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.
Similar content being viewed by others
References
Abel S, Theologies A (1996) Early genes and auxin action. Plant Physiol 111:9–17
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
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
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
de Jong M, Mariani C, Vriezen WH (2009a) The role of auxin and gibberellin in tomato fruit set. J Exp Bot 60:1523–1532
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
Dharmasiri N, Dharmasiri S, Estelle M (2005) The F-box protein TIR1 is an auxin receptor. Nature 435:441–445
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
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
Gillaspy G, Ben-David H, Gruissem W (1993) Fruits: a developmental perspective. Plant Cell 5:1439–1451
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
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
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
Guilfoyle TJ, Hagen G (2001) Auxin response factors. J Plant Growth Regul 10:281–291
Guilfoyle TJ, Hagen G (2007) Auxin response factors. Curr Opin Plant Biol 10:453–460
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
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
Gustafson FG (1936) Inducement of fruit development by growth promoting chemicals. Proc Natl Acad Sci USA 22:628–636
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
Hagen G, Guilfoyle T (2002) Auxin-responsive gene expression: genes, promoters and regulatory factors. Plant Mol Biol 49:373–385
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
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
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
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
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
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
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
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
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
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
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
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
Lynch M, Conery JS (2000) The evolutionary fate and consequences of duplicate genes. Science 290:1151–1155
Lynch M, Force A (2000) The probability of duplicate gene preservation by subfunctionalization. Genetics 154:459–473
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
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
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
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
Ouellet F, Overvoorde PJ, Theologis A (2001) IAA17/AXR3: biochemical insight into an auxin mutant phenotype. Plant Cell 13:829–841
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
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
Robinson R, Tomes M (1968) Ripening inhibitor: a gene with multiple effects on ripening. Rep Tomato Genet Coop 18:36–37
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
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
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
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
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
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
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
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
Tigchelaar E, McGlasson W, Buescher R (1978) Genetic regulation of tomato fruit ripening. Hort Sci 13:508–513
Tiwari SB, Hagen G, Guilfoyle T (2003) The roles of auxin response factor domains in auxin-responsive transcription. Plant Cell 15:533–543
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
Ulmasov T, Hagen G, Guilfoyle TJ (1997) ARF1, a transcription factor that binds to auxin response elements. Science 276:1865–1868
Ulmasov T, Hagen G, Guilfoyle TJ (1999a) Dimerization and DNA binding of auxin response factors. Plant J 19:309–319
Ulmasov T, Hagen G, Guilfoyle TJ (1999b) Activation and repression of transcription by auxin-response factors. Proc Natl Acad Sci USA 96:5844–5849
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
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
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
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
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
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
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
Authors and Affiliations
Corresponding author
Additional information
Communicated by A. Schnittger.
Electronic supplementary material
Below is the link to the electronic supplementary material.
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)
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
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00438-011-0602-7