Genetics and control of tomato fruit ripening and quality attributes

Annual Review of Genetics

Volumn 45, Issue , 2011, Pages 41-59

  Klee, Harry J ^a   Giovannoni, James J ^b  

^a UNIVERSITY OF FLORIDA   (United States)

^b United States Department of Agriculture Agricultural Research Service and Boyce Thompson Institute for Plant Research   (United States)

Author keywords

Fleshy fruits; Hormone signaling; MADS box; Seed dispersal; Transcription factor

Indexed keywords

ETHYLENE; PHYTOHORMONE; RECEPTOR; UBIQUITINATED PROTEIN;

ABSCISSION; ARABIDOPSIS; ARTICLE; ENDOPLASMIC RETICULUM; FRUIT RIPENING; GENE EXPRESSION; GENE MUTATION; GENETIC TRANSCRIPTION; GENETICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; SENESCENCE; SIGNAL TRANSDUCTION; TOMATO;

ARABIDOPSIS; CHLOROPLASTS; ETHYLENES; FLAVORING AGENTS; FRUIT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; LYCOPERSICON ESCULENTUM; PROTEIN KINASES; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION; SPECIES SPECIFICITY; TRANSCRIPTION FACTORS; VOLATILE ORGANIC COMPOUNDS;

ANIMALIA; LYCOPERSICON ESCULENTUM;

EID: 80755169485     PISSN: 00664197     EISSN: 15452948     Source Type: Book Series    
DOI: 10.1146/annurev-genet-110410-132507     Document Type: Article

References (90)

