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Genome-wide investigation and expression analysis suggest diverse roles of auxin-responsive GH3 genes during development and response to different stimuli in tomato (Solanum lycopersicum)

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Abstract

In plants, auxin-mediated responses are regulated by diverse proteins. One such class of proteins, i.e. GH3, is involved in the conjugation of IAA to amino acids and provides a negative feedback loop to control auxin homoeostasis. In order to have a better understanding of the mechanism of the auxin action, 15 genes encoding GH3 members were identified using existing EST databases of tomato. Their orthologs were identified from tobacco, potato, N. benthemiana, pepper, and petunia. Phylogenetic analysis of AtGH3, SlGH3, and their Solanaceae orthologs provided insights into various orthologous relationships among these proteins. These genes were found to be responsive to a variety of signals including, phytohormones and environmental stresses. Analysis of AuxRE elements in their promoters showed variability in the sequence as well as number of this element. Up-regulation of only 11 SlGH3 genes, in response to exogenous auxin, suggested possible relationship between the diversity in the sequence and number of AuxRE element with the auxin inducibility. Expression analysis of SlGH3 genes in different vegetative and reproductive tissues/stages suggested limited or no role for most of the SlGH3 genes at the initiation of fruit ripening. However, up-regulation of SlGH3-1 and -2 at the onset of fruit ripening indicates that these genes could have a role in fruit ripening. The present study characterizes GH3 gene family of tomato and its evolutionary relationship with members of this family from other Solanaceae species and Arabidopsis. It could help in the identification of GH3 genes and revelation of their function during vegetative/reproductive development stages from other Solanaceae members.

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References

  • Abel S, Theologis A (1996) Early genes and auxin action. Plant Physiol 111:9–17

    Article  PubMed  CAS  Google Scholar 

  • Böttcher C, Keyzers RA, Boss PK, Davies C (2010) Sequestration of auxin by the indole-3-acetic acid-amido synthetase GH3–1 in grape berry (Vitis vinifera L.) and the proposed role of auxin conjugation during ripening. J Exp Bot 61:3615–3625

    Article  PubMed  Google Scholar 

  • Böttcher C, Boss PK, Davies C (2011) Acyl substrate preferences of an IAA-amido synthetase account for variations in grape (Vitis vinifera L.) berry ripening caused by different auxinic compounds indicating the importance of auxin conjugation in plant development. J Exp Bot 62:4267–4280

    Article  PubMed  Google Scholar 

  • Chen Q, Westfall CS, Hicks LM, Wang S, Jez JM (2010) Kinetic basis for the conjugation of auxin by a GH3 family indole-acetic acid-amido synthetase. J Biol Chem 285:29780–29786

    Article  PubMed  CAS  Google Scholar 

  • Cohen JD (1982) Identification and quantitative analyses of indole-3- acetyl-L-aspartate from seeds of Glycine max L. Plant Physiol 70:749–753

    Article  PubMed  CAS  Google Scholar 

  • Delker C, Raschke A, Quint M (2008) Auxin dynamics: the dazzling complexity of a small molecule’s message. Planta 227:929–941

    Article  PubMed  CAS  Google Scholar 

  • DeWald DB, Sadka A, Mullet JE (1994) Sucrose modulation of soybean vsp gene expression is inhibited by auxin. Plant Physiol 104:439–444

    PubMed  CAS  Google Scholar 

  • Ding X, Cao Y, Huang L, Zhao J, Xu C, Li X, Wang S (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 

  • 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 Microbe Interact 22:201–210

    Article  PubMed  CAS  Google Scholar 

  • Fei Z, Tang X, Alba R, Giovannoni J (2006) Tomato Expression Database (TED): a suite of data presentation and analysis tools. Nucleic Acids Res 34:D766–D770

    Article  PubMed  CAS  Google Scholar 

  • Felton J, Kohler A, Morin E, Bhalerao RP, Palme K, Martin F, Ditengou FA, Legue V (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  Google Scholar 

