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Molecular and genetic regulation of fruit ripening

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Abstract

Fleshy fruit undergo a novel developmental program that ends in the irreversible process of ripening and eventual tissue senescence. During this maturation process, fruit undergo numerous physiological, biochemical and structural alterations, making them more attractive to seed dispersal organisms. In addition, advanced or over-ripening and senescence, especially through tissue softening and eventual decay, render fruit susceptible to invasion by opportunistic pathogens. While ripening and senescence are often used interchangeably, the specific metabolic activities of each would suggest that ripening is a distinct process of fleshy fruits that precedes and may predispose the fruit to subsequent senescence.

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References

  • Adams DO, Yang SF (1979) Ethylene biosynthesis: identification of 1-aminocyclopropane-1-carboxylic acid as an intermediate in the conversion of methionine to ethylene. Proc Natl Acad Sci USA 76:170–174

    Article  PubMed  CAS  Google Scholar 

  • Adams-Phillips L, Barry C, Kannan P, Leclercq J, Bouzayen M, Giovannoni J (2004) Evidence that CTR1-mediated ethylene signal transduction in tomato is encoded by a multigene family whose members display distinct regulatory features. Plant Mol Biol 54:387–404

    Article  PubMed  CAS  Google Scholar 

  • Adato A, Mandel T, Mintz-Oron S, Venger I, Levy D, Yativ M, Dominguez E, Wang Z, De Vos RCH, Jetter R, Schreiber L, Heredia A, Rogachev I, Aharoni A (2009) Fruit-surface flavonoid accumulation in tomato is controlled by a SlMYB12-regulated transcriptional network. PLoS Genet 5:e1000777

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Atkinson RG, Bolitho KM, Wright MA, Iturriagagoitia-Bueno T, Reid SJ, Ross GS (1998) Apple ACC-oxidase and polygalacturonase: ripening-specific gene expression and promoter analysis in transgenic tomato. Plant Mol Biol 38:449–460

    Article  PubMed  CAS  Google Scholar 

  • Atkinson RG, Gunaseelan K, Wang MY, Luo L, Wang T, Norling CL, Johnston SL, Maddumage R, Schröder R, Schaffer RJ (2011) Dissecting the role of climacteric ethylene in kiwifruit (Actinidia chinensis) ripening using a 1-aminocyclopropane-1-carboxylic acid oxidase knockdown line. J Exp Bot 62:3821–3835

    Article  PubMed  CAS  Google Scholar 

  • Ayub R, Guis M, Ben Amor M, Gillot L, Roustan JP, Latché A, Bouzayen M, Pech JC (1996) Expression of ACC oxidase antisense gene inhibits ripening of cantaloupe melon fruits. Nat Biotechnol 14:862–866

    Article  PubMed  CAS  Google Scholar 

  • Baldwin EA, Scott JW, Shewmaker CK, Schuch W (2000) Flavour trivia and tomato aroma: biochemistry and possible mechanisms for control of important aroma components. HortScience 35:1013–1022

    CAS  Google Scholar 

  • Ballester AR, Molthoff J, de Vos R, Hekkert BT, Orzaez D, Fernández-Moreno JP, Tripodi P, Grandillo S, Martin C, Heldens J, Ykema M, Granell A, Bovy A (2010) Biochemical and molecular analysis of pink tomatoes: deregulated expression of the gene encoding transcription factor SlMYB12 leads to pink tomato fruit color. Plant Physiol 152:71–84

    Article  PubMed  CAS  Google Scholar 

  • Bapat VA, Trivedi PK, Ghosh A, Sane VA, Ganapathi TR, Nath P (2010) Ripening of fleshy fruit: molecular insight and the role of ethylene. Biotechnol Adv 28:94–107

    Article  PubMed  CAS  Google Scholar 

  • Barry CS, Giovannoni JJ (2006) Ripening in the tomato green-ripe mutant is inhibited by ectopic expression of a protein that disrupts ethylene signaling. Proc Natl Acad Sci USA 103:7923–7928

    Article  PubMed  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, McQuinn RP, Thompson AJ, Seymour GB, Grierson D, Giovannoni JJ (2005) Ethylene insensitivity conferred by the Green-ripe and Never-ripe 2 ripening mutants of tomato. Plant Physiol 138:267–275

    Article  PubMed  CAS  Google Scholar 

  • Barry C, McQuinn R, Chung M, Besuden A, Giovannoni J (2008) Amino acid substitutions in homologs of the STAY-GREEN (SGR) protein are responsible for the green-flesh and chlorophyll retainer mutations of tomato and pepper. Plant Physiol 147:179–187

    Article  PubMed  CAS  Google Scholar 

  • Barry CS, Aldridge GM, Herzog G, Ma Q, McQuinn RP, Hirschberg J, Giovannoni JJ (2012) Altered chloroplast development and delayed fruit ripening caused by mutations in a zinc metalloprotease at the lutescent2 locus of tomato. Plant Physiol 159:1086–1098

    Article  PubMed  CAS  Google Scholar 

  • Belding RD, Blankenship SM, Young E, Leidy RB (1998) Composition and variability of epicuticular waxes in apple cultivars. J American Society for Hort Sci 123:348–356

    CAS  Google Scholar 

  • Bemer M, Karlova R, Ballester AR, Tikunov YM, Bovy AG, Wolters-Arts M, Rossetto Pde B, Angenent GC, de Maagd RA (2012) The tomato FRUITFULL homologs TDR4/FUL1 and MBP7/FUL2 regulate ethylene-independent aspects of fruit ripening. Plant Cell 24:4437–4451

    Article  PubMed  CAS  Google Scholar 

  • Blackman FF, Parija P (1928) Analytic studies in plant respiration. I. The respiration of a population of senescent ripening apples. Proc R Soc (Lond) B 103:412–445

    Article  CAS  Google Scholar 

  • Borovsky Y, Paran I (2008) Chlorophyll breakdown during pepper fruit ripening in the chlorophyll retainer mutation is impaired at the homolog of the senescence-inducible stay-green gene. Theor Appl Genet 117:235–240

