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



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 14:57PubMedCentralPubMedCrossRefGoogle Scholar
  2. ARKive (2013) Galápagos tomato (Solanum cheesmaniae). Accessed 5 Feb 2014
  3. Bai Y, Lindhout P (2007) Domestication and breeding of tomatoes: what have we gained and what can we gain in the future? Ann Bot 100:1085–1094PubMedCentralPubMedCrossRefGoogle Scholar
  4. 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 501:52–62PubMedCrossRefGoogle 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 136:823–832PubMedCrossRefGoogle Scholar
  6. Birchler JA, Yao H, Chudalayandi S et al (2010) Heterosis. Plant Cell 22:2105–2112PubMedCentralPubMedCrossRefGoogle Scholar
  7. Bomblies K, Weigel D (2007) Hybrid necrosis: autoimmunity as a potential gene-flow barrier in plant species. Nat Rev Genet 8:382–393PubMedCrossRefGoogle Scholar
  8. Boyko A, Kovalchuk I (2008) Epigenetic control of plant stress response. Environ Mol Mutagen 49:61–72PubMedCrossRefGoogle Scholar
  9. Brodersen P, Voinnet O (2006) The diversity of RNA silencing pathways in plants. Trends Genet 22:268–280PubMedCrossRefGoogle Scholar
  10. Burge GK, Morgan ER, Seelye JF (2002) Opportunities for synthetic plant chimeral breeding: past and future. Plant Cell Tiss Org Cult 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 17:1012–1024PubMedCentralPubMedCrossRefGoogle Scholar
  12. Chu G, Chang E (1988) Xeroderma pigmentosum group E cells lack a nuclear factor that binds to damaged DNA. Science 242:564–567PubMedCrossRefGoogle Scholar
  13. Cubas P, Vincent C, Coen E (1999) An epigenetic mutation responsible for natural variation in floral symmetry. Nature 401:157–161PubMedCrossRefGoogle 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 103:29–38PubMedCentralPubMedCrossRefGoogle 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 30:731–743PubMedCentralPubMedCrossRefGoogle 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 136:4184–4197PubMedCentralPubMedCrossRefGoogle Scholar
  18. FAO (2013) Food and Agriculture Organization of the United Nations. Accessed 5 Feb 2014
  19. Ferreira e Silva GF, Silva EM, Azevedo Mda S et al (2014) microRNA156-targeted SPL/SBP box transcription factors regulate tomato ovary and fruit development. Plant J 78:604–618PubMedCrossRefGoogle Scholar
  20. Gillpasy G, Ben-David H, Gruissem W (1993) Fruits: a developmental perspective. Plant Cell 5:1439–1451CrossRefGoogle Scholar
  21. 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 11:94PubMedCentralPubMedCrossRefGoogle Scholar
  22. 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 8:864–872PubMedCentralPubMedCrossRefGoogle Scholar
  23. 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, New York, pp 207–221Google Scholar
  24. 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 3:39PubMedCentralPubMedCrossRefGoogle Scholar
  25. 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 8:1277–1283PubMedCrossRefGoogle Scholar
  26. 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 71:51–59PubMedCrossRefGoogle Scholar
  27. 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 121:857–869PubMedCentralPubMedCrossRefGoogle Scholar
  28. Kalisz S, Purugganan MD (2004) Epialleles via DNA methylation: consequences for plant evolution. Trends Ecol Evol 19:309–314PubMedCrossRefGoogle Scholar
  29. 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 9:451PubMedCentralPubMedCrossRefGoogle Scholar
  30. 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 64:1863–1878PubMedCentralPubMedCrossRefGoogle Scholar
  31. Kouzarides T (2007) Chromatin modifications and their function. Cell 128:693–705PubMedCrossRefGoogle Scholar
  32. 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 19:42–56PubMedCentralPubMedCrossRefGoogle Scholar
  33. Lindroth AM, Cao X, Jackson JP et al (2001) Requirement of CHROMOMETHYLASE3 for maintenance of CpXpG methylation. Science 292:2077–2080PubMedCrossRefGoogle Scholar
  34. 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:e42621PubMedCentralPubMedCrossRefGoogle Scholar
  35. 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 29:1005–1017PubMedCentralPubMedCrossRefGoogle Scholar
  36. 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 38:948–952PubMedCrossRefGoogle Scholar
  37. 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 157:1568–1579PubMedCentralPubMedCrossRefGoogle Scholar
  38. Martienssen R, Colot V (2001) DNA methylation and epigenetic inheritance in plants and filamentous fungi. Science 293:1070–1074PubMedCrossRefGoogle Scholar
  39. 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 67:232–246PubMedCrossRefGoogle Scholar
  40. Molnar A, Melnyk CW, Bassett A et al (2010) Small silencing RNAs in plants are mobile and direct epigenetic modification in recipient cells. Science 328:872–875PubMedCrossRefGoogle Scholar
