Skip to main content
SpringerLink
Log in

Transcriptome analysis of rin mutant fruit and in silico analysis of promoters of differentially regulated genes provides insight into LeMADS-RIN-regulated ethylene-dependent as well as ethylene-independent aspects of ripening in tomato

  • Original Paper
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

A thorough understanding of molecular mechanisms underlying ripening is the prerequisite for genetic manipulation of fruits for better shelf-life and nutritional quality. Mutation in LeMADS-RIN, a MADS-box gene, leads to non-ripening phenotype of rin fruits in tomato. Characterization of ripening-inhibitor (rin) mutant has elucidated important role of ethylene in the regulation of climacteric fruit ripening. A complete understanding of this mutation will unravel novel genetic regulatory mechanisms involved in fruit ripening. In this study, fruit transcriptomes of two genotypes, including a cultivated Indian cultivar Solanum lycopersicum cv. Pusa Ruby and a homozygous line harboring the rin mutation (LA1795) were compared to get better insight into RIN-regulated ethylene-dependent and ethylene-independent events during ripening. Cluster analysis of ripening-related genes indicated a major shift in their expression profiles in rin mutant fruit. A total of 112 genes, exhibiting expression patterns similar to that of LeMADS-RIN in wild-type fruits, showed down regulation of expression in the rin mutant. In silico analysis of putative promoters of these genes for the presence of CArG box along with ERE and ethylene inducibility of these genes revealed that genes lacking CArG box in their regulatory regions could be indirectly regulated by LeMADS-RIN. New regulators of ethylene-dependent aspect of ripening were also identified. In this study, we have made an attempt to distinguish between ethylene-dependent and ethylene-independent aspects of ripening, which will be useful for developing strategies to improve fruit-related agronomic traits in tomato and other crops.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Alba R, Payton P, Fei Z, McQuinn R, Debbie P, Martin GB, Tanksley SD, Giovannoni JJ (2005) Transcriptome and selected metabolite analyses reveal multiple points of ethylene control during tomato fruit development. Plant Cell 17:2954–2965

    Article  PubMed  CAS  Google Scholar 

  • Anjanasree KN, Srivastava A, Handa A, Bansal KC (2005) Identification of differentially expressed ripening-related cDNA clones from tomato (Lycopersicon esculentum) using tomato EST array. Curr Sci 88:792–796

    CAS  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 8:242

    Article  PubMed  Google Scholar 

  • Barry C, Giovannoni JJ (2007) Ethylene and fruit ripening. J Plant Growth Regul 26:143–159

    Article  CAS  Google Scholar 

  • Barry CS, Blume B, Bouzayen M, Cooper W, Hamilton AJ, Grierson D (1996) Differential expression of the 1-aminocyclopropane-1-carboxylate oxidase gene family of tomato. Plant J 9:525–535

    Article  PubMed  CAS  Google Scholar 

  • Barry CS, Llop-Tous MI, Grierson D (2000) The regulation of 1-aminocyclopropane-1-carboxylic acid synthase gene expression during the transition from system-1 to system-2 ethylene synthesis in tomato. Plant Physiol 123:979–986

    Article  PubMed  CAS  Google Scholar 

  • Busi MV, Bustamante C, D’Angelo C, Hidalgo-Cuevas M, Boggio SB, Valle EM, Zabaleta E (2003) MADS-box genes expressed during tomato seed and fruit development. Plant Mol Biol 52:801–815

    Article  PubMed  CAS  Google Scholar 

  • Carrari F, Fernie AR (2006) Metabolic regulation underlying tomato fruit development. J Exp Bot 57:1883–1897

    Article  PubMed  CAS  Google Scholar 

  • Causier B, Kieffer M, Davies B (2002) MADS-Box genes reach maturity. Science 296:275–276

    Article  PubMed  CAS  Google Scholar 

  • Chen G, Hu Z, Grierson D (2008) Differential regulation of tomato ethylene responsive factor LeERF3b, a putative repressor, and the activator Pti4 in ripening mutants and in response to environmental stresses. J Plant Physiol 165:662–670

