Epigenetic Basis of Somaclonal Variation

  1. Linacero de la Fuente, María Rosario 1
  2. Ballesteros Redondo, Isabel 1
  1. 1 Universidad Complutense de Madrid
    info

    Universidad Complutense de Madrid

    Madrid, España

    ROR 02p0gd045

Livre:
Somaclonal Variation: Basic and Practical Aspects

Éditorial: Sánchez-Romero, Carolina

ISBN: 9783031516252 9783031516269

Année de publication: 2024

Pages: 21-35

Type: Chapitre d'ouvrage

DOI: 10.1007/978-3-031-51626-9_2 GOOGLE SCHOLAR lock_openAccès ouvert editor

Résumé

Epigenetic changes induced in in vitro culture affect gene expression in a more or less permanent way, and in some cases are transmitted to the progeny. These changes affect chromatin structure and include changes in DNA methylation, histone modifications and the expression of small RNAs involved in DNA methylation (RNA-directed DNA methylation; RdDM). DNA methylation is one of the best studied epigenetic marks in regenerated plants, and changes in the methylation pattern have been reported to be the cause of somaclonal variation in many species. This chapter reviews the epigenetic basis of somaclonal variation and the tools used to detect it.

Références bibliographiques

  • Ashapkin VV, Kutueva LI, Aleksandrushkina NI, Vanyushin BF (2020) Epigenetic mechanisms of plant adaptation to biotic and abiotic stresses. Int J Mol Sci 21:7457. https://doi.org/10.3390/ijms21207457
  • Axtell MJ, Meyers BC (2018) Revisiting criteria for plant microRNA annotation in the era of big data. Plant Cell 30:272–284. https://doi.org/10.1105/tpc.17.00851
  • Baránek M, Čechová J, Kovacs T et al (2016) Use of combined MSAP and NGS techniques to identify differentially methylated regions in somaclones: a case study of two stable somatic wheat mutants. PLoS ONE 11:e0165749. https://doi.org/10.1371/JOURNAL.PONE.0165749
  • Bednarek PT, Orłowska R (2020) Plant tissue culture environment as a switch-key of (epi)genetic changes. Plant Cell Tissue Organ Cult 140:245–257. https://doi.org/10.1007/s11240-019-01724-1
  • Bednarek PT, Orłowska R, Koebner RMD, Zimny J (2007) Quantification of the tissue-culture induced variation in barley (Hordeum vulgare L.). BMC Plant Biol 7:1–9. https://doi.org/10.1186/1471-2229-7-10
  • Bobadilla Landey R, Cenci A, Georget F et al (2013) High genetic and epigenetic stability in Coffea arabica plants derived from embryogenic suspensions and secondary embryogenesis as revealed by AFLP, MSAP and the phenotypic variation rate. PLoS ONE 8:e56372. https://doi.org/10.1371/journal.pone.0056372
  • Bobadilla Landey R, Cenci A, Guyot R et al (2015) Assessment of genetic and epigenetic changes during cell culture ageing and relations with somaclonal variation in Coffea arabica. Plant Cell Tissue Organ Cult 122:517–531. https://doi.org/10.1007/s11240-015-0772-9
  • Borges F, Donoghue MTA, LeBlanc C et al (2021) Loss of small-RNA-directed DNA methylation in the plant cell cycle promotes germline reprogramming and somaclonal variation. Curr Biol 31:591-600.e4. https://doi.org/10.1016/j.cub.2020.10.098
  • Bouyer D, Roudier F, Heese M et al (2011) Polycomb repressive complex 2 controls the embryo-to-seedling phase transition. PLoS Genet 7:1002014. https://doi.org/10.1371/journal.pgen.1002014
  • Cao Q, Feng Y, Dai X et al (2021) Dynamic changes of DNA methylation during wild strawberry (Fragaria nilgerrensis) tissue culture. Front Plant Sci 12:1–13. https://doi.org/10.3389/fpls.2021.765383
  • Cheng C, Daigen M, Hirochika H (2006) Epigenetic regulation of the rice retrotransposon Tos17. Mol Genet Genomics 276:378–390. https://doi.org/10.1007/s00438-006-0141-9
  • Cokus SJ, Feng S, Zhang X et al (2008) Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature 452:215–219. https://doi.org/10.1038/nature06745
