Plant Fidelity in Somatic Embryogenesis-Regenerated Plants

  • Hervé EtienneEmail author
  • Romain Guyot
  • Thierry Beulé
  • Jean-Christophe Breitler
  • Estelle Jaligot


This chapter reviews the literature on somaclonal variation affecting the micropropagation through somatic embryogenesis. The first part covers the following aspects: (i) principle, protocols, and applications of somatic embryogenesis and (ii) epigenetic reprogramming and changes in cell fate that underlie somatic embryogenesis. The second part addresses the problem of somaclonal variation in somatic embryogenesis by first (i) assessing their impact on somatic embryo-derived plant production and (ii) describing the multiple origins of somaclonal variation (chromosomal aberrations, genetic alterations, epigenetic regulations, and transposable elements). The last part focuses on how to manage somaclonal variation in commercial productions of SE-derived plants by covering different aspects: (i) detection of undesirable phenotypes: screening out the variants, (ii) strategies of avoidance and incidence limitation, (iii) generation and exploitation of desirable phenotypes in plant breeding, (iv) beyond the induction of stress-tolerant somaclonal variants: a plant breeder’s perspective.


Somatic Embryo Somatic Embryogenesis Somaclonal Variation Somatic Embryo Development Short Intersperse Nuclear Element 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



