The Pliable Genome: Epigenomics of Norway Spruce

  • Igor YakovlevEmail author
  • Marcos Viejo
  • Carl Gunnar Fossdal
Part of the Compendium of Plant Genomes book series (CPG)


Recent discoveries have highlighted multiple mitotically and meiotically inherited alterations in gene expression that could not be explained solely by changes in the DNA sequence but were acknowledged as epigenetic. The modern view on epigenetics considers it as an integral part of genetics. Epigenetic mechanisms are encoded by genes in the genome and contribute to an essential part of genomic diversity, significantly extending its regulatory abilities. Epigenetic mechanisms involve molecular chromatin alterations through DNA methylation and histone modifications, as well as, complex non-coding RNAs and related enzyme machinery leading to changes in gene expression and resulting in changing phenotypes. In plants, epigenetic mechanisms may occur over their lifetime and across multiple generations, and can contribute substantially to phenotypic plasticity, stress responses, disease resistance, acclimation and adaptation to habitat conditions. In this review, we summarize recent advances with regards to Norway spruce epigenomics. We first consider the large size of the spruce genome that is linked to epigenetic mechanisms and why epigenomics is vitally important for spruce. Then, we discuss the molecular machinery supporting epigenetic mechanisms in Norway spruce and putative gene models involved. We presume substantial extension of gene families of epigenetic regulators and non-coding RNAs, especially in reproductive tissues. Norway spruce was the first species among forest trees in which epigenetic memory and epigenetic mechanisms were studied. The induction of an epigenetic memory during sexual reproduction and somatic embryogenesis has been described in Norway spruce. We discuss the latest results of epigenomic variation and epigenetic memory studies in Norway spruce and define the future perspectives for epigenetic studies. However, there is still a long way to decipher how the epigenetic mechanisms are involved in maintaining the stability of the spruce epigenome, how the epigenome is set to produce the epigenetic memory phenomenon and how these may result in an increased rate of adaptation to a changing environment.


Norway spruce Epigenetic mechanisms DNA methylation Histone modifications Non-coding RNAs Epigenetic memory Adaptation 

Supplementary material

476904_1_En_5_MOESM1_ESM.xlsx (159 kb)
Supplementary material (XLSX 158 KB)


  1. Allen E, Howell MD (2010) miRNAs in the biogenesis of trans-acting siRNAs in higher plants. Semin Cell Dev Biol 21(8):798–804. Scholar
  2. Allen E, Xie Z, Gustafson AM, Carrington JC (2005) MicroRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121(2):207–221. Scholar
  3. Angel A, Song J, Dean C, Howard M (2011) A polycomb-based switch underlying quantitative epigenetic memory. Nature 476(7358):105–108. Scholar
  4. Arnaudo A, Garcia B (2013) Proteomic characterization of novel histone post-translational modifications. Epigenetics & Chromatin 6(1):24CrossRefGoogle Scholar
  5. Arrowsmith CH, Bountra C, Fish PV, Lee K, Schapira M (2012) Epigenetic protein families: a new frontier for drug discovery. Nat Rev Drug Discov 11(5):384–400CrossRefGoogle Scholar
  6. Ausin I, Feng S, Yu C, Liu W, Kuo HY, Jacobsen EL, Zhai J, Gallego-Bartolome J, Wang L, Egertsdotter U, Street NR, Jacobsen SE, Wang H (2016) DNA methylome of the 20-gigabase Norway spruce genome. PNAS. Scholar
  7. Avramova Z (2015) Transcriptional ‘memory’ of a stress: transient chromatin and memory (epigenetic) marks at stress-response genes. Plant J 83(1):149–159. Scholar
  8. Axtell MJ (2013) Classification and comparison of small RNAs from plants. Annu Rev Plant Biol 64(1):137–159. Scholar
  9. Axtell M, Westholm J, Lai E (2011) Vive la difference: biogenesis and evolution of microRNAs in plants and animals. Genome Biol 12(4):221CrossRefGoogle Scholar
  10. Bannister AJ, Kouzarides T (2011) Regulation of chromatin by histone modifications. Cell Res 21(3):381–395. Scholar
  11. Barth TK, Imhof A (2010) Fast signals and slow marks: the dynamics of histone modifications. Trends Biochem Sci 35(11):618–626CrossRefGoogle Scholar
  12. Berger SL, Kouzarides T, Shiekhattar R, Shilatifard A (2009) An operational definition of epigenetics. Genes Dev 23(7):781–783. Scholar