    Article  PubMed  CAS  Google Scholar 

  • Broun P (2005) Transcriptional control of flavonoid biosynthesis: a complex network of conserved regulators involved in multiple aspects of differentiation in Arabidopsis. Curr Op Plant Biol 8:272–279

    Article  CAS  Google Scholar 

  • Brummell DA (2006) Cell wall disassembly in ripening fruit. Funct Plant Bio 33:103–119

    Article  CAS  Google Scholar 

  • Brummell DA, Harpster MH (2001) Cell wall metabolism in fruit softening and quality and its manipulation in transgenic plants. Plant Mol Biol 47:311–340

    Article  PubMed  CAS  Google Scholar 

  • Brummell DA, Harpster MH, Civello PM, Palys JM, Bennett AB, Dunsmuir P (1999) Modification of expansin protein abundance in tomato fruit alters softening and cell wall polymer metabolism during ripening. Plant Cell 11:2203–2216

    PubMed  CAS  Google Scholar 

  • Buchanan-Wollaston V (2007) Senescence in plants. eLS. doi:10.1002/9780470015902.a0020133

  • Butelli E, Titta L, Giorgio M, Mock HP, Matros A, Peterek S, Schijlen EG, Hall RD, Bovy AG, Luo J, Martin C (2008) Enrichment of tomato fruit with health-promoting anthocyanins by expression of select transcription factors. Nat Biotechnol 26:1301–1308

    Article  PubMed  CAS  Google Scholar 

  • Buttery RG (1993) Quantitative and sensory aspects of flavour of tomato and other vegetables and fruits. In: Acree TE, Teranishshi R (eds) Flavor science: sensible principles and techniques. American Chemical Society, Washington, DC, pp 259–286

    Google Scholar 

  • Buttery RG, Ling LC (1993) Volatile components of tomato fruit and plant parts: relationship and biogenesis. ACS Symp Ser 525:23–34

    Article  CAS  Google Scholar 

  • Carpita NC, Gibeaut DM (1993) Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J 3:1–30

    Article  PubMed  CAS  Google Scholar 

  • Cevik V, Ryder CD, Popovich A, Manning K, King GJ, Seymour GB (2010) A FRUITFULL-like gene is associated with genetic variation for fruit flesh firmness in apple (Malus domestica Borkh.). Tree Genet Genomes 6:271–279

    Article  Google Scholar 

  • Chen YF, Randlett MD, Findell JL, Schaller GE (2002) Localization of the ethylene receptor ETR1 to the endoplasmic reticulum of Arabidopsis. J Biol Chem 277:19861–19866

    Article  PubMed  CAS  Google Scholar 

  • Chen G, Hackett R, Walker D, Talor A, Lin Z, Grierson D (2004) Identification of a specific isoform of tomato lipoxygenase (TomloxC) involved in the generation of fatty acid derived flavor compounds. Plant Physiol 136:2641–2651

    Article  PubMed  CAS  Google Scholar 

  • Che-Radziah CMZ, Nurul-Shahnadz AH, Nairatul-Ain AN, Zainal Z (2011) Genetic transformation of antisense ACC oxidase in Carica papaya L. cv Sekaki via particle bombardment. Malays Appl Biol 40:39–45

    Google Scholar 

  • Chung M, 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 

  • Cin V, Tieman DM, Tohge T, McQuinn R, de Vos RC, Osorio S, Schmelz EA, Taylor MG, Smits-Kroon MT, Schuurink RC, Haring MA, Giovannoni J, Fernie AR, Klee HJ (2010) Identific-ation of genes in the phenylalanine metabolic pathway by ectopic expression of a MYB transcription factor in tomato fruit. Plant Cell 23:2738–2753

    Google Scholar 

  • Cunningham FX Jr, Pogson B, Sun Z, McDonald KA, DellaPenna D, Gantt E (1996) Functional analysis of the b and e lycopene cyclase enzymes of Arabidopsis reveals a mechanism for control of cyclic carotenoid formation. Plant Cell 8:1613–1626

    PubMed  CAS  Google Scholar 

  • Davidovich-Rikanati R, Sitrit Y, Tadmor Y, Iijima Y, Bilenko N, Bar E, Carmona B, Fallik E, Dudai N, Simon JE, Pichersky E, Lewinsohn E (2007) Enrichment of tomato flavor by diversion of the early plastidial terpenoid pathway. Nat Biotech 25:899–901

    Article  CAS  Google Scholar 

  • DeFillipi BG, Manriquez D, Luengwilai K, Gonzalez-Aguero M (2009) Aroma volatiles: biosynthesis and mechanisms of modulation during fruit ripening. Adv Bot Res 50:1–37

    Article  CAS  Google Scholar 

  • Dong H, Deng Y, Mu J, Lu Q, Wang Y, Xu Y, Chu C, Chong K, Lu C, Zuo J (2007) The Arabidopsis Spontaneous Cell Death1 gene, encoding a z-carotene desaturase essential for carotenoid biosynthesis, is involved in chloroplast development, photoprotection and retrograde signaling. Nat Cell Res 17:458–470

    CAS  Google Scholar 

  • Egea I, Barsan C, Bian W, Purgatto E, Latche A, Chervin C, Bouzayen M, Pech J-C (2010) Chromoplast differentiation: current status and perspectives. Plant Cell Physiol 51:1601–1611

    Article  PubMed  CAS  Google Scholar 

  • Elitzur T, Vrebalov J, Giovannoni JJ, Goldschmidt EE, Friedman H (2010) The regulation of MADS-box gene expression during ripening of banana and their regulatory interaction with ethylene. J Exp Bot 61:1523–1535

    Article  PubMed  CAS  Google Scholar 

  • Espley RV, Hellens RP, Putterill J, Stevenson DE, Kutty-Amma S, Allan AC (2007) Red colouration in apple fruit is due to the activity of the MYB transcription factor, MdMYB10. Plant J 49:414–427