  • Ghanashyam C, Jain M (2009) Role of auxin-responsive genes in biotic stress responses. Plant Signal Behav 4:846–848

    Article  PubMed  CAS  Google Scholar 

  • Goda H, Sawa S, Asami T, Fujioka S, Shimada Y, Yoshida S (2004) Comprehensive comparison of auxin-regulated and brassinosteroid-regulated genes in Arabidopsis. Plant Physiol 134:1555–1573

    Article  PubMed  CAS  Google Scholar 

  • Guilfoyle TJ, Hagen G (2007) Auxin response factors. Curr Opin Plant Biol 10:453–460

    Article  PubMed  CAS  Google Scholar 

  • Hagen G, Guilfoyle T (2002) Auxin-responsive gene expression: genes, promoters and regulatory factors. Plant Mol Biol 49:373–385

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Hagen G, Martin G, Li Y, Guilfoyle TJ (1991) Auxin-induced expression of the soybean GH3 promoter in transgenic tobacco plants. Plant Mol Biol 17:567–579

    Article  PubMed  CAS  Google Scholar 

  • Heinekamp T, Strathmann A, Kuhlmann M, Froissard M, Muller A, Perrot-Rechenmann C, Droge-Laser W (2004) The tobacco bZIP transcription factor BZI-1 binds the GH3 promoter in vivo and modulates auxin-induced transcription. Plant J 38:298–309

    Article  PubMed  CAS  Google Scholar 

  • Hewett ER (2006) An overview of preharvest factors influencing postharvest quality of horticultural products. Int J Postharvest Technol Innov 1:4–15

    Article  Google Scholar 

  • Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res 27:297–300

    Article  PubMed  CAS  Google Scholar 

  • Jagadeeswaran G, Raina S, Acharya BR, Maqbool SB, Mosher SL, Appel HM, Schultz JC, Klessig DF, Raina R (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 

  • Jain M, Khurana JP (2009) Transcript profiling reveals diverse roles of auxin-responsive genes during reproductive development and abiotic stress in rice. FEBS J 276:3148–3162

    Article  PubMed  CAS  Google Scholar 

  • Jain M, Kaur N, Garg R, Thakur JK, Tyagi AK, Khurana JP (2006a) Structure and expression analysis of early auxin-responsive Aux/IAA gene family in rice (Oryza sativa). Funct Integr Genomics 6:47–59

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Jain M, Tyagi AK, Khurana JP (2006c) Genome-wide analysis, evolutionary expansion, and expression of early auxin-responsive SAUR gene family in rice (Oryza sativa). Genomics 88:360–371

    Article  PubMed  CAS  Google Scholar 

  • Khan S, Stone JM (2007a) Arabidopsis thaliana GH3.9 in auxin and jasmonate cross talk. Plant Signal Behav 2:483–485

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Kuang JF, Zhang Y, Chen JY, Chen QJ, Jiang YM, Lin HT, Xu SJ, Lu WJ (2011) Two GH3 genes from longan are differentially regulated during fruit growth and development. Gene 485:1–6

    Article  PubMed  CAS  Google Scholar 

  • Kumar R, Tyagi AK, Sharma AK (2011) Genome-wide analysis of auxin response factor (ARF) gene family from tomato and analysis of their role in flower and fruit development. Mol Genet Genomics 285:245–260

    Article  PubMed  CAS  Google Scholar 

  • Li Y, Liu ZB, Shi X, Hagen G, Guilfoyle TJ (1994) An auxin-inducible element in soybean SAUR promoters. Plant Physiol 106:37–43

    Article  PubMed  CAS  Google Scholar 

  • Liu K, Kang BC, Jiang H, Moore SL, Li H, Watkins CB, Setter TL, Jahn MM (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 (2011) Auxin conjugates: their role for plant development and in the evolution of land plants. J Exp Bot 62:1757–1773

    Article  PubMed  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 

  • Lynch M, Conery JS (2000) The evolutionary fate and consequences of duplicate genes. Science 290:1151–1155