    Article  PubMed  CAS  Google Scholar 

  • Chung MY, Vrebalov J, Alba R, Lee J, McQuinn R, Chung JD, Klein P, Giovannoni J (2010) A tomato (Solanum lycopersicum) APETALA2/ERF gene, SlAP2a, is a negative regulator of fruit ripening. Plant J 64:936–947

    Article  PubMed  CAS  Google Scholar 

  • Coen ES, Meyerowitz EM (1991) The war of the whorls: genetic interactions controlling flower development. Nature 353:31–37

    Article  PubMed  CAS  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 

  • Dellapenna D, Kates DS, Bennett AB (1987) Polygalacturonase gene expression in Rutgers, rin, nor, and Nr tomato fruits. Plant Physiol 85:502–507

    Article  PubMed  CAS  Google Scholar 

  • Dellapenna D, Lincoln JE, Fischer RL, Bennett AB (1989) Transcriptional analysis of Polygalacturonase and other ripening-associated genes in Rutgers, rin, nor, and Nr tomato fruit. Plant Physiol 90:1372–1377

    Article  PubMed  CAS  Google Scholar 

  • Dellapenna D, Lashbrook CC, Toenjes K, Giovannoni JJ, Fischer RL, Bennett AB (1990) Polygalacturonase isozymes and pectin depolymerization in transgenic rin tomato fruit. Plant Physiol 94:1882–1886

    Article  PubMed  CAS  Google Scholar 

  • Eriksson EM, Bovy A, Manning K, Harrison L, Andrews J, De Silva J, Tucker GA, Seymour GB (2004) Effect of the Colorless non-ripening mutation on cell wall biochemistry and gene expression during tomato fruit development and ripening. Plant Physiol 136:4184–4197

    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 

  • Fraser PD, Truesdale MR, Bird CR, Schuch W, Bramley PM (1994) Carotenoid biosynthesis during tomato fruit development (evidence for tissue-specific gene expression). Plant Physiol 105:405–413

    PubMed  CAS  Google Scholar 

  • Fujisawa M, Nakano T, Ito Y (2011) Identification of potential target genes for the tomato fruit-ripening regulator RIN by chromatin immunoprecipitation. BMC Plant Biol 11:26

    Article  PubMed  CAS  Google Scholar 

  • Giovannoni J (2001) Molecular biology of fruit maturation and ripening. Annu Rev Plant Physiol Plant Mol Biol 52:725–749

    Article  PubMed  CAS  Google Scholar 

  • Giovannoni JJ (2004) Genetic regulation of fruit development and ripening. Plant Cell 16(Suppl):S170–S180

    Article  PubMed  CAS  Google Scholar 

  • Giuliano G, Bartley GE, Scolnik PA (1993) Regulation of carotenoid biosynthesis during tomato development. Plant Cell 5:379–387

    Article  PubMed  CAS  Google Scholar 

  • Griffiths A, Barry C, Alpuche-Solis A, Grierson D (1999) Ethylene and developmental signals regulate expression of lipoxygenase genes during tomato fruit ripening. J Exp Bot 50:793–798

    Article  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Guo X, Chen J, Brackett RE, Beuchat LR (2001) Survival of salmonellae on and in tomato plants from the time of inoculation at flowering and early stages of fruit development through fruit ripening. Appl Environ Microbiol 67:4760–4764

    Article  PubMed  CAS  Google Scholar 

  • Gupta V, Mathur S, Solanke AU, Sharma MK, Kumar R, Vyas S, Khurana P, Khurana JP, Tyagi AK, Sharma AK (2009) Genome analysis and genetic enhancement of tomato. Crit Rev Biotechnol 29:152–181

    Article  PubMed  CAS  Google Scholar 

  • Herner RC, Sink KC (1973) Ethylene production and respiratory behavior of the rin tomato mutant. Plant Physiol 52:38–42

    Article  PubMed  CAS  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 

  • Hileman LC, Sundstrom JF, Litt A, Chen M, Shumba T, Irish VF (2006) Molecular and phylogenetic analyses of the MADS-box gene family in tomato. Mol Biol Evol 23:2245–2258

