The Epigenome and Transcriptional Dynamics of Fruit Ripening

Annual Review of Plant Biology

Volumn 68, Issue , 2017, Pages 61-84

  Giovannoni, James ^a,b,c   Nguyen, Cuong ^c,e   Ampofo, Betsy ^c   Zhong, Silin ^d   Fei, Zhangjun ^b  

^a AGRICULTURAL RESEARCH SERVICE   (United States)

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

^c Department of Obstetrics Gynecology   (United States)

^d CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^e UNIVERSITY OF FLORIDA   (United States)

Author keywords

DNA methylation; Epigenome; Fruit ripening; Tomato; Transcription factor

Indexed keywords

EID: 85019002711     PISSN: 15435008     EISSN: 15452123     Source Type: Book Series    
DOI: 10.1146/annurev-arplant-042916-040906     Document Type: Review

References (106)

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
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. Allis D, Jenuwein T. 2016. The hallmarks of epigenetic control. Nat. Rev. Genet. 17:487-500
4. Aquea F, Timmermann T, Arce-Johnson P. 2010. Analysis of histone acetyltransferase and deacetylase families of Vitis vinifera. Plant Physiol. Biochem. 48:194-99
5. Ayub R, Guis M, Ben Amor M, Gillot L, Roustan JP, et al. 1996. Expression of ACC oxidase antisense gene inhibits ripening of cantaloupe melon fruits. Nat. Biotechnol. 14:862-66
6. Baubec T, Ivanek R, Lienert F, Schubeler D. 2013. Methylation-dependent and -independent genomic targeting principles of the MBD protein family. Cell 153:480-92
7. Becker C, Hagmann J, Muller J, Koenig D, Stegle O, et al. 2011. Spontaneous epigenetic variation in the Arabidopsis thaliana methylome. Nature 480:245-49
8. Bemer M, Karlova R, Ballester AR, Tikunov YM, Bovy AG, et al. 2012. The tomato FRUITFULL homologs TDR4/FUL1 and MBP7/FUL2 regulate ethylene-independent aspects of fruit ripening. Plant Cell 24:4437-51
9. Bi F, Meng X, Ma C, Yi G. 2015. Identification of miRNAs involved in fruit ripening of Cavendish bananas by deep sequencing. BMC Genom. 16:776
10. Boureau L, How-Kit A, Teyssier E, Drevensek S, Rainieri M, et al. 2016. A CURLY LEAF homologue controls both vegetative and reproductive development of tomato plants. Plant Mol. Biol. 90:485-501
11. Breitel DA, Chappell-Maor L, Meir S, Panizel I, Puig CP, et al. 2016. AUXIN RESPONSE FACTOR 2 intersects hormonal signals in the regulation of tomato fruit ripening. PLOS Genet. 12:e1005903
12. Burg SP, Burg EA. 1965. Ethylene action and ripening of fruits: Ethylene influences growth and development of plants and is the hormone which initiates fruit ripening. Science 148:1190-96
13. Burkhardt PK, Beyer P, Wunn J, Kloti A, Armstrong GA, et al. 1997. Transgenic rice (Oryza sativa) endosperm expressing daffodil (Narcissus pseudonarcissus) phytoene synthase accumulates phytoene, a key intermediate of provitamin A biosynthesis. Plant J. 11:1071-78
14. Candaele J, Demuynck K, Mosoti D, Beemster GTS, InzéD, Nelissen H. 2014. Differential methylation during maize leaf growth targets developmentally regulated genes. Plant Physiol. 164:1350-64
15. Chahrour M, Jung SY, Shaw C, Zhou X, Wong ST, et al. 2008. MeCP2, a key contributor to neurological disease, activates and represses transcription. Science 320:1224-29
16. Chen H, Shen Y, Tang X, Yu L, Wang J, et al. 2006. Arabidopsis CULLIN4 forms an E3 ubiquitin ligase with RBX1 and the CDD complex in mediating light control of development. Plant Cell 18:1991-2004
17. Chen W, Kong J, Qin C, Yu S, Tan J, et al. 2015. Requirement of CHROMOMETHYLASE3 for somatic inheritance of the spontaneous tomato epimutation colourless non-ripening. Sci. Rep. 5:9192