1. 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 whosemembers display distinct regulatory features. Plant Mol. Biol. 54:387-404 (Pubitemid 39059564)
2. Alba R, Payton P, Fei Z, McQuinn R, Debbie P, et al. 2005. Transcriptome and selected metabolite analyses reveal multiple points of ethylene control during tomato fruit development. Plant Cell 17:2954-65
3. Baldwin EA, Scott JW, Shewmaker CK, Schuch W. 2000. Flavor trivia and tomato aroma: biochemistry and possible mechanisms for control of important aroma components. HortScience 35:1013-22
4. 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 103:7923-28
5. 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. 9:525-35
6. 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. 147:179-87 (Pubitemid 352844352)
7. Barsan C, Sanchez-Bel P, Rombaldi C, Egea I, Rossignol M, et al. 2010. Characteristics of the tomato chromoplast revealed by proteomic analysis. J. Exp. Bot. 61:2413-31
8. Bartley GE, Ishida BK. 2003. Developmental gene regulation during tomato fruit ripening and in vitro sepal morphogenesis. BMC Plant Biol. 7:4
9. 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. Genetics 2:235-40
10. Burg SP, Burg EA. 1962. Role of ethylene in fruit ripening. Plant Physiol. 37:179-89
11. Cancel JD, Larsen PB. 2002. Loss-of-functionmutations in the ethylene receptor ETR1 cause enhanced sensitivity and exaggerated response to ethylene in Arabidopsis. Plant Physiol. 129:1557-67 (Pubitemid 34923219)
12. Centeno DC, Osorio S, Nunes-Nesi A, Bertolo AL F, Carneiro RT, et al. 2011. Malate plays a crucial role in starch metabolism, ripening, and soluble solid content of tomato fruit and affects postharvest softening. Plant Cell 23:162-84
13. Chang C, Stadler, R. 2001. Ethylene hormone receptor action in Arabidopsis. Bioessays 23:619-27 (Pubitemid 32665015)
14. Chen G, Alexander L, GriersonD. 2004. Constitutive expression of EIL-like transcription factor partially restores ripening in the ethylene-insensitive Nr tomato mutant. J. Exp. Bot. 55:1491-97 (Pubitemid 38940861)
15. Chung M, Vrebalov J, Alba R, Lee J, McQuinn R, et al. 2010. A tomato (Solanum lycopersicum) APETALA2/ERF gene, SlAP2a, is a negative regulator of fruit ripening. Plant J. 64:936-47
16. Ciardi J, Tieman D, Lund S, Jones J, Stall R, Klee H. 2000. Response to Xanthomonas campestris pv. vesicatoria in tomato is regulated by changes in both ethylene synthesis and perception. Plant Physiol. 123:81-92 (Pubitemid 30322819)
17. Coen ES, Meyerowitz EM. 1991. The war of the whorls: genetic interactions controlling flower development. Nature 353:31-37 (Pubitemid 21912446)
18. Egea I, Barsan C, Bian WP, Purgatto E, Latche A, et al. 2010. Chromoplast differentiation: current status and perspectives. Plant Cell Physiol. 51:1601-11
19. Elitzur T, Vrebalov J, Giovannoni JJ, Goldschmidt EE, Friedman H. 2010. The regulation of MADSbox gene expression during ripening of banana and their regulatory interaction with ethylene. J. Exp Bot. 61:1523-35
20. Eriksson EM, Bovy A, Manning K, Harrison L, Andrews J, et al. 2004. Effects of the colourless nonripening (Cnr) mutation on gene expression and cell wall biochemistry during tomato fruit development and ripening. Plant Physiol. 136:4184-97
21. Eshed Y, Zamir D. 1995An introgression line population of Lycopersicon pennellii in the cultivated tomato enables the identification and fine mapping of yield-associated QTL. Genetics 141:1147-62
22. 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
23. Filatti JJ, Kiser J, Rose R, Comai L. 1987. Efficient transfer of a glyphosate tolerance gene into tomato using a binary Agrobacterium tumefaciens vector. Biotechnology 5:726-30
24. Gagne JM, Smalle J, Gingerich DJ, Walker JM, Yoo S, et al. 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 101:6803-8 (Pubitemid 38586055)