    Article  PubMed  CAS  Google Scholar 

  • Itkin M, Seybold H, Breitel D, Rogachev I, Meir S, Aharoni A (2009) The TOMATO AGAMOUS-LIKE 1 is a component of the fruit ripening regulatory network. Plant J 60:1081–1095

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Janssen BJ, Thodey K, Schaffer RJ, Alba R, Balakrishnan L, Bishop R, Bowen JH, Crowhurst RN, Gleave AP, Ledger S, McArtney S, Pichler FB, Snowden KC, Ward S (2008) Global gene expression analysis of apple fruit development from the floral bud to ripe fruit. BMC Plant Biol 8:16

    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

    Article  PubMed  CAS  Google Scholar 

  • Karlova R, Rosin FM, Busscher-Lange J, Parapunova V, Do PT, Fernie AR, Fraser PD, Baxter C, Angenent GC, de Maagd RA (2010) Transcriptome and metabolite profiling show that APETALA2a is a major regulator of tomato fruit ripening. Plant Cell 23:923–941

    Article  Google Scholar 

  • Katz YS, Galili G, Amir R (2006) Regulatory role of cystathionine-gamma-synthase and de novo synthesis of methionine in ethylene production during tomato fruit ripening. Plant Mol Biol 61:255–268

    Article  PubMed  CAS  Google Scholar 

  • Klee HJ (2002) Control of ethylene-mediated processes in tomato at the level of receptors. J Exp Bot 53:2057–2063

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Kok EJ, Franssen-van Hal NL, Winnubst LN, Kramer EH, Dijksma WT, Kuiper HA, Keijer J (2007) Assessment of representational difference analysis (RDA) to construct informative cDNA microarrays for gene expression analysis of species with limited transcriptome information, using red and green tomatoes as a model. J Plant Physiol 164:337–349

    Article  PubMed  CAS  Google Scholar 

  • Kolotilin I, Koltai H, Tadmor Y, Bar-Or C, Reuveni M, Meir A, Nahon S, Shlomo H, Chen L, Levin I (2007) Transcriptional profiling of high pigment −2dg tomato mutant links early fruit plastid biogenesis with its overproduction of phytonutrients. Plant Physiol 145:389–401

    Article  PubMed  CAS  Google Scholar 

  • Kumar R, Tyagi AK, Sharma AK (2010) 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  Google Scholar 

  • Lanahan MB, Yen HC, Giovannoni JJ, Klee HJ (1994) The never ripe mutation blocks ethylene perception in tomato. Plant Cell 6:521–530

    Article  PubMed  CAS  Google Scholar 

  • Lashbrook CC, Gonzalez-Bosch C, Bennett AB (1994) Two divergent endo-beta-1, 4-glucanase genes exhibit overlapping expression in ripening fruit and abscising flowers. Plant Cell 6:1485–1493

    Article  PubMed  CAS  Google Scholar 

  • Lelievre JM, Tichit L, Dao P, Fillion L, Nam YW, Pech JC, Latche A (1997) Effects of chilling on the expression of ethylene biosynthetic genes in Passe-Crassane pear (Pyrus communis L.) fruits. Plant Mol Biol 33:847–855

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Lenka SK, Lohia B, Kumar A, Chinnusamy V, Bansal KC (2009) Genome-wide targeted prediction of ABA responsive genes in rice based on over-represented cis-motif in co-expressed genes. Plant Mol Biol 69:261–271

    Article  PubMed  CAS  Google Scholar 

  • Leseberg CH, Eissler CL, Wang X, Johns MA, Duvall MR, Mao L (2008) Interaction study of MADS-domain proteins in tomato. J Exp Bot 59:2253–2265

    Article  PubMed  CAS  Google Scholar 

  • Li Y, Zhu B, Xu W, Zhu H, Chen A, Xie Y, Shao Y, Luo Y (2007) LeERF1 positively modulated ethylene triple response on etiolated seedling, plant development and fruit ripening and softening in tomato. Plant Cell Rep 26:1999–2008

    Article  PubMed  CAS  Google Scholar 

  • Li L, Zhu B, Fu D, Luo Y (2011a) RIN transcription factor plays an important role in ethylene biosynthesis of tomato fruit ripening. J Sci Food Agric 91:2308–2314