Amplified fragment length polymorphism




2,4-dichlorophenoxyacetic acid


Long terminal repeats


Plant growth regulators


Random amplified polymorphic DNA


Somatic embryogenesis


Simple sequence repeat


Somaclonal variation


Transgenerational epigenetic inheritance


Transposable elements


  1. Al Zahim MA, Ford Loyd BV, Newbury HJ (1999) Detection of somaclonal variation in garlic (Allium sativum L.) using RAPD and cytological analysis. Plant Cell Rep 18:473–477. doi: 10.1007/s002990050606 CrossRefGoogle Scholar
  2. Angers B, Castonguay E, Massicote R (2010) Environmentally induced phenotypes and DNA methylation: how to deal with unpredictable conditions until the next generation and after. Mol Ecol 19:1283–1295. doi: 10.1111/j.1365-294X.2010.04580.x CrossRefPubMedGoogle Scholar
  3. Arteaga-Vazquez MA, Chandler VL (2010) Paramutation in maize: RNA mediated trans-generational gene silencing. Curr Opin Genet Dev 20:156–163. doi: 10.1016/j.gde.2010.01.008 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Avramova Z (2015) Transcriptional “memory” of a stress: transient chromatin and memory (epigenetic) marks at stress-response genes. Plant J 83:149–159. doi: 10.1111/tpj.12832 CrossRefPubMedGoogle Scholar
  5. Bairu MW, Aremu AO, Van Staden J (2011) Somaclonal variation in plants: causes and detection methods. Plant Growth Regul 63:147–173. doi: 10.1007/s10725-010-9554-x CrossRefGoogle Scholar
  6. Baroux C, Raissig MT, Grossniklaus U (2011) Epigenetic regulation and reprogramming during gamete formation in plants. Curr Opin Genet Dev 21:124–133. doi: 10.1016/j.gde.2011.01.017 CrossRefPubMedGoogle Scholar
  7. Baurens F-C, Nicolleau J, Legavre T et al (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 24:401–407. doi: 10.1093/treephys/24.4.401 CrossRefPubMedGoogle Scholar
  8. Belele CL, Sidorenko L, Stam M et al (2013) Specific tandem repeats are sufficient for paramutation-induced trans-generational silencing. PLoS Genet 9:e1003773. doi: 10.1371/journal.pgen.1003773 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Bennetzen JL, Wang H (2014) The contributions of transposable elements to the structure, function, and evolution of plant genomes. Annu Rev Plant Biol 65:505–530. doi: 10.1146/annurev-arplant-050213-035811 CrossRefPubMedGoogle Scholar
  10. Bilichak A, Ilnystkyy Y, Hollunder J, Kovalchuk I (2012) The progeny of Arabidopsis thaliana plants exposed to salt exhibit changes in DNA methylation, histone modifications and gene expression. PLoS ONE 7:e30515. doi: 10.1371/journal.pone.0030515 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Birchler JA, Veitia RA (2007) The gene balance hypothesis: from classical genetics to modern genomics. Plant Cell 19:395–402. doi: 10.1105/tpc.106.049338
  12. Biswas MK, Dutt M, Roy UK et al (2009) Development and evaluation of in vitro somaclonal variation in strawberry for improved horticultural traits. Sci Hortic 122:409–416. doi: 10.1016/j.scienta.2009.06.002 CrossRefGoogle Scholar
  13. 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. doi: 10.1371/journal.pone.0056372 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Bobadilla Landey R, Cenci A, Bertrand B et al (2015) Assessment of genetic and epigenetic changes during cell culture ageing in coffee and relations with somaclonal variation. Plant Cell Tissue Org 3:517–531. doi: 10.1007/s11240-015-0772-9 CrossRefGoogle Scholar
  15. Bossdorf O, Richards CL, Pigliucci M (2008) Epigenetics for ecologists. Ecol Lett 11:106–115. doi: 10.1111/j.1461-0248.2007.01130.x PubMedGoogle Scholar
  16. Bourc’his D, Voinnet O (2010) A small-RNA perspective on gametogenesis, fertilization, and early zygotic development. Science 330:617–622. doi: 10.1126/science.1194776 CrossRefPubMedGoogle Scholar
  17. Boyko A, Kovalchuk I (2011) Genome instability and epigenetic modification—heritable responses to environmental stress? Curr Opin Plant Biol 14:260–266. doi: 10.1016/j.pbi.2011.03.003 CrossRefPubMedGoogle Scholar
  18. Bruce TJA, Matthes MC, Napier JA, Pickett JA (2007) Stressful “memories” of plants: evidence and possible mechanisms. Plant Sci 173:603–608. doi: 10.1016/j.plantsci.2007.09.002 CrossRefGoogle Scholar
  19. Bukowska B (2006) Toxicity of 2,4-dichlorophenoxyacetic acid—molecular mechanisms. Polish J Environ Stud 15:365–374Google Scholar
  20. Bui QT, Grandbastien M-A (2012) LTR retrotransposons as controlling elements of genome response to stress? In: Grandbastien M-A, Casacuberta JM (eds) Plant transposable elements. Springer Berlin Heidelberg, p 273–296. doi: 10.1007/978-3-642-31842-9_14
  21. Calarco JP, Martienssen RA (2011) Genome reprogramming and small interfering RNA in the Arabidopsis germline. Curr Opin Genet Dev 21:134–139. doi: 10.1016/j.gde.2011.01.014 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Cantone I, Fisher AG (2013) Epigenetic programming and reprogramming during development. Nat Struct Mol Biol 20:282–289. doi: 10.1038/nsmb.2489 CrossRefPubMedGoogle Scholar
  23. Cao X, Aufsatz W, Zilberman D et al (2003) Role of the DRM and CMT3 methyltransferases in RNA-Directed DNA methylation. Curr Biol 13:2212–2217. doi: 10.1016/j.cub.2003.11.052 CrossRefPubMedGoogle Scholar
  24. Capy P, Gasperi G, Biémont C, Bazin C (2000) Stress and transposable elements: co-evolution or useful parasites? Heredity 85:101–106. doi: 10.1046/j.1365-2540.2000.00751.x CrossRefPubMedGoogle Scholar
  25. Carrier G, Le Cunff L, Dereeper A, Legrand D, Sabot F et al (2012) Transposable elements are a major cause of somatic polymorphism in Vitis vinifera L. PLoS ONE 7:e32973. doi: 10.1371/journal.pone.0032973 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Casacuberta E, Gonzalez J (2013) The impact of transposable elements in environmental adaptation. Mol Ecol 22:1503–1517. doi: 10.1111/mec.12170 CrossRefPubMedGoogle Scholar
  27. Chénais B, Caruso A, Hiard S, Casse N (2012) The impact of transposable elements on eukaryotic genomes: from genome size increase to genetic adaptation to stressful environments. Gene 509:7–15. doi: 10.1016/j.gene.2012.07.042 CrossRefPubMedGoogle Scholar
  28. Choulet F, Wicker T, Rustenholz C, Paux E, Salse J, Leroy P, Schlub S, Le Paslier M-C, Magdelenat G, Gonthier C, Couloux A, Budak H, Breen J, Pumphrey M, Liu S, Kong X, Jia J, Gut M, Brunel D, Anderson JA, Gill BS, Appels R, Keller B, Feuillet C (2010) Megabase Level Sequencing Reveals Contrasted Organization and Evolution Patterns of the Wheat Gene and Transposable Element Spaces. Plant Cell tpc.110.074187. doi:  10.1105/tpc.110.074187