25. Gamble RL, Coonfield M. Schaller GE. 1998. Histidine kinase activity of the ETR1 ethylene receptor from Arabidopsis. Proc. Natl Acad. Sci. USA 95:7825-29 (Pubitemid 28293338)
26. Gimenez E, Pineda B, Capel J, Anton MT, Atares A, et al. 2010. Functional analysis of the Arlequin mutant corroborates the essential role of the ARLEQUIN/TAGL1 gene during reproductive development of tomato. PLoS ONE 5(12):e14427
27. Giovannoni JJ. 2001. Molecular regulation of fruit ripening. Ann. Rev. Plant Physiol. Plant Mol. Biol. 52:725-49
28. Giovannoni J. 2007. Fruit ripening mutants yield insights into ripening control. Curr. Opin. Plant Biol. 10:283-89 (Pubitemid 46710481)
29. Goff SA, Klee HJ. 2006. Plant volatile compounds: sensory cues for health and nutritional value? Science 311:815-19 (Pubitemid 43228838)
30. Guo H, Ecker JR. 2003. Plant responses to ethylene gas are mediated by SCFEBF1/EBF2-dependent proteolysis of EIN3 transcription factor. Cell 115:667-77 (Pubitemid 38030296)
31. Hall AE, Bleecker AB. 2003. Analysis of combinatorial loss-of-function mutants in the Arabidopsis ethylene receptors reveals that the ers1 etr1 double mutant has severe developmental defects that are EIN2 dependent. Plant Cell 15:2032-41 (Pubitemid 37144059)
32. Hamilton AJ, Lycett GW, Grierson D. 1990. Antisense gene that inhibits synthesis of the hormone ethylene in transgenic plants. Nature 346:284-87 (Pubitemid 120005886)
33. 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. 23:2245-58 (Pubitemid 44536830)
34. Ho LC, Sjut V, Hoad GV. 1983. The effect of assimilate supply in fruit growth and hormone level in tomato plants. Plant Growth Regul. 1:155-71
35. Hua J, Meyerowitz EM. 1998. Ethylene responses are negatively regulated by a receptor gene family in Arabidopsis thaliana. Cell 94:261-71 (Pubitemid 28348013)
36. Iijima Y, Fujiwara Y, Tokita T, Ikeda T, Nohara T, et al. 2009. Involvement of ethylene in the accumulation of esculeoside A during fruit ripening of tomato (Solanum lycopersicum). J. Agric. Food Chem. 57:3247-52
37. Iijima Y, Nakamura Y, Ogata Y, Tanaka K, Sakurai N, et al. 2008. Metabolite annotations based on the integration of mass spectral information. Plant J. 54:949-62 (Pubitemid 351744774)
38. Isaacson T, Kisma DK, Matas AJ, Buda GJ, He Y, et al. 2009. Cutin deficiency in the tomato cuticle consistently affects resistance to microbial infection and biochemical properties, but not transpirational water loss. Plant J. 60:364-77
39. Itkin M, Seybold H, Breitel D, Rogachev I, Meir S, Aharoni A. 2009. Tomato AGAMOUS-LIKE 1 is a component of the fruit ripening regulatory network. Plant J. 60:1081-95
40. Jaakola L, Poole M, Jones MO, Hohtola A, Haggman H, et al. 2010. A MADS box gene involved in the regulation of anthocyanin accumulation in bilberry fruits. Plant Physiol. 153:1619-29
41. Kamiyoshihara Y, Iwata M, Fukaya T, Tatsuki M, Mori H. 2010. Turnover of LeACS2, a woundinducible 1-aminocyclopropane-1-carboxylic acid synthase in tomato, is regulated by phosphorylation/dephosphorylation. Plant J. 64:140-50.
42. Karlova R, Rosin F, Busscher-Lange J, Parapunova V, Do P, et al. 2011. Transcriptome and metabolite profiling show that APETALA2a is a major regulator of tomato fruit ripening. Plant Cell 23:923-41
43. 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. 51:458-67 (Pubitemid 47106552)
44. 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 3:1187-94
45. Kovacs K, Fray RG, Tikunov Y, Graham N, Bradley G, et al. 2009. Effect of tomato pleiotropic ripening mutations on flavour volatile biosynthesis. Phytochem. 70:1003-8
46. Lanahan MB, Yen H-C, Giovannoni JJ, Klee HJ. 1994. The Never-Ripe mutation blocks ethylene perception in tomato. Plant Cell 6:521-30
47. Lashbrook C, Tieman D, Klee H. 1998. Differential regulation of the tomato ETR gene family throughout plant development. Plant J. 15:243-52
