Skip to main content

Genome-wide analysis of auxin response factor (ARF) gene family from tomato and analysis of their role in flower and fruit development

Molecular Genetics and Genomics volume 285, pages 245–260 (2011)Cite this article

Abstract

Auxin response transcription factors have been widely implicated in auxin-mediated responses during various developmental processes ranging from root and shoot development to flower and fruit development in plants. In order to use them for improvement of agronomic traits related to fruit, we need to have better understanding of their role during fruit development. In this study, 17 SlARF genes have been identified from tomato (Solanum lycopersicum), using various publically available tomato EST databases. Phylogenetic analysis of the 23 AtARF and 17 SlARF proteins results in formation of three major classes and a total of 14 sister pairs, including seven SlARF–AtARF, four SlARF–SlARF and three AtARF–AtARF sister pairs, providing insights into various orthologous relationships between AtARFs and SlARFs. Further, search for orthologs of these SlARFs resulted in identification of nine, ten, four and three ARF genes from potato, tobacco, N. benthemiana and pepper, respectively. A phylogenetic analysis of these genes, along with their orthologs from Solanaceae species, suggests the presence of a common set of the ARF genes in this family. Comparison of the expression of these SlARF genes in wild type and rin mutant provides an insight into their role during different stages of flower and fruit development. This study suggests that ARF genes may play diverse role during flower and fruit development. Comprehensive data generated here will provide a platform for identification of ARF genes and elucidation of their function during reproductive development stages in Solanaceae in general and fruit development in tomato, in particular.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

References

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

    CAS  Article  PubMed  Google Scholar 

  • Arora R, Agarwal P, Ray S, Singh AK, Singh VP, Tyagi AK, Kapoor S (2007) MADS-box gene family in rice: genome-wide identification, organization and expression profiling during reproductive development and stress. BMC Genomics 8:1–21

    Article  Google Scholar 

  • Bailey TL, Elkan C (1994) Fitting a mixture model by expectation maximization to discover motifs in biopolymers. In: Proceedings of the second international conference on intelligent systems for molecular biology, AAAI Press, pp 28–36

  • Catoni M, Miozzi L, Fiorilli V, Lanfranco L, Accotto GP (2009) Comparative analysis of expression profiles in shoots and roots of tomato systemically infected by Tomato spotted wilt virus reveals organ-specific transcriptional responses. Mol Plant Microbe Interact 22:1504–1513

    CAS  Article  PubMed  Google Scholar 

  • de Bodt S, Raes J, Florquin K, Rombauts S, Rouze P, Theissen G, Van de Peer Y (2003) Genome wide structural annotation and evolutionary analysis of the type I MADS-box genes in plants. J Mol Evol 56:573–586

    Article  PubMed  Google Scholar 

  • de Jong M, Mariani C, Vriezen WH (2009a) The role of auxin and gibberellin in tomato fruit set. J Exp Bot 60:1523–1532

    Article  PubMed  Google Scholar 

  • de Jong M, Wolters-Arts M, Feron R, Mariani C, Vriezen WH (2009b) The Solanum lycopersicum auxin response factor 7 (SlARF7) regulates auxin signaling during tomato fruit set and development. Plant J 57:160–170

    Article  PubMed  Google Scholar 

  • Dharmasiri N, Dharmasiri S, Estelle M (2005) The F-box protein TIR1 is an auxin receptor. Nature 435:441–445

    CAS  Article  PubMed  Google Scholar 

  • Ellis CM, Nagpal P, Young JC, Hagen G, Guilfoyle TJ, Reed JW (2005) Auxin Response Factor 1 and Auxin Response Factor 2 regulate senescence and floral organ abscission in Arabidopsis thaliana. Development 132:4563–4574

    CAS  Article  PubMed  Google Scholar 

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

    CAS  Article  PubMed  Google Scholar 

  • Gillaspy G, Ben-David H, Gruissem W (1993) Fruits: a developmental perspective. Plant Cell 5:1439–1451