18. Cherian S, Figueroa CR, Nair H. 2014. 'Movers and shakers' in the regulation of fruit ripening: a cross-dissection of climacteric versus non-climacteric fruit. J. Exp. Bot. 65:4705-22
19. Christou P, Ford T, Kofron M. 1991. Production of transgenic rice (Oryza sativa L.) plants from agronomically important Indica and Japonica varieties via electric discharge particle acceleration of exogenous DNA into immature zygotic embryos. Nat. Biotechnol. 9:957-62
20. Chung MY, 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
21. Cigliano RA, Sanseverino W, Cremona G, Ercolano MR, Conicella C, Consiglio FM. 2013. Genomewide analysis of histone modifiers in tomato: gaining an insight into their developmental roles. BMC Genom. 14:57
22. Daminato M, Guzzo F, Casadoro G. 2013. A SHATTERPROOF-like gene controls ripening in nonclimacteric strawberries, and auxin and abscisic acid antagonistically affects its expression. J. Exp. Bot. 64:3775-86
23. Dandekar AM, Teo G, Defilippi BG, Uratsu SL, Passey AJ, et al. 2004. Effect of down-regulation of ethylene biosynthesis on fruit flavor complex in apple fruit. Transgenic Res. 13:373-84
24. DellaPenna D, Alexander DC, Bennett AB. 1986. Molecular cloning of tomato fruit polygalacturonase: analysis of polygalacturonase mRNA levels during ripening. PNAS 83:6420-24
25. D'Hont A, Denoeud F, Aury J-M, Baurens F-C, Carreel F, et al. 2012. The banana (Musa acuminata) genome and the evolution of monocotyledonous plants. Nature 488:213-17
26. Dong T, Hu Z, Deng L, Wang Y, Zhu M, et al. 2013. A tomato MADS-box transcription factor, SlMADS1, acts as a negative regulator of fruit ripening. Plant Physiol. 163:1026-36
27. Dowen RH, Pelizzola M, Schmitz RJ, Lister R, Dowen JM, et al. 2012. Widespread dynamic DNA methylation in response to biotic stress. PNAS 109:E2183-91
28. Elitzur T, Yakir E, Quansah L, Fei Z, Vrebalov J, et al. 2016. Banana MaMADS transcription factors are necessary for fruit ripening and molecular tools to promote shelf-life and food security. Plant Physiol. 171:380-91
29. Fich EA, Segerson NA, Rose JKC. 2016. The plant polyester cutin: biosynthesis, structure, and biological roles. Annu. Rev. Plant Biol. 67:207-33
30. Fisher AJ, Franklin KA. 2011. Chromatin remodeling in plant light signaling. Physiol. Plant. 142:305-13
31. 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
32. Fujisawa M, Nakano T, Shima Y, Ito Y. 2013. A large-scale identification of direct targets of the tomato MADS box transcription factor RIPENING INHIBITOR reveals the regulation of fruit ripening. Plant Cell. 25:371-86
33. Fujisawa M, Shima K, Nakagawa H, Kitagawa M, Kimbara J, et al. 2014. Transcriptional regulation of fruit ripening by tomato FRUITFULL homologs and associated MADS box proteins. Plant Cell 26:89-101
34. Gallusci P, Hodgman C, Teyssier E, Seymour GB. 2016. DNA methylation and chromatin regulation during fleshy fruit development and ripening. Front. Plant Sci. 7:807
35. García-Aguilar M, Gillmor CS. 2015. Zygotic genome activation and imprinting: parent-of-origin gene regulation in plant embryogenesis. Curr. Opin. Plant Biol. 27:29-35
36. Garcia-Mas J, Benjak A, Sanseverino W, Bourgeois M, Mir G, et al. 2012. The genome ofmelon (Cucumis melo L.). PNAS 109:11872-77
37. Gimenez E, Castañeda L, Pineda P, Pan IL, Moreno V, et al. 2016. TOMATO AGAMOUS1 and ARLEQUIN/TOMATO AGAMOUS-LIKE1 MADS-box genes have redundant and divergent functions required for tomato reproductive development. Plant Mol. Biol. 91:513-31
38. Giovannoni J, Tanksley S, Vrebalov J, Noensie E. 2004. NOR gene for use in manipulation of fruit quality and ethylene response. US Patent No. 6762347
39. Gouil Q, Novák O, Baulcombe D. 2016. SLTAB2 is the paramutated SULFUREA locus in tomato. J. Exp. Bot. 67:2655-64