  13. Bewick AJ, Niederhuth CE, Ji L, Rohr NA, Griffin PT, Leebens-Mack J, Schmitz RJ (2017) The evolution of CHROMOMETHYLASES and gene body DNA methylation in plants. Genome Biol 18(1):65. Scholar
  14. Biswas S, Rao CM (2018) Epigenetic tools (The Writers, The Readers and The Erasers) and their implications in cancer therapy. Eur J Pharmacol 837:8–24. Scholar
  15. Bond DM, Baulcombe DC (2014) Small RNAs and heritable epigenetic variation in plants. Trends Cell Biol 24(2):100–107. Scholar
  16. Bourque G, Burns KH, Gehring M, Gorbunova V, Seluanov A, Hammell M, Imbeault M, Izsvák Z, Levin HL, Macfarlan TS, Mager DL, Feschotte C (2018) Ten things you should know about transposable elements. Genome Biol 19(1):199. Scholar
  17. Bousios A, Gaut BS (2016) Mechanistic and evolutionary questions about epigenetic conflicts between transposable elements and their plant hosts. Curr Opin Plant Biol 30:123–133. Scholar
  18. Boyko A, Kovalchuk I (2010) Transgenerational response to stress in Arabidopsis thaliana. Plant Signal Behav 5(8):995–998CrossRefGoogle Scholar
  19. Bräutigam K, Vining KJ, Lafon-Placette C, Fossdal CG, Mirouze M, Marcos JG, Fluch S, Fraga MF, Guevara MÁ, Abarca D, Johnsen Ø, Maury S, Strauss SH, Campbell MM, Rohde A, Díaz-Sala C, Cervera M-T (2013) Epigenetic regulation of adaptive responses of forest tree species to the environment. Ecol Evol 3(2):399–415. Scholar
  20. Browse J, Xin Z (2001) Temperature sensing and cold acclimation. Curr Opin Plant Biol 4(3):241–246. Scholar
  21. Bultmann S, Stricker SH (2018) Entering the post-epigenomic age: back to epigenetics. Open Biol 8(3):180013. Scholar
  22. Carneros E, Yakovlev I, Viejo M, Olsen JE, Fossdal CG (2017) The epigenetic memory of temperature during embryogenesis modifies the expression of bud burst-related genes in Norway spruce epitypes. Planta 246:553–566.
  23. Carthew RW, Sontheimer EJ (2009) Origins and Mechanisms of miRNAs and siRNAs. Cell 136(4):642–655CrossRefGoogle Scholar
  24. Casola C, Koralewski TE (2018) Pinaceae show elevated rates of gene turnover that are robust to incomplete gene annotation. Plant J 95(5):862–876. Scholar
  25. Chan SWL, Henderson IR, Jacobsen SE (2005) Gardening the genome: DNA methylation in Arabidopsis thaliana. Nat Rev Genet 6(5):351–360CrossRefGoogle Scholar
  26. Chen X (2009) Small RNAs and their roles in plant development. Annu Rev Cell Dev Biol 25:21–44. Scholar
  27. Chen M, Lv S, Meng Y (2010) Epigenetic performers in plants. Dev Growth Diff 52(6):555–566. Scholar
  28. Clapier CR, Cairns BR (2009) The biology of chromatin remodeling complexes. Annu Rev Biochem 78(1):273–304. Scholar
  29. Conrath U (2011) Molecular aspects of defence priming. Trends Plant Sci 16(10):524–531. Scholar
  30. Conrath U, Beckers GJM, Flors V, García-Agustín P, Jakab G, Mauch F, Newman M-A, Pieterse CMJ, Poinssot B, Pozo MJ, Pugin A, Schaffrath U, Ton J, Wendehenne D, Zimmerli L, Mauch-Mani B (2006) Priming: getting ready for battle. Mol Plant-Microbe Interact 19(10):1062–1071. Scholar
  31. Cossu RM, Casola C, Giacomello S, Vidalis A, Scofield DG, Zuccolo A (2017) LTR retrotransposons show low levels of unequal recombination and high rates of intraelement gene conversion in large plant genomes. Genome Biol Evol 9(12):3449–3462. Scholar
  32. Costa FF (2010) Non-coding RNAs: meet thy masters. BioEssays 32(7):599–608. Scholar
  33. D’Urso A, Brickner JH (2014) Mechanisms of epigenetic memory. Trends Genet 30(6):230–236. Scholar
  34. De La Torre AR, Birol I, Bousquet J, Ingvarsson PK, Jansson S, Jones SJM, Keeling CI, MacKay J, Nilsson O, Ritland K, Street N, Yanchuk A, Zerbe P, Bohlmann J (2014) Insights into conifer giga-genomes. Plant Physiol 166(4):1724–1732. Scholar
  35. De La Torre AR, Li Z, Van de Peer Y, Ingvarsson PK (2017) Contrasting rates of molecular evolution and patterns of selection among gymnosperms and flowering plants. Mol Biol Evol 34(6):1363–1377. Scholar
  36. Dewan S, Vander Mijnsbrugge K, De Frenne P, Steenackers M, Michiels B, Verheyen K (2018) Maternal temperature during seed maturation affects seed germination and timing of bud set in seedlings of European black poplar. For Ecol Manag 410:126–135. Scholar
  37. Dewan S, De Frenne P, Leroux O, Nijs I, Vander Mijnsbrugge K, Verheyen K (2019) Phenology and growth of Fagus sylvatica and Quercus robur seedlings in response to temperature variation in the parental versus offspring generation. Plant Biol 0(0).