    Article  PubMed  CAS  Google Scholar 

  • Espley RV, Brendolise C, Chagne D, Kutty-Amma S, Green S, Volz R, Putterill J, Schouten HJ, Gardiner SE, Hellens RP, Allan AC (2009) Multiple repeats of a promoter segment causes transcription factor autoregulation in red apples. Plant Cell 21:168–183

    Article  PubMed  CAS  Google Scholar 

  • Fray RG, Grierson D (1993) Identification and genetic analysis of normal and mutant phytoene synthase genes of tomato by sequencing, complementation and co-suppression. Plant Mol Biol 22:589–602

    Article  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 

  • Gagne JM, Smalle J, Gingerich DJ, Walker JM, Yoo SD, Yanagisawa S, Vierstra RD (2004) Arabidopsis EIN3-binding F-box 1 and 2 form ubiquitin-protein ligases that repress ethylene action and promote growth by directing EIN3 degradation. Proc Natl Acad Sci USA 101:6803–6808

    Article  PubMed  CAS  Google Scholar 

  • Galpaz N, Ronen G, Khalfa Z, Zamir D, Hirschberg J (2006) A chromoplast-specific carotenoid biosynthetic pathway is revealed by cloning of the tomato white-flower locus. Plant Cell 18:1947–1960

    Article  PubMed  CAS  Google Scholar 

  • Gan S, Amasino RM (1995) Inhibition of leaf senescence by autoregulated production of cytokinin. Science 270:1986–1988

    Article  PubMed  CAS  Google Scholar 

  • Garcia-Limones C, Schnabele K, Blanco-Portales R, Bellido ML, Caballero JL, Schwab W, Munoz-Blanco J (2008) Functional characterization of FaCCD1: a carotenoid cleavage dioxygenase from strawberry involved in lutein degradation during fruit ripening. J Agric Food Chem 56:9277–9285

    Article  PubMed  CAS  Google Scholar 

  • Giovannoni JJ (2007) Fruit ripening mutants yield insights into ripening control. Curr Opin Plant Biol 10:283–289

    Google Scholar 

  • Giovannoni JJ, DellaPenna D, Bennett AB, Fischer RL (1989) Expression of a chimeric polygalacturonase gene in transgenic rin (ripening inhibitor) tomato fruit results in polyuronide degradation but not fruit softening. Plant Cell 1:53–63

    PubMed  CAS  Google Scholar 

  • Girard AL, Mounet F, Lemaire-Chamley M, Gaillard C, Elmorjani K, Vivancos J, Runavot J-L, Quemener B, Petit J, Germain V, Rothan C, Marion D, Bakan B (2012) Tomato GDSL1 is required for cutin deposition in the fruit cuticle. Plant Cell 24:3106–3121

    Article  CAS  Google Scholar 

  • Goulao LF, Oliveira CM (2007) Cell wall modifications during fruit ripening: when a fruit is not the fruit. Trends Food Sci Technol 19:4–25

    Article  CAS  Google Scholar 

  • Goulet C, Mageroy MH, Lam N, Floystad A, Tieman DM, Klee HJ (2012) The role of an esterase in flavor volatile variation within the tomato clade. Proc Natl Acad Sci USA 109:19009–19014

    Article  PubMed  CAS  Google Scholar 

  • Guo H, Ecker JR (2003) Plant responses to ethylene gas are mediated by SCF (EBF1/EBF2)-dependent proteolysis of EIN3 transcription factor. Cell 115:667–677

    Article  PubMed  CAS  Google Scholar 

  • Guo Y, Gan S (2006) AtNAP, a NAC family transcription factor, has an important role in leaf senescence. Plant J 46:601–612

    Article  PubMed  CAS  Google Scholar 

  • Hamilton AJ, Lycett GW, Grierson D (1990) Antisense gene that inhibits synthesis of the hormone ethylene in transgenic plants. Nature 346:284–287

    Article  CAS  Google Scholar 

  • Hancock RD, Viola R (2005) Biosynthesis and catabolism of L-ascorbic acid in plants. Crit Rev Plant Sci 24:167–188

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Hirschberg J (2001) Carotenoid biosynthesis in flowering plants. Curr Opin Plant Biol 4:210–218

    Article  PubMed  CAS  Google Scholar 

  • Hovav R, Chehanovsky N, Moy M, Jetter R, Schaffer AA (2007) The identification of a gene (Cwp1), silenced during Solanum evolution, which causes cuticle microfissuring and dehydration when expressed in tomato fruit. Plant J 52:627–639

    Article  PubMed  CAS  Google Scholar 

  • Ioannidi E, Kalamaki MS, Engineer C, Pateraki I, Alexandrou D, Mellidou I, Giovannoni JJ, Kanellis AK (2009) Expression profiling of ascorbic acid-related genes during tomato fruit development and ripening and in response to stress conditions. J Exp Bot 60:663–678

    Article  PubMed  CAS  Google Scholar 

  • Isaacson T, Ronen G, Zamir D, Hirschberg J (2002) Cloning of tangerine from tomato reveals a carotenoid isomerase essential for the production of b-carotene and xanthophylls in plants. Plant Cell 14:333–342

    Article  PubMed  CAS  Google Scholar 

  • Isaacson T, Kosma DK, Matas AJ, Buda GJ, He Y, Yu B, Pravitasari A, Batteas JD, Stark RE, Jenks MA, Rose JKC (2009) Cutin deficiency in the tomato fruit cuticle consistently affects resistance to microbial infection and biomechanical properties, but not transpirational water loss. Plant J 60:363–377

    Article  PubMed  CAS  Google Scholar 

  • Itai A, Ishihara K, Bewley JD (2003) Characterization of expression, and cloning, of beta-D-xylosidase and alpha-L-arabinofuranosidase in developing and ripening tomato (Lycopersicon esculentum Mill.) fruit. J Exp Bot 54:2615–2622