48. 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. 130:1132-42 (Pubitemid 35352941)
49. Lewinsohn E, Sitrit Y, Bar E, Azulay Y, Meir A, et al. 2005. Carotenoid pigmentation affects the volatile composition of tomato and watermelon fruits, as revealed by comparative genetic analyses. J. Agric. Food Chem. 53:3142-48 (Pubitemid 40525279)
50. Lin Z, Hong Y, Yin M, Li C, Zhang K, GriersonD. 2008. A tomatoHD-zip homeobox protein, LeHB-1, plays an important role in floral organogenesis and ripening. Plant J. 55:301-10
51. Liljegren S, Ditta G, Eshed Y, Savidge B, Bowman J, Yanofsky M. 2000. SHATTERPROOF MADS-box genes control seed dispersal in Arabidopsis. Nature 404:766-70 (Pubitemid 30212404)
52. Manning K, Tor M, Poole M, Hong Y, Thompson A, et al. 2006. A naturally occurring epigenetic mutation in a gene encoding an SPB-box transcription factor inhibits tomato fruit ripening. Nat. Genet. 38:949-52
53. Moussatche P, Klee H. 2004. Autophosphorylation activity of the Arabidopsis ethylene receptor multigene family. J. Biol. Chem. 279:48734-41 (Pubitemid 39625750)
54. Nakatsuka A, Murachi S, Okunishi H, Shiomi S, Nakano R, et al. 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. 118:1295-305 (Pubitemid 128653063)
55. O'Malley RC, Rodriguez FI, Esch JJ, Binder BM, O'Donnell P, et al. 2005. Ethylene-binding activity, gene expression levels, and receptor system output for ethylene receptor family members from Arabidopsis and tomato. Plant J. 41:651-59 (Pubitemid 40335997)
56. Oeller PW, MinWong L, Taylor LP, Pike DA, Theologis A. 1991. Reversible inhibition of tomato fruit senescence by antisense RNA. Science 254:437-39 (Pubitemid 21917362)
57. Pan I, McQuinn R, Giovannoni J, Irish V. 2010. Functional diversification of AGAMOUS lineage genes in regulating tomato flower and fruit development. J. Exp. Bot. 61:1795-806
58. Pnueli L, Hareven D, Rounsley SD, YanofskyM F, LifschitzE. 1994. Isolation of the tomatoAGAMOUS gene TAG1 and analysis of its homeotic role in transgenic plants. Plant Cell 6:163-73
59. Peralta IE, Spooner DM, Knapp S. 2008. Taxonomy of wild tomatoes and their relatives (Solanum sect. Lycopersicoides, sect. Junglandifolia, sect. Lycopersicon; Solanaceae. Syst. Bot. Monogr. 84:1-186
60. Potuschak T, Lechner E, Parmentier Y, Yanagisawa S, Grava S, et al. 2003. EIN3-dependent regulation of plant ethylene hormone signalling by two Arabidopsis F-box proteins: EBF1 and EBF2. Cell 115:679-89 (Pubitemid 38030297)
61. Pyke KA, Howells CA. 2002. Plastid and stromule morphogenesis in tomato. Ann. Bot. 90:559-66 (Pubitemid 35293898)
62. 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 103:7917-22
63. Rick C, Butler L. 1956. Cytogenetics of the tomato. Adv. Genet. 8:267-382
64. Rick CM, Uhlig JW, Jones AD. 1994. High α-tomatine content in ripe fruit of Andean Lycopersicon esculentum var. cerasiforme: developmental and genetic aspects. Proc. Natl. Acad. Sci. USA 91:12877-81
65. Rodriguez F, Esch J, Hall A, Binder B, Schaller GE, Bleecker AB. 1999. A copper cofactor for the ETR1 receptor from Arabidopsis. Science 283:996-98
66. Rottmann WH, Peter GF, Oeller PW, Keller JA, Shen NF, et al. 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. 222:937-62
67. Santner A, Estelle M. 2009. Recent advances and emerging trends in plant hormone signaling. Nature 459:1071-78
68. Saladie M, Matas AJ, Isaacson T, JenksM A, Goodwin SM, et al. 2007. A re-evaluation of the key factors that contribute to tomato fruit softening and integrity. Plant Physiol. 144:1012-28 (Pubitemid 46944765)
69. Schaller GE, Bleecker AB. 1995. Ethylene binding sites generated in yeast expressing the Arabidopsis ETR1 gene. Science 270:1809-11. (Pubitemid 26007225)
70. Seymour G, Ryder C, Cevik V, Hammond J, Popovich A, et al. 2010. A SEPALLATA gene is involved in the development and ripening of strawberry (Fragaria x annanassa Duch.) fruit, a non-climacteric tissue. J. Exp. Bot. 62:1179-88