    Article  PubMed  Google Scholar 

  • Goetz M, Hooper LC, Johnson SD, Rodrigues JC, Vivian-Smith A, Koltunow AM (2007) Expression of aberrant forms of auxin response factor 8 stimulates parthenocarpy in Arabidopsis and tomato. Plant Physiol 145:351–366

    CAS  Article  PubMed  Google Scholar 

  • Goff SA, Ricke D, Lan TH, Presting G, Wang R, Dunn M, Glazebrook J, Sessions A, Oeller P, Varma H, Hadley D, Hutchison D, Martin C, Katagiri F, Lange BM, Moughamer T, Xia Y, Budworth P, Zhong J, Miguel T, Paszkowski U, Zhang S, Colbert M, Sun WL, Chen L, Cooper B, Park S, Wood TC, Mao L, Quail P, Wing R, Dean R, Yu Y, Zharkikh A, Shen R, Sahasrabudhe S, Thomas A, Cannings R, Gutin A, Pruss D, Reid J, Tavtigian S, Mitchell J, Eldredge G, Scholl T, Miller RM, Bhatnagar S, Adey N, Rubano T, Tusneem N, Robinson R, Feldhaus J, Macalma T, Oliphant A, Briggs S (2002) A draft sequence of the rice genome (Oryza sativa Lssp. japonica). Science 296:92–100

    CAS  Article  PubMed  Google Scholar 

  • Gorguet B, Eggink PM, Ocana J, Tiwari A, Schipper D, Finkers R, Visser RG, van Heusden AW (2008) Mapping and characterization of novel parthenocarpy QTLs in tomato. Theor Appl Genet 116:755–767

    Article  PubMed  Google Scholar 

  • Guilfoyle TJ, Hagen G (2001) Auxin response factors. J Plant Growth Regul 10:281–291

    Article  Google Scholar 

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

    CAS  Article  PubMed  Google Scholar 

  • Guilfoyle TJ, Ulmasov T, Hagen G (1998) The ARF family of transcription factors and their role in plant hormone-responsive transcription. Cell Mol Life Sci 54:619–627

    CAS  Article  PubMed  Google Scholar 

  • Guillon F, Philippe S, Bouchet B, Devaux MF, Frasse P, Jones B, Bouzayen M, Lahaye M (2008) Down-regulation of an Auxin Response Factor in the tomato induces modification of fine pectin structure and tissue architecture. J Exp Bot 59:273–288

    CAS  Article  PubMed  Google Scholar 

  • Gustafson FG (1936) Inducement of fruit development by growth promoting chemicals. Proc Natl Acad Sci USA 22:628–636

    CAS  Article  PubMed  Google Scholar 

  • Gutierrez L, Bussell JD, Pacurar DI, Schwambach J, Pacurar M, Bellini C (2009) Phenotypic plasticity of adventitious rooting in Arabidopsis is controlled by complex regulation of auxin response factor transcripts and microRNA abundance. Plant Cell 21:3119–3132

    CAS  Article  PubMed  Google Scholar 

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

    CAS  Article  PubMed  Google Scholar 

  • Hardtke CS, Ckurshumova W, Vidaurre DP, Singh SA, Stamatiou G, Tiwari SB, Hagen G, Guilfoyle TJ, Berleth T (2004) Overlapping and non-redundant functions of the Arabidopsis auxin response factors Monopteros and Nonphoto Hypocotyl 4. Development 131:1089–1100

    CAS  Article  PubMed  Google Scholar 

  • Harper RM, Stowe-Evans EL, Luesse DR, Muto H, Tatematsu K, Watahiki MK, Yamamoto K, Liscum E (2000) The NPH4 locus encodes the auxin response factor ARF7, a conditional regulator of differential growth in aerial Arabidopsis tissue. Plant Cell 12:757–770