    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 

  • Jaakola L, Poole M, Jones MO, Kämäräinen-Karppinen T, Koskimäki JJ, Hohtola A, Häggman H, Fraser PD, Manning K, King GJ, Thomson H, Seymour GB (2010) A SQUAMOSA MADS box gene involved in the regulation of anthocyanin accumulation in bilberry fruits. Plant Physiol 153:1619–1629

    Article  PubMed  CAS  Google Scholar 

  • Kamiyoshihara Y, Tieman DM, Huber DJ, Klee HJ (2012) Ligand-induced alterations in the phosphorylation state of ethylene receptors in tomato fruit. Plant Physiol 160:488–497

    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 (2011) Transcriptome and metabolite profiling show that APETALA2a is a major regulator of tomato fruit ripening. Plant Cell 23:923–941

    Article  PubMed  CAS  Google Scholar 

  • Kerstiens G (1996) Cuticular water permeability and its physiological significance. J Exp Bot 47:1813–1832

    Article  CAS  Google Scholar 

  • Kevany B, Tieman DM, Taylor M, Dal Cin V, Klee H (2007) Ethylene receptor degradation controls the timing of ripening in tomato fruit. Plant J 51:458–567

    Article  PubMed  CAS  Google Scholar 

  • Kevany BM, Taylor MG, Klee HJ (2008) Fruit-specific suppression of the ethylene receptor LeETR4 results in early-ripening tomato fruit. Plant Biotechnol J 6:295–300

    Article  PubMed  CAS  Google Scholar 

  • Klee HJ (2004) Ethylene signal transduction. Moving beyond Arabidopsis. Plant Physiol 135:660–667

    Article  PubMed  CAS  Google Scholar 

  • Klee HJ (2010) Improving the flavor of fresh fruits: genomics, biochemistry, and biotechnology. New Phytol 187:44–56

    Article  PubMed  CAS  Google Scholar 

  • Klee HJ, Giovannoni JJ (2011) Genetics and control of tomato fruit ripening and quality attributes. Annu Rev Genet 45:41–59

    Article  PubMed  CAS  Google Scholar 

  • Klee HJ, Hayford MB, Kretzmer KA, Barry GF, Kishore GM (1991) Control of ethylene synthesis by expression of a bacterial enzyme in transgenic tomato plants. Plant Cell 3:1187–1194

    PubMed  CAS  Google Scholar 

  • Kosma DK, Parsons EP, Isaacson T, Lu S, Rose JKC, Jenks MA (2010) Fruit cuticle lipid compositions during development in tomato ripening mutants. Physiol Plant 139:107–117

    Article  PubMed  CAS  Google Scholar 

  • Kou X, Watkins CB, Gan SS (2012) Arabidopsis AtNAP regulates fruit senescence. J Exp Bot 63:6139–6147

    Article  PubMed  CAS  Google Scholar 

  • Kovacs K, Fray RG, Tikunov Y, Graham N, Bradley G, Seymour GB, Bovy AG, Grierson D (2009) Effect of pleiotropic ripening mutations on flavour volatile biosynthesis. Phytochemistry 70:1003–1008

    Article  PubMed  CAS  Google Scholar 

  • Kumar R, Sharma MK, Kapoor S, Tyagi AK, Sharma AK (2012) 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

    Article  PubMed  CAS  Google Scholar 

  • Laguna L, Casado CG, Heredia A (1998) Flavonoid biosynthesis in tomato fruit cuticles after in vivo incorporation of 3H-phenylalanine precursor. Physiol Plant 105:491–498

    Article  Google Scholar 

  • Leclercq J, Adams-Phillips L, Zegzouti H, Jones B, Latche A et al (2002) LECTR1, a tomato CTR1-like gene, demonstrates ethylene signaling ability in Arabidopsis and novel expression patterns in tomato. Plant Physiol 130:1132–1142

    Article  PubMed  CAS  Google Scholar 

  • Lee JM, Joung JG, McQuinn R, Chung MY, Fei Z, Tieman D, Klee H, Giovannoni J (2012) Combined transcriptome, genetic diversity and metabolite profiling in tomato fruit reveals that the ethylene response factor SlERF6 plays an important role in ripening and carotenoid accumulation. Plant J 70:191–204

    Article  PubMed  CAS  Google Scholar 

  • Lewinsohn E, Sitrit Y, Bar E, Azulay Y, Meir A, Zamir D, Tadmor Y (2005a) Carotenoid pigmentation affects the volatile composition of tomato and watermelon fruits, as revealed by comparative genetic analysis. J Agric Food Chem 53:3142–3148

    Article  PubMed  CAS  Google Scholar 

  • Lewinsohn E, Sitrit Y, Bar E, Azulay Y, Ibdah M, Meir A, Yosef E, Zamir D, Tadmor Y (2005b) Not just colors – carotenoid degradation as a link between pigmentation and aroma in tomato and watermelon fruit. Trends Food Sci Technol 16:407–415

    Article  CAS  Google Scholar 

  • Li F, Murillo C, Wurtzel ET (2007) Maize Y9 encodes a product essential for 15-cis-z-carotene Isomerization. Plant Physiol 144:1181–1189

    Article  PubMed  CAS  Google Scholar 

  • Lin Z, Arciga-Reyes L, Zhong S, Alexander L, Hackett R, Wilson I, Grierson D (2008a) SlTPR1, a tomato tetratricopeptide repeat protein, interacts with the ethylene receptors NR and LeETR1, modulating ethylene and auxin responses and development. J Exp Bot 59:4271–4287

    Article  PubMed  CAS  Google Scholar 

  • Lin Z, Hong Y, Yin M, Li C, Zhang K, Grierson D (2008b) 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 

  • Lin Z, Zhong S, Grierson D (2009) Recent advances in ethylene research. J Exp Bot 60:3311–3336

    Article  PubMed  CAS  Google Scholar 

  • Luque P, Bruque S, Heredia A (1995) Water permeability of isolated cuticular membranes: a structural analysis. Arch Biochem Biophys 317:417–422

    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 SPB-box transcription factor inhibits tomato fruit ripening. Nat Genet 38:949–952

