Tomato Epigenetics: Deciphering the “Beyond” Genetic Information in a Vegetable Fleshy-Fruited Crop

  • Fabio T. S. Nogueira


The first natural plant mutant for which the molecular basis was determined to be an epimutation rather than a change in DNA sequence was a peloric variant of toadflax, Linaria vulgaris. Remarkably, the second example of a natural epimutant came from the vegetable fleshy-fruited crop tomato (Solanum lycopersicum). The discovery of the molecular basis for the Colorless nonripening (Cnr) epimutation was a landmark for plant epigenetics and, importantly, linked epigenetic mechanisms with an important agronomical trait. More recently, several studies on tomato have contributed to our better understanding of epigenetic mechanisms underlying important heritable crop traits, such as ripening and stress response. Epigenetic mechanisms have also been associated with transgressive segregation in hybrids generated from crosses between cultivated tomato and close wild relatives. Therefore, we can only envision that tomato will became a model for studying the epigenetic basis of economically important phenotypes, allowing for their more efficient exploitation in plant breeding.


Tomato Small RNAs DNA methylation Epiallele 


  1. Aiese Cigliano R, Sanseverino W, Cremona G et al (2013) Genome-wide analysis of histone modifiers in tomato: gaining an insight into their developmental roles. BMC Genomics 14:57CrossRefGoogle Scholar
  2. Arkive (2013) Galápagos tomato (Solanum cheesmaniae). Accessed 5 Feb 2014
  3. Bai M, Yang GS, Chen WT et al (2012) Genome-wide identification of Dicer-like, Argonaute and RNA-dependent RNA polymerase gene families and their expression analyses in response to viral infection and abiotic stresses in Solanum lycopersicum. Gene 501:52–62CrossRefGoogle Scholar
  4. Bai Y, Lindhout P (2007) Domestication and breeding of tomatoes: what have we gained and what can we gain in the future? Ann Bot 100:1085–1094CrossRefGoogle Scholar
  5. Berger Y, Harpaz-Saad S, Brand A et al (2009) The NAC-domain transcription factor GOBLET specifies leaflet boundaries in compound tomato leaves. Development 136:823–832CrossRefGoogle Scholar
  6. Birchler JA, Yao H, Chudalayandi S et al (2010) Heterosis. Plant Cell 22:2105–2112CrossRefGoogle Scholar
  7. Bomblies K, Weigel D (2007) Hybrid necrosis: autoimmunity as a potential gene-flow barrier in plant species. Nat Rev Genet 8:382–393CrossRefGoogle Scholar
  8. Boyko A, Kovalchuk I (2008) Epigenetic control of plant stress response. Environ Mol Mutagen 49:61–72CrossRefGoogle Scholar
  9. Brodersen P, Voinnet O (2006) The diversity of RNA silencing pathways in plants. Trends Genet 22:268–280CrossRefGoogle Scholar
  10. Burge GK, Morgan ER, Seelye JF (2002) Opportunities for synthetic plant chimeral breeding: Past and future. Plant Cell Tissue Organ Culture 70:13–21CrossRefGoogle Scholar
  11. Chen D, Meng Y, Yuan C et al (2011) Plant siRNAs from introns mediate DNA methylation of host genes. RNA 17:1012–1024CrossRefGoogle Scholar
  12. Chu G, Chang E (1988) Xeroderma pigmentosum group E cells lack a nuclear factor that binds to damaged DNA. Science 242:564–567CrossRefGoogle Scholar
  13. Cubas P, Vincent C, Coen E (1999) An epigenetic mutation responsible for natural variation in floral symmetry. Nature 401:157–161CrossRefGoogle Scholar
  14. Darwin C (1868) The variation of animals and plants under domestication. John Murray, LondonGoogle Scholar
  15. Ding D, Zhang LF, Wang H et al (2009) Differential expression of miRNAs in response to salt stress in maize roots. Ann Bot 103:29–38CrossRefGoogle Scholar
  16. Dumbliauskas E, Lechner E, Jaciubek M et al (2011) The Arabidopsis CUL4-DDB1 complex interacts with MSI1 and is required to maintain MEDEA parental imprinting. EMBO J 30:731–743CrossRefGoogle Scholar
