Plant Cell, Tissue and Organ Culture

, Volume 91, Issue 2, pp 75–86 | Cite as

Involvement of DNA methylation in tree development and micropropagation

  • Luis Valledor
  • Rodrigo Hasbún
  • Mónica Meijón
  • Jose Luis Rodríguez
  • Estrella Santamaría
  • Marcos Viejo
  • Maria Berdasco
  • Isabel Feito
  • Mario F. Fraga
  • Maria  Jesús Cañal
  • Roberto Rodríguez
Original paper

Abstract

Genes constitute only a small portion of the total genome and precisely controlling their expression represents a substantial problem for their regulation. Furthermore, non-coding DNA, that contains introns repetitive elements and active transposable elements, demands effective mechanisms to silence it long-term. Cell differentiation and development are controlled through temporal and spatial activation and silencing of specific genes. These patterns of gene expression must remain stable for many cell generations and last or change when inductive developmental signals have disappeared or new ones induce new programmes.

What turns genes on and off? Among others, gene regulation is controlled by epigenetic mechanisms, defined as any gene-regulating activity that does not also involve changes in the DNA code and is capable of persisting. It has become apparent that epigenetic control of transcription is mediated through specific states of the chromatin structure. Associations of specific chromosomal proteins, posttranslational histone modifications and DNA methylation are some of the epigenetic mechanisms that are involved in controlling chromatin states. DNA methylation research can be approached from several standpoints, since there is a wide range of techniques available to study the occurrence and localisation of methyldeoxycytosine in the genome. Several studies dealing with DNA methylation in relation to tree development, microproprogation and somaclonal variation will be presented, with the final aim of demonstrating that DNA methylation levels are hallmarks for growing seasonal periods and are related to open windows of competence in plants.

Keywords

Epigenetic Somaclonal variation 5-Methyl-2-deoxycytosine Phase change Dormancy Ageing In vitro tissue culture 