  • Coronel CJ, González AI, Ruiz ML, Polanco C (2018) Analysis of somaclonal variation in transgenic and regenerated plants of Arabidopsis thaliana using methylation related metAFLP and TMD markers. Plant Cell Rep 37:137–152. https://doi.org/10.1007/s00299-017-2217-x
  • Francischini JHMB, Kemper EL, Costa JB et al (2017) DNA methylation in sugarcane somaclonal variants assessed through methylation-sensitive amplified polymorphism. Genet Mol Res 16:16029585. https://doi.org/10.4238/gmr16029585
  • Gimenez MD, Yañez-Santos AM, Paz RC et al (2016) Assessment of genetic and epi-genetic changes in virus-free garlic (Allium sativum L.) plants obtained by meristem culture followed by in vitro propagation. Plant Cell Rep 35:129–141. https://doi.org/10.1007/s00299-015-1874-x
  • González AI, Sáiz A, Acedo A et al (2013) Analysis of genomic DNA methylation patterns in regenerated and control plants of rye (Secale cereale L.). Plant Growth Regul 70:227–236. https://doi.org/10.1007/s10725-013-9794-7
  • Goyali JC, Igamberdiev AU, Debnath SC (2018) DNA methylation in lowbush blueberry (Vaccinium angustifolium Ait.) propagated by softwood cutting and tissue culture. Can J Plant Sci 98:1035–1044. https://doi.org/10.1139/cjps-2017-0297
  • Gulyás A, Dobránszki J, Kiss E et al (2019) Changes in DNA methylation pattern of apple long-term in vitro shoot culture and acclimatized plants. J Plant Physiol 239:18–27. https://doi.org/10.1016/j.jplph.2019.05.007
  • Guo WL, Wu R, Zhang YF et al (2007) Tissue culture-induced locus-specific alteration in DNA methylation and its correlation with genetic variation in Codonopsis lanceolata Benth. et Hook. f. Plant Cell Rep 26:1297–1307. https://doi.org/10.1007/s00299-007-0320-0
  • Han Z, Crisp PA, Stelpflug S et al (2018) Heritable epigenomic changes to the maize methylome resulting from tissue culture. Genetics 209:983–995. https://doi.org/10.1534/genetics.118.300987
  • Horstman A, Bemer M, Boutilier K (2017) A transcriptional view on somatic embryogenesis. Regeneration 4:201. https://doi.org/10.1002/REG2.91
  • Jaligot E, Rival A, Beulé T et al (2000) Somaclonal variation in oil palm (Elaeis guineesis Jacq.): the DNA methylation hypothesis. Plant Cell Rep 19:684–690. https://doi.org/10.1007/s002999900177
  • Kaeppler SM, Kaeppler HF, Rhee Y (2000) Epigenetic aspects of somaclonal variation in plants. Plant Mol Biol 43:179–188. https://doi.org/10.1023/A:1006423110134
  • Kaufmann K, Muiño JM, Østerås M et al (2010) Chromatin immunoprecipitation (ChIP) of plant transcription factors followed by sequencing (ChIP-SEQ) or hybridization to whole genome arrays (ChIP-CHIP). Nat Protoc 53(5):457–472. https://doi.org/10.1038/nprot.2009.244
  • Komatsu M, Shimamoto K, Kyozuka J (2003) Two-step regulation and continuous retrotransposition of the rice LINE-type retrotransposon Karma. Plant Cell 15:1934–1944. https://doi.org/10.1105/tpc.011809
  • Krizova K, Fojtova M, Depicker A, Kovarik A (2009) Cell culture-induced gradual and frequent epigenetic reprogramming of invertedly repeated tobacco transgene epialleles. Plant Physiol 149:1493. https://doi.org/10.1104/PP.108.133165
  • Kwiatkowska A, Zebrowski J, Oklejewicz B et al (2014) The age-dependent epigenetic and physiological changes in an Arabidopsis T87 cell suspension culture during long-term cultivation. Biochem Biophys Res Commun 447:285–291. https://doi.org/10.1016/j.bbrc.2014.03.141
  • Lee K, Seo PJ (2018) Dynamic epigenetic changes during plant regeneration. Trends Plant Sci 23:235–247. https://doi.org/10.1016/J.TPLANTS.2017.11.009
  • Li X, Xiaoming AE, Ae Y et al (2007) Genetic and epigenetic instabilities induced by tissue culture in wild barley (Hordeum brevisubulatum (Trin.) Link). Plant Cell Tissue Organ Cult 90:153–168. https://doi.org/10.1007/s11240-007-9224-5
  • Lin W, Xiao X, Zhang H et al (2019) Whole-genome bisulfite sequencing reveals a role for DNA methylation in variants from callus culture of pineapple (Ananas comosus l.). Genes (Basel) 10:877. https://doi.org/10.3390/genes10110877
