH3 mutant that is involved in hypocotyl and root elongation. Plant J 37:471–483

    Article  PubMed  CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  PubMed  CAS  Google Scholar 

  • Terol J, Domingo C, Talon M (2006) The GH3 family in plants: genome wide analysis in rice and evolutionary history based on EST analysis. Gene 371:279–290

    Article  PubMed  CAS  Google Scholar 

  • Thornton JW, Kolaczkowski B (2005) No magic pill for phylogenetic error. Trends Genet 21:310–311

    Article  PubMed  CAS  Google Scholar 

  • Toufighi K, Brady SM, Austin R, Ly E, Provart NJ (2005) The botany array resource: E-northerns, expression angling, and promoter analyses. Plant J 43:153–163

    Article  PubMed  CAS  Google Scholar 

  • Trennheuser F, Burkhard G, Becker H (1994) Anthocerodiazonin, an alkaloid from Antheroceros agretis. Phytochemistry 37:899–903

    Article  CAS  Google Scholar 

  • Tuskan GA, DiFazio S, Jansson S, Bohlmann J, Grigoriev I et al (2006) The genome of black cottonwood, populus trichocarpa (torr. & gray). Science 313:1596–1604

    Article  PubMed  CAS  Google Scholar 

  • Warren RF, Merritt PM, Holub E, Innes RW (1999) Identification of three putative signal transduction genes involved in R gene-specified disease resistance in Arabidopsis. Genetics 152:401–412

    PubMed  CAS  Google Scholar 

  • Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV et al (2007) An “electronic fluorescent pictograph” browser for exploring and analyzing large-scale biological data sets. PLoS One 2:e718

    Article  PubMed  Google Scholar 

  • Wise RP, Caldo RA, Hong L, Shen L, Cannon E et al (2007) Barleybase/plexdb: a unified expression profiling database for plants and plant pathogens. In: Edwards D (ed) Plant bioinformatics—methods and protocols. Humana Press, Totowa, pp 347–363

    Google Scholar 

  • Woodward AW, Bartel B (2005) Auxin: regulation, action, and interaction. Ann Bot 95:707–735

    Article  PubMed  CAS  Google Scholar 

  • Wu CA, Lowry DB, Cooley AM, Wright KM, Lee YW et al (2007) Mimulus is an emerging model system for the integration of ecological and genomic studies. Heredity 100:220–230

    Article  PubMed  Google Scholar 

  • Zhang Z, Li Q, Li Z, Staswick PE, Wang M et al (2007) Dual regulation role of GH3.5 in salicylic acid and auxin signaling during Arabidopsis-Pseudomonas syringae interaction. Plant Physiol 145:450–464

    Article  PubMed  CAS  Google Scholar 

  • Zhang S-W, Li C-H, Cao J, Zhang Y-C, Zhang S-Q et al (2009) Altered architecture and enhanced drought tolerance in rice via the down-regulation of indole-3-acetic acid by tld1/osgh3.13 activation. Plant Physiol 151:1889–1901

    Article  PubMed  CAS  Google Scholar 

  • Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W (2004) GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol 136:2621–2632

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We would like to thank Dr. Eric Lyons for his assistance with the CoGe browser, Dr. Divya Chandran for careful reading of the manuscript, and the William Carroll Smith Graduate Research Fellowship in Plant Pathology (to R.A.O) and UC Berkeley awards (to M.C.W.) for financial support. Some of the genome sequence data described here was analyzed prior to publication by the sequencing projects. Of these, the Aquilegia coerulea, Mimulus guttatus, and Selaginella moellendorffii data were produced by the US Department of Energy Joint Genome Institute. Carica papaya data were produced by the ASGPB Hawaii Papaya Genome Project (http://www.asgpb.mhpcc.hawaii.edu/papaya/). Zea mays data were produced by the Genome Sequencing Center at Washington University School of Medicine in St. Louis and can be obtained from http://www.maizesequence.org/.

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  1. Rachel A. Okrent

    Present address: Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR, 97331, USA

Authors and Affiliations

  1. Department of Plant and Microbial Biology, University of California, 221 Koshland Hall, Berkeley, 94720, USA

    Rachel A. Okrent & Mary C. Wildermuth

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Correspondence to Mary C. Wildermuth.

Additional information

Accession numbers: AtGH3.1, At2g14960; AtGH3.2, At4g37390; AtGH3.3, At2g23170; AtGH3.4, At1g59500; AtGH3.5, At4g27260; AtGH3.6, At5g54510; AtGH3.7, At1g23160; AtGH3.8, At5g51470; AtGH3.9, At2g47750; AtGH3.10, At4g03400; AtGH3.11, At2g46370; AtGH3.12, At5g13320; AtGH3.13, At5g13350; AtGH3.14, At5g13360; AtGH3.15, At5g13370; AtGH3.16, At5g13380; AtGH3.17, At1g28130; AtGH3.18, At1g48670; AtGH3.19, At1g48660.

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Okrent, R.A., Wildermuth, M.C. Evolutionary history of the GH3 family of acyl adenylases in rosids. Plant Mol Biol 76, 489–505 (2011). https://doi.org/10.1007/s11103-011-9776-y

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