  29. Colomé-Tatché M, Cortijo S, Wardenaar R, Morgado L, Lahouze B, Sarazin A, Etcheverry M, Martin A, Feng S, Duvernois-Berthet E, Labadie K, Wincker P, Jacobsen SE, Jansen RC, Colot V, Johannes F (2012) Features of the Arabidopsis recombination landscape resulting from the combined loss of sequence variation and DNA methylation. PNAS 109:16240–16245. doi:  10.1073/pnas.1212955109
  30. Combes M-C, Cenci A, Baraille H et al (2012) Homeologous gene expression in response to growing temperature in a recent allopolyploid (Coffea arabica L.). J Hered 103:36–46. doi: 10.1093/jhered/esr120 CrossRefPubMedGoogle Scholar
  31. Corley RHV, Lee CH, Law IM, Wong CY (1986) Abnormal flower development in oil palm clones. Planter 62:233–240Google Scholar
  32. Cui X, Cao X (2014) Epigenetic regulation and functional exaptation of transposable elements in higher plants. Curr Opin Plant Biol 21:83–88. doi: 10.1016/j.pbi.2014.07.001 CrossRefPubMedGoogle Scholar
  33. Daron J, Glover NL, Pingault S et al (2014) Organization and evolution of transposable elements along the bread wheat chromosome 3B. Genome Biol 15:546. doi: 10.1186/s13059-014-0546-4 CrossRefPubMedPubMedCentralGoogle Scholar
  34. D’Amato Baylissb FMW (1985) Cytogenetics of plant cells and tissue cultures and their regenerates. Crit Rev Plant Sci 3:73–112. doi: 10.1080/07352688509382204 CrossRefGoogle Scholar
  35. De la Puente R, Gonzalez AI, Ruiz ML, Polanco C (2008) Somaclonal variation in rye (Secale cereale L.) analyzed using polymorphic and sequenced AFLP markers. In Vitro Cell Dev-Pl 44:419–426. doi: 10.1007/s11627-008-9152-z CrossRefGoogle Scholar
  36. de la Paz Sanchez M, Aceves-García P, Petrone E et al (2015) The impact of Polycomb group (PcG) and Trithorax group (TrxG) epigenetic factors in plant plasticity. New Phytol 208:684–694. doi: 10.1111/nph.13486 CrossRefGoogle Scholar
  37. de Touchet B, Duval Y, Pannetier C (1991) Plant regeneration from embryogenic suspension cultures of oil palm (Elaeis guineensis Jacq.). Plant Cell Rep 10:529–532. doi: 10.1007/BF00234588 CrossRefPubMedGoogle Scholar
  38. Denoeud F, Carretero-Paulet L, Dereeper A et al (2014) The coffee genome provides insight into the convergent evolution of caffeine biosynthesis. Science 345:1181–1184. doi: 10.1126/science.1255274 CrossRefPubMedGoogle Scholar
  39. de Vega-Bartol JJ, Simões M, Lorenz WW et al (2013) Transcriptomic analysis highlights epigenetic and transcriptional regulation during zygotic embryo development of Pinus pinaster. BMC Plant Biol 13:123. doi: 10.1186/1471-2229-13-123 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Ding Y, Virlouvet L, Liu N et al (2014) Dehydration stress memory genes of Zea mays; comparison with Arabidopsis thaliana. BMC Plant Biol 14:141. doi: 10.1186/1471-2229-14-141 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Ding Y, Wang X, Su L et al (2007) SDG714, a Histone H3K9 methyltransferase, is involved in tos17 DNA methylation and transposition in rice. Plant Cell 19:9–22. doi: 10.1105/tpc.106.048124 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Duncan RR (1997) Tissue culture-induced variation and crop improvement. Adv Agron 58:201–240. doi: 10.1016/bs.agron.2015.11.006 CrossRefGoogle Scholar
  43. Durand-Gasselin T, Labeyrie A, Amblard P et al (2010) Strategies to develop oil palm clones for Latin American and Africa. In: Proceeding of Advanced Oil Palm Tissue Culture. 29th May 2010 Yogyak. Indones. Accessed 5 Oct 2015
  44. Eichten SR, Springer NM (2015) Minimal evidence for consistent changes in maize DNA methylation patterns following environmental stress. Front Plant Sci 6:308. doi: 10.3389/fpls.2015.00308 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Elbl P, Lira BS, Andrade SCS et al (2014) Comparative transcriptome analysis of early somatic embryo formation and seed development in Brazilian pine, Araucaria angustifolia (Bertol.) Kuntze. Plant Cell Tiss Org 120:903–915. doi: 10.1007/s11240-014-0523-3 CrossRefGoogle Scholar
  46. Etienne H, Bertrand B (2001) The effect of the embryogenic cell suspension micropropagation technique on the trueness to type, field performance, bean biochemical content and cup quality of Coffea arabica trees. Tree Physiol 21:1031–1038CrossRefPubMedGoogle Scholar
  47. Etienne H, Bertrand B (2003) Somaclonal variation in Coffea arabica: effects of genotype and embryogenic cell suspension age on frequency and phenotype of variants. Tree Physiol 23:419–426. doi: 10.1093/treephys/23.6.419 CrossRefPubMedGoogle Scholar
  48. Etienne H, Bertrand B, Montagnon C et al (2012) Un exemple de transfert technologique réussi en micropropagation: la multiplication de Coffea arabica par embryogenèse somatique. Cah Agric 21:115–124. doi: 10.1684/agr.2012.0553 Google Scholar
  49. Etienne H, Dechamp E, Barry Etienne D, Bertrand B (2006) Bioreactors in coffee micropropagation (Review). Braz J Plant Physiol 18:45–54. doi: 10.1590/S1677-04202006000100005 CrossRefGoogle Scholar
  50. Exner V, Hennig L (2008) Chromatin rearrangements in development. Curr Opin Plant Biol 11:64–69. doi: 10.1016/j.pbi.2007.10.004 CrossRefPubMedGoogle Scholar
  51. Fehér A (2015) Somatic embryogenesis—stress-induced remodeling of plant cell fate. Biochim Biophys Acta BBA—Gene Regul Mech 1849:385–402. doi: 10.1016/j.bbagrm.2014.07.005 CrossRefGoogle Scholar
  52. Feng S, Cokus SJ, Zhang X et al (2010a) Conservation and divergence of methylation patterning in plants and animals. Proc Natl Acad Sci (USA) 107:8689–8694. doi: 10.1073/pnas.1002720107 CrossRefGoogle Scholar
  53. Feng S, Jacobsen SE (2011) Epigenetic modifications in plants: an evolutionary perspective. Curr Opin Plant Biol 14:179–186. doi: 10.1016/j.pbi.2010.12.002 CrossRefPubMedPubMedCentralGoogle Scholar
  54. Feng S, Jacobsen SE, Reik W (2010b) Epigenetic reprogramming in plant and animal development. Science 330:622–627. doi: 10.1126/science.1190614 CrossRefPubMedPubMedCentralGoogle Scholar
  55. Feschotte C (2008) The contribution of transposable elements to the evolution of regulatory networks. Nat Rev Genet 9:397–405. doi: 10.1038/nrg2337 CrossRefPubMedPubMedCentralGoogle Scholar
  56. Finnegan EJ (2002) Epialleles—a source of random variation in times of stress. Curr Opin Plant Biol 5:101–106. doi: 10.1016/S1369-5266(02)00233-9 CrossRefPubMedGoogle Scholar
  57. Fraga HPF, Vieira LN, Caprestano CA et al (2012) 5-Azacytidine combined with 2,4-D improves somatic embryogenesis of Acca sellowiana (O. Berg) Burret by means of changes in global DNA methylation levels. Plant Cell Rep 31:2165–2176. doi: 10.1007/s00299-012-1327-8 CrossRefPubMedGoogle Scholar
  58. Fu D, Mason AS, Xiao M, Yan H (2016) Effects of genome structure variation, homeologous genes and repetitive DNA on polyploid crop research in the age of genomics. Plant Sci 242:37–46. doi: 10.1016/j.plantsci.2015.09.017 CrossRefPubMedGoogle Scholar