    Article  PubMed  CAS  Google Scholar 

  • Li L, Zhu B, Yang P, Fu D, Zhu Y, Luo Y (2011b) The regulation mode of RIN transcription factor involved in ethylene biosynthesis in tomato fruit. J Sci Food Agric 91:1822–1828

    Article  PubMed  CAS  Google Scholar 

  • Lin Z, Hong Y, Yin M, Li C, Zhang K, Grierson D (2008) A tomato HD-Zip homeobox protein, LeHB-1, plays an important role in floral organogenesis and ripening. Plant J 55:301–310

    Article  PubMed  CAS  Google Scholar 

  • Lincoln JE, Fischer RL (1988) Regulation of gene expression by ethylene in wild-type and rin tomato (Lycopersicon esculentum) fruit. Plant Physiol 88:370–374

    Article  PubMed  CAS  Google Scholar 

  • Lincoln JE, Cordes S, Read E, Fischer RL (1987) Regulation of gene expression by ethylene during Lycopersicon esculentum (tomato) fruit development. Proc Natl Acad Sci USA 84:2793–2797

    Article  PubMed  CAS  Google Scholar 

  • Lincoln JE, Campbell AD, Oetiker J, Rottmann WH, Oeller PW, Shen NF, Theologis A (1993) Le-ACS4, a fruit ripening and wound-induced 1-aminocyclopropane-1-carboxylate synthase gene of tomato (Lycopersicon esculentum). Expression in Escherichia coli, structural characterization, expression characteristics, and phylogenetic analysis. J Biol Chem 268:19422–19430

    PubMed  CAS  Google Scholar 

  • Lois LM, Rodriguez-Concepcion M, Gallego F, Campos N, Boronat A (2000) Carotenoid biosynthesis during tomato fruit development: regulatory role of 1-deoxy-d-xylulose 5-phosphate synthase. Plant J 22:503–513

    Article  PubMed  CAS  Google Scholar 

  • Manning K, Tor M, Poole M, Hong Y, Thompson AJ, King GJ, Giovannoni JJ, Seymour GB (2006) A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening. Nat Genet 38:948–952

    Article  PubMed  CAS  Google Scholar 

  • Martel C, Vrebalov J, Giovannoni JJ (2011) The tomato (Solanum lycopersicum) MADS-box transcription factor RIN interacts with promoters involved in numerous ripening processes in a CNR dependent manner. Plant Physiol. doi:10.1104/pp.111.181107

  • Martin MN, Saftner RA (1995) Purification and Characterization of 1-aminocyclopropane-1-carboxylic acid N-malonyltransferase from tomato fruit. Plant Physiol 108:1241–1249

    PubMed  CAS  Google Scholar 

  • Meli VS, Ghosh S, Prabha TN, Chakraborty N, Chakraborty S, Datta A (2010) Enhancement of fruit shelf life by suppressing N-glycan processing enzymes. Proc Natl Acad Sci USA 107:2413–2418

    Article  PubMed  CAS  Google Scholar 

  • Mintz-Oron S, Mandel T, Rogachev I, Feldberg L, Lotan O, Yativ M, Wang Z, Jetter R, Venger I, Adato A, Aharoni A (2008) Gene expression and metabolism in tomato fruit surface tissues. Plant Physiol 147:823–851

    Article  PubMed  CAS  Google Scholar 

  • Mounet F, Moing A, Garcia V, Petit J, Maucourt M, Deborde C, Bernillon S, Le Gall G, Colquhoun I, Defernez M, Giraudel JL, Rolin D, Rothan C, Lemaire-Chamley M (2009) Gene and metabolite regulatory network analysis of early developing fruit tissues highlights new candidate genes for the control of tomato fruit composition and development. Plant Physiol 149:1505–1528

    Article  PubMed  CAS  Google Scholar 

  • Nakatsuka A, Murachi S, Okunishi H, Shiomi S, Nakano R, Kubo Y, Inaba A (1998) Differential expression and internal feedback regulation of 1-aminocyclopropane-1-carboxylate synthase, 1-aminocyclopropane-1-carboxylate oxidase, and ethylene receptor genes in tomato fruit during development and ripening. Plant Physiol 118:1295–1305