  17. Eriksson EM, Bovy A, Manning K et al (2004) Effect of the Colorless non-ripening mutation on cell wall biochemistry and gene expression during tomato fruit development and ripening. Plant Physiol 136:4184–4197CrossRefGoogle Scholar
  18. FAO (2013) Food and Agriculture Organization of the United Nations. Accessed 5 Feb 2014
  19. Gillpasy G, Ben-David H, Gruissem W (1993) Fruits: a developmental perspective. Plant Cell 5:1439–1451CrossRefGoogle Scholar
  20. González RM, Ricardi MM, Iusem ND (2011) Atypical epigenetic mark in an atypical location: cytosine methylation at asymmetric (CNN) sites within the body of a non-repetitive tomato gene. BMC Plant Biol 11:94CrossRefGoogle Scholar
  21. González RM, Ricardi MM, Iusem ND (2013) Epigenetic marks in an adaptive water stress-responsive gene in tomato roots under normal and drought conditions. Epigenetics 8:864–872CrossRefGoogle Scholar
  22. Hamzeiy H, Allmer J, Yousef M (2014) Computational methods for MicroRNA target prediction. In: Yousef M, Allmer J (eds) miRNomics: MicroRNA biology and computational analysis. Methods in molecular biology, vol 1107. Springer Science + Business Media, New York, pp 207–221CrossRefGoogle Scholar
  23. Haroldsen VM, Szczerba MW, Aktas H et al (2012) Mobility of transgenic nucleic acids and proteins within grafted rootstocks for agricultural improvement. Front Plant Sci 3:39CrossRefGoogle Scholar
  24. Higa LA, Wu M, Ye T et al (2006) CUL4-DDB1 ubiquitin ligase interacts with multiple WD40-repeat proteins and regulates histone methylation. Nat Cell Biol 8:1277–1283CrossRefGoogle Scholar
  25. Jia XY, Wang WX, Ren LG et al (2009) Differential and dynamic regulation of miR398 in response to ABA and salt stress in Populus tremula and Arabidopsis thaliana. Plant Mol Biol 71:51–59CrossRefGoogle Scholar
  26. Joubès J, Phan TH, Just D et al (1999) Molecular and biochemical characterization of the involvement of cyclin-dependent kinase A during the early development of tomato fruit. Plant Physiol 121:857–869CrossRefGoogle Scholar
  27. Kalisz S, Purugganan MD (2004) Epialleles via DNA methylation: consequences for plant evolution. Trends Ecol Evol 19:309–314CrossRefGoogle Scholar
  28. Kapoor M, Arora R, Lama T et al (2008) Genome-wide identification, organization and phylogenetic analysis of Dicer-like, Argonaute and RNA-dependent RNA polymerase gene families and their expression analysis during reproductive development and stress in rice. BMC Genomics 9:451CrossRefGoogle Scholar
  29. Karlova R, van Haarst JC, Maliepaard C et al (2013) Identification of microRNA targets in tomato fruit development using high-throughput sequencing and degradome analysis. J Exp Bot 64:1863–1878CrossRefGoogle Scholar
  30. Kouzarides T (2007) Chromatin modifications and their function. Cell 128:693–705CrossRefGoogle Scholar
  31. Kuang H, Padmanabhan C, Li F et al (2009) Identification of miniature inverted-repeat transposable elements (MITEs) and biogenesis of their siRNAs in the Solanaceae: new functional implications for MITEs. Genome Res 19:42–56CrossRefGoogle Scholar
  32. Lindroth AM, Cao X, Jackson JP et al (2001) Requirement of CHROMOMETHYLASE3 for maintenance of CpXpG methylation. Science 292:2077–2080CrossRefGoogle Scholar
  33. Liu J, Tang X, Gao L et al (2012) A role of tomato UV-damaged DNA binding protein 1 (DDB1) in organ size control via an epigenetic manner. PLoS One 7:e42621CrossRefGoogle Scholar
  34. Lu C, Chen J, Zhang Y et al (2012) Miniature inverted-repeat transposable elements (MITEs) have been accumulated through amplification bursts and play important roles in gene expression and species diversity in Oryza sativa. Mol Biol Evol 29:1005–1017CrossRefGoogle Scholar
  35. Manning K, Tör M, Poole M et al (2006) A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening. Nat Genet 38:948–952CrossRefGoogle Scholar