References

  1. Altman A, Loberant B (2000) Micropropagation of plants: principles and practices. In: Tj R (ed) Encyclopedia of Cell Technology, vol 1. John Wiley & Sons, Inc., New York, pp 916–929Google Scholar
  2. Alvarez-Venegas R, Avramova Z (2005) Methylation patterns of histone H3 Lys 4, Lys 9 and Lys 27 in transcriptionally active and inactive Arabidopsis genes and in atx1 mutants. NAR 33:5199–5207PubMedCrossRefGoogle Scholar
  3. Anderson J, Chao W, Horvath D. (2001) A current review on the regulation of dormancy in vegetative buds. Weed Sci 49:581–589CrossRefGoogle Scholar
  4. Arnholdt-Schmitt B, Herterich S, Neumann K (1995) Physiological aspects of genome variavility in tissue culture. I. growth phase-dependent differential DNA methylation of the carrot genome (Daucus carota L.) during primary culture. TAG 91:809–815Google Scholar
  5. Baurens FC, Nicolleau J, Legavre T, Verdeil JL, Monteuuis O (2004) Genomic DNA methylation of juvenile and mature Acacia mangium micropropagated in vitro with reference to leaf morphology as a phase change marker. Tree Physiol 24:401–407PubMedGoogle Scholar
  6. Bender J (2004) DNA methylation and epigenetics. Ann Rev Plant Biol 55:31–68Google Scholar
  7. Bonga JM, von Aderkas P (1993) Rejuvenation of tissues from mature conifers and its implications for propagation in vitro. In: Ahuja MR, Libby WJ (eds) Clonal forestry I, genetics and biotechnology. Springer-Verlag, Berlin, Heidelberg, pp 182–199Google Scholar
  8. Brar DS, Jain SM (1998) Somaclonal variation: mechanisms and applications in crop improvement. In: Jain SM, Brar DS, Ahloowalia BS (eds) Somaclonal variation and induced mutations in crop improvement. Kluwer Academic Publishers, Boston, USA, pp17–37Google Scholar
  9. Burn JE, Bagnall DJ, Metzger JD, Dennis ES, Peacock WJ (1993) DNA methylation, vernalization and the initiation of flowering. PNAS 90(1):287–291PubMedCrossRefGoogle Scholar
  10. Causevic A, Delaunay A, Ounnar S, Righezza M, Delmotte F, Brignolas F, Hagège D, Maury S (2005) DNA methylation and demethylating treatments modify phenotype and cell wall differentiation state in sugarbeet cell lines. Plant Physiol Biochem 43:681–691PubMedCrossRefGoogle Scholar
  11. Charbit E, Legavre T, Lardet L, Bourgeois E, Ferrière N, Carron MP (2004) Identification of differentially expressed cDNA sequences and histological characteristics of Hevea brasiliensis calli in relation to their embryogenic and regenerative capacities. Plant Cell Rep 22:539–548PubMedCrossRefGoogle Scholar
  12. de Diego JG, Rodríguez FD, Rodríguez Lorenzo JL, Cervantes E, Grappin P (2006) cDNA-AFLP analysis of seed germination in Arabidopsis thaliana identifies transposons and new genomic sequences . J Plant Physiol 163:452–462PubMedCrossRefGoogle Scholar
  13. de Keukeleire P, Maes T, Sauer M, Zethof J, Van Montagu M, Gerats T (2001) Analysis by Transposon Display of the behavior of the dTph1 element family during ontogeny and inbreeding of Petunia hybrida. Mol Genet Genomics 265:72–81PubMedCrossRefGoogle Scholar
  14. Finnegan EJ, Genger RK, Peacock WJ, Dennis ES (1998) DNA methylation in plants. Annu Rev Plant Physiol Plant Mol Biol 49:223–247PubMedCrossRefGoogle Scholar
  15. Finnegan EJ, Kovak KA (2000) Plant DNA methyltransferases. Plant Mol Biol 43:189–201PubMedCrossRefGoogle Scholar
  16. Finnegan J, Kovak KA, Jaligot E, Sheldon CC, Peacock WJ, Dennis ES (2005) The downregulation of Flowering Locus C (FLC) expression in plants with low levels of DNA methylation and by vernalization occurs by distinct mechanisms. Plant J 44(20):420–432CrossRefGoogle Scholar