    Article  CAS  Google Scholar 

  • Marín-Rodríguez MC, Orchard J, Seymour GB (2002) Pectate lyases, cell wall degradation and fruit softening. J Exp Bot 53:2115–2119

    Article  PubMed  Google Scholar 

  • Martel C, Vrebalov J, Tafelmeyer P, Giovannoni JJ (2011) The tomato MADS-box transcription factor RIPENING INHIBITOR interacts with promoters involved in numerous ripening processes in a COLORLESS NONRIPENING-dependent manner. Plant Physiol 157:1568–1579

    Article  PubMed  CAS  Google Scholar 

  • Matas AJ, Gapper NE, Chung MY, Giovannoni JJ, Rose JK (2009) Biology and genetic engineering of fruit maturation for enhanced quality and shelf-life. Curr Opin Biotechnol 20:197–203

    Article  PubMed  CAS  Google Scholar 

  • Matas AJ, Yeats TH, Buda GJ, Zheng Y, Chatterjee S, Tohge T, Ponnala L, Adato A, Aharoni A, Stark R, Fernie AR, Fei Z, Giovannoni JJ, Rose JK (2011) Tissue- and cell-type specific transcriptome profiling of expanding tomato fruit provides insights into metabolic and regulatory specialization and cuticle formation. Plant Cell 23:3893–3910

    Article  PubMed  CAS  Google Scholar 

  • Mathieu S, Dal Cin V, Fei Z, Li H, Bliss P, Taylor M, Klee H, Tieman D (2009) Flavor compounds in tomato fruits: identification of loci and potential pathways affecting volatile composition. J Exp Bot 60:325–337

    Article  PubMed  CAS  Google Scholar 

  • Matthews PD, Luo RB, Wurtzel ET (2003) Maize phytoene desaturase and z-carotene desaturase catalyze a poly-Z desaturation pathway: implications for genetic engineering of carotenoid content among cereal crops. J Exp Bot 54:2215–2230

    Article  PubMed  CAS  Google Scholar 

  • McMurchie EJ, McGlasson WB, Eaks IL (1972) Treatment of fruit with propylene gives information about the biogenesis of ethylene. Nature 237:235–236

    Article  PubMed  CAS  Google Scholar 

  • Miao Y, Zentgraf U (2007) The antagonist function of Arabidopsis WRKY53 and ESR/ESP in leaf senescence is modulated by the jasmonic and salicylic acid equilibrium. Plant Cell 19:819–830

    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 

  • Mohorianu I, Schwach F, Jing R, Lopez-Gomollon S, Moxon S, Szittya G, Sorefan K, Moulton V, Dalmay T (2011) Profiling of short RNAs during fleshy fruit development reveals stage-specific sRNAome expression patterns. Plant J 67:232–246

    Article  PubMed  CAS  Google Scholar 

  • Moxon S, Jing R, Szittya G, Schwach F, Rusholme Pilcher RL, Moulton V, Dalmay T (2008) Deep sequencing of tomato short RNAs identifies microRNAs targeting genes involved in fruit ripening. Genome Res 18:1602–1609

    Article  PubMed  CAS  Google Scholar 

  • Muir SR, Collins GJ, Robinson S, Hughes S, Bovy A, De Vos RCH, van Tunen AJ, Verhoeyen ME (2001) Overexpression of petunia chalcone isomerase in tomato results in fruit containing increased levels of flavonols. Nat Biotechnol 19:470–474

    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 

  • Nashilevitz S, Melamed-Bessudo C, Izkovich Y, Rogachev I, Osorio S, Itkin M, Adato A, Pankratov I, Hirschberg J, Fernie AR, Wolf S, Usadel B, Levy AA, Rumeau D, Aharoni A (2010) An orange ripening mutant links plastid NAD(P)H dehydrogenase complex activity to central and specialized metabolism during tomato fruit maturation. Plant Cell 22:1977–1997

    Article  PubMed  CAS  Google Scholar 

  • Oeller PW, Wong LM, Taylor LP, Pike DA, Theologis A (1991) Reversible inhibition of tomato fruit senescence by antisense RNA. Science 254:437–439

    Google Scholar 

  • O’Malley RC, Rodriguez FI, Esch JJ, Binder BM, O’Donnell P, Klee HJ, Bleecker AB (2005) Ethylene-binding activity, gene expression levels, and receptor system output for ethylene receptor family members from Arabidopsis and tomato. Plant J 41:651–659

    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 

  • Pan IL, McQuinn R, Giovannoni JJ, Irish VF (2010) Functional diversification of AGAMOUS lineage genes in regulating tomato flower and fruit development. J Exp Bot 61:1795–1806

    Article  PubMed  CAS  Google Scholar 

  • Pan Y, Bradley G, Pyke K, Ball G, Lu C, Fray R, Marshall A, Jayasuta S, Baxter C, van Wijk R, Boyden L, Cade R, Chapman NH, Fraser PD, Hodgman C, Seymour GB (2013) Network inference analysis identifies an APRR2-like gene linked to pigment accumulation in tomato and pepper fruits. Plant Physiol 161:1476–1485

    Article  PubMed  CAS  Google Scholar 

  • Peschel S, Franke R, Schreiber L, Knoche M (2007) Composition of the cuticle of developing sweet cherry fruit. Phytochemistry 68:1017–1025

    Article  PubMed  CAS  Google Scholar 

  • Picton S, Barton SL, Bouzayen M, Hamilton AJ, Grierson D (1993) Altered fruit ripening and leaf senescence in tomatoes expressing an antisense ethylene-forming enzyme transgene. Plant J 3:469–481

    Article  CAS  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 

  • Pnueli L, Hareven D, Rounsley SD, Yanofsky MF, Lifschitz E (1994) Isolation of the tomato AGAMOUS gene TAG1 and analysis of its homeotic role in transgenic plants. Plant Cell 6:163–173