    Article  PubMed  CAS  Google Scholar 

  • Mapelli S, Frova C, Torti G, Soressi GP (1978) Relationship between set, development and activities of growth regulators in tomato fruits. Plant Cell Physiol 19:1281–1288

    CAS  Google Scholar 

  • Matsui A, Ishida J, Morosawa T, Mochizuki Y, Kaminuma E, Endo TA, Okamoto M, Nambara E, Nakajima M, Kawashima M, Satou M, Kim JM, Kobayashi N, Toyoda T, Shinozaki K, Seki M (2008) Arabidopsis transcriptome analysis under drought, cold, high-salinity and ABA treatment conditions using a tiling array. Plant Cell Physiol 49:1135–1149

    Article  PubMed  CAS  Google Scholar 

  • Minglin L, Yuxiu Z, Tuanyao C (2005) Identification of genes up-regulated in response to Cd exposure in Brassica juncea L. Gene 363:151–158

    Article  PubMed  Google Scholar 

  • Mueller LA, Solow TH, Taylor N, Skwarecki B, Buels R, Binns J, Lin C, Wright MH, Ahrens R, Wang Y, Herbst EV, Keyder ER, Menda N, Zamir D, Tanksley SD (2005) The SOL Genomics Network: a comparative resource for Solanaceae biology and beyond. Plant Physiol 138:1310–1317

    Article  PubMed  CAS  Google Scholar 

  • Nakazawa M, Yabe N, Ichikawa T, Yamamoto YY, Yoshizumi T, Hasunuma K, Matsui M (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 

  • Nebenfuhr A, White TJ et al (2000) The diageotropica mutation alters auxin induction of a subset of the Aux/IAA gene family in tomato. Plant Mol Biol 44:73–84

    Article  PubMed  CAS  Google Scholar 

  • Nemhauser JL, Hong F, Chory J (2006) Different plant hormones regulate similar processes through largely nonoverlapping transcriptional responses. Cell 126:467–475

    Article  PubMed  CAS  Google Scholar 

  • Nobuta K, Okrent RA, Stoutemyer M, Rodibaugh N, Kempema L, Wildermuth MC, Innes RW (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, Wildermuth MC (2011) Evolutionary history of the GH3 family of acyl adenylases in rosids. Plant Mol Biol 76:489–505

    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 

  • Paponov IA, Paponov M, Teale W, Menges M, Chakrabortee S, Murray JA, Palme K (2008) Comprehensive transcriptome analysis of auxin responses in Arabidopsis. Mol Plant 1:321–337

    Article  PubMed  CAS  Google Scholar 

  • Park JE, Park JY, Kim YS, Staswick PE, Jeon J, Yun J, Kim SY, Kim J, Lee YH, Park CM (2007) GH3-mediated auxin homeostasis links growth regulation with stress adaptation response in Arabidopsis. J Biol Chem 282:10036–10046

    Article  PubMed  CAS  Google Scholar 

  • Rambaut A (2008) FigTree v1.1.1: Tree figure drawing tool. Available: http://tree.bio.ed.ac.uk/software/figtree/

  • Rampey RA, LeClere S, Kowalczyk M, Ljung K, Sandberg G, Bartel B (2004) A family of auxin-conjugate hydrolases that contributes to free indole-3-acetic acid levels during Arabidopsis germination. Plant Physiol 135:978–988

    Article  PubMed  CAS  Google Scholar 

  • Riemann M, Takano M (2008) Rice JASMONATE RESISTANT 1 is involved in phytochrome and jasmonate signalling. Plant Cell Environ 31:783–792

    Article  PubMed  CAS  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    PubMed  CAS  Google Scholar 

  • Sawa S, Ohgishi M, Goda H, Higuchi K, Shimada Y, Yoshida S, Koshiba T (2002) The HAT2 gene, a member of the HD-Zip gene family, isolated as an auxin inducible gene by DNA microarray screening, affects auxin response in Arabidopsis. Plant J 32:1011–1022