  17. Finnegan EJ, Peacock WJ, Dennis ES (2000) DNA methylation, a key regulator of plant development and other processes. Curr Opin Gen Dev 10:217–223CrossRefGoogle Scholar
  18. Fraga M, Cañal M, Rodriguez R (2002a) Phase-change related epigenetic and physiological changes in Pinus radiata D. Don Planta 215:672–678CrossRefGoogle Scholar
  19. Fraga MF, Esteller M (2002) DNA Methylation: A profile of methods and applications. BioTechniques 33(3):632–649PubMedGoogle Scholar
  20. Fraga MF, Rodriguez R, Cañal MJ (2002c) Genomic DNA methylation–demethylation during aging and reinvigoration of Pinus radiata. Tree Physiol 22:813–816PubMedGoogle Scholar
  21. Fraga MF, Uriol E, Diego LB, Berdasco M, Esteller M, Cañal MJ, Rodríguez R (2002b) High-performance capillary electrophoretic method for the quantification of 5-methyl 2′-deoxycytidine in genomic DNA: Application to plant, animal and human cancer tissues. Electrophoresis 23:1677–1681PubMedCrossRefGoogle Scholar
  22. Frommer M, McDonald LE, Millar DS, Collis CM, Watt F, Grigg GW, Molloy PL, Paul CL (1992) A genomic sequencing protocol that yields a positive display of 5-methylcytosine residues in individual DNA strands. PNAS 89:1827–1831PubMedCrossRefGoogle Scholar
  23. Galaud JP, Gaspa T, Boyer N (1993a) Effect of anti-DNA methylation drugs on growth, level of methylated DNA, peroxidase activity and ethylene production of Bryonia dioica internodes. Physiologia plantarum 87:528–534CrossRefGoogle Scholar
  24. Galaud JP, Gaspa T, Boyer N (1993b) Inhibition of internode growth due to mechanical stress in Bryonia dioica: relationship between changes in DNA methylation and ethylene metabolism. Physiologia plantarum 87:25–30CrossRefGoogle Scholar
  25. Gerger RK, Peacock WJ, Dennis ES, Finnegan EJ (2003) Opposing effects of reduced DNA methylation on flowering time in Arabidopsis thaliana. Planta 2003(3):461–466Google Scholar
  26. Goodrich J, Tweedie S (2002) Remembrance of things past: Chromatin remodelling in plan development. Ann Rev Cell Dev Biol 18:707–746CrossRefGoogle Scholar
  27. Grandbastien M (1998) Activation of plant retrotransposons under stress conditions. Trends Plant Sci Rev 3:181–187CrossRefGoogle Scholar
  28. Grant-Downton RT, Dickinson HG (2005) Epigenetics and its implications for plant biology. 1. The epigenetic network in plants. Ann Bot 96:1143–1164PubMedCrossRefGoogle Scholar
  29. Grant-Downton RT, Dickinson HG (2006) Epigenetics and its implications for plant biology 2. The ‘epigenetic epiphany’: epigenetics, evolution and beyond. Ann Bot 97:11–27PubMedCrossRefGoogle Scholar
  30. Hasbún R, Valledor L, Berdasco M, Santamaría E, Cañal MJ, Rodríguez R, Rios D, Sánchez M (2005) In vitro proliferation and Genome DNA methylation in adult chesnuts. Act Hort 693:333–339Google Scholar
  31. Hasbún R, Valledor L, Berdasco M, Santamaría E, Cañal MJ, Rodríguez R, (2007) Dynamics of DNA methylation during chestnut trees development, Application to breeding programs. Act Hort (in press)Google Scholar
  32. Hirochika H, Sugimoto K, Otsuki Y, Tsugawa H, Kanda M (1996) Retrotransposons of rice involved in mutations induced by tissue culture. PNAS 93:7783–7788PubMedCrossRefGoogle Scholar
  33. Horvath D, Chao W, Anderson J, Foley M. (2003) Knowing when to grow: signal transduction processes regulating dormancy in vegetative buds. Trends Plant Sci 8:534–540PubMedCrossRefGoogle Scholar
  34. Jaligot E, Rival A, Beulé T, Dussert S, Verdeil JL (2000) Somaclonal variation in oil palm (Elaeis guineensis Jacq.): the DNA methylation hypothesis. Plant Cell Rep 19:684–690CrossRefGoogle Scholar
  35. Jenuwein T, Allis CD (2001) Translating the Histone code. Science 293:1074–1080PubMedCrossRefGoogle Scholar