  59. Giacopelli BJ, Hollick JB (2015) Trans-Homolog Interactions facilitating paramutation in maize. Plant Physiol 168:1226–1236. doi: 10.1104/pp.15.00591 CrossRefPubMedPubMedCentralGoogle Scholar
  60. Gliwicka M, Nowak K, Balazadeh S et al (2013) Extensive modulation of the transcription factor transcriptome during somatic embryogenesis in Arabidopsis thaliana. PLoS ONE 8:e69261. doi: 10.1371/journal.pone.0069261 CrossRefPubMedPubMedCentralGoogle Scholar
  61. Giorgetti L, Castiglione M, Turrini A et al (2011) Cytogenetic and histological approach for early detection of “mantled” somaclonal variants of oil palm regenerated by somatic embryogenesis: first results on the characterization of regeneration system. Caryologia 64:223–234. doi: 10.1080/00087114.2002.10589787 CrossRefGoogle Scholar
  62. Gong Z, Morales-Ruiz T, Ariza RR et al (2002) ROS1, a repressor of transcriptional gene silencing in arabidopsis, encodes a DNA glycosylase/lyase. Cell 111:803–814. doi: 10.1016/S0092-8674(02)01133-9 CrossRefPubMedGoogle Scholar
  63. Gorret N, bin Rosli SK, Oppenheim SF et al (2004) Bioreactor culture of oil palm (Elaeis guineensis) and effects of nitrogen source, inoculum size, and conditioned medium on biomass production. J Biotechnol 108:253–263. doi: 10.1016/j.jbiotec.2003.12.009 CrossRefPubMedGoogle Scholar
  64. Gözükirmizi N, Ari S, Oraler G et al (1990) Callus induction, plant regeneration and chromosomal variations in barley. Acta Bot Neerl 39:379–387. doi: 10.1111/j.1438-8677.1990.tb01416.x CrossRefGoogle Scholar
  65. Grafi G, Chalifa-Caspi V, Nagar T et al (2011) Plant response to stress meets dedifferentiation. Planta 233:433–438. doi: 10.1007/s00425-011-1366-3 CrossRefPubMedGoogle Scholar
  66. Grandbastien M-A (2015) LTR retrotransposons, handy hitchhikers of plant regulation and stress response. Biochim Biophys Acta BBA—Gene Regul Mech 1849:403–416. doi: 10.1016/j.bbagrm.2014.07.017 CrossRefGoogle Scholar
  67. Grandbastien M-A, Spielmann A, Caboche M (1989) Tnt1, a mobile retroviral-like transposable element of tobacco isolated by plant cell genetics. Nature 337:376–380. doi: 10.1038/337376a0 CrossRefPubMedGoogle Scholar
  68. Greaves I, Groszmann M, Dennis ES, Peacock WJ (2012) Trans-chromosomal methylation. Epigenetics 7:800–805. doi: 10.4161/epi.20820 CrossRefPubMedPubMedCentralGoogle Scholar
  69. Greaves IK, Groszmann M, Wang A et al (2014) Inheritance of trans chromosomal methylation patterns from Arabidopsis F1 hybrids. Proc Natl Acad Sci (USA) 111:2017–2022. doi: 10.1073/pnas.1323656111 CrossRefGoogle Scholar
  70. Hajkova P, Ancelin K, Waldmann T et al (2008) Chromatin dynamics during epigenetic reprogramming in the mouse germ line. Nature 452:877–881. doi: 10.1038/nature06714 CrossRefPubMedGoogle Scholar
  71. Hao YI, Deng XX (2002) Occurrence of chromosomal variations and plant regeneration from long-term-cultured citrus callus. In Vitro Cell Dev-Pl 38:472–476. doi: 10.1079/IVP2002317 CrossRefGoogle Scholar
  72. Heard E, Martienssen RA (2014) Transgenerational epigenetic inheritance: myths and mechanisms. Cell 157:95–109. doi: 10.1016/j.cell.2014.02.045 CrossRefPubMedPubMedCentralGoogle Scholar
  73. Heinze B, Schmidt J (1995) Monitoring genetic fidelity vs somaclonal variation in Norway spruce (Picea abies) somatic embryogenesis by RAPD analysis. Euphytica 85:341–345. doi: 10.1007/BF00023965 CrossRefGoogle Scholar
  74. Henry Y, Marcotte JL, de Buyser J (1996) The effects of aneuploidy on karyotype abnormalities in wheat plants regenerated from short- and long-term somatic embryogenesis. Plant Sci 114:101–109. doi: 10.1016/0168-9452(95)04304-7 CrossRefGoogle Scholar
  75. Hemberger M, Dean W, Reik W (2009) Epigenetic dynamics of stem cells and cell lineage commitment: digging Waddington’s canal. Nat Rev Mol Cell Biol 10:526–537. doi: 10.1038/nrm2727 CrossRefPubMedGoogle Scholar
  76. Hirochika H (1993) Activation of tobacco retrotransposons during tissue culture. EMBO J 12:2521–2528PubMedPubMedCentralGoogle Scholar
  77. Hirochika H, Sugimoto K, Otsuki Y et al (1996) Retrotransposons of rice involved in mutations induced by tissue culture. Proc Natl Acad Sci (USA) 93:7783–7788CrossRefGoogle Scholar
  78. Hoen DR, Bureau TE (2012) Transposable element exaptation in plants. In: Grandbastien M-A, Casacuberta JM (eds) Plant transposable elements. Springer Berlin Heidelberg, p 219–251. doi: 10.1007/978-3-642-31842-9_12
  79. Holeski LM, Jander G, Agrawal AA (2012) Transgenerational defense induction and epigenetic inheritance in plants. Trends Ecol Evol 27:618–626. doi: 10.1016/j.tree.2012.07.011 CrossRefPubMedGoogle Scholar
  80. Hu H, Xiong L, Yang Y (2005) Rice SERK1 gene positively regulates somatic embryogenesis of cultured cell and host defense response against fungal infection. Planta 222:107–117. doi: 10.1007/s00425-005-1534-4 CrossRefPubMedGoogle Scholar
  81. Ibarra CA, Feng X, Schoft VK et al (2012) Active DNA demethylation in plant companion cells reinforces transposon methylation in gametes. Science 337:1360–1364. doi: 10.1126/science.1224839 CrossRefPubMedPubMedCentralGoogle Scholar
  82. Ikeuchi M, Sugimoto K, Iwase A (2013) Plant callus: mechanisms of induction and repression. Plant Cell 25:3159–3173. doi: 10.1105/tpc.113.116053 CrossRefPubMedPubMedCentralGoogle Scholar
  83. Ingouff M, Rademacher S, Holec S et al (2010) Zygotic resetting of the HISTONE 3 variant repertoire participates in epigenetic reprogramming in arabidopsis. Curr Biol 20:2137–2143. doi: 10.1016/j.cub.2010.11.012 CrossRefPubMedGoogle Scholar
  84. Ito H, Gaubert H, Bucher E et al (2011) An siRNA pathway prevents transgenerational retrotransposition in plants subjected to stress. Nature 472:115–119. doi: 10.1038/nature09861 CrossRefPubMedGoogle Scholar
  85. Iwasaki M, Paszkowski J (2014) Identification of genes preventing transgenerational transmission of stress-induced epigenetic states. Proc Natl Acad Sci (USA) 111:8547–8552. doi: 10.1073/pnas.1402275111 CrossRefGoogle Scholar
  86. Jacob Y, Martienssen RA (2011) Chromatin reprogramming: gender equality during Arabidopsis germline differentiation. Curr Biol 21:R20–R22. doi: 10.1016/j.cub.2010.11.052 CrossRefPubMedGoogle Scholar
  87. Jähne A, Lazzeri PA, Jäger Gussen M, Lörz H (1991) Plant regeneration from embryogenic cell suspensions derived from anther cultures of barley (Hordeum vulgare L.). Theor Appl Gen 82:74–80. doi: 10.1007/BF00231280 CrossRefGoogle Scholar
  88. Jaligot E, Adler S, Debladis E et al (2011) Epigenetic imbalance and the floral developmental abnormality of the in vitro-regenerated oil palm Elaeis guineensis. Ann Bot 108:1463–1475. doi: 10.1093/aob/mcq266 CrossRefGoogle Scholar