  38. Dillon S, Zhang X, Trievel R, Cheng X (2005) The SET-domain protein superfamily: protein lysine methyltransferases. Genome Biol 6(8):227CrossRefGoogle Scholar
  39. Dolgosheina EV, Morin RD, Aksay G, Sahinalp SC, Magrini V, Mardis ER, Mattsson J, Unrau PJ (2008) Conifers have a unique small RNA silencing signature. RNA 14(8):1508–1515. Scholar
  40. Donohue K (2014) The epigenetics of adaptation: focusing on epigenetic stability as an evolving trait. Evolution 68(3):617–619. Scholar
  41. Duncan EJ, Gluckman PD, Dearden PK (2014) Epigenetics, plasticity, and evolution: How do we link epigenetic change to phenotype? J Exp Zool Part B: Mol Dev Evol 322(4):208–220. Scholar
  42. Eckardt NA (2006) Genetic and epigenetic regulation of embryogenesis. Plant Cell 18(4):781–784. Scholar
  43. Ecker S, Pancaldi V, Valencia A, Beck S, Paul DS (2018) Epigenetic and transcriptional variability shape phenotypic plasticity. BioEssays 40(2):1700148. Scholar
  44. Espinas NA, Saze H, Saijo Y (2016) Epigenetic control of defense signaling and priming in plants. Front Plant Sci 7(1201).
  45. Fedoroff NV (2012) Transposable elements, epigenetics, and genome evolution. Science 338(6108):758–767. Scholar
  46. Fehér A (2014) Somatic embryogenesis—stress-induced remodeling of plant cell fate. Biochim Biophys Acta (0).
  47. Fortes A, Gallusci P (2017) Plant stress responses and phenotypic plasticity in the Epigenomics era: perspectives on the grapevine scenario, a model for perennial crop plants. Front Plant Sci 8(82).
  48. Franklin KA (2010) Plant chromatin feels the heat. Cell 140(1):26–28. Scholar
  49. Franks SJ, Hoffmann AA (2012) Genetics of climate change adaptation. Annu Rev Genet 46(1):185–208. Scholar
  50. Friedrich T, Faivre L, Bäurle I, Schubert D (2018) Chromatin-based mechanisms of temperature memory in plants. Plant Cell Environ 0(0).
  51. Fuchs Wightman F, Giono LE, Fededa JP, de la Mata M (2018) Target RNAs strike back on MicroRNAs. Front Genet 9:435. Scholar
  52. Gömöry D, Foffová E, Longauer R, Krajmerová D (2015) Memory effects associated with early-growth environment in Norway spruce and European larch. Eur J For Res 134(1):89–97. Scholar
  53. Gömöry D, Hrivnák M, Krajmerová D, Longauer R (2017) Epigenetic memory effects in forest trees: a victory of “Michurinian biology”? Cent Eur For J 63(4):173–179. Scholar
  54. Grossniklaus U, Kelly WG, Ferguson-Smith AC, Pembrey M, Lindquist S (2013) Transgenerational epigenetic inheritance: how important is it? Nat Rev Genet 14:228. Scholar
  55. Hagmann J, Becker C, Müller J, Stegle O, Meyer RC, Wang G, Schneeberger K, Fitz J, Altmann T, Bergelson J, Borgwardt K, Weigel D (2015) Century-scale methylome stability in a recently diverged arabidopsis thaliana lineage. PLoS Genet 11(1):e1004920. Scholar
  56. He Y, Li Z (2018) Epigenetic environmental memories in plants: establishment, maintenance, and reprogramming. Trends Genet 34(11):856–866. Scholar
  57. Heer K, Ullrich KK, Hiss M, Liepelt S, Schulze Brüning R, Zhou J, Opgenoorth L, Rensing SA (2018) Detection of somatic epigenetic variation in Norway spruce via targeted bisulfite sequencing. Ecol Evol 0:1–11.
  58. Heo JB, Sung S (2011) Encoding memory of winter by noncoding RNAs. Epigenetics 6(5):544–547. Scholar
  59. Heo J, Lee Y-S, Sung S (2013) Epigenetic regulation by long noncoding RNAs in plants. Chromosom Res 21(6–7):685–693. Scholar
  60. Herman JJ, Sultan SE (2016) DNA methylation mediates genetic variation for adaptive transgenerational plasticity. Proc R Soc B: Biol Sci 283(1838).
  61. Hilker M, Schwachtje J, Baier M, Balazadeh S, Bäurle I, Geiselhardt S, Hincha DK, Kunze R, Mueller-Roeber B, Rillig MC, Rolff J, Romeis T, Schmülling T, Steppuhn A, van Dongen J, Whitcomb SJ, Wurst S, Zuther E, Kopka J (2016) Priming and memory of stress responses in organisms lacking a nervous system. Biol Rev 91(4):1118–1133. Scholar
  62. Hirsch CD, Springer NM (2017) Transposable element influences on gene expression in plants. Biochim Biophys Acta 1860(1):157–165. Scholar
  63. Hollick JB, Patterson GI, Coe EH, Cone KC, Chandler VL (1995) Allelic interactions heritably alter the activity of a metastable maize pl allele. Genetics 141(2):709–719PubMedPubMedCentralGoogle Scholar
  64. Hollister JD, Gaut BS (2009) Epigenetic silencing of transposable elements: A trade-off between reduced transposition and deleterious effects on neighboring gene expression. Genome Res 19(8):1419–1428. Scholar
  65. Houben A, Demidov D, Caperta AD, Karimi R, Agueci F, Vlasenko L (2007) Phosphorylation of histone H3 in plants—a dynamic affair. Biochim et Biophys Acta (BBA) - Gene Struct Expr 1769(5–6):308–315.