  36. Martel C, Vrebalov J, Tafelmeyer P et al (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 157:1568–1579CrossRefGoogle Scholar
  37. Martienssen R, Colot V (2001) DNA methylation and epigenetic inheritance in plants and filamentous fungi. Science 293:1070–1074CrossRefGoogle Scholar
  38. Mohorianu I, Schwach F, Jing R et al (2011) Profiling of short RNAs during fleshy fruit development reveals stage-specific sRNAome expression patterns. Plant J 67:232–246CrossRefGoogle Scholar
  39. Molnar A, Melnyk CW, Bassett A et al (2010) Small silencing RNAs in plants are mobile and direct epigenetic modification in recipient cells. Science 328:872–875CrossRefGoogle Scholar
  40. Montgomery TA, Howell MD, Cuperus JT et al (2008) Specificity of ARGONAUTE7-miR390 interaction and dual functionality in TAS3 trans-acting siRNA formation. Cell 133:128–141CrossRefGoogle Scholar
  41. Moxon S, Jing R, Szittya G et al (2008) Deep sequencing of tomato short RNAs identifies microRNAs targeting genes involved in fruit ripening. Genome Res 18:1602–1609CrossRefGoogle Scholar
  42. Nuez F, Provens J, Blanca JM (2004) Relationships, origin, and diversity of Galapagos tomatoes: implications for the conservation of natural populations. Am J Bot 91:86–99CrossRefGoogle Scholar
  43. Ori N, Cohen AR, Etzioni A et al (2007) Regulation of LANCEOLATE by miR319 is required for compound-leaf development in tomato. Nat Genet 39:787–791CrossRefGoogle Scholar
  44. Ortiz-Morea FA, Vicentini R, Silva GF et al (2013) Global analysis of the sugarcane microtranscriptome reveals a unique composition of small RNAs associated with axillary bud outgrowth. J Exp Bot 64:2307–2320CrossRefGoogle Scholar
  45. Paterson AH, Bowers JE, Bruggmann R et al (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457:551–556CrossRefGoogle Scholar
  46. Pekker I, Alvarez JP, Eshed Y (2005) Auxin response factors mediate Arabidopsis organ asymmetry via modulation of KANADI activity. Plant Cell 17:2899–2910CrossRefGoogle Scholar
  47. Peralta IE, Spooner DM (2005) Morphological characterization and relationships of wild tomatoes (Solanum L. Section Lycopersicon). In: Keating RC, Hollowell VC, Croat TB (eds) A Festschrift for William G. D'arcy: the legacy of a taxonomist. Missouri Botanical Garden Press, St. Louis, pp 227–257Google Scholar
  48. Piriyapongsa J, Mariño-Ramírez L, Jordan IK (2007) Origin and evolution of human microRNAs from transposable elements. Genetics 176:1323–1337CrossRefGoogle Scholar
  49. Preston JC, Hileman LC (2013) Functional evolution in the plant SQUAMOSA-PROMOTER BINDING PROTEIN-LIKE (SPL) gene family. Front Plant Sci 4:80PubMedPubMedCentralGoogle Scholar
  50. Qian Y, Cheng Y, Cheng X et al (2011) Identification and characterization of Dicer-like, Argonaute and RNA-dependent RNA polymerase gene families in maize. Plant Cell Rep 30:1347–1363CrossRefGoogle Scholar
  51. Rieseberg LH, Archer MA, Wayne RK (1999) Transgressive segregation, adaptation and speciation. Heredity 83:363–372CrossRefGoogle Scholar
  52. Sadeh R, Allis CD (2011) Genome-wide “re”-modeling of nucleosome positions. Cell 147:263–266CrossRefGoogle Scholar
  53. Salinas M, Xing S, Höhmann S et al (2012) Genomic organization, phylogenetic comparison and differential expression of the SBP-box family of transcription factors in tomato. Planta 235:1171–1184CrossRefGoogle Scholar
  54. Seymour G, Poole M, Manning K et al (2008) Genetics and epigenetics of fruit development and ripening. Curr Opin Plant Biol 11:58–63CrossRefGoogle Scholar
  55. Shivaprasad PV, Dunn RM, Santos BA et al (2012) Extraordinary transgressive phenotypes of hybrid tomato are influenced by epigenetics and small silencing RNAs. EMBO J 31:257–266CrossRefGoogle Scholar
  56. Silva GFF (2012) Regulação do desenvolvimento e determinação do fruto de tomateiro (Solanum lycopersicum) pela via microRNA156/ SQUAMOSA Promoter-Binding Protein-Like (SPL). Master Dissertation, University of Sao Paulo, BrazilGoogle Scholar