  36. Johnston JW, Harding K, Bremner DH, Souch G, Green J, Lynch PT, Grout B, Benson EE (2005) HPLC analysis of plant DNA methylation: a study of critical methodological factors. Plant Physiol Biochem 43:844–853PubMedCrossRefGoogle Scholar
  37. Jones L, Ratcliff F, Baulcombe DC (2001) RNA-directed transcriptional gene silencing in plants can be inherited independently of the RNA trigger and requires Met1 for maintenance. Curr Biol 11:747–757PubMedCrossRefGoogle Scholar
  38. Joyce SM, Cassells AC (2002) Variation in potato microplant morphology in vitro and DNA methylation. Plant Cell Tissue Organ Cult 70:125–137CrossRefGoogle Scholar
  39. Kaeppler SM, Kaeppler HF, Rhee Y (2000) Epigenetic aspects of somaclonal variation in plants. Plant Mol Biol 43:179–188PubMedCrossRefGoogle Scholar
  40. Kaeppler SM, Phillips RL (1993) Tissue culture-induced DNA methylation variation in maize. PNAS 90:8773–8776PubMedCrossRefGoogle Scholar
  41. Kalendar R, Tanskanen J, Immonen S, Nevo E, Schulman AH (2000) Genome evolution in wild barley (Hordeum spontaneum) by BARE-1 retrotransposon dynamics in response to sharp microclimatic divergence. PNAS 97:6603–6607PubMedCrossRefGoogle Scholar
  42. Karp A (1994) Origins, causes, and uses of variation in plant tissue cultures. In: Vasil IK, Thorpe TA (eds) Plant cell and tissue culture. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 139–151Google Scholar
  43. Kashkush K, Feldman M, Levy AA (2003) Transcriptional activation of retrotransposons alters the expression of adjacent genes in wheat. Nat Genet 33:102–106PubMedCrossRefGoogle Scholar
  44. Kovarìk A, Matyásek R, Leitch B, Gazdová B, Fulnecek J, Bezdek M (1997) Variability in CpNpG methylation in higher plant genomes. Gene 204:308–315CrossRefGoogle Scholar
  45. Kubis SE, Castilho AMF, Vershinin AV, Heslop-Harrison JS (2003) Retroelements, transposons and methylation status in the genome of oil palm (Elaeis guineensis) and the relationship to somaclonal variation. Plant Mol Biol 52:69–79PubMedCrossRefGoogle Scholar
  46. Liu ZL, Han FP, Tan M, Shan XH, Dong YZ, Wang XZ, Fedak GS, Hao·Bao L (2004) Activation of a rice endogenous retrotransposon Tos17 in tissue culture is accompanied by cytosine demethylation and causes heritable alteration in methylation pattern of flanking genomic regions. TAG 109:200–209PubMedCrossRefGoogle Scholar
  47. Maekawa M, Hase Y, Shikazono N, Tanaka A (2003) Induction of somatic instability in stable yellow leaf Mutant of rice by ion beam irradiation. Nucl Instr and Meth in Phys Res B 206:579–585CrossRefGoogle Scholar
  48. Mathieu O, Bender J (2004) RNA-directed DNA methylation. J Cell Sci 117:4881–4888PubMedCrossRefGoogle Scholar
  49. Meijón M (2005) Desarrollo vegetativo y floral en azalea. Marcadores moleculares y fisiológicos de calidad de planta. Dissertation, University of OviedoGoogle Scholar
  50. Miura A, Yonebayashi S, Watanabe K, Toyama T, Shimada H, Kakutani T (2001) Mobilization of transposons by a mutation Abolishing full DNA methylation in Arabidopsis. Nature 411:212–214PubMedCrossRefGoogle Scholar
  51. Morales-Ruiz T, Ortega-Galisteo AP, Ponferrada-Marín MI, Martínez-Macias MI, Ariza RR, Roldán Arjona T (2006) Demeter and Repressor Of Silencing 1 encode 5-methylcytosine-DNA glycosylases. PNAS 103:6853–6858PubMedCrossRefGoogle Scholar
  52. Nakabayashi K, Okamoto M, Koshiba T,Kamiya Y,Nambara E (2005) Genome-wide profiling of stored mRNA in Arabidopsis thaliana seed germination: epigenetic and genetic regulation of transcription in seed. Plant J 41(5):697–709PubMedCrossRefGoogle Scholar