  66. Ikeda Y, Nishimura T (2015) The role of DNA methylation in transposable element silencing and genomic imprinting. In: Pontes O, Jin H (eds) Nuclear functions in plant transcription, signaling and development. Springer New York, pp 13–29.
  67. Iwasaki M, Paszkowski J (2014) Epigenetic memory in plants. EMBO J 33(18):1987–1998. Scholar
  68. 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(1):50–55. Scholar
  69. Johannes F, Schmitz RJ (2018) Spontaneous epimutations in plants. New Phytol 0(0).
  70. Johannes F, Colot V, Jansen RC (2008) Epigenome dynamics: a quantitative genetics perspective. Nat Rev Genet 9:883. Scholar
  71. Johannes F, Porcher E, Teixeira FK, Saliba-Colombani V, Simon M, Agier N, Bulski A, Albuisson J, Heredia F, Audigier P, Bouchez D, Dillmann C, Guerche P, Hospital F, Colot V (2009) Assessing the impact of transgenerational epigenetic variation on complex traits. PLoS Genet 5(6):e1000530. Scholar
  72. Johnsen Ø, Daehlen OG, Østreng G, Skrøppa T (2005a) Daylength and temperature during seed production interactively affect adaptive performance of Picea abies progenies. New Phytol 168(3):589–596. Scholar
  73. Johnsen Ø, Fossdal CG, Nagy N, Molmann J, Dælen OG, Skrøppa T (2005b) Climatic adaptation in Picea abies progenies is affected by the temperature during zygotic embryogenesis and seed maturation. Plant Cell Environ 28(9):1090–1102. Scholar
  74. Johnson LJ, Tricker PJ (2010) Epigenomic plasticity within populations: its evolutionary significance and potential. Heredity 105(1):113–121. Scholar
  75. Kalavacharla V, Subramani M, Ayyappan V, Dworkin MC, Hayford RK (2017) Plant epigenomics. In: Tollefsbol TO (ed) Handbook of epigenetics, 2nd edn. Academic Press, pp 245–258.
  76. Kalisz S, Purugganan MD (2004) Epialleles via DNA methylation: consequences for plant evolution. Trends Ecol Evol 19(6):309–314. Scholar
  77. Källman T, Chen J, Gyllenstrand N, Lagercrantz U (2013) A significant fraction of 21 nt sRNA originates from phased degradation of resistance genes in several perennial species. Plant Physiol 162:741–754. Scholar
  78. Kamp HD, Higgins DE (2011) A protein thermometer controls temperature-dependent transcription of flagellar motility genes in listeria monocytogenes. PLoS Pathog 7(8):e1002153. Scholar
  79. Kinoshita T, Seki M (2014) Epigenetic memory for stress response and adaptation in plants. Plant Cell Physiol 55:1859–1863. Scholar
  80. Klose RJ, Kallin EM, Zhang Y (2006) JmjC-domain-containing proteins and histone demethylation. Nat Rev Genet 7(9):715–727CrossRefGoogle Scholar
  81. Knight MR, Knight H (2012) Low-temperature perception leading to gene expression and cold tolerance in higher plants. New Phytol 195(4):737–751. Scholar
  82. Kouzarides T (2007) Chromatin modifications and their function. Cell 128(4):693–705. Scholar
  83. Kovalchuk I (2018) Role of epigenetics in transgenerational changes: genome stability in response to plant stress. In: Baluska F, Gagliano M, Witzany G (eds) Memory and learning in plants. Springer International Publishing, Cham, pp 79–109.
  84. Krokene P (2016) Carbon castles and insect invaders: dissecting physical defences in conifer stems. Plant Cell Environ 39(8):1643–1645. Scholar
  85. Kumar S (2018) Epigenomics of plant responses to environmental stress. Epigenomes 2(1):6CrossRefGoogle Scholar
  86. Kumar SV, Wigge PA (2010) H2A.Z-containing nucleosomes mediate the thermosensory response in Arabidopsis. Cell 140(1):136–147.