  89. Jaligot E, Beulé T, Baurens FC et al (2004) Search for methylation-sensitive amplification polymorphisms associated with the “mantled” variant phenotype in oil palm (Elaeis guineensis Jacq.). Genome 47:224–228. doi: 10.1139/g03-085 CrossRefPubMedGoogle Scholar
  90. Jaligot E, Beulé T, Rival A (2002) Methylation-sensitive RFLPs: characterisation of two oil palm markers showing somaclonal variation-associated polymorphism. Theor Appl Genet 104:1263–1269. doi: 10.1007/s00122-002-0906-4 CrossRefPubMedGoogle Scholar
  91. Jaligot E, Rival A, Beulé T et al (2000) Somaclonal variation in oil palm (Elaeis guineensis Jacq.): the DNA methylation hypothesis. Plant Cell Rep 19:684–690. doi: 10.1007/s002999900177 CrossRefGoogle Scholar
  92. Jambhale ND, Patil SC, Jadhav AS et al (2001) Effect of number of subcultures on in vitro multiplication of four banana clones. Infomusa 10:38–39Google Scholar
  93. Jaskiewicz M, Conrath U, Peterhänsel C (2011) Chromatin modification acts as a memory for systemic acquired resistance in the plant stress response. EMBO Rep 12:50–55. doi: 10.1038/embor.2010.186 CrossRefPubMedGoogle Scholar
  94. Jiang N, Bao Z, Zhang X et al (2003) An active DNA transposon family in rice. Nature 421:163–167. doi: 10.1038/nature01214 CrossRefPubMedGoogle Scholar
  95. Jiang C, Mithani A, Gan X et al (2011) Regenerant Arabidopsis lineages display a distinct genome-wide spectrum of mutations conferring variant phenotypes. Curr Biol 21:1385–1390. doi: 10.1016/j.cub.2011.07.002 CrossRefPubMedPubMedCentralGoogle Scholar
  96. Jin F, Hu L, Yuan D et al (2014) Comparative transcriptome analysis between somatic embryos (SEs) and zygotic embryos in cotton: evidence for stress response functions in SE development. Plant Biotechnol J 12:161–173. doi: 10.1111/pbi.12123 CrossRefPubMedGoogle Scholar
  97. Jin S, Mushke R, Zhu H, Tu L, Lin Z et al (2008) Detection of somaclonal variation of cotton (Gossypium hirsutum) using cytogenetics, flow cytometry and molecular markers. Plant Cell Rep 27:1303–1316. doi: 10.1007/s00299-008-0557-2 CrossRefPubMedGoogle Scholar
  98. Johannes F, Porcher E, Teixeira FK et al (2009) Assessing the Impact of transgenerational epigenetic variation on complex traits. PLoS Genet 5:e1000530. doi: 10.1371/journal.pgen.1000530 CrossRefPubMedPubMedCentralGoogle Scholar
  99. Kaeppler SM, Kaeppler HF, Rhee Y (2000) Epigenetic aspects of somaclonal variation in plants. Plant Mol Biol 43:179–188. doi: 10.1023/A:1006423110134 CrossRefPubMedGoogle Scholar
  100. Kaeppler SM, Phillips RL (1993) DNA methylation and tissue culture-induced DNA methylation variation in plants. In Vitro Cell Dev-Pl 29:125–130. doi: 10.1007/BF02632283 CrossRefGoogle Scholar
  101. Kalendar R, Tanskanen J, Immonen S et al (2000) Genome evolution of wild barley (Hordeum spontaneum) by BARE-1 retrotransposon dynamics in response to sharp microclimatic divergence. Proc Natl Acad Sci (USA) 97:6603–6607. doi: 10.1073/pnas.110587497 CrossRefGoogle Scholar
  102. Karp A (1991) On the current understanding of somaclonal variation. In: Miflin BJ (ed) Oxford surveys of plant molecular and cell biology, 7:1–58, Oxford University PressGoogle Scholar
  103. Karp A (1994) Origins, causes and uses of variation in plant tissue cultures. In: Vasil IK, Thorpe TA (eds) Plant cell and tissue culture. Dordrecht: Kluwer Academic Publishers. p 139–151. doi: 10.1007/978-94-017-2681-8_6
  104. 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. doi: 10.1105/tpc.011809 CrossRefPubMedPubMedCentralGoogle Scholar
  105. Kou HP, Li Y, Song XX et al (2011) Heritable alteration in DNA methylation induced by nitrogen-deficiency stress accompanies enhanced tolerance by progenies to the stress in rice (Oryza sativa L.). J Plant Physiol 168:1685–1693. doi: 10.1016/j.jplph.2011.03.017 CrossRefPubMedGoogle Scholar
  106. Kumar PS, Mathur VL (2004) Chromosomal instability in callus culture of Pisum sativum. Plant Cell Tiss Org 78:267–271. doi: 10.1023/B:TICU.0000025669.11442.3e CrossRefGoogle Scholar
  107. La H, Ding B, Mishra GP et al (2011) A 5-methylcytosine DNA glycosylase/lyase demethylates the retrotransposon Tos17 and promotes its transposition in rice. Proc Natl Acad Sci (USA) 108:15498–15503. doi: 10.1073/pnas.1112704108 CrossRefGoogle Scholar
  108. Lambé P, Mutambel HSN, Fouche JG et al (1997) DNA methylation as a key process in regulation of organogenic totipotency and plant neoplastic progression. In Vitro Cell Dev-Pl 33:155–162. doi: 10.1007/s11627-997-0015-9 CrossRefGoogle Scholar
  109. Lang-Mladek C, Popova O, Kiok K et al (2010) Transgenerational inheritance and resetting of stress-induced loss of epigenetic gene silencing in arabidopsis. Mol Plant 3:594–602. doi: 10.1093/mp/ssq014 CrossRefPubMedPubMedCentralGoogle Scholar
  110. Larkin PJ, Scowcroft WR (1981) Somaclonal variation—a novel source of variability from cell cultures for plant improvement. Theor Appl Genet 60:197–214. doi: 10.1007/BF02342540 CrossRefPubMedGoogle Scholar
  111. Le TN, Miyazaki Y, Takuno S, Saze H (2015) Epigenetic regulation of intragenic transposable elements impacts gene transcription in Arabidopsis thaliana. Nucleic Acids Res 43:3911–3921. doi: 10.1093/nar/gkv258 CrossRefPubMedPubMedCentralGoogle Scholar
  112. Leal F, Loureiro J, Rodriguez E et al (2006) Nuclear DNA content of Vitis vinifera cultivars and ploidy level analyses of somatic embryo-derived plants obtained from anther culture. Plant Cell Rep 25:978–985. doi: 10.1007/s00299-006-0162-1 CrossRefPubMedGoogle Scholar
  113. Lee ML, Phillips RL (1988) The chromosomal basis of somaclonal variation. Ann Rev Plant Physiol Plant Mol Biol 39:413–437. doi: 10.1146/annurev.pp.39.060188.002213 CrossRefGoogle Scholar
  114. Lelu M-A, Bastien C, Drugeault A et al (1999) Somatic embryogenesis and plantlet development in Pinus sylvestris and Pinus pinaster on medium with and without growth regulators. Physiol Plant 105:719–728. doi: 10.1034/j.1399-3054.1999.105417.x CrossRefGoogle Scholar
  115. Lelu-Walter M-A, Thompson D, Harvengt L et al (2013) Somatic embryogenesis in forestry with a focus on Europe: state-of-the-art, benefits, challenges and future direction. Tree Gen Genom 9:883–899. doi: 10.1007/s11295-013-0620-1 CrossRefGoogle Scholar
  116. Li T, Chen J, Qiu S et al (2012) Deep sequencing and microarray hybridization identify conserved and species-specific microRNAs during somatic embryogenesis in hybrid yellow poplar. PLoS ONE 7:e43451. doi: 10.1371/journal.pone.0043451 CrossRefPubMedPubMedCentralGoogle Scholar
  117. Lippman Z, Gendrel A-V, Black M et al (2004) Role of transposable elements in heterochromatin and epigenetic control. Nature 430:471–476. doi: 10.1038/nature02651 CrossRefPubMedGoogle Scholar