    Article  PubMed  CAS  Google Scholar 

  • Seo PJ, Park CM (2009) Auxin homeostasis during lateral root development under drought condition. Plant Signal Behav 4:1002–1004

    Article  PubMed  CAS  Google Scholar 

  • Sitbon F, Ostin A, Sundberg B, Olsson O, Sandberg G (1993) Conjugation of indole-3-acetic acid (IAA) in wild-type and IAA-overproducing transgenic tobacco plants, and identification of the main conjugates by frit-fast atom bombardment liquid chromatography-mass spectrometry. Plant Physiol 101:313–320

    PubMed  CAS  Google Scholar 

  • Staswick PE (2009) Plant hormone conjugation: a signal decision. Plant Signal Behav 4:757–759

    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, Maldonado MC, Suza W (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 

  • 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 

  • 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 

  • Thompson JD, Gibson TJ, Higgins DG (2002) Multiple sequence alignment using ClustalW and ClustalX. Curr Protoc Bioinforma (Chapter 2: Unit 2.3)

  • Tian CE, Muto H, Higuchi K, Matamura T, Tatematsu K, Koshiba T, Yamamoto KT (2004) Disruption and overexpression of auxin response factor 8 gene of Arabidopsis affect hypocotyl elongation and root growth habit, indicating its possible involvement in auxin homeostasis in light condition. Plant J 40:333–343

    Article  PubMed  CAS  Google Scholar 

  • Tiryaki I, Staswick PE (2002) An Arabidopsis mutant defective in jasmonate response is allelic to the auxin-signaling mutant axr1. Plant Physiol 130:887–894

    Article  PubMed  CAS  Google Scholar 

  • Ulmasov T, Liu ZB, Hagen G, Guilfoyle TJ (1995) Composite structure of auxin response elements. Plant Cell 7:1611–1623

    Article  PubMed  CAS  Google Scholar 

  • Wang S, Bai Y, Shen C, Wu Y, Zhang S, Jiang D, Guilfoyle TJ, Chen M, Qi Y (2010) Auxin-related gene families in abiotic stress response in Sorghum bicolor. Funct Integr Genomics 10:533–546

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Zhang Z, Li Q, Li Z, Staswick PE, Wang M, Zhu Y, He Z (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 SW, Li CH, Cao J, Zhang YC, Zhang SQ, Xia YF, Sun DY, Sun Y (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 

  • Zhao Y, Dai X, Blackwell HE, Schreiber SL, Chory J (2003) SIR1, an upstream component in auxin signaling identified by chemical genetics. Science 301:1107–1110

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was financially supported by grants received from the Department of Biotechnology, Government of India. RK and PA acknowledge CSIR and UGC, respectively, for the fellowship granted during their tenure as research fellows. Authors also acknowledge the Solanaceae Genomics Network as Tomato BAC Sequence and WGS (Sl2.40) Databases were used to retrieve putative promoter sequences.

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Correspondence to Arun K. Sharma.

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Communicated by S. Hohmann.

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Supplementary file S1: List of SlGH3 primers used for QPCR analysis.

Supplementary file S2: Protein sequences encoded by SlGH3 genes in tomato.

Supplementary file S3: Percentage identities among the SlGH3 proteins.

Supplementary file S4: Cis-element study of promoter architecture (2 kb upstream sequence from the start codon) of SlGH3 genes.

Supplementary file S5: Identification of SlGH3 orthologous genes from six Solanaceae species.

Supplementary file S6: Protein sequences encoded by SlGH3 orthologous genes from other Solanaceae members.

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Kumar, R., Agarwal, P., Tyagi, A.K. et al. Genome-wide investigation and expression analysis suggest diverse roles of auxin-responsive GH3 genes during development and response to different stimuli in tomato (Solanum lycopersicum). Mol Genet Genomics 287, 221–235 (2012). https://doi.org/10.1007/s00438-011-0672-6

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