  87. Kurdyukov S, Bullock M (2016) DNA methylation analysis: choosing the right method. Biology 5(1):3. Scholar
  88. Kvaalen H, Johnsen O (2008) Timing of bud set in Picea abies is regulated by a memory of temperature during zygotic and somatic embryogenesis. New Phytol 177(1):49–59. Scholar
  89. Lämke J, Bäurle I (2017) Epigenetic and chromatin-based mechanisms in environmental stress adaptation and stress memory in plants. Genome Biol 18(1):124. Scholar
  90. Latzel V, Rendina González AP, Rosenthal J (2016) Epigenetic memory as a basis for intelligent behavior in clonal plants. Front Plant Sci 7:1354. Scholar
  91. Law JA, Jacobsen SE (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11(3):204–220CrossRefGoogle Scholar
  92. Lee JT (2012) Epigenetic regulation by long noncoding RNAs. Science 338(6113):1435–1439. Scholar
  93. Li C, Zhang B (2016) MicroRNAs in control of plant development. J Cell Physiol 231(2):303–313. Scholar
  94. Li Y, Kumar S, Qian W (2018) Active DNA demethylation: mechanism and role in plant development. Plant Cell Rep 37(1):77–85. Scholar
  95. Liu C, Lu F, Cui X, Cao X (2010) Histone methylation in higher plants. Annu Rev Plant Biol 61(1):395–420. Scholar
  96. Lu D (2013) Epigenetic modification enzymes: catalytic mechanisms and inhibitors. Acta Pharm Sin B 3(3):141–149. Scholar
  97. Mahfouz MM (2010) RNA-directed DNA methylation. Plant Signal Behav 5(7):806–816. Scholar
  98. Mahrez W, Arellano MST, Moreno-Romero J, Nakamura M, Shu H, Nanni P, Köhler C, Gruissem W, Hennig L (2016) H3K36ac is an evolutionary conserved plant histone modification that marks active genes. Plant Physiol 170(3):1566–1577. Scholar
  99. Manning BJ, Peterson CL (2013) Releasing the brakes on a chromatin-remodeling enzyme. Nat Struct Mol Biol 20(1):5–7. Scholar
  100. Martinez-Medina A, Flors V, Heil M, Mauch-Mani B, Pieterse CMJ, Pozo MJ, Ton J, van Dam NM, Conrath U (2016) Recognizing plant defense priming. Trends Plant Sci 21(10):818–822. Scholar
  101. Matzke MA, Mosher RA (2014) RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nat Rev Genet 15(6):394–408. Scholar
  102. Matzke MA, Kanno T, Matzke AJM (2015) RNA-directed DNA methylation: the evolution of a complex epigenetic pathway in flowering plants. Annu Rev Plant Biol 66(1):243–267. Scholar
  103. Mauch-Mani B, Baccelli I, Luna E, Flors V (2017) Defense priming: an adaptive part of induced resistance. Annu Rev Plant Biol 68(1):485–512. Scholar
  104. Meyers BC, Axtell MJ, Bartel B, Bartel DP, Baulcombe D, Bowman JL, Cao X, Carrington JC, Chen X, Green PJ, Griffiths-Jones S, Jacobsen SE, Mallory AC, Martienssen RA, Poethig RS, Qi Y, Vaucheret H, Voinnet O, Watanabe Y, Weigel D, Zhu J-K (2008) Criteria for annotation of plant MicroRNAs. Plant Cell tpc.108.064311.
  105. Michael TP (2014) Plant genome size variation: bloating and purging DNA. Brief Funct Genomics. Scholar
  106. Mittler R, Finka A, Goloubinoff P (2012) How do plants feel the heat? Trends Biochem Sci 37(3):118–125. Scholar
  107. Molinier J, Ries G, Zipfel C, Hohn B (2006) Transgeneration memory of stress in plants. Nature 442:1046. Scholar
  108. Musselman CA, Lalonde M-E, Côté J, Kutateladze TG (2012) Perceiving the epigenetic landscape through histone readers. Nat Struct Mol Biol 19(12):1218–1227. Scholar
  109. Narlikar Geeta J, Sundaramoorthy R, Owen-Hughes T (2013) Mechanisms and functions of ATP-dependent chromatin-remodeling enzymes. Cell 154(3):490–503. Scholar
  110. Nathan D, Sterner DE, Berger SL (2003) Histone modifications: now summoning sumoylation. Proc Natl Acad Sci USA 100(23):13118–13120. Scholar
  111. Nicholson TB, Veland N, Chen T (2015) Writers, readers, and erasers of epigenetic marks. In: Gray SG (ed) Epigenetic cancer therapy. Academic Press, Boston, pp 31–66.
  112. Nicoglou A, Merlin F (2017) Epigenetics: A way to bridge the gap between biological fields. Stud Hist Philos Sci Part C: Stud Hist Philos Biol Biomed Sci
  113. Nystedt B, Street NR, Wetterbom A, Zuccolo A, Lin Y-C, Scofield DG, Vezzi F, Delhomme N, Giacomello S, Alexeyenko A, Vicedomini R, Sahlin K, Sherwood E, Elfstrand M, Gramzow L, Holmberg K, Hallman J, Keech O, Klasson L, Koriabine M, Kucukoglu M, Kaller M, Luthman J, Lysholm F, Niittyla T, Olson A, Rilakovic N, Ritland C, Rossello JA, Sena J, Svensson T, Talavera-Lopez C, Theiszen G, Tuominen H, Vanneste K, Wu Z-Q, Zhang B, Zerbe P, Arvestad L, Bhalerao R, Bohlmann J, Bousquet J, Garcia Gil R, Hvidsten TR, de Jong P, MacKay J, Morgante M, Ritland K, Sundberg B, Lee Thompson S, Van de Peer Y, Andersson B, Nilsson O, Ingvarsson PK, Lundeberg J, Jansson S (2013) The Norway spruce genome sequence and conifer genome evolution. Nature 497:579–584. Scholar
  114. Ong-Abdullah M, Ordway JM, Jiang N, Ooi S-E, Kok S-Y, Sarpan N, Azimi N, Hashim AT, Ishak Z, Rosli SK, Malike FA, Bakar NAA, Marjuni M, Abdullah N, Yaakub Z, Amiruddin MD, Nookiah R, Singh R, Low E-TL, Chan K-L, Azizi N, Smith SW, Bacher B, Budiman MA, Van Brunt A, Wischmeyer C, Beil M, Hogan M, Lakey N, Lim C-C, Arulandoo X, Wong C-K, Choo C-N, Wong W-C, Kwan Y-Y, Alwee SSRS, Sambanthamurthi R, Martienssen RA (2015) Loss of Karma transposon methylation underlies the mantled somaclonal variant of oil palm. Nature 525(7570):533–537. Scholar
  115. Pascual J, Cañal MJ, Correia B, Escandon M, Hasbún R, Meijón M, Pinto G, Valledor L (2014) Can epigenetics help forest plants to adapt to climate change? In: Epigenetics in plants of agronomic importance: fundamentals and applications: transcriptional regulation and chromatin remodelling in plants. Springer International Publishing, Cham, pp 125–146.