  57. Stadler MB, Murr R, Burger L et al (2011) DNA-binding factors shape the mouse methylome at distal regulatory regions. Nature 480:490–495PubMedPubMedCentralGoogle Scholar
  58. Stegemann S, Keuthe M, Greiner S et al (2012) Horizontal transfer of chloroplast genomes between plant species. Proc Natl Acad Sci USA 109:2434–2438CrossRefGoogle Scholar
  59. Tang X, Liu J, Huang S et al (2012) Roles of UV-damaged DNA binding protein 1 (DDB1) in epigenetically modifying multiple traits of agronomic importance in tomato. Plant Signal Behav 7:1529–1532CrossRefGoogle Scholar
  60. Teixeira FK, Colot V (2009) Gene body DNA methylation in plants: a means to an end or an end to a means? EMBO J 28:997–998CrossRefGoogle Scholar
  61. Teyssier E, Bernacchia G, Maury S et al (2008) Tissue dependent variations of DNA methylation and endoreduplication levels during tomato fruit development and ripening. Planta 228:391–399CrossRefGoogle Scholar
  62. The Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815CrossRefGoogle Scholar
  63. The Tomato Genome Consortium (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485:635–641CrossRefGoogle Scholar
  64. Thompson AJ, Tor M, Barry CS et al (1999) Molecular and genetic characterization of a novel pleiotropic tomato-ripening mutant. Plant Physiol 120:383–390CrossRefGoogle Scholar
  65. Thyssen G, Svab Z, Maliga P (2012) Cell-to-cell movement of plastids in plants. Proc Natl Acad Sci USA 109:2439–2443CrossRefGoogle Scholar
  66. Vrebalov J, Ruezinsky D, Padmanabhan V et al (2002) A MADS-box gene necessary for fruit ripening at the tomato ripening-inhibitor (rin) locus. Science 296:343–346CrossRefGoogle Scholar
  67. Wang WS, Pan YJ, Zhao XQ et al (2011) Drought-induced site-specific DNA methylation and its association with drought tolerance in rice (Oryza sativa L.). J Exp Bot 62:1951–1960CrossRefGoogle Scholar
  68. Wu R, Wang X, Lin Y et al (2013) Inter-species grafting caused extensive and heritable alterations of DNA methylation in Solanaceae plants. PLoS One 8:e61995CrossRefGoogle Scholar
  69. Xian Z, Yang Y, Huang W et al (2013) Molecular cloning and characterisation of SlAGO family in tomato. BMC Plant Biol 13:126CrossRefGoogle Scholar
  70. Yifhar T, Pekker I, Peled D et al (2012) Failure of the tomato trans-acting short interfering RNA program to regulate AUXIN RESPONSE FACTOR3 and ARF4 underlies the wiry leaf syndrome. Plant Cell 24:3575–3589CrossRefGoogle Scholar
  71. Zamir D, Tanksley SD (1988) Tomato genome is comprised largely of fast-evolving, low copy-number sequences. Mol Gen Genet 213:254–261CrossRefGoogle Scholar
  72. Zanca AS, Vicentini R, Ortiz-Morea FA et al (2010) Identification and expression analysis of microRNAs and targets in the biofuel crop sugarcane. BMC Plant Biol 10:260CrossRefGoogle Scholar
  73. Zhang J, Zeng R, Chen J et al (2008) Identification of conserved microRNAs and their targets from Solanum lycopersicum Mill. Gene 423:1–7CrossRefGoogle Scholar
  74. Zhang X, Yazaki J, Sundaresan A et al (2006) Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell 126:1189–1201CrossRefGoogle Scholar
  75. Zhang X, Zou Z, Zhang J et al (2011) Over-expression of sly-miR156a in tomato results in multiple vegetative and reproductive trait alterations and partial phenocopy of the sft mutant. FEBS Lett 585:435–439CrossRefGoogle Scholar
  76. Zhong S, Fei Z, Chen YR et al (2013) Single-base resolution methylomes of tomato fruit development reveal epigenome modifications associated with ripening. Nat Biotechnol 31:154–159CrossRefGoogle Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Fabio T. S. Nogueira
    • 1
  1. 1.Laboratory of Molecular Genetics of Plant Development, Department of GeneticsInstituto de Biociências, State University of Sao Paulo (UNESP)Sao PauloBrazil

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