    CAS  Article  PubMed  Google Scholar 

  • Ito Y, Kitagawa M, Ihashi N, Yabe K, Kimbara J, Yasuda J, Ito H, Inakuma T, Hiroi S, Kasumi T (2008) DNA-binding specificity, transcriptional activation potential, and the rin mutation effect for the tomato fruit-ripening regulator RIN. Plant J 55:212–223

    CAS  Article  PubMed  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

    CAS  Article  PubMed  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

    CAS  Article  PubMed  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

    CAS  Article  PubMed  Google Scholar 

  • Jones B, Frasse P, Olmos E, Zegzouti H, Li ZG, Latche A, Pech JC, Bouzayen M (2002) Down-regulation of DR12, an auxin-response-factor homolog, in the tomato results in a pleiotropic phenotype including dark green and blotchy ripening fruit. Plant J 32:603–613

    CAS  Article  PubMed  Google Scholar 

  • Kalluri UC, Difazio SP, Brunner AM, Tuskan GA (2007) Genome-wide analysis of Aux/IAA and ARF gene families in Populus trichocarpa. BMC Plant Biol 7:1–14

    Article  Google Scholar 

  • Kaufmann K, Muino JM, Jauregui R, Airoldi CA, Smaczniak C, Krajewski P, Angenent GC (2009) Target genes of the MADS transcription factor SEPALLATA3: integration of developmental and hormonal pathways in the Arabidopsis flower. PLoS Biol 7:854–875

    CAS  Article  Google Scholar 

  • Knapp J, Moureau P, Schuch W, Grierson D (1989) Organization and expression of polygalacturonase and other ripening genes in Ailsa Craig ‘Neverripe ‘and ‘ripening inhibitor’ tomato mutants. Plant Mol Biol 12:105–116

    CAS  Article  Google Scholar 

  • Lemaire-Chamley M, Petit J, Garcia V, Just D, Baldet P, Germain V, Fagard M, Mouassite M, Cheniclet C, Rothan C (2005) Changes in transcriptional profiles are associated with early fruit tissue specialization in tomato. Plant Physiol 139:750–769

    CAS  Article  PubMed  Google Scholar 

  • Li J, Dai X, Zhao Y (2006) A role for auxin response factor 19 in auxin and ethylene signaling in Arabidopsis. Plant Physiol 140:899–908

    CAS  Article  PubMed  Google Scholar 

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

    CAS  Article  PubMed  Google Scholar 

  • Lynch M, Force A (2000) The probability of duplicate gene preservation by subfunctionalization. Genetics 154:459–473

    CAS  PubMed  Google Scholar 

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

    CAS  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

    CAS  Article  PubMed  Google Scholar 

  • Nagpal P, Ellis CM, Weber H, Ploense SE, Barkawi LS, Guilfoyle TJ, Hagen G, Alonso JM, Cohen JD, Farmer EE, Ecker JR, Reed JW (2005) Auxin response factors ARF6 and ARF8 promote jasmonic acid production and flower maturation. Development 132:4107–4118

    CAS  Article  PubMed  Google Scholar 

  • Okushima Y, Overvoorde PJ, Arima K, Alonso JM, Chan A, Chang C, Ecker JR, Hughes B, Lui A, Nguyen D, Onodera C, Quach H, Smith A, Yu G, Theologis A (2005) Functional genomic analysis of the auxin response factor gene family members in Arabidopsis thaliana: unique and overlapping functions of ARF7 and ARF19. Plant Cell 17:444–463

    CAS  Article  PubMed  Google Scholar 

  • Ouellet F, Overvoorde PJ, Theologis A (2001) IAA17/AXR3: biochemical insight into an auxin mutant phenotype. Plant Cell 13:829–841

    CAS  Article  PubMed  Google Scholar 

  • Raes J, Vandepoele K, Simillion C, Saeys Y, Van de Peer Y (2003) Investigating ancient duplication events in the Arabidopsis genome. J Struct Funct Genomics 3:117–129

    CAS  Article  PubMed  Google Scholar 

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

  • Reymond P, Weber H, Damond M, Farmer EE (2000) Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis. Plant Cell 12:707–720