  116. Pastor V, Luna E, Mauch-Mani B, Ton J, Flors V (2013) Primed plants do not forget. Environ Exp Bot 94:46–56. Scholar
  117. Patkin EL, Sofronov GA (2013) Population epigenetics, ecotoxicology, and human diseases. Russ J Genet: Appl Res 3(5):338–351. Scholar
  118. Penfield S (2008) Temperature perception and signal transduction in plants. New Phytol 179(3):615–628. Scholar
  119. Pikaard CS, Mittelsten Scheid O (2014) Epigenetic regulation in plants. Cold Spring Harb Perspect Biol 6(12):a019315. Scholar
  120. Quadrana L, Almeida J, Asís R, Duffy T, Dominguez PG, Bermúdez L, Conti G, Corrêa da Silva JV, Peralta IE, Colot V, Asurmendi S, Fernie AR, Rossi M, Carrari F (2014) Natural occurring epialleles determine vitamin E accumulation in tomato fruits. Nat Commun 5:4027. Scholar
  121. Rapp RA, Wendel JF (2005) Epigenetics and plant evolution. New Phytol 168(1):81–91. Scholar
  122. Richards EJ (2006) Inherited epigenetic variation—revisiting soft inheritance. Nat Rev Genet 7:395. Scholar
  123. Richards CL, Bossdorf O, Verhoeven KJF (2010) Understanding natural epigenetic variation. New Phytol 187(3):562–564. Scholar
  124. Roessler K, Bousios A, Meca E, Gaut BS (2018) Modeling interactions between transposable elements and the plant epigenetic response: a surprising reliance on element retention. Genome Biol Evol 10(3):803–815. Scholar
  125. Rohde A, Junttila O (2008) Remembrances of an embryo: long-term effects on phenology traits in spruce. New Phytol 177(1):2–5. Scholar
  126. Rosa S, Shaw P (2013) Insights into chromatin structure and dynamics in plants. Biology 2(4):1378–1410CrossRefGoogle Scholar
  127. Rossetto D, Avvakumov N, Côté J (2012) Histone phosphorylation: a chromatin modification involved in diverse nuclear events. Epigenetics 7(10):1098–1108. Scholar
  128. Sang Y, Silva-Ortega CO, Wu S, Yamaguchi N, Wu M-F, Pfluger J, Gillmor CS, Gallagher KL, Wagner D (2012) Mutations in two non-canonical Arabidopsis SWI2/SNF2 chromatin remodeling ATPases cause embryogenesis and stem cell maintenance defects. Plant J: For Cell Mol Biol 72(6):1000–1014. Scholar
  129. Santo T, Pereira R, Leitão J (2017) The Pea (Pisum sativum L.) Rogue paramutation is accompanied by alterations in the methylation pattern of specific genomic sequences. Epigenomes 1(1):6Google Scholar
  130. Saroha M, Singroha G, Sharma M, Mehta G, Gupta O, Sharma P (2017) sRNA and epigenetic mediated abiotic stress tolerance in plants. Indian J Plant Physiol 22(4):458–469.