40. Hadfield KA, Dandekar AM, Romani RJ. 1993. Demethylation of ripening specific genes in tomato fruit. Plant Sci. 92:13-18
41. Hamilton AJ, Lycett GW, Grierson D. 1990. Antisense gene that inhibits synthesis of the hormone ethylene in transgenic plants. Nature 346:284-87
42. Hao Y, Hu G, Breitel D, Liu M, Mila I, et al. 2015. Auxin response factor SlARF2 is an essential component of the regulatory mechanism controlling fruit ripening in tomato. PLOS Genet. 11:1-23
43. Harjes CE, Rocheford TR, Bai L, Brutnell TP, Kandianis CB, et al. 2008. Natural genetic variation in lycopene epsilon cyclase tapped for maize biofortification. Science 319:330-33
44. Hen-Avivi S, Lashbrooke J, Costa F, Aharoni A. 2014. Scratching the surface: genetic regulation of cuticle assembly in fleshy fruit. J. Exp. Bot. 65:4653-64
45. Hirakawa H, Shirasawa K, Miyatake K, Nunome T, Negoro S, et al. 2014. Draft genome sequence of eggplant (Solanum melongena L.): the representative Solanum species indigenous to the old world. DNA Res. 21:649-60
46. How Kit AH, Boureau L, Stammitti-Bert L, Rolin D, Teyssier E, Gallusci P. 2010. Functional analysis of SlEZ1 a tomato Enhancer of zeste (E(z)) gene demonstrates a role in flower development. Plant Mol. Biol. 74:201-13
47. Hsieh TF, Shin J, Uzawa R, Silva P, Cohen S, et al. 2011. Regulation of imprinted gene expression in Arabidopsis endosperm. PNAS 108:1755-62
48. 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
49. Jackson JP, Lindroth AM, Cao X, Jacobsen SE. 2002. Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature 416:556-60
50. Ji K, Kai W, Zhao B, Sun Y, Yuan B, et al. 2014. SlNCED1 and SlCYP707A2: key genes involved in ABA metabolism during tomato fruit ripening. J. Exp. Bot. 65:5243-55
51. Kadomura-Ishikawa Y, Miyawaki K, Takahashi A, Masuda T, Noji S. 2015. Light and abscisic acid independently regulate FaMYB10 in Fragaria × ananassa fruit. Planta 241:953-65
52. Karlova R, Chapman N, David K, Angenent GC, Seymour GB, de Maagd RA. 2014. Transcriptional control of fleshy fruit development and ripening. J. Exp. Bot. 65:4527-41
53. Karlova R, Rosin FM, Busscher-Lange J, Parapunova V, Do PT, et al. 2011. Transcriptome and metabolite profiling show that APETALA2a is a major regulator of tomato fruit ripening. Plant Cell 23:923-41
54. Kim S, Park M, Yeom S-I, Kim Y-M, Lee JM, et al. 2014. Genome sequence of the hot pepper provides insights into the pungency in Capsicum species. Nat. Genet. 46:270-78
55. King G. 2015. Crop epigenetics and the molecular hardware of genotype × environment interactions. Front. Plant Sci. 6:968
56. Klee HJ, Giovannoni JJ. 2011. Genetics and control of tomato fruit ripening and quality attributes. Annu. Rev. Genet. 45:41-59
57. Kou X, Liu C, Han L, Wang S, Xue Z. 2016. NAC transcription factors play an important role in ethylene biosynthesis, reception and signaling of tomato fruit ripening. Mol. Genet. Genom. 291:1205-17
58. Kuhn N, Guan L, Dai ZW, Wu BH, Lauvergeat V, et al. 2014. Berry ripening: recently heard through the grapevine. J. Exp. Bot. 65:4543-59
59. Kullan JB, Pinto DLP, Bertolini E, Fasoli M, Zenoni S, et al. 2015. miRVine: a microRNA expression atlas of grapevine based on small RNA sequencing. BMC Genom. 16:393
60. Law JA, Jacobsen SE. 2010. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat. Rev. Genet. 11:204-20
61. Lee J, Joung J, McQuinn R, Chung M, Fei Z, et al. 2012. Combined transcriptome, genetic diversity andmetabolite profiling in tomato fruit reveals the ethylene response factor SlERF6 to play an important role in ripening and carotenoid accumulation. Plant J. 70:191-204