    CAS  Article  PubMed  Google Scholar 

  • Robinson R, Tomes M (1968) Ripening inhibitor: a gene with multiple effects on ripening. Rep Tomato Genet Coop 18:36–37

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Schlereth A, Moller B, Liu W, Kientz M, Flipse J, Rademacher EH, Schmid M, Jurgens G, Weijers D (2010) Monopteros controls embryonic root initiation by regulating a mobile transcription factor. Nature 464:913–916

    CAS  Article  PubMed  Google Scholar 

  • Schruff MC, Spielman M, Tiwari S, Adams S, Fenby N, Scott RJ (2006) The auxin response factor 2 gene of Arabidopsis links auxin signalling, cell division, and the size of seeds and other organs. Development 133:251–261

    CAS  Article  PubMed  Google Scholar 

  • Serrani JC, Fos M, Atares A, Garcia-Martinez JL (2007) Effect of gibberellin and auxin on parthenocarpic fruit growth induction in the cv MicroTom of tomato. J Plant Growth Regul 26:211–221

    CAS  Article  Google Scholar 

  • Sessions A, Nemhauser JL, McColl A, Roe JL, Feldmann KA, Zambryski PC (1997) ETTIN patterns the Arabidopsis floral meristem and reproductive organs. Development 124:4481–4491

    CAS  PubMed  Google Scholar 

  • Simillion C, Vandepoele K, Van Montagu MC, Zabeau M, Van de Peer Y (2002) The hidden duplication past of Arabidopsis thaliana. Proc Natl Acad Sci USA 99:13627–13632

    CAS  Article  PubMed  Google Scholar 

  • Solanke AU, Sharma MK, Tyagi AK, Sharma AK (2009) Characterization and phylogenetic analysis of environmental stress-responsive SAP gene family encoding A20/AN1 zinc finger proteins in tomato. Mol Genet Genomics 282:153–164

    CAS  Article  PubMed  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    CAS  Article  PubMed  Google Scholar 

  • Tigchelaar E, McGlasson W, Buescher R (1978) Genetic regulation of tomato fruit ripening. Hort Sci 13:508–513

    CAS  Google Scholar 

  • Tiwari SB, Hagen G, Guilfoyle T (2003) The roles of auxin response factor domains in auxin-responsive transcription. Plant Cell 15:533–543

    CAS  Article  PubMed  Google Scholar 

  • Todd AT, Liu E, Polvi SL, Pammett RT, Page JE (2010) A functional genomics screen identifies diverse transcription factors that regulate alkaloid biosynthesis in Nicotiana benthamiana. Plant J 62:589–600

    CAS  Article  PubMed  Google Scholar 

  • Ulmasov T, Hagen G, Guilfoyle TJ (1997) ARF1, a transcription factor that binds to auxin response elements. Science 276:1865–1868

    CAS  Article  PubMed  Google Scholar 

  • Ulmasov T, Hagen G, Guilfoyle TJ (1999a) Dimerization and DNA binding of auxin response factors. Plant J 19:309–319

    CAS  Article  PubMed  Google Scholar 

  • Ulmasov T, Hagen G, Guilfoyle TJ (1999b) Activation and repression of transcription by auxin-response factors. Proc Natl Acad Sci USA 96:5844–5849

    CAS  Article  PubMed  Google Scholar 

  • Vrebalov J, Ruezinsky D, Padmanabhan V, White R, Medrano D, Drake R, Schuch W, Giovannoni J (2002) A MADS-box gene necessary for fruit ripening at the tomato ripening-inhibitor (rin) locus. Science 296:343–346

    CAS  Article  PubMed  Google Scholar 

  • Vriezen WH, Feron R, Maretto F, Keijman J, Mariani C (2008) Changes in tomato ovary transcriptome demonstrate complex hormonal regulation of fruit set. New Phytol 17:60–76