    PubMed  CAS  Google Scholar 

  • Potuschak T, Lechner E, Parmentier Y, Yanagisawa S, Grava S, Koncz C, Genschik P (2003) EIN3-dependent regulation of plant ethylene hormone signaling by two Arabidopsis F box proteins: EBF1 and EBF2. Cell 115:679–689

    Article  PubMed  CAS  Google Scholar 

  • Powell AL, Nguyen CV, Hill T, Cheng KL, Figueroa-Balderas R, Aktas H, Ashrafi H, Pons C, Fernández-Muñoz R, Vicente A, Lopez-Baltazar J, Barry CS, Liu Y, Chetelat R, Granell A, Van Deynze A, Giovannoni JJ, Bennett AB (2012) Uniform ripening encodes a Golden 2-like transcription factor regulating tomato fruit chloroplast development. Science 336:1711–1715

    Article  PubMed  CAS  Google Scholar 

  • Prasanna V, Prabha TN, Tharanathan RN (2007) Fruit ripening phenomena-an overview. Critical Rev Food Sci Nut 47:1–19

    Article  CAS  Google Scholar 

  • Qiao H, Chang KN, Yazaki J, Ecker JR (2009) Interplay between ethylene, ETP1/ETP2 F-box proteins, and degradation of EIN2 triggers ethylene responses in Arabidopsis. Genes Dev 23:512–521

    Article  PubMed  CAS  Google Scholar 

  • Qin G, Gu H, Ma L, Peng Y, Deng XW, Chen Z, Qu L-J (2007) Disruption of phytoene desaturase gene results in albino and dwarf phenotypes in Arabidopsis by impairing chlorophyll, carotenoid, and gibberellin biosynthesis. Nature Cell Res 17:471–482

    Article  CAS  Google Scholar 

  • Qin G, Wang Y, Cao B, Wang W, Tian S (2012) Unraveling the regulatory network of the MADS box transcription factor RIN in fruit ripening. Plant J 70:243–255

    Article  PubMed  CAS  Google Scholar 

  • Reina-Pinto JJ, Yephremov A (2009) Surface lipids and plant defenses. Plant Physiol Biochem 47:540–549

    Article  PubMed  CAS  Google Scholar 

  • Resnick JS, Wen C-K, Shockey JA, Chang C (2006) REVERSION-TO-ETHYLENE SENSITIVITY1, a conserved gene that regulates ethylene receptor function in Arabidopsis. Proc Natl Acad Sci USA 103:7917–7922

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez F, Esch J, Hall A, Binder B, Schaller GE, Bleecker AB (1999) A copper cofactor for the ETR1 receptor from Arabidopsis. Science 283:996–998

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez-Concepcion M, Boronat A (2002) Elucidation of the methylerythritol phosphate pathway for isoprenoid biosynthesis in bacteria and plastids. A metabolic milestone achieved through genomics. Plant Physiol 130:1079–1089

    Article  PubMed  CAS  Google Scholar 

  • Rodríguez-Gacio MC, Iglesias-Fernández R, Carbonero P, Matilla AJ (2012) Softening-up mannan-rich cell walls. J Exp Bot 63:3976–3988

    Article  CAS  Google Scholar 

  • Rohdich F, Zepeck F, Adam P, Hecht S, Kaiser J, Laupitz R, Grawert T, Amslinger S, Eisenreich W, Bacher A, Arigoni D (2003) The deoxyxylulose phosphate pathway of isoprenoid biosynthesis: studies on the mechanisms of the reactions catalyzed by IspG and IspH protein. Proc Natl Acad Sci USA 100:1586–1591

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Rottmann WH, Peter GF, Oeller PW, Keller JA, Shen NF, Nagy BP, Taylor LP, Campbell AD, Theologis A (1991) 1-aminocyclopropane-1-carboxylate synthase in tomato is encoded by a multigene family whose transcription is induced during fruit and floral senescence. J Mol Biol 222:937–961

    Article  PubMed  CAS  Google Scholar 

  • Sacher JA (1973) Senescence and post harvest physiology. Annu Rev Plant Physiol 24:197–310

    Article  CAS  Google Scholar 

  • Saladié M, Rose JK, Cosgrove DJ, Catalá C (2006) Characterization of a new xyloglucan endotransglucosylase/hydrolase (XTH) from ripening tomato fruit and implications for the diverse modes of enzymic action. Plant J. 47:282–295

    Article  PubMed  CAS  Google Scholar 

  • Saladié M, Matas AJ, Isaacson T, Jenks MA, Goodwin SM, Niklas KJ, Xiaolin R, Labavitch JM, Shackel KA, Fernie AR, Lytovchenko A, O'Neill MA, Watkins CB, Rose JK (2007) A reevaluation of the key factors that influence tomato fruit softening and integrity. Plant Physiol 144:1012–1028

    Google Scholar 

  • Schaffer RJ, Friel EN, Souleyre EJF, Bolitho K, Ledger KTS, Bowen JH, Ma J-H, Nain B, Cohen D, Gleave AP, Crowhurst RN, Janssen BJ, Yao J-L, Newcomb RD (2007) A genomics approach reveals that aroma production in apple is controlled by ethylene predominantly at the final step in each biosynthetic pathway. Plant Physiol 144:1899–1912

    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 

  • Seymour GB, Ryder CD, Cevik V, Hammond JP, Popovich A, King GJ, Vrebalov J, Giovannoni JJ, Manning K (2011) A SEPALLATA gene is involved in the development and ripening of strawberry (Fragaria × ananassa Duch.) fruit, a non-climacteric tissue. J Exp Bot 62:1179–1188

    Article  PubMed  CAS  Google Scholar 

  • Seymour GB, Østergaard L, Chapman NH, Sandra Knapp S, Martin C (2013) Fruit development and ripening. Annu Rev Plant Biol 64:1–11

    Article  CAS  Google Scholar 

  • Shi JX, Adato A, Alkan N, He Y, Lashbrooke J, Matas AJ, Meir S, Malitsky S, Isaacson T, Prusky D, Leshkowitz D, Schreiber L, Granell AR, Widemann E, Grausem B, Pinot F, Rose JK, Rogachev I, Rothan C, Aharoni A (2013) The tomato SlSHINE3 transcription factor regulates fruit cuticle formation and epidermal patterning. New Phytol 197:468–480