62. Li Y, Deng H, Miao M, Li H, Huang S, et al. 2015. Tomato MBD5, a methyl CpG binding domain protein, physically interacting with UV-damaged DNA binding protein-1 functions in multiple processes. New Phytol. 210:208-26
63. 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
64. 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. 55:301-10
65. Lincoln JE, Cordes S, Read E, Fischer RL. 1987. Regulation of gene expression by ethylene during Lycopersicon esculentum (tomato) fruit development. PNAS 84:2793-97
66. Lippman ZB, Semel Y, Zamir D. 2007. An integrated view of quantitative trait variation using tomato interspecific introgression lines. Curr. Opin. Genet. Dev. 17:545-52
67. Liu DD, Zhou LJ, Fang MJ, Dong QL, An XH, et al. 2016. Polycomb-group protein SlMSI1 represses the expression of fruit-ripening genes to prolong shelf life in tomato. Sci. Rep. 6:31806
68. Liu R, How-Kit A, Stammitti L, Teyssier E, Rolin D, et al. 2015. A DEMETER-like DNA demethylase governs tomato fruit ripening. PNAS 112:10804-9
69. Liu Y, Roof S, Ye Z, Barry C, van Tuinen A, et al. 2004. Manipulation of light signal transduction as a means of modifying fruit nutritional quality in tomato. PNAS 101:9897-902
70. Lopez AB, Van Eck J, Conlin BJ, Paolillo DJ, O'Neill J, Li L. 2008. Effect of the cauliflower Or transgene on carotenoids accumulation and chromoplast formation in transgenic potato tubers. J. Exp. Bot. 59:213-23
71. 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
72. Martel C, Vrebalov J, Tafelmeyer P, Giovannoni J. 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. 157:1568-79
73. Martin LB, Rose JKC. 2014. There's more than one way to skin a fruit: formation and functions of fruit cuticles. J. Exp. Bot. 65:4639-51
74. Matzke MA, Kanno T, Matzke AJM. 2015. RNA-directedDNA methylation: the evolution of a complex epigenetic pathway in flowering plants. Annu. Rev. Plant Biol. 66:243-67
75. McMurchie EJ, McGlasson WB, Eaks IL. 1972. Treatment of fruit with propylene gives information about the biogenesis of ethylene. Nature 237:235-36
76. Messeguer R, Ganal M, Steffens J, Tanksley SD. 1991. Characterization of the level, target sites and inheritance of cytosine methylation in tomato nuclear DNA. Plant Mol. Biol. 16:753-70
77. Mustilli AC, Fenzi F, Ciliento R, Alfano F, Bowler C. 1999. Phenotype of the tomato high pigment-2 mutant is caused by a mutation in the tomato homolog of DEETIOLATED1. Plant Cell 11:145-57
78. Nguyen C, Vrebalov J, Gapper N, Zheng Y, Zhong S, et al. 2014. Tomato Golden 2-like (GLK) transcription factors revealmolecular gradients functioning during fruit development and ripening. Plant Cell 26:585-601
79. Oeller PW, MinWong L, Taylor LP, Pike DA, Theologis A. 1991. Reversible inhibition of tomato fruit senescence by antisense RNA. Science 254:437-39
80. Palumbo MC, Zenoni S, Fasoli M, Massonnet M, Farina L, et al. 2014. Integrated network analysis identifies fight-club nodes and a class of hubs encompassing key putative switch genes that induce major transcriptome reprogramming during grapevine development. Plant Cell 26:4617-35
81. Pnueli L, Hareven D, Rounsley SD, Yanofsky MF, Lifschitz E. 1994. Isolation of the tomatoAGAMOUS gene TAG1 and analysis of its homeotic role in transgenic plants. Plant Cell 6:163-73
82. Powell A, Nguyen C, Hill T, Cheng K, Figueroa-Balderas R, et al. 2012. Uniform ripening encodes a Golden 2-like transcription factor regulating tomato fruit chloroplast development. Science 336:1711-15
83. Quadrana L, Almeida J, Asis R, Duffy T, Dominguez PG, et al. 2014. Natural occurring epialleles determine vitamin E accumulation in tomato fruits. Nat. Commun. 5:4027
84. Rodrigues J, Zilberman D. 2015. Evolution and function of genomic imprinting in plants. Genes Dev. 29:2517-31