  118. Lisch D (2009) Epigenetic regulation of transposable elements in plants. Annu Rev Plant Biol 60:43–66. doi: 10.1146/annurev.arplant.59.032607.092744 CrossRefPubMedGoogle Scholar
  119. Lisch D (2013) How important are transposons for plant evolution? Nat Rev Genet 14:49–61. doi: 10.1038/nrg3374 CrossRefPubMedGoogle Scholar
  120. Liu ZL, Han FP, Tan M et al (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. Theor Appl Genet 109:200–209. doi: 10.1007/s00122-004-1618-8 CrossRefPubMedGoogle Scholar
  121. LoSchiavo F, Pitto L, Giuliano G et al (1989) DNA methylation of embryogenic carrot cell cultures and its variations as caused by mutation, differentiation, hormones and hypomethylating drugs. Theor Appl Genet 77:325–331. doi: 10.1007/BF00305823 CrossRefPubMedGoogle Scholar
  122. Lu S, Wang Z, Peng X, Guo Z, Zhang G et al (2006) An efficient callus suspension culture system for triploid bermudagrass (Cynodon transvaalensis x C. dactylon) and somaclonal variations. Plant Cell Tiss Org 87:77–84. doi: 10.1007/s11240-006-9138-7 CrossRefGoogle Scholar
  123. Lukens L, Zhan S (2007) The plant genome’s methylation status and response to stress: implications for plant improvement. Curr Opin Plant Biol 10:317–322. doi: 10.1016/j.pbi.2007.04.012 CrossRefPubMedGoogle Scholar
  124. Mahdavi-Darvari F, Noor NM, Ismanizan I (2014) Epigenetic regulation and gene markers as signals of early somatic embryogenesis. Plant Cell Tiss Org 120:407–422. doi: 10.1007/s11240-014-0615-0 CrossRefGoogle Scholar
  125. Ma J, He Y, Hu Z et al (2012) Characterization and expression analysis of AcSERK2, a somatic embryogenesis and stress resistance related gene in pineapple. Gene 500:115–123. doi: 10.1016/j.gene.2012.03.013 CrossRefPubMedGoogle Scholar
  126. Makarevitch I, Harris C (2010) Aneuploidy causes tissue specific qualitative changes in global gene expression patterns in maize. Plant Physiol 152:927–938. doi: 10.1104/pp.110.900315 CrossRefPubMedPubMedCentralGoogle Scholar
  127. Makarevitch I, Waters AJ, West PT et al (2015) Transposable elements contribute to activation of maize genes in response to abiotic stress. PLoS Genet 11:e1004915. doi: 10.1371/journal.pgen.1004915 CrossRefPubMedPubMedCentralGoogle Scholar
  128. Mantiri FR, Kurdyukov S, Lohar DP et al (2008) The transcription factor mtserf1 of the erf subfamily identified by transcriptional profiling is required for somatic embryogenesis induced by auxin plus cytokinin in Medicago truncatula. Plant Physiol 146:1622–1636. doi: 10.1104/pp.107.110379 CrossRefPubMedPubMedCentralGoogle Scholar
  129. Matthes M, Singh R, Cheah SC, Karp A (2001) Variation in oil palm (Elaeis guineensis Jacq.) tissue culture-derived regenerants revealed by AFLPs with methylation-sensitive enzymes. Theor Appl Genet 102:971–979. doi: 10.1007/s001220000491 CrossRefGoogle Scholar
  130. McClintock B (1984) The significance of responses of the genome to challenge. Science 226:792–801. doi: 10.1126/science.15739260 CrossRefPubMedGoogle Scholar
  131. McCue AD, Slotkin RK (2012) Transposable element small RNAs as regulators of gene expression. Trends Genet 28:616–623. doi: 10.1016/j.tig.2012.09.001 CrossRefPubMedGoogle Scholar
  132. Ménendez Yuffá A, Da Silva R, Rios L, Xena de Enrech N (2000) Mitotic aberrations in coffee (Coffea arabica cv. ‘Catimor’) leaf explants and their derived embryogenic calli. Electron J Biotechnol 3:1–6CrossRefGoogle Scholar
  133. Miguel C, Marum L (2011) An epigenetic view of plant cells cultured in vitro: somaclonal variation and beyond. J Exp Bot 62:3713–3725. doi: 10.1093/jxb/err155 CrossRefPubMedGoogle Scholar
  134. Mirouze M, Reinders J, Bucher E et al (2009) Selective epigenetic control of retrotransposition in Arabidopsis. Nature 461:427–430. doi: 10.1038/nature08328 CrossRefPubMedGoogle Scholar
  135. Mirouze M, Vitte C (2014) Transposable elements, a treasure trove to decipher epigenetic variation: insights from Arabidopsis and crop epigenomes. J Exp Bot 65:2801–2812. doi: 10.1093/jxb/eru120 CrossRefPubMedGoogle Scholar
  136. Molinier J, Ries G, Zipfel C, Hohn B (2006) Transgeneration memory of stress in plants. Nature 442:1046–1049. doi: 10.1038/nature05022 CrossRefPubMedGoogle Scholar
  137. Monteuuis O, Doulbeau S, Verdeil J-L (2008) DNA methylation in different origin clonal offspring from a mature Sequoiadendron giganteum genotype. Trees 22:779–784. doi: 10.1007/s00468-008-0238-3 CrossRefGoogle Scholar
  138. Mujib A, Banerjee S, Dev Ghosh P (2007) Callus induction, somatic embryogenesis and chromosomal instability in tissue culture-raised hippeastrum (Hippeastrum hybridum cv. United Nations). Propag Ornam Plants 7:169–174Google Scholar
  139. Neelakandan A, 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. doi: 10.1007/s00299-011-1202-z CrossRefPubMedGoogle Scholar
  140. Nehra NS, Kartha KK, Stushnoff C, Giles KL (1992) The influence of plant growth regulator concentrations and callus age on somaclonal variation in callus culture regenerants of strawberry. Plant Cell Tiss Org 29:257–268. doi: 10.1007/BF00034361 CrossRefGoogle Scholar
  141. 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. doi: 10.1186/1471-2229-9-91 CrossRefPubMedPubMedCentralGoogle Scholar
  142. Nic-Can GI, López-Torres A, Barredo-Pool F et al (2013) New insights into somatic embryogenesis: LEAFY COTYLEDON1, BABY BOOM1 and WUSCHEL-RELATED HOMEOBOX4 are epigenetically regulated in Coffea canephora. PLoS ONE 8:e72160. doi: 10.1371/journal.pone.0072160 CrossRefPubMedPubMedCentralGoogle Scholar
  143. Nicotra AB, Atkin OK, Bonser SP et al (2010) Plant phenotypic plasticity in a changing climate. Trends Plant Sci 15:684–692. doi: 10.1016/j.tplants.2010.09.008 CrossRefPubMedGoogle Scholar
  144. Noceda C, Salaj T, Pérez M et al (2009) DNA demethylation and decrease on free polyamines is associated with the embryogenic capacity of Pinus nigra Arn. cell culture. Trees 23:1285–1293. doi: 10.1007/s00468-009-0370-8 CrossRefGoogle Scholar
  145. 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. doi: 10.1038/nature15365 CrossRefPubMedPubMedCentralGoogle Scholar
  146. Ono A, Yamaguchi K, Fukada-Tanaka S et al (2012) A null mutation of ROS1a for DNA demethylation in rice is not transmittable to progeny. Plant J 71:564–574. doi: 10.1111/j.1365-313X.2012.05009.x CrossRefPubMedGoogle Scholar
  147. Orton TJ (1983) Experimental approaches to the study of somaclonal variation. Plant Mol Biol Rep 1:67–76. doi: 10.1007/BF02680301 CrossRefGoogle Scholar
  148. Ou X, Zhang Y, Xu C et al (2012) Transgenerational inheritance of modified DNA methylation patterns and enhanced tolerance induced by heavy metal stress in rice (Oryza sativa L.). PLoS ONE 7:e41143. doi: 10.1371/journal.pone.0041143 CrossRefPubMedPubMedCentralGoogle Scholar