    Article  PubMed  CAS  Google Scholar 

  • Shivaprasad PV, Chen HM, Patel K, Bond DM, Santos BA, Baulcombe DC (2012) A microRNA superfamily regulates nucleotide binding site-leucine-rich repeats and other mRNAs. Plant Cell 24:859–874

    Article  PubMed  CAS  Google Scholar 

  • Smirnoff N, Conklin PL, Loewus FA (2001) Biosynthesis of ascorbic acid in plants: a renaissance. Annu Rev Plant Physiol Plant Mol Biol 52:437–467

    Article  PubMed  CAS  Google Scholar 

  • Smith CJ, Watson CF, Bird CR, Ray J, Schuch W, Grierson D (1990) Expression of a truncated tomato polygalacturonase gene inhibits expression of the endogenous gene in transgenic plants. Mol Gen Genet 224:477–481

    Article  PubMed  CAS  Google Scholar 

  • Smith DL, Abbott JA, Gross KC (2002) Down-regulation of tomato beta-galactosidase 4 results in decreased fruit softening. Plant Physiol 129:1755–1762

    Article  PubMed  CAS  Google Scholar 

  • Sozzi GO, Greve LC, Prody GA, Labavitch JM (2002) Gibberellic acid, synthetic auxins, and ethylene differentially modulate alpha-L-arabinofuranosidase activities in antisense 1-aminocyclopropane-1-carboxylic acid synthase tomato pericarp discs. Plant Physiol 129:1330–1340

    Article  PubMed  CAS  Google Scholar 

  • Speirs J, Lee E, Holt K, Yong-Duk K, Scott NS, Schuch W, Loveys B (1998) Genetic manipulation of alcohol dehydrogenase levels in ripening tomato fruit affects the balance of some flavor aldehydes and alcohols. Plant Physiol 117:1047–1058

    Article  PubMed  CAS  Google Scholar 

  • Tacken E, Ireland H, Gunaseelan K, Karunairetnam S, Wang D, Schultz K, Bowen J, Atkinson RG, Johnston JW, Putterill J, Hellens RP, Schaffer RJ (2010) The role of ethylene and cold temperature in the regulation of the apple POLYGALACTURONASE1 gene and fruit softening. Plant Physiol 153:294–305

    Article  PubMed  CAS  Google Scholar 

  • Tadiello A, Pavanello A, Zanin D, Caporali E, Colombo L, Rotino GL, Trainotti L, Casadoro G (2009) A PLENA-like gene of peach is involved in carpel formation and subsequent transformation into a fleshy fruit. J Exp Bot 60:651–661

    Article  PubMed  CAS  Google Scholar 

  • Tatsuki M, Mori H (2001) Phosphorylation of tomato 1-aminocyclopropane-1-carboxylic acid synthase, LE-ACS2, at the C-terminal region. J Biol Chem 276:28051–28057

    Article  PubMed  CAS  Google Scholar 

  • Thomas TR, Shackel KA, Matthews MA (2008) Mesocarp cell turgor in Vitis vinifera L. berries throughout development and its relation to firmness, growth, and the onset of ripening. Planta 228:1067–1076

    Article  PubMed  CAS  Google Scholar 

  • Tian MS, Prakash S, Elgar HJ, Young H, Burmeister DM, Ross GS (2000) Responses of strawberry fruit to 1-methylcyclopropene (1-MCP) and ethylene. Plant Growth Regul 32:83–90

    Article  CAS  Google Scholar 

  • Tian L, Magallanes-Lundback M, Musetti V, DellaPenna D (2003) Functional analysis of b- and e-ring carotenoid hydroxylases in Arabidopsis. Plant Cell 15:1320–1330

    Article  PubMed  CAS  Google Scholar 

  • Tieman DM, Taylor MG, Ciardi JA, Klee HJ (2000) The tomato ethylene receptors NR and LeETR4 are negative regulators of ethylene response and exhibit functional compensation within a multigene family. Proc Natl Acad Sci USA 97:5663–5668

    Article  PubMed  CAS  Google Scholar 

  • Tieman DM, Ciardi JA, Taylor MG, Klee HJ (2001) Members of the tomato LeEIL (EIN3-like) gene family are functionally redundant and regulate ethylene responses throughout plant development. Plant J 26:47–58

    Article  PubMed  CAS  Google Scholar 

  • Tieman D, Taylor M, Schauer N, Fernie AR, Hanson AD, Klee HJ (2006) Tomato aromatic amino acid decarboxylases participate in synthesis of the flavor volatiles 2-phenylethanol and 2 phenylacetaldehyde. Proc Natl Acad Sci USA 103:8287–8292

    Article  PubMed  CAS  Google Scholar 

  • Tieman DM, Zeigler M, Schmelz E, Taylor MG, Rushing S, Jones JB, Klee HJ (2010) Functional analysis of a tomato salicylic acid methyl transferase and its role in synthesis of the flavor volatile methyl salicylate. Plant J 62:113–123

    Article  PubMed  CAS  Google Scholar 

  • Tieman DM, McIntyre L, Blandon-Ubeda A, Bies D, Odabasi A, Rodriguez G, van der Knaap E, Taylor M, Goulet C, Mageroy MH, Snyder D, Colquoun T, Moskowitz H, Sims C, Clark D, Bartoshuk L, Klee H (2012) The chemical interactions underlying tomato flavor preferences. Curr Biol 22:1–5

    Article  CAS  Google Scholar 

  • Tigchelaar EC, Mcglasson WB, Franklin MJ (1978) Natural and ethephon-stimulated ripening of F1 hybrids of the ripening inhibitor (rin) and non-ripening (nor) mutants of tomato (Lycopersicon esculentum Mill.) Australian J. Plant Physiol 5:449–456