  53. Phillips RL, Kaeppler SM, Olhoft P (1994) Genetic instability of plant tissue cultures: breakdown of normal controls. PNAS 91:5222–5226PubMedCrossRefGoogle Scholar
  54. Portis E, Acquadro A, Lanteri S (2004) Analysis of DNA methylation during germination of pepper (Capsicum annuum L.) seeds using methylation-sensitive amplification polymorphism (MSAP). Plant Sci 166(1):169–178CrossRefGoogle Scholar
  55. Rabinowicz PD, Palmer LE, May BP, Hemann MT, Lowe SW, McCombie WR, Martienssen RA (2003) Genes and transposons are differentially methylated in pants, but not in mammals. Genome Res 13:2658–2664PubMedCrossRefGoogle Scholar
  56. Ramchandani S, Bhattacharya SK, Cervoni M, Szyf M (1999) DNA methylation is a reversible biological signal. PNAS 96:6107–6112PubMedCrossRefGoogle Scholar
  57. Rey M, Diaz-Sala C, Rodríguez R (1994) Effect of repeated severe pruning on endogenous polyamine content in hazelnut trees. Physiologia Plantarum 92(3):487–492CrossRefGoogle Scholar
  58. Reyes Rosa JC, Gruissem HW (2002) Chromatin-Remodeling and Memory Factors. New Regulators of Plant Development. Plant Physiol 130(3):1090–1101CrossRefGoogle Scholar
  59. Richards EJ, Elgin SC (2002) Epigenetic codes for heterochromatin formation and silencing: rounding up the usual suspects. Cell 108:489–500PubMedCrossRefGoogle Scholar
  60. Rodríguez R, Fraga MF, Pacheco J, Cañal MJ (1998) Envejecimiento vegetal. Una barrera a la propagación vegetativa. Alternativas In: Ríos DG, Olate MS (eds)Google Scholar
  61. Rohde A, Prensen E, De Rycke R, Engler G, Van Montagu M, Boerjan W (2002) PtABI3 impinges on the growth and differentiation of embryonic leaves during bud set in poplar. Plant Cell 14:1885–1901PubMedCrossRefGoogle Scholar
  62. Ronemus MJ, Galbiati M, Ticknor C, Chen J, Dellaporta SL (1996) Demethylation-induced developmental pleiotropy in Arabidopsis. Science 273:654–657PubMedCrossRefGoogle Scholar
  63. Ruiz-García L, Cervera M, Martínez-Zapater J (2005) DNA methylation increases throughout Arabidopsis development. Planta 222:201–206CrossRefGoogle Scholar
  64. Russo VEA, Martienssen RA, Riggs AD (1996) Epigenetic mechanisms of gene regulation. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NYGoogle Scholar
  65. Salajova T, Salaj J, Kormutak A, (1999) Initiation of embryogenic tissues and plantlet regeneration from somatic embryos of Pinus nigra Arn. Plant Sci 145:33–40CrossRefGoogle Scholar
  66. Saze H, Scheid OM, Paszkowski J (2003) Maintenance of CpG methylation is essential for epigenetic inheritance during plant gametogenesis. Nat Gen 34:65–69CrossRefGoogle Scholar
  67. Schrader J, Moyle R, Bhalerao R, Hertzberg M, Lundeberg J, Nilsson P, Bhalerao R (2004) Cambial meristem dormancy in trees involves extensive remodelling of the transcriptome. Plant J 40:173–187PubMedCrossRefGoogle Scholar
  68. Shapiro R, Servis RE, Welcher M (1970) Reactions of uracil and cytosine derivatives with sodium bisulfite:a specific deamination method. J Am Chem Soc 92:422–424CrossRefGoogle Scholar
  69. Sheldon CC, Burn JE, Perez PP, Metzger J, Edwards A, Peacock WJ, Dennis ES (1999) The FLF Mads Box gene: a repressor of flowering in Arabidopsis regulated by vernalization and methylation. Plant Cell 11:445–458PubMedCrossRefGoogle Scholar
  70. Shimizu-Sato S, Mori H (2001) Control of outgrowth and dormancy in axillary buds. Plant Physiol 127:1405–1413PubMedCrossRefGoogle Scholar
  71. Shiraishi M, Hayatsu H (2004) High-speed conversion of cytosine to uracil in bisulfite genomic sequencing analysis of dna methylation. DNA Res 11:409–415PubMedCrossRefGoogle Scholar