  149. Palomino G, Martínez J, Méndez I (2008) Karyotype studies in cultivars of Agave tequilana Weber. Caryologia 61(2):144–153. doi: 10.1080/00087114.2008.10589622 CrossRefGoogle Scholar
  150. Paszkowski J (2015) Controlled activation of retrotransposition for plant breeding. Curr Opin Biotechnol 32:200–206. doi: 10.1016/j.copbio.2015.01.003 CrossRefPubMedGoogle Scholar
  151. Paterson AH, Bowers JE, Bruggmann R et al (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457:551–556. doi: 10.1038/nature07723 CrossRefPubMedGoogle Scholar
  152. Paux E, Roger D, Badaeva E et al (2006) Characterizing the composition and evolution of homoeologous genomes in hexaploid wheat through BAC-end sequencing on chromosome 3B. Plant J 48:463–474. doi: 10.1111/j.1365-313X.2006.02891.x CrossRefPubMedGoogle Scholar
  153. Pecinka A, Rosa M, Schikora A et al (2009) Transgenerational stress memory is not a general response in Arabidopsis. PLoS ONE 4:e5202. doi: 10.1371/journal.pone.0005202 CrossRefPubMedPubMedCentralGoogle Scholar
  154. Pélissier T, Mathieu O (2012) Glue for jumping elements: epigenetic means for controlling transposable elements in plants. In: Grandbastien M-A, Casacuberta JM (eds) Plant transposable elements. Springer Berlin Heidelberg, p 125–145. doi: 10.1007/978-3-642-31842-9_8
  155. Pierik RLM (1997) In vitro culture of higher plants. Springer Science & Business MediaGoogle Scholar
  156. Pillot M, Baroux C, Vazquez MA et al (2010) Embryo and endosperm inherit distinct chromatin and transcriptional states from the female gametes in Arabidopsis. Plant Cell 22:307–320. doi: 10.1105/tpc.109.071647 CrossRefPubMedPubMedCentralGoogle Scholar
  157. Rai MK, Kalia RK, Singh R et al (2011) Developing stress tolerant plants through in vitro selection—an overview of the recent progress. Environ Exp Bot 71:89–98. doi: 10.1016/j.envexpbot.2010.10.021 CrossRefGoogle Scholar
  158. Rani V, Singh KP, Shiran B et al (2000) Evidence for new nuclear and mitochondrial genome organizations among high-frequency somatic embryogenesis-derived plants of allotetraploid Coffea arabica L. (Rubiaceae). Plant Cell Rep 19:1013–1020. doi: 10.1007/s002990000228 CrossRefGoogle Scholar
  159. Rao V, Donough CR (1990) Preliminary evidence of a genetic cause for the floral abnormalities in some oil palm ramets. Elaeis (Malaysia)Google Scholar
  160. Rapp RA, Wendel JF (2005) Epigenetics and plant evolution. New Phytol 168:81–91. doi: 10.1111/j.1469-8137.2005.01491.x CrossRefPubMedGoogle Scholar
  161. Reed BM, Sarasan V, Kane M et al (2011) Biodiversity conservation and conservation biotechnology tools. In Vitro Cell Dev-Pl 47:1–4. doi: 10.1007/s11627-010-9337-0 CrossRefGoogle Scholar
  162. Reinders J, Wulff BBH, Mirouze M et al (2009) Compromised stability of DNA methylation and transposon immobilization in mosaic Arabidopsis epigenomes. Genes Dev 23:939–950. doi: 10.1101/gad.524609 CrossRefPubMedPubMedCentralGoogle Scholar
  163. Richards EJ (2011) Natural epigenetic variation in plant species: a view from the field. Curr Opin Plant Biol 14:204–209. doi: 10.1016/j.pbi.2011.03.009 CrossRefPubMedGoogle Scholar
  164. Rigal M, Mathieu O (2011) A “mille-feuille” of silencing: Epigenetic control of transposable elements. Biochim Biophys Acta BBA—Gene Regul Mech 1809:452–458. doi: 10.1016/j.bbagrm.2011.04.001 CrossRefGoogle Scholar
  165. Rival A (2000) Somatic embryogenesis in oil palm. In: Gupta PK, Newton RJ (eds) Jain SM. Somatic Embryogenesis in Woody Plants, Kluwer Academic Publishers, pp 249–290Google Scholar
  166. Rival A, Aberlenc-Bertossi F, Beulé T et al (1998) Multiplication clonale du palmier à huile par embryogenèse somatique (Elaeis guineensis Jacq.)—Programmes de recherche liés au transfert d’échelle. Cah Agric 7:492–498Google Scholar
  167. Rival A, Beulé T, Barre P, Hamon S, Duval Y et al (1997) Comparative flow cytometric estimation of nuclear DNA content in oil palm (Elaeis guineensis Jacq.) tissue cultures and seed-derived plants. Plant Cell Rep 16:884–887. doi: 10.1007/s002990050339 CrossRefGoogle Scholar
  168. Rival A, Ilbert P, Labeyrie A et al (2013) Variations in genomic DNA methylation during the long-term in vitro proliferation of oil palm embryogenic suspension cultures. Plant Cell Rep 32:359–368. doi: 10.1007/s00299-012-1369-y CrossRefPubMedGoogle Scholar
  169. Rival A, Jaligot E, Beulé T, Finnegan EJ (2008) Isolation and expression analysis of genes encoding MET, CMT, and DRM methyltransferases in oil palm (Elaeis guineensis Jacq.) in relation to the “mantled” somaclonal variation. J Exp Bot 59:3271–3281. doi: 10.1093/jxb/ern178 CrossRefPubMedGoogle Scholar
  170. Rival A, Parveez GK (2005) 4.2 Elaeis guineensis Oil Palm. In: Biotechnology of fruit and nut crops, CABI Publishing. Litz, F.H., p 113–143Google Scholar
  171. Rodríguez López CM, Wetten AC, Wilkinson MJ (2010) Progressive erosion of genetic and epigenetic variation in callus-derived. New Phytol 186:856–868. doi: 10.1111/j.1469-8137.2010.03242.x CrossRefPubMedGoogle Scholar
  172. Roux NS; Toloza A; Dolezel J; Panis B (2004) Usefulness of embryogenic cell suspension cultures for the induction and selection of mutants in Musa spp. In: Banana improvement: cellular, molecular biology, and induced mutations. Jain SM, Swennen R (eds) Proceedings of a meeting held in Leuven, Belgium, 24–28 Sept 2001, p 33–43Google Scholar
  173. Schnable PS, Ware D, Fulton RS et al (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326:1112–1115. doi: 10.1126/science.1178534 CrossRefPubMedGoogle Scholar
  174. Santos D, Fevereiro P (2002) Loss of DNA methylation affects somatic embryogenesis in Medicago truncatula. Plant Cell Tiss Org 70:155–161. doi: 10.1023/A:1016369921067 CrossRefGoogle Scholar
  175. Sato M, Hosokawa M (2011) Doi M Somaclonal variation is induced de novo via the tissue culture process: a study quantifying mutated cells in Saintpaulia. PLoS ONE 6:e23541. doi: 10.1371/journal.pone.0023541 CrossRefPubMedPubMedCentralGoogle Scholar
  176. Saze H, Kakutani T (2011) Differentiation of epigenetic modifications between transposons and genes. Curr Opin Plant Biol 14:81–87. doi: 10.1016/j.pbi.2010.08.017 CrossRefPubMedGoogle Scholar
  177. Schlichting CD, Wund MA (2014) Phenotypic plasticity and epigenetic marking: an assessment of evidence for genetic accommodation. Evolution 68:656–672. doi: 10.1111/evo.12348 CrossRefPubMedGoogle Scholar
  178. Schmitz RJ, Schultz MD, Lewsey MG et al (2011) Transgenerational epigenetic instability is a source of novel methylation variants. Science 334:369–373. doi: 10.1126/science.1212959 CrossRefPubMedPubMedCentralGoogle Scholar