    Article  PubMed  CAS  Google Scholar 

  • Osorio S, Alba R, Damasceno CM, Lopez-Casado G, Lohse M, Zanor MI, Tohge T, Usadel B, Rose JK, Fei Z, Giovannoni JJ, Fernie AR (2011) Systems biology of tomato fruit development: combined transcript, protein, and metabolite analysis of tomato transcription factor (nor, rin) and ethylene receptor (Nr) mutants reveals novel regulatory interactions. Plant Physiol 157:405–425

    Article  PubMed  CAS  Google Scholar 

  • Ozaki S, Ogata Y, Suda K, Kurabayashi A, Suzuki T, Yamamoto N, Iijima Y, Tsugane T, Fujii T, Konishi C, Inai S, Bunsupa S, Yamazaki M, Shibata D, Aoki K (2010) Coexpression analysis of tomato genes and experimental verification of coordinated expression of genes found in a functionally enriched coexpression module. DNA Res 17:105–116

    Article  PubMed  CAS  Google Scholar 

  • Pelaz S, Ditta GS, Baumann E, Wisman E, Yanofsky MF (2000) B and C floral organ identity functions require SEPALLATA MADS-box genes. Nature 405:200–203

    Article  PubMed  CAS  Google Scholar 

  • Picton S, Gray JE, Payton S, Barton SL, Lowe A, Grierson D (1993) A histidine decarboxylase-like mRNA is involved in tomato fruit ripening. Plant Mol Biol 23:627–631

    Article  PubMed  CAS  Google Scholar 

  • Pilati S, Perazzolli M, Malossini A, Cestaro A, Dematte L, Fontana P, Dal Ri A, Viola R, Velasco R, Moser C (2007) Genome-wide transcriptional analysis of grapevine berry ripening reveals a set of genes similarly modulated during three seasons and the occurrence of an oxidative burst at veraison. BMC Genomics 8:428

    Article  PubMed  Google Scholar 

  • Pirrello J, Jaimes-Miranda F, Sanchez-Ballesta MT, Tournier B, Khalil-Ahmad Q, Regad F, Latche A, Pech JC, Bouzayen M (2006) Sl-ERF2, a tomato ethylene response factor involved in ethylene response and seed germination. Plant Cell Physiol 47:1195–1205

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Rohrmann J, Tohge T, Alba R, Osorio S, Caldana C, McQuinn R, Arvidsson S, van der Merwe MJ, Riano-Pachon DM, Mueller-Roeber B, Fei Z, Nesi AN, Giovannoni JJ, Fernie AR (2011) Combined transcription factor profiling, microarray analysis and metabolite profiling reveals the transcriptional control of metabolic shifts occurring during tomato fruit development. Plant J. doi:10.1111/j.1365-313X.2011.04750.x

  • Rose JK, Lee HH, Bennett AB (1997) Expression of a divergent expansin gene is fruit-specific and ripening-regulated. Proc Natl Acad Sci USA 94:5955–5960

    Article  PubMed  CAS  Google Scholar 

  • Rose JK, Cosgrove DJ, Albersheim P, Darvill AG, Bennett AB (2000) Detection of expansin proteins and activity during tomato fruit ontogeny. Plant Physiol 123:1583–1592

    Article  PubMed  CAS  Google Scholar 

  • Seymour GB, Manning K, Eriksson EM, Popovich AH, King GJ (2002) Genetic identification and genomic organization of factors affecting fruit texture. J Exp Bot 53:2065–2071

    Article  PubMed  CAS  Google Scholar 

  • Sharma MK, Kumar R, Solanke AU, Sharma R, Tyagi AK, Sharma AK (2010) Identification, phylogeny, and transcript profiling of ERF family genes during development and abiotic stress treatments in tomato. Mol Genet Genomics 284:455–475

    Article  PubMed  CAS  Google Scholar 

  • Srivastava A, Gupta AK, Datsenka T, Mattoo AK, Handa AK (2010) Maturity and ripening-stage specific modulation of tomato (Solanum lycopersicum) fruit transcriptome. GM Crops 1:237–249