  131. Satake A, Iwasa Y (2012) A stochastic model of chromatin modification: cell population coding of winter memory in plants. J Theor Biol 302:6–17. Scholar
  132. Saze H (2008) Epigenetic memory transmission through mitosis and meiosis in plants. Semin Cell Dev Biol 19(6):527–536. Scholar
  133. Schmitz RJ, Schultz MD, Lewsey MG, O’Malley RC, Urich MA, Libiger O, Schork NJ, Ecker JR (2011) Transgenerational epigenetic instability is a source of novel methylation variants. Science 334(6054):369–373. Scholar
  134. Sengupta P, Garrity P (2013) Sensing temperature. Curr Biol 23(8):R304–R307. Scholar
  135. Seymour DK, Becker C (2017) The causes and consequences of DNA methylome variation in plants. Curr Opin Plant Biol 36:56–63. Scholar
  136. Shiio Y, Eisenman RN (2003) Histone sumoylation is associated with transcriptional repression. Proc Natl Acad Sci USA 100(23):13225–13230. Scholar
  137. Silveira AB, Trontin C, Cortijo S, Barau J, Del Bem LEV, Loudet O, Colot V, Vincentz M (2013) Extensive natural epigenetic variation at a de novo originated gene. PLoS Genet 9(4):e1003437. Scholar
  138. Singh A, Gautam V, Singh S, Sarkar Das S, Verma S, Mishra V, Mukherjee S, Sarkar AK (2018) Plant small RNAs: advancement in the understanding of biogenesis and role in plant development. Planta 248(3):545–558. Scholar
  139. Skrøppa T, Tollefsrud MM, Sperisen C, Johnsen Ø (2010) Rapid change in adaptive performance from one generation to the next in Picea abies—central European trees in a Nordic environment. Tree Genet Genom 6(1):93–99. Scholar
  140. Soloaga A, Thomson S, Wiggin GR, Rampersaud N, Dyson MH, Hazzalin CA, Mahadevan LC, Arthur JSC (2003) MSK2 and MSK1 mediate the mitogen‐ and stress‐induced phosphorylation of histone H3 and HMG‐14 22(11):2788–2797.
  141. Sow MD, Allona I, Ambroise C, Conde D, Fichot R, Gribkova S, Jorge P, Le-Provost G, Pâques L, Plomion C, Salse J, Sanchez L, Segura V, Tost J, Maury S (2018) Epigenetics in forest trees: state of the art and potential implications for breeding and management in a context of climate change. In: Gallusci P, Bucher E, Mirouze M (eds) Plant epigenetics coming of age for breeding applications, vol 88. Academic Press, pp 387–453.
  142. Stricker SH, Köferle A, Beck S (2016) From profiles to function in epigenomics. Nat Rev Genet 18:51. Scholar
  143. Stroud H, Do T, Du J, Zhong X, Feng S, Johnson L, Patel DJ, Jacobsen SE (2013) Non-CG methylation patterns shape the epigenetic landscape in Arabidopsis. Nat Struct Mol Biol 21:64.
  144. Suganuma T, Workman JL (2011) Signals and combinatorial functions of histone modifications. Annu Rev Biochem 80(1):473–499. Scholar
  145. Sunkar R, Li Y, Jagadeeswaran G (2012) Functions of microRNAs in plant stress. Trends Plant Sci 17:196–203CrossRefGoogle Scholar
  146. Suzuki MM, Bird A (2008) DNA methylation landscapes: provocative insights from epigenomics. Nat Rev Genet 9:465. Scholar
  147. Takuno S, Ran J-H, Gaut BS (2016) Evolutionary patterns of genic DNA methylation vary across land plants. Nature Plants 2:15222.,
  148. Tarakhovsky A (2010) Tools and landscapes of epigenetics. Nat Immunol 11(7):565–568CrossRefGoogle Scholar
  149. Thellier M, Lüttge U (2013) Plant memory: a tentative model. Plant Biol 15(1):1–12. Scholar
  150. Turck F, Coupland G (2014) Natural variation in epigenetic gene regulation and its effects on plant developmental traits. Evolution 68(3):620–631. Scholar
  151. Valdés A, Marteinsdottir B, Ehrlén J (2018) A natural heating experiment: phenotypic and genotypic responses of plant phenology to geothermal soil warming. Glob Chang Biol 0(ja).
  152. Van Oosten MJ, Bressan RA, Zhu J-K, Bohnert HJ, Chinnusamy V (2014) The role of the epigenome in gene expression control and the epimark changes in response to the environment. Crit Rev Plant Sci 33(1):64–87. Scholar
  153. Vazquez F, Hohn T (2013) Biogenesis and biological activity of secondary siRNAs in plants. Scientifica 2013:12. Scholar
  154. Vazquez F, Vaucheret H, Rajagopalan R, Lepers C, Gasciolli V, Mallory AC, Hilbert JL, Bartel DP, Crete P (2004) Endogenous trans-acting siRNAs regulate the accumulation of Arabidopsis mRNAs. Mol Cell 16(1):69–79. Scholar
  155. Verhoeven KJF, Jansen JJ, van Dijk PJ, Biere A (2010) Stress-induced DNA methylation changes and their heritability in asexual dandelions. New Phytol 185(4):1108–1118. Scholar
  156. Verhoeven KJF, vonHoldt BM, Sork VL (2016) Epigenetics in ecology and evolution: what we know and what we need to know. Mol Ecol 25(8):1631–1638. Scholar
  157. Vlot AC, Klessig DF, Park S-W (2008) Systemic acquired resistance: the elusive signal(s). Curr Opin Plant Biol 11(4):436–442. Scholar