  41. Montgomery TA, Howell MD, Cuperus JT et al (2008) Specificity of ARGONAUTE7-miR390 interaction and dual functionality in TAS3 trans-acting siRNA formation. Cell 133:128–141PubMedCrossRefGoogle Scholar
  42. 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 18:1602–1609PubMedCentralPubMedCrossRefGoogle Scholar
  43. Nuez F, Provens J, Blanca JM (2004) Relationships, origin, and diversity of Galapagos tomatoes: implications for the conservation of natural populations. Am J Bot 91:86–99PubMedCrossRefGoogle Scholar
  44. Ori N, Cohen AR, Etzioni A et al (2007) Regulation of LANCEOLATE by miR319 is required for compound-leaf development in tomato. Nat Genet 39:787–791PubMedCrossRefGoogle Scholar
  45. 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 64:2307–2320PubMedCentralPubMedCrossRefGoogle Scholar
  46. Paterson AH, Bowers JE, Bruggmann R et al (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457:551–556PubMedCrossRefGoogle Scholar
  47. Pekker I, Alvarez JP, Eshed Y (2005) Auxin response factors mediate Arabidopsis organ asymmetry via modulation of KANADI activity. Plant Cell 17:2899–2910PubMedCentralPubMedCrossRefGoogle Scholar
  48. 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, IL, pp 227–257Google Scholar
  49. Piriyapongsa J, Mariño-Ramírez L, Jordan IK (2007) Origin and evolution of human microRNAs from transposable elements. Genetics 176:1323–1337PubMedCentralPubMedCrossRefGoogle Scholar
  50. Preston JC, Hileman LC (2013) Functional evolution in the plant SQUAMOSA-PROMOTER BINDING PROTEIN-LIKE (SPL) gene family. Front Plant Sci 4:80PubMedCentralPubMedGoogle Scholar
  51. 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 30:1347–1363PubMedCrossRefGoogle Scholar
  52. Rieseberg LH, Archer MA, Wayne RK (1999) Transgressive segregation, adaptation and speciation. Heredity 83:363–372PubMedCrossRefGoogle Scholar
  53. Sadeh R, Allis CD (2011) Genome-wide “re”-modeling of nucleosome positions. Cell 147:263–266PubMedCentralPubMedCrossRefGoogle Scholar
  54. 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 235:1171–1184PubMedCrossRefGoogle Scholar
  55. Seymour G, Poole M, Manning K et al (2008) Genetics and epigenetics of fruit development and ripening. Curr Opin Plant Biol 11:58–63PubMedCrossRefGoogle Scholar
  56. 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 31:257–266PubMedCentralPubMedCrossRefGoogle Scholar
  57. Stadler MB, Murr R, Burger L et al (2011) DNA-binding factors shape the mouse methylome at distal regulatory regions. Nature 480:490–495PubMedGoogle Scholar
  58. Stegemann S, Keuthe M, Greiner S et al (2012) Horizontal transfer of chloroplast genomes between plant species. Proc Natl Acad Sci U S A 109:2434–2438PubMedCentralPubMedCrossRefGoogle 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 7:1529–1532PubMedCentralPubMedCrossRefGoogle 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 28:997–998PubMedCentralPubMedCrossRefGoogle 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 228:391–399PubMedCrossRefGoogle 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 120:383–390PubMedCentralPubMedCrossRefGoogle Scholar
  65. Thyssen G, Svab Z, Maliga P (2012) Cell-to-cell movement of plastids in plants. Proc Natl Acad Sci U S A 109:2439–2443PubMedCentralPubMedCrossRefGoogle 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 296:343–346PubMedCrossRefGoogle 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 62:1951–1960PubMedCentralPubMedCrossRefGoogle 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:e61995PubMedCentralPubMedCrossRefGoogle Scholar
  69. Xian Z, Yang Y, Huang W et al (2013) Molecular cloning and characterisation of SlAGO family in tomato. BMC Plant Biol 13:126PubMedCentralPubMedCrossRefGoogle 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 24:3575–3589PubMedCentralPubMedCrossRefGoogle 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 10:260PubMedCentralPubMedCrossRefGoogle Scholar
  73. Zhang X, Yazaki J, Sundaresan A et al (2006) Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell 126:1189–1201PubMedCrossRefGoogle Scholar
  74. Zhang J, Zeng R, Chen J et al (2008) Identification of conserved microRNAs and their targets from Solanum lycopersicum Mill. Gene 423:1–7PubMedCrossRefGoogle 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 585:435–439PubMedCrossRefGoogle 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 31:154–159PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  1. 1.Laboratory of Molecular Genetics of Plant Development, Department of Genetics, Instituto de BiociênciasState University of Sao Paulo (UNESP)BotucatuBrazil

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