85. Schmidz RJ, Schultz MD, Lewsey MG, O'Malley RC, Urich MA, et al. 2011. Transgenerational epigenetic instability is a source of novel methylation variants. Science 334:369-73
86. Schnable PS, Springer NM. 2013. Progress toward understanding heterosis in crop plants. Annu. Rev. Plant Biol. 64:71-88
87. Seymour GB, Østergaard L, Chapman NH, Knapp S, Martin C. 2013. Fruit development and ripening. Annu. Rev. Plant Biol. 64:219-41
88. Seymour GB, Ryder C, Cevik V, Hammond J, Popovich A, et al. 2011. A SEPALLATA gene is involved in the development and ripening of strawberry (Fragaria × ananassa Duch.) fruit, a non-climacteric tissue. J. Exp. Bot. 62:1179-88
89. Shivaprasad PV, Dunn RM, Santos BACM, Bassett A, Baulcombe DC. 2012. Extraordinary transgressive phenotypes of hybrid tomatoes are influenced by epigenetics and small silencing RNAs. EMBOJ. 31:257-66
90. Tadiello A, Pavanello A, Zanin D, Caporali E, Colombo L, et al. 2009. A PLENA-like gene of peach is involved in carpel formation and subsequent transformation into a fleshy fruit. J. Exp. Bot. 60:651-61
91. Tang X, Miao M, Niu X, Zhang D, Cao X, et al. 2015. Ubiquitin-conjugated degradation of golden 2-like transcription factor is mediated by CUL4-DDB1-based E3 ligase complex in tomato. New Phytol. 209:1028-39
92. Taylor IB, Linforth RST, Al-Naieb RJ, Bowman WR, Marples BA. 1988. The wilty tomato mutants flacca and sitiens are impaired in the oxidation of ABA-aldehyde to ABA. Plant Cell Environ. 11:739-45
93. 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
94. 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. PNAS 97:5663-68
95. Tomato Genom. Consort. 2012. The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485:635-41
96. Uluisik S, Chapman NH, Smith R, Poole M, Adams G, et al. 2016. Genetic improvement of tomato by targeted control of fruit softening. Nat. Biotechnol. 34:950-52
97. Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, et al. 2010. The genome of the domesticated apple (Malus × domestica Borkh.). Nat. Genet. 42:833-39
98. 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
99. Vrebalov J, Ruezinsky D, Padmanabhan V, White R, Medrano D, et al. 2002. AMADS-box gene necessary for fruit ripening at the tomato ripening-inhibitor (rin) locus. Science 296:343-46
100. Woo HR, Dittmer TA, Richards EJ. 2008. Three SRA-domain methylcytosine-binding proteins cooperate tomaintain global CpG methylation and epigenetic silencing in Arabidopsis. PLOS Genet. 4:e1000156
101. Wu W, Yang YL, He WM, Rouard M, Li WM, et al. 2016. Whole genome sequencing of a banana wild relative Musa itinerans provides insights into lineage-specific diversification of the Musa genus. Sci. Rep. 6:31586
102. Ye X, Al-Babili S, Kloti A, Zhang J, Lucca P, et al. 2000. Engineering the provitamin A (β-carotene) biosynthetic pathway into (carotenoids-free) rice endosperm. Science 287:303-5
103. Zemach A, Kim MY, Silva P, Rodrigues JA, Dotson B, et al. 2010. Local DNAhypomethylation activates genes in rice endosperm. PNAS 107:18729-34
104. Zhao L, Lu J, Zhang J, Wu PY, Yang S, Wu K. 2014. Identification and characterization of histone deacetylases in tomato (Solanum lycopersicum). Front. Plant Sci. 5:760
105. Zhong S, Fei Z, Chen Y, Zheng Y, Huang M, et al. 2013. Single-base resolution methylomes of tomato fruit development reveal epigenome modifications associated with ripening. Nat. Biotechnol. 31:154-59
106. Zhu M, Chen G, Zhou S, Tu Y, Wang Y, et al. 2014. A new tomatoNAC(NAM/ATAF1/2/CUC2) transcription factor, SlNAC4, functions as a positive regulator of fruit ripening and carotenoid accumulation. Plant Cell Physiol. 55:119-35