  158. Voinnet O (2009) Origin, biogenesis, and activity of plant MicroRNAs. Cell 136(4):669–687. Scholar
  159. Wang Y, Dasso M (2009) SUMOylation and deSUMOylation at a glance. J Cell Sci 122(23):4249–4252. Scholar
  160. Waterborg JH (2011) Plant histone acetylation: In the beginning…. Biochim Biophys Acta 1809(8):353–359. Scholar
  161. Whittle CA, Otto SP, Johnston MO, Krochko JE (2009) Adaptive epigenetic memory of ancestral temperature regime in Arabidopsis thaliana. Botany 87(6):650–657. Scholar
  162. Wigge PA (2013) Ambient temperature signalling in plants. Curr Opin Plant Biol 16(5):661–666. Scholar
  163. Williams BP, Gehring M (2017) Stable transgenerational epigenetic inheritance requires a DNA methylation-sensing circuit. Nat Commun 8(1):2124. Scholar
  164. Woo HR, Dittmer TA, Richards EJ (2008) Three SRA-domain methylcytosine-binding proteins cooperate to maintain global CpG methylation and epigenetic silencing in Arabidopsis. PLoS Genet 4(8):e1000156. Scholar
  165. Wu G (2013) Plant microRNAs and development. J Genet Genomics 40(5):217–230. Scholar
  166. Xia R, Xu J, Arikit S, Meyers BC (2015) Extensive families of miRNAs and PHAS Loci in Norway Spruce demonstrate the origins of complex phasiRNA networks in seed plants. Mol Biol Evol 32(11):2905–2918. Scholar
  167. Xie N, Zhou Y, Sun Q, Tang B (2018) Novel Epigenetic Techniques Provided by the CRISPR/Cas9 System. Stem Cells Int 2018:7834175. Scholar
  168. Yadav CB, Pandey G, Muthamilarasan M, Prasad M (2018) Epigenetics and epigenomics of plants. In: Varshney RK, Pandey MK, Chitikineni A (eds) Plant genetics and molecular biology. Springer International Publishing, Cham, pp 237–261.
  169. Yakovlev IA, Fossdal CG (2017) In Silico analysis of small RNAs suggest roles for novel and conserved miRNAs in the formation of epigenetic memory in somatic embryos of Norway Spruce. Front Physiol 8(674):1–17. Scholar
  170. Yakovlev IA, Fossdal CG, Johnsen Ø (2010) MicroRNAs, the epigenetic memory and climatic adaptation in Norway spruce. New Phytol 187(4):1154–1169. Scholar
  171. Yakovlev IA, Lee Y, Rotter B, Olsen JE, Skrøppa T, Johnsen Ø, Fossdal CG (2014) Temperature-dependent differential transcriptomes during formation of an epigenetic memory in Norway spruce embryogenesis. Tree Genet Genom 10:355–366. Scholar
  172. Yakovlev IA, Carneros E, Lee Y, Olsen JE, Fossdal CG (2016) Transcriptional profiling of epigenetic regulators in somatic embryos during temperature induced formation of an epigenetic memory in Norway spruce. Planta 243(5):1237–1249. Scholar
  173. Yoshikawa M (2013) Biogenesis of trans-acting siRNAs, endogenous secondary siRNAs in plants. Genes Genet Syst 88(2):77–84CrossRefGoogle Scholar
  174. Yun M, Wu J, Workman JL, Li B (2011) Readers of histone modifications. Cell Res 21(4):564–578. Scholar
  175. Zhang Y (2003) Transcriptional regulation by histone ubiquitination and deubiquitination. Genes Dev 17(22):2733–2740. Scholar
  176. Zhang X, Yazaki J, Sundaresan A, Cokus S, Chan SWL, Chen H, Henderson IR, Shinn P, Pellegrini M, Jacobsen SE, Ecker Joseph R (2006) Genome-wide high-resolution mapping and functional analysis of DNA methylation in arabidopsis. Cell 126(6):1189–1201CrossRefGoogle Scholar
  177. Zhang H, He X, Zhu J-K (2013a) RNA-directed DNA methylation in plants. RNA Biol 10(10):1593–1596. Scholar
  178. Zhang Y-Y, Fischer M, Colot V, Bossdorf O (2013b) Epigenetic variation creates potential for evolution of plant phenotypic plasticity. New Phytol 197(1):314–322. Scholar
  179. Zhang L, Yu H, Ma B, Liu G, Wang J, Wang J, Gao R, Li J, Liu J, Xu J, Zhang Y, Li Q, Huang X, Xu J, Li J, Qian Q, Han B, He Z, Li J (2017) A natural tandem array alleviates epigenetic repression of IPA1 and leads to superior yielding rice. Nat Commun 8:14789. Scholar
  180. Zheng X, Pontes O, Zhu J, Miki D, Zhang F, Li W-X, Iida K, Kapoor A, Pikaard CS, Zhu J-K (2008) ROS3 is an RNA-binding protein required for DNA demethylation in Arabidopsis. Nature 455:1259. Scholar
  181. Zilberman D, Coleman-Derr D, Ballinger T, Henikoff S (2008) Histone H2A.Z and DNA methylation are mutually antagonistic chromatin marks. Nature 456(7218):125–129.

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  • Igor Yakovlev
    • 1
    Email author
  • Marcos Viejo
    • 1
    • 2
  • Carl Gunnar Fossdal
    • 1
  1. 1.Division of Forestry and Forest ResourcesNorwegian Institute for Bioeconomy ResearchÅsNorway
  2. 2.Department of Plant SciencesNorwegian University of Life SciencesÅsNorway

Personalised recommendations