    Article  PubMed  Google Scholar 

  • Tanksley SD, Ganal MW, Prince JP, de Vicente MC, Bonierbale MW, Broun P, Fulton TM, Giovannoni JJ, Grandillo S, Martin GB, Messeguer R, Miller JC, Paterson AH, Pineda O, Roder MS, Wing RA, Young ND (1992) High density molecular linkage maps of the tomato and potato genomes. Genetics 132:1141–1160

    PubMed  CAS  Google Scholar 

  • Theissen G, Becker A, Di Rosa A, Kanno A, Kim JT, Munster T, Winter KU, Saedler H (2000) A short history of MADS-box genes in plants. Plant Mol Biol 42:115–149

    Article  PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Tournier B, Sanchez-Ballesta MT, Jones B, Pesquet E, Regad F, Latche A, Pech JC, Bouzayen M (2003) New members of the tomato ERF family show specific expression pattern and diverse DNA-binding capacity to the GCC box element. FEBS Lett 550:149–154

    Article  PubMed  CAS  Google Scholar 

  • Trainotti L, Tadiello A, Casadoro G (2007) The involvement of auxin in the ripening of climacteric fruits comes of age: the hormone plays a role of its own and has an intense interplay with ethylene in ripening peaches. J Exp Bot 58:3299–3308

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Vrebalov J, Pan IL, Arroyo AJ, McQuinn R, Chung M, Poole M, Rose J, Seymour G, Grandillo S, Giovannoni J, Irish VF (2009) Fleshy fruit expansion and ripening are regulated by the tomato SHATTERPROOF gene TAGL1. Plant Cell 21:3041–3062

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Yokotani N, Tamura S, Nakano R, Inaba A, McGlasson WB, Kubo Y (2004) Comparison of ethylene- and wound-induced responses in fruit of wild-type, rin and nor tomatoes. Postharvest Biol Technol 32:247–252

    Article  CAS  Google Scholar 

  • Zegzouti H, Jones B, Marty C, Lelievre JM, Latche A, Pech JC, Bouzayen M (1997) ER5, a tomato cDNA encoding an ethylene-responsive LEA-like protein: characterization and expression in response to drought, ABA and wounding. Plant Mol Biol 35:847–854

    Article  PubMed  CAS  Google Scholar 

  • Zegzouti H, Jones B, Frasse P, Marty C, Maitre B, Latch A, Pech JC, Bouzayen M (1999) Ethylene-regulated gene expression in tomato fruit: characterization of novel ethylene-responsive and ripening-related genes isolated by differential display. Plant J 18:589–600

    Article  PubMed  CAS  Google Scholar 

  • Zhang Z, Zhang H, Quan R, Wang XC, Huang R (2009) Transcriptional regulation of the ethylene response factor LeERF2 in the expression of ethylene biosynthesis genes controls ethylene production in tomato and tobacco. Plant Physiol 150:365–377

    Article  PubMed  CAS  Google Scholar 

  • Zheng Y, Ren N, Wang H, Stromberg AJ, Perry SE (2009) Global identification of targets of Arabidopsis MADS domain protein AGAMOUS-Like15. Plant Cell 21:2563–2577

    Article  PubMed  CAS  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

Authors and Affiliations

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

    Rahul Kumar, Manoj K. Sharma, Sanjay Kapoor, Akhilesh K. Tyagi & Arun K. Sharma

  2. Department of Plant Pathology, University of California, Davis, CA, 95616, USA

    Manoj K. Sharma

  3. 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. Manoj K. Sharma
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sanjay Kapoor
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Akhilesh K. Tyagi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. 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 S. Hohmann.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kumar, R., Sharma, M.K., Kapoor, S. et al. Transcriptome analysis of rin mutant fruit and in silico analysis of promoters of differentially regulated genes provides insight into LeMADS-RIN-regulated ethylene-dependent as well as ethylene-independent aspects of ripening in tomato. Mol Genet Genomics 287, 189–203 (2012). https://doi.org/10.1007/s00438-011-0671-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-011-0671-7

Keywords

Search

Navigation