  72. Singer T, Yordan C, Martienssen RA (2001) Robertson’s mutator transposons in A. thaliana are regulated by the chromatin-re-modelling gene Decrease in DNA Methylation (DDM1). Genes Dev 15:591–602PubMedCrossRefGoogle Scholar
  73. Smulders MJM, Rus-Kortekaas W, Vosman B (1995) Tissue culture-induced DNA methylation polymorphisms in repetitive DNA of tomato calli and regenerated plants. TAG 91:1257–1264Google Scholar
  74. Steimer A, Schob H, Grossniklaus U (2004) Epigenetic control of plant development: new layers of complexity. Curr Opin Plant Biol 7:11–19PubMedCrossRefGoogle Scholar
  75. Sung S, Amasino R (2004) Vernalization and epigenetics: how plants remember winter. Curr Opin Plant Biol 7:4–10PubMedCrossRefGoogle Scholar
  76. Tariq M, Paszkowski J (2004) DNA and histone methylation in plants. Trends Genet 20:244–251PubMedCrossRefGoogle Scholar
  77. Valledor L (2005) Monitorización epigenética de la producción comercial de cuatro clones de Pinus radiata D. Don mediante estaquillado y macroinjerto. Dissertation, University of OviedoGoogle Scholar
  78. Vlasova TI, Demidenko ZN, Kirnos MD, Vanyushin BF (1995) In vitro DNA methylation by wheat nuclear cytosine DNA methytransferase: effect of phytohormones. Gene 157:279–281PubMedCrossRefGoogle Scholar
  79. von Aderkas P, Bonga J (2000) Influencing micropropagation and somatic embrygenesis in mature trees by manipulation of phase change, stress and culture environment. Tree Physiol 20:921–928Google Scholar
  80. Vongs A, Kakutani T, Martienssen RA, Richards EJ (1993) Arabidopsis thaliana DNA methylation mutants. Science 260:1926–1928PubMedCrossRefGoogle Scholar
  81. Walbot V, Cullis CA (1985) Rapid genomic change in higher plants. Annu Rev Plant Physiol 36:367–396CrossRefGoogle Scholar
  82. Warnecke PM, Stirzaker C, Song J, Grunau C, Melki JR, Clarka SJ (2002) Identification and resolution of artifacts in bisulfite sequencing. Methods 27:101–107PubMedCrossRefGoogle Scholar
  83. Whitelaw E, Martin DIK (2001) Retrotransposons as epigenetic mediators of phenotypic variation in mammals. Nat Genet 27:361–365PubMedCrossRefGoogle Scholar
  84. Xiong Z, Laird PW (1997) COBRA: a sensitive and quantitative DNA methylation assay. Nucleic Acids Res 25:2532–2534PubMedCrossRefGoogle Scholar
  85. Yang I, Park IY, Jang S-M, Shi LH, Ku H-K, Park S-R (2006) Rapid quantification of DNA methylation through dNMP analysis following bisulfite-PCR. Nucl Acids Res 34(e61):61–69CrossRefGoogle Scholar
  86. Zhang X, Yazaki J, Sundaresan A, Cokus S, Chan SW-L, Chen H, Henderson IR, Shinn P, Pellegrini M, Jacobsen SE, Ecker JR (2006) Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell 126:1189–1201PubMedCrossRefGoogle Scholar
  87. Zluvova J, Janousek B, Vyskot B (2001) Immunohistochemical study of DNA methylation dynamics during plant development. J Exp Bot 52:2265–2273PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  • Luis Valledor
    • 1
    • 2
  • Rodrigo Hasbún
    • 1
    • 2
  • Mónica Meijón
    • 1
    • 2
    • 3
  • Jose Luis Rodríguez
    • 1
    • 2
  • Estrella Santamaría
    • 1
    • 2
  • Marcos Viejo
    • 1
  • Maria Berdasco
    • 4
  • Isabel Feito
    • 3
  • Mario F. Fraga
    • 4
  • Maria  Jesús Cañal
    • 1
    • 2
  • Roberto Rodríguez
    • 1
    • 2
  1. 1.Plant Physiology, Epiphysage Research Group, B.O.S. Department, Faculty of BiologyUniversity of OviedoOviedoSpain
  2. 2.Asturias Institute of Biotechnology (Associated with CSIC)AsturiasSpain
  3. 3.SERIDAAsturias Service of Agricultural Research, CtraVillaviciosaSpain
  4. 4.Cancer Epigenetics Laboratory, Molecular Pathology ProgrammeNational Cancer Centre (CNIO)MadridSpain

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