  • Linacero R, Rueda J, Esquivel E et al (2011) Genetic and epigenetic relationship in rye, Secale cereale L., somaclonal variation within somatic embryo-derived plants. In Vitro Cell Dev Biol Plant 47:618–628. https://doi.org/10.1007/s11627-011-9407-y
  • Long Y, Yang Y, Pan G, Shen Y (2022) New insights into tissue culture plant-regeneration mechanisms. Front Plant Sci 13:926752. https://doi.org/10.3389/fpls.2022.926752
  • Machczyńska J, Zimny J, Bednarek PT (2015) Tissue culture-induced genetic and epigenetic variation in triticale (× Triticosecale spp. Wittmack ex A. Camus 1927) regenerants. Plant Mol Biol 89:279–292. https://doi.org/10.1007/s11103-015-0368-0
  • Meng L, Zhang S, Lemaux PG (2010) Toward molecular understanding of in vitro and in planta shoot organogenesis. CRC Crit Rev Plant Sci 29:108–122. https://doi.org/10.1080/07352681003617327
  • Miguel C, Marum L (2011) An epigenetic view of plant cells cultured in vitro: somaclonal variation and beyond. J Exp Bot 62:3713–3725. https://doi.org/10.1093/jxb/err155
  • Miyao A, Iwasaki Y, Kitano H et al (2007) A large-scale collection of phenotypic data describing an insertional mutant population to facilitate functional analysis of rice genes. Plant Mol Biol 63:625. https://doi.org/10.1007/S11103-006-9118-7
  • Mohn F, Weber M, Schübeler D, Roloff T-C (2009) Methylated DNA Immunoprecipitation (MeDIP). In: Tost J (ed) DNA methylation: methods and protocols. Humana Press, Totowa, NJ, pp 55–64. https://doi.org/10.1007/978-1-59745-522-0_5
  • Neelakandan AK, Wang K (2012) Recent progress in the understanding of tissue culture-induced genome level changes in plants and potential applications. Plant Cell Rep 31:597–620. https://doi.org/10.1007/s00299-011-1202-z
  • Ngezahayo F, Xu C, Wang H et al (2009) Tissue culture-induced transpositional activity of mPing is correlated with cytosine methylation in rice. BMC Plant Biol 9:91. https://doi.org/10.1186/1471-2229-9-91
  • Nodine MD, Bartel DP (2010) MicroRNAs prevent precocious gene expression and enable pattern formation during plant embryogenesis. Genes Dev 24:2678–2692. https://doi.org/10.1101/gad.1986710
  • Ong-Abdullah M, Ordway JM, Jiang N et al (2015) Loss of Karma transposon methylation underlies the mantled somaclonal variant of oil palm. Nature 525:533–537. https://doi.org/10.1038/nature15365
  • Orłowska R, Bednarek PT (2020) Precise evaluation of tissue culture-induced variation during optimisation of in vitro regeneration regime in barley. Plant Mol Biol 103:33–50. https://doi.org/10.1007/s11103-020-00973-5
  • Orłowska R, Machczyńska J, Oleszczuk S et al (2016) DNA methylation changes and TE activity induced in tissue cultures of barley (Hordeum vulgare L.). J Biol Res 23:1–12. https://doi.org/10.1186/s40709-016-0056-5
  • Pawełkowicz ME, Skarzyńska A, Koter MD et al (2022) miRNA profiling and its role in multi-omics regulatory networks connected with somaclonal variation in cucumber (Cucumis sativus L.). Int J Mol Sci 23:4317. https://doi.org/10.3390/ijms23084317
  • Peraza-Echeverria S, Herrera-Valencia VA, Kay AJ (2001) Detection of DNA methylation changes in micropropagated banana plants using methylation-sensitive amplification polymorphism (MSAP). Plant Sci 161:359–367. https://doi.org/10.1016/S0168-9452(01)00421-6
  • Pikaard CS, Scheid OM (2014) Epigenetic regulation in plants. Cold Spring Harb Perspect Biol 6:a019315. https://doi.org/10.1101/CSHPERSPECT.A019315
  • Rakocevic A, Mondy S, Tirichine L et al (2009) MERE1, a low-copy-number copia-type retroelement in Medicago truncatula active during tissue culture. Plant Physiol 151:1250–1263. https://doi.org/10.1104/pp.109.138024
  • Renau-Morata B, Nebauer SG, Arrillaga I, Segura J (2005) Assessments of somaclonal variation in micropropagated shoots of Cedrus: consequences of axillary bud breaking. Tree Genet Genomes 1:3–10. https://doi.org/10.1007/S11295-004-0001-X