71. Simkin A, Schwartz S, Auldridge M, Taylor M, Klee H. 2004. The tomato CCD1 (CAROTENOID CLEAVAGE DIOXGENASE 1) genes contribute to the formation of the flavor volatiles β-ionone, pseudoionone and geranylacetone. Plant J. 40:882-92 (Pubitemid 40047628)
72. Sisler EC, Dupille E, Serek M. 1996. Effect of 1-methylcyclopropene and methylenecyclopropane on ethylene binding and ethylene action on cut carnations. Plant Growth Regul. 18:79-86
73. Speirs J, Lee E, Holt K, Yong-Duk K, Scott NS, et al. 1998. Genetic manipulation of alcohol dehydrogenase levels in ripening tomato fruit affects the balance of some flavor aldehydes and alcohols. Plant Physiol. 117:1047-58 (Pubitemid 128652878)
74. Tieman DM, Klee HJ. 1999. Differential expression of two novel members of the tomato ethylenereceptor family. Plant Physiol. 120:165-72 (Pubitemid 29375419)
75. 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 97:5663-68 (Pubitemid 30313775)
76. Tieman D, Taylor M, Schauer N, Fernie AR, Hanson AD, Klee HJ. 2006. Aromatic amino acid decarboxylases participate in the synthesis of the flavor and aroma volatiles 2-phenylethanol and 2-phenylacetaldehyde in tomato fruits. Proc. Nat. Acad. Sci. USA 103:8287-92 (Pubitemid 43801090)
77. 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 (Pubitemid 32489183)
78. Vancanneyt G, Sanz C, Farmaki T, Paneque M, Ortego F, et al. 2001. Hydroperoxide lyase depletion in transgenic potato plants leads to an increase in aphid performance. Proc. Natl. Acad. Sci. USA 98:8139-44 (Pubitemid 32642700)
79. Vogel JT, Tan BC, McCarty DR, Klee HJ. 2008. The carotenoid cleavage dioxygenase 1 enzyme has broad substrate specificity, cleaving multiple carotenoids at two different bond positions. J. Biol. Chem. 283:11364-73
80. Vogel JT, Tieman DM, Sims CA, Odabasi AZ, Clark DG, Klee HJ. 2010. Carotenoid content impacts flavor acceptability in tomato (Solanum lycopersicum). J. Sci. Food Agric. 90:2233-40
81. Vrebalov J, Ruezinsky D, Padmanabhan V, White R, Medrano D, et al. 2002. A MADS-box gene necessary for fruit ripening at the tomato ripening-inhibitor (rin) locus. Science 296:343-46 (Pubitemid 34303688)
82. Vrebalov J, Pan I, Matas A, McQuinn R, Chung M, et al. 2009. Fleshy fruit expansion and ripening are regulated by the tomato SHATTERPROOF gene, TAGL1. Plant Cell 21:3041-62
83. Wang WY, Hall AE, O'Malley R, Bleecker AB. 2003. Canonical histidine kinase activity of the transmitter domain of the ETR1 ethylene receptor from Arabidopsis is not required for signal transmission. Proc. Natl. Acad. Sci. USA 100:352-57 (Pubitemid 36078078)
84. Wilkinson JQ, LanahanM B, Yen H-C, Giovannoni JJ, Klee HJ. 1995. An ethylene-inducible component of signal transduction encoded by Never-Ripe. Science 270:1807-9 (Pubitemid 26007224)
85. Yang SF. 1987. The role of ethylene and ethylene synthesis in fruit ripening. In Plant Senescence: Its Biochemistry and Physiology, ed. W Thompson, E Nothnagel, R Huffaker, pp. 156-65, Rockville, MD: Am. Soc. Plant Physiol.
86. Yang Y, Wu Y, Pirrello J, Regad F, Bouzayen M, et al. 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
87. Yokotani N, Tamura S, Nakano R, Inaba A, Kubo Y. 2003. Characterization of a novel tomato EIN3-like gene (LeEIL4). J. Exp. Bot. 54:2775-76 (Pubitemid 37537868)
88. Ytterberg AJ, Peltier JB, van Wijk KJ. 2006. Protein profiling of plastoglobules in chloroplasts and chromoplasts. Asurprising site for differential accumulation ofmetabolic enzymes. Plant Physiol. 140:984-97 (Pubitemid 43956251)
89. Zahn LM, Komg H, Leebens-Mack JH, Kim S, Soltis PS, et al. 2005. The evolution of the SEPALLATA subfamily of MADS-box genes. Genetics 169:2209-23
90. Zhou D, Mattoo A, Tucker M. 1996. Molecular cloning of a tomato cDNA encoding an ethylene receptor. Plant Physiol. 110:1435-36