  179. Scoville AG, Barnett LL, Bodbyl Roels S et al (2011) Differential regulation of a MYB transcription factor is correlated with transgenerational epigenetic inheritance of trichome density in Mimulus guttatus. New Phytol 191:251–263. doi: 10.1111/j.1469-8137.2011.03656.x CrossRefPubMedPubMedCentralGoogle Scholar
  180. Slaughter A, Daniel X, Flors V et al (2012) Descendants of primed arabidopsis plants exhibit resistance to biotic stress. Plant Physiol 158:835–843. doi: 10.1104/pp.111.191593 CrossRefPubMedGoogle Scholar
  181. Slotkin RK, Martienssen RA (2007) Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet 8:272–285. doi: 10.1038/nrg2072 CrossRefPubMedGoogle Scholar
  182. Slotkin RK, Vaughn M, Borges F et al (2009) Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 136:461–472. doi: 10.1016/j.cell.2008.12.038 CrossRefPubMedPubMedCentralGoogle Scholar
  183. Smulders MJM, de Klerk GJ (2011) Epigenetics in plant tissue culture. Plant Growth Regul 63:137–146. doi: 10.1007/s10725-010-9531-4 CrossRefGoogle Scholar
  184. Smýkal P, Valledor L, Rodriguez 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. doi: 10.1007/s00299-007-0413-9 CrossRefPubMedGoogle Scholar
  185. Springer NM (2013) Epigenetics and crop improvement. Trends Genet 29:241–247. doi: 10.1016/j.tig.2012.10.009 CrossRefPubMedGoogle Scholar
  186. Sugimoto K, Jiao Y, Meyerowitz EM (2010) Arabidopsis regeneration from multiple tissues occurs via a root development pathway. Dev Cell 18:463–471. doi: 10.1016/j.devcel.2010.02.004 CrossRefPubMedGoogle Scholar
  187. Suoniemi A, Narvanto A, Schulman AH (1996) The BARE-1 retrotransposon is transcribed in barley from an LTR promoter active in transient assays. Plant Mol Biol 31:295–306. doi: 10.1007/BF00021791 CrossRefPubMedGoogle Scholar
  188. Teixeira JB, Söndahl MR, Nakamura T, Kirby EG (1995) Establishment of oil palm cell suspensions and plant regeneration. Plant Cell Tiss Org 40:105–111. doi: 10.1007/BF00037662 CrossRefGoogle Scholar
  189. Teyssier C, Maury S, Beaufour M et al (2014) In search of markers for somatic embryo maturation in hybrid larch (Larix × eurolepis): global DNA methylation and proteomic analyses. Physiol Plant 150:271–291. doi: 10.1111/ppl.12081 CrossRefPubMedGoogle Scholar
  190. Thibaud-Nissen F, Shealy RT, Khanna A, Vodkin LO (2003) Clustering of Microarray Data Reveals Transcript Patterns Associated with Somatic Embryogenesis in Soybean. Plant Physiol 132:118–136. doi: 10.1104/pp.103.019968 CrossRefPubMedPubMedCentralGoogle Scholar
  191. Todorovska E (2007) Retrotransposons and their role in plant—genome evolution. Biotechnol Biotechnol Equip 21:294–305. doi: 10.1080/13102818.2007.10817464 CrossRefGoogle Scholar
  192. Tremblay L, Levasseur C, Tremblay FM (1999) Frequency of somaclonal variation in black spruce (Picea mariana, Pinaceae) and White spruce (P. glauca, Pinaceae) derived from somatic embryogenesis and identification of some factors involved in genetic instability. Ame J Bot 86:1373–1381CrossRefGoogle Scholar
  193. Us-Camas R, Rivera-Solís G, Duarte-Aké F, De-la-Peña C (2014) In vitro culture: an epigenetic challenge for plants. Plant Cell Tiss Org 118:187–201. doi: 10.1007/s11240-014-0482-8 CrossRefGoogle Scholar
  194. Van Zanten M, Tessadori F, Peeters AJM, Fransz P (2012) Shedding light on large-scale chromatin reorganization in Arabidopsis thaliana. Mol Plant 5:57–64. doi: 10.1093/mp/sss030 Google Scholar
  195. Verhoeven KJF, Jansen JJ, van Dijk PJ, Biere A (2010) Stress induced DNA methylation changes and their heritability in asexual dandelions. New Phytol 185:1108–1118. doi: 10.1111/j.1469-8137.2009.03121.x CrossRefPubMedGoogle Scholar
  196. Von Aderkas P, Bonga J (2000) Influencing micropropagation and somatic embryogenesis in mature trees by manipulation of phase change, stress and culture environment. Tree Physiol 20:921–928CrossRefGoogle Scholar
  197. Wada Y, Miyamoto K, Kusano T, Sano H (2004) Association between up-regulation of stress-responsive genes and hypomethylation of genomic DNA in tobacco plants. Mol Genet Genomics 271:658–666. doi: 10.1007/s00438-004-1018-4 CrossRefPubMedGoogle Scholar
  198. Wang Q-M, Wang L (2012) An evolutionary view of plant tissue culture: somaclonal variation and selection. Plant Cell Rep 31:1535–1547. doi: 10.1007/s00299-012-1281-5 CrossRefPubMedGoogle Scholar
  199. Wheeler BS (2013) Small RNAs, big impact: small RNA pathways in transposon control and their effect on the host stress response. Chromosome Res 21:587–600. doi: 10.1007/s10577-013-9394-4 CrossRefPubMedGoogle Scholar
  200. Wicker T, Sabot F, Hua-Van A et al (2007) A unified classification system for eukaryotic transposable elements. Nat Rev Genet 8:973–982. doi: 10.1038/nrg2165 CrossRefPubMedGoogle Scholar
  201. Wollmann H, Berger F (2012) Epigenetic reprogramming during plant reproduction and seed development. Curr Opin Plant Biol 15:63–69. doi: 10.1016/j.pbi.2011.10.001 CrossRefPubMedGoogle Scholar
  202. Wu X-M, Liu M-Y, Ge X-X et al (2010) Stage and tissue-specific modulation of ten conserved miRNAs and their targets during somatic embryogenesis of valencia sweet orange. Planta 233:495–505. doi: 10.1007/s00425-010-1312-9 CrossRefPubMedGoogle Scholar
  203. Wu X-M, Kou S-J, Liu Y-L, Fang Y-N, Xu Q, Guo W-W (2015) Genomewide analysis of small RNAs in nonembryogenic and embryogenic tissues of citrus: microRNA- and siRNA-mediated transcript cleavage involved in somatic embryogenesis. Plant Biotechnol J 13:383–394. doi:  10.1111/pbi.12317
  204. Yoo M-J, Liu X, Pires JC et al (2014) Nonadditive gene expression in polyploids. Ann Rev Genet 48:485–517. doi: 10.1146/annurev-genet-120213-092159 CrossRefPubMedGoogle Scholar
  205. Zhang S, Liu X, Lin Y et al (2010) Characterization of a ZmSERK gene and its relationship to somatic embryogenesis in a maize culture. Plant Cell Tiss Org 105:29–37. doi: 10.1007/s11240-010-9834-1 CrossRefGoogle Scholar
  206. Zhang Y, Zhang S, Han S et al (2012) Transcriptome profiling and in silico analysis of somatic embryos in Japanese larch (Larix leptolepis). Plant Cell Rep 31:1637–1657. doi: 10.1007/s00299-012-1277-1 CrossRefPubMedGoogle Scholar
  207. Zoriniants SE, Nosov AV, Monforte Gonzalez M, Mendes Zeel M, Loyola-Vargas VM (2003) Variation of nuclear DNA content during somatic embryogenesis and plant regeneration of Coffea arabica L. using cytophotometry. Plant Sci 164:141–146. doi: 10.1016/S0168-9452(02)00322-9 CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Hervé Etienne
    • 1
    Email author
  • Romain Guyot
    • 2
  • Thierry Beulé
    • 3
  • Jean-Christophe Breitler
    • 1
  • Estelle Jaligot
    • 3
  1. 1.CIRAD, UMR IPMEMontpellierFrance
  2. 2.IRD, UMR IPMEMontpellierFrance
  3. 3.CIRAD, UMR DIADEMontpellierFrance

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