  • Rhee Y, Sekhon RS, Chopra S, Kaeppler S (2010) Tissue culture-induced novel epialleles of a Myb transcription factor encoded by pericarp color1 in maize. Genetics 186:843–855. https://doi.org/10.1534/GENETICS.110.117929
  • Singh A, Gautam V, Singh S et al (2018) Plant small RNAs: advancement in the understanding of biogenesis and role in plant development. Planta 248:545–558. https://doi.org/10.1007/s00425-018-2927-5
  • Smulders MJM, de Klerk GJ (2011) Epigenetics in plant tissue culture. Plant Growth Regul 63:137–146. https://doi.org/10.1007/S10725-010-9531-4/FIGURES/3
  • Smýkal P, Valledor L, Rodríguez R, Griga M (2007) Assessment of genetic and epigenetic stability in long-term in vitro shoot culture of pea (Pisum sativum L.). Plant Cell Rep 26:1985–1998. https://doi.org/10.1007/S00299-007-0413-9
  • Stelpflug SC, Eichten SR, Hermanson PJ et al (2014) Consistent and heritable alterations of DNA methylation are induced by tissue culture in maize. Genetics 198:209–218. https://doi.org/10.1534/genetics.114.165480
  • Stroud H, Ding B, Simon SA et al (2013) Plants regenerated from tissue culture contain stable epigenome changes in rice. Elife 2013:1–14. https://doi.org/10.7554/eLife.00354
  • Su YH, Liu YB, Zhou C et al (2016) The microRNA167 controls somatic embryogenesis in Arabidopsis through regulating its target genes ARF6 and ARF8. Plant Cell Tissue Organ Cult 124:405–417. https://doi.org/10.1007/s11240-015-0903-3
  • Tanurdzic M, Vaughn MW, Jiang H et al (2008) Epigenomic consequences of immortalized plant cell suspension culture. PLOS Biol 6:e302. https://doi.org/10.1371/JOURNAL.PBIO.0060302
  • Valledor L, Hasbún R, Meijón M et al (2007) Involvement of DNA methylation in tree development and micropropagation. Plant Cell Tissue Organ Cult 91:75–86. https://doi.org/10.1007/s11240-007-9262-z
  • Vashisht D, Nodine MD (2014) MicroRNA functions in plant embryos. Biochem Soc Trans 42:352–357. https://doi.org/10.1042/BST20130252
  • Vázquez AM (2001) Insight into somaclonal variation. Plant Biosyst 135:57–62. https://doi.org/10.1080/11263500112331350650
  • Wang C, Xu J, Zhang D et al (2010) An effective approach for identification of in vivo protein-DNA binding sites from paired-end ChIP-Seq data. BMC Bioinform 11:1–8. https://doi.org/10.1186/1471-2105-11-81
  • Wang N, Yu Y, Zhang D et al (2022) Modification of gene expression, DNA methylation and small RNAs expression in rice plants under in vitro culture. Agronomy 12:1675. https://doi.org/10.3390/agronomy12071675
  • Wibowo A, Becker C, Durr J et al (2018) Partial maintenance of organ-specific epigenetic marks during plant asexual reproduction leads to heritable phenotypic variation. Proc Natl Acad Sci U S A 115:E9145–E9152. https://doi.org/10.1073/pnas.1805371115
  • Xu Z, Yan X, Maurais S et al (2004) Jittery, a mutator distant relative with a paradoxical mobile behavior: excision without reinsertion. Plant Cell 16:1105–1114. https://doi.org/10.1105/TPC.019802
  • Yaish M, Peng M, Rothstein SJ (2014) Global DNA methylation analysis using methyl-sensitive amplification polymorphism (MSAP). Methods Mol Biol 1062:285–298. https://doi.org/10.1007/978-1-62703-580-4_16
  • Zakrzewski F, Schmidt M, Van Lijsebettens M, Schmidt T (2017) DNA methylation of retrotransposons, DNA transposons and genes in sugar beet (Beta vulgaris L.). Plant J 90:1156–1175. https://doi.org/10.1111/tpj.13526
  • Zhang M, Dong Y, Nie L et al (2015) High-throughput sequencing reveals miRNA effects on the primary and secondary production properties in long-term subcultured Taxus cells. Front Plant Sci 6:604. https://doi.org/10.3389/fpls.2015.00604
  • Zhang H, Lang Z, Zhu J-K (2018) Dynamics and function of DNA methylation in plants. Nat Rev Mol Cell Biol 19:489–506. https://doi.org/10.1038/s41580-018-0016-z