    Google Scholar 

  • Wang H, Jones B, Li Z, Frasse P, Delalande C, Regad F, Chaabouni S, Latche A, Pech JC, Bouzayen M (2005) The tomato Aux/IAA transcription factor IAA9 is involved in fruit development and leaf morphogenesis. Plant Cell 17:2676–2692

    CAS  Article  PubMed  Google Scholar 

  • Wang D, Pei K, Fu Y, Sun Z, Li S, Liu H, Tang K, Han B, Tao Y (2007) Genome-wide analysis of the auxin response factors (ARF) gene family in rice (Oryza sativa). Gene 394:13–24

    CAS  Article  PubMed  Google Scholar 

  • Wang H, Schauer N, Usadel B, Frasse P, Zouine M, Hernould M, Latche A, Pech JC, Fernie AR, Bouzayen M (2009) Regulatory features underlying pollination-dependent and independent tomato fruit set revealed by transcript and primary metabolite profiling. Plant Cell 21:1428–1452

    CAS  Article  PubMed  Google Scholar 

  • Wilmoth JC, Wang S, Tiwari SB, Joshi AD, Hagen G, Guilfoyle TJ, Alonso JM, Ecker JR, Reed JW (2005) NPH4/ARF7 and ARF19 promote leaf expansion and auxin-induced lateral root formation. Plant J 43:118–130

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was financially supported by grants received from the Department of Biotechnology, Government of India. RK acknowledges CSIR for the fellowship granted during his tenure as a research fellow. Authors also acknowledge use of the draft tomato genome sequence, which was generated by the International Tomato Genome Sequencing Consortium (http://solgenomics.net/tomato/).

Author information

Affiliations

  1. Department of Plant Molecular Biology, University of Delhi South Campus, New Delhi, 110021, India

    Rahul Kumar, Akhilesh K. Tyagi & Arun K. Sharma

  2. National Institute of Plant Genome Research, New Delhi, 110067, India

    Akhilesh K. Tyagi

Authors
  1. Rahul Kumar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Akhilesh K. Tyagi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Arun K. Sharma
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Arun K. Sharma.

Additional information

Communicated by A. Schnittger.

Electronic supplementary material

Below is the link to the electronic supplementary material.

List of primers used for QPCR analysis (XLSX 10 kb)

Amino acid sequence comparison between the predicted full-length auxin response factor (SlARF) genes (XLS 32 kb)

438_2011_602_MOESM3_ESM.doc

Multiple alignment profile of full SlARF proteins obtained with the ClustalX program. All the sequences show high level of amino acids conservation. Gaps (marked with dashes) have been introduced to maximize the alignments (DOC 1074 kb)

Protein sequences of ARF family genes in tomato and other Solanaceae members (DOC 54 kb)

438_2011_602_MOESM5_ESM.xls

Summary and taxonomic hierarchy of conserved motifs identified from SlARF proteins. MEME Suite version 4.0.0 (Optimum width 6-200 AA; Any number of repetitions; Maximum number of motifs 25) was used to identify conserved motifs in SlARFs. BLAST search was performed in NCBI database, using conserved motif sequences as probes, to find homologous sequences from other plants and non-plant organisms to study taxonomic hierarchy of these motifs. Comparison of motifs in other orthologous ARF proteins of Arabidopsis and other Solanaceae members has also been represented (XLS 155 kb)

438_2011_602_MOESM6_ESM.ppt

Phylogenetic analysis of tomato ARF proteins. The unrooted tree was generated using the ClustalX program by neighbor-joining method and viewed in FigTree v1.2.2. Scale bar represents 0.1 amino acid substitutions per site (PPT 105 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Kumar, R., Tyagi, A.K. & Sharma, A.K. 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 (2011). https://doi.org/10.1007/s00438-011-0602-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-011-0602-7

Keywords

  • ARF gene
  • Auxin
  • Phylogenetic analysis
  • QPCR
  • rin Mutant
  • Solanaceae
  • Tomato