    CAS  Google Scholar 

  • Tomato Genome Consortium (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485:635–641

    Article  CAS  Google Scholar 

  • Treutter D (2005) Significance of flavonoids in plant resistance and enhancement of their biosynthesis. Plant Biol 7:581–591

    Article  PubMed  CAS  Google Scholar 

  • Verhoeyen ME, Bovy A, Gollins G, Muir S, Robinson S, de Vos CHR, Colliver S (2002) Increasing antioxidant levels in tomatoes through modification of the flavonoid biosynthetic pathway. J Exp Bot 53:2099–2106

    Article  PubMed  CAS  Google Scholar 

  • Vicente AR, Saladié M, Rose JKC, Labavitch JM (2007) The linkage between cell wall metabolism and fruit softening: looking to the future. J Sci Food Agric 87:1435–1448

    Article  CAS  Google Scholar 

  • Vogel JT, Tieman DM, Sins CA, Odabasi AZ, Clark DG, Klee HJ (2010) Carotenoid content impacts flavor acceptability in tomato (Solanum lycopersicum). J Sci Food Agric 90:2233–2240

    Article  PubMed  CAS  Google Scholar 

  • Vogg G, Fischer S, Leide J, Emmanuel E, Jetter R, Levy AA, Riederer M (2004) Tomato fruit cuticular waxes and their effects on transpiration barrier properties: functional characterization of a mutant deficient in a very-long-chain fatty acid b-ketoacyl-CoA synthase. J Exp Bot 55:1401–1410

    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 

  • Wakabayashi K, Hoson T, Huber DJ (2003) Methyl de-esterification as a major factor regulating the extent of pectin depolymerization during fruit ripening: a comparison of the action of avocado (Persea americana) and tomato (Lycopersicon esculentum) polygalacturonases. J Plant Physiol 160:667–673

    Article  PubMed  CAS  Google Scholar 

  • Wang J, Chen G, Hu Z, Chen X (2007) Cloning and characterization of the EIN2-homology gene LeEIN2 from tomato. DNA Seq 18:33–38

    PubMed  CAS  Google Scholar 

  • Wheeler GL, Jones MA, Smirnoff N (1998) The biosynthetic pathway of vitamin C in higher plants. Nature 393:365–369

    Article  PubMed  CAS  Google Scholar 

  • Wilkinson JQ, LanahanMB YenH-C, Giovannoni JJ, Klee HJ (1995) An ethylene-inducible component of signal transduction encoded by Never-Ripe. Science 270:1807–1809

    Article  PubMed  CAS  Google Scholar 

  • Winkel-Shirley B (2001) Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol 126:485–493

    Article  PubMed  CAS  Google Scholar 

  • Wong D (2008) Enzymatic deconstruction of backbone structures of the ramified regions in pectins. Protein J 27:30–42

    Article  PubMed  CAS  Google Scholar 

  • Yahia EM, Contreras-Padilla M, Gonzalez-Aguilar G (2001) Ascorbic acid content in relation to ascorbic acid oxidase activity and polyamine content in tomato and bell pepper fruits during development, maturation, and senescence. Lebensm-Wiss u-Technol 34:452–457

    Article  CAS  Google Scholar 

  • Yang Y, Wu Y, Pirrello J, Regad F, Bouzayen M, Deng W, Li Z (2010) Silencing Sl-EBF1 and Sl-EBF2 expression causes constitutive ethylene response phenotype, accelerated plant senescence, and fruit ripening in tomato. J Exp Bot 61:697–708

    Article  PubMed  CAS  Google Scholar 

  • Yeats TH, Howe KJ, Matas AJ, Buda GJ, Thannhauser TW, Rose JKC (2010) Mining the surface proteome of tomato (Solanum lycopersicum) fruit for proteins associated with cuticle biogenesis. J Exp Bot 61:3759–3771

    Article  PubMed  CAS  Google Scholar 

  • Yeats TH, Buda GJ, Wang Z, Chehanovsky N, Moyle LC, Jetter R, Schaffer AA, Rose JKC (2012a) The fruit cuticle of wild tomato species exhibit architectural and chemical diversity, providing a new model for studying the evolution of cuticle function. Plant J 69:655–666

    Article  PubMed  CAS  Google Scholar 

  • Yeats TH, Martin LBB, Viart HM-F, Isaacson T, He Y, Zhao L, Matas AJ, Buda GJ, Domozych DS, Clausen MH, Rose JKC (2012b) The identification of cutin synthase: formation of the plant polyester cutin. Nat Chem Bio 8:609–611

    Article  CAS  Google Scholar 

  • Zhang B, Chen K, Bowen J, Allan A, Espley R, Karunairetnam S, Ferguson I (2006) Differential expression within the LOX gene family in ripening kiwifruit. J Exp Bot 57:3825–3836

    Article  PubMed  CAS  Google Scholar 

  • Zhong S, Lin Z, Grierson D (2008) Tomato ethylene receptor-CTR interactions: visualization of NEVER-RIPE interactions with multiple CTRs at the endoplasmic reticulum. J Exp Bot 59:965–972

    Article  PubMed  CAS  Google Scholar 

  • Zhong S, Fei Z, Chen Y-R, Zheng Y, Huang M, Vrebalov J, McQuinn R, Gapper N, Liu B, Xiang J, Shao Y, Giovannoni JJ (2013) Single-base resolution methylomes of tomato fruit development reveal epigenome modifications associated with ripening. Nat Biotechnol 31:154–159

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

Work in the Giovannoni laboratory was funded by the National Science Foundation, US Department of Agriculture–Agricultural Research Service, US Department of Agriculture–National Institute of Food and Agriculture, and the US-Israel Binational Agricultural Research and Development Fund. NEG was funded by the New Zealand Foundation for Research Science and Technology.

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Gapper, N.E., McQuinn, R.P. & Giovannoni, J.J. Molecular and genetic regulation of fruit ripening. Plant Mol Biol 82, 575–591 (2013). https://doi.org/10.1007/s11103-013-0050-3

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