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Temperature-dependent differential transcriptomes during formation of an epigenetic memory in Norway spruce embryogenesis

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Abstract

Embryogenesis is the initial stage of plant life, when the basics of body plan and the post-embryonic development are laid down. Epigenetic memory formed in the Norway spruce embryos permanently affect the timing of bud burst and bud set in progenies, vitally important adaptive traits in this long-lived forest species. The epigenetic memory marks are established in response to the temperature conditions prevailing during zygotic and somatic embryogenesis; the epitype is fixed by the time the embryo is fully developed and is mitotically propagated throughout the tree’s life span. Somatic embryogenesis closely mimics the natural zygotic embryo formation and results in epigenetically different plants in a predictable temperature-dependent manner with respect to altered phenology. Using Illumina-based Massive Analysis of cDNA Ends, the transcriptome changes were monitored in somatic embryos during morphogenesis stage under two different temperatures (18 vs. 30 °C). We found distinct differences in transcriptomes between the genetically identical embryogenic tissues grown under the two epitype-inducing temperatures suggesting temperature-dependent canalizing of gene expression during embryo formation, putatively based on chromatin modifications. From 448 transcripts of genes coding for proteins involved in epigenetic machinery, we found 35 of these to be differentially expressed at high level under the epitype-inducing conditions. Therefore, temperature conditions during embryogenesis significantly alter transcriptional profiles including numerous orthologs of transcriptional regulators, epigenetic-related genes, and large sets of unknown and uncharacterized transcripts.

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Abbreviations

MACE:

Massive Analysis of cDNA Ends

DE:

Differentially expressed

CE:

“Cold” embryogenesis environment (18 °C or C in libraries definitions)

WE:

“Warm” embryogenesis environment (30 °C or W in libraries definitions)

RT-PCR:

Real-time reverse transcription polymerase chain reaction

References

  • Ahmad A, Zhang Y, Cao X-F (2010) Decoding the epigenetic language of plant development. Mol Plant 3(4):719–728

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Angel A, Song J, Dean C, Howard M (2011) A Polycomb-based switch underlying quantitative epigenetic memory. Nature 476(7358):105–108

    Article  CAS  PubMed  Google Scholar 

  • Audic S, Claverie J-M (1997) The significance of digital gene expression profiles. Genome Res 7(10):986–995

    CAS  PubMed  Google Scholar 

  • Besnard G, Acheré V, Jeandroz S, Johnsen Ø, Rampant PF, Baumann R, Müller-Starck G, Skrøppa T, Favre J-M (2008) Does maternal environmental condition during reproductive development induce genotypic selection in Picea abies? Ann Forest Sci 65(1):109

    Article  Google Scholar 

  • Boyko A, Kovalchuk I (2010) Transgenerational response to stress in Arabidopsis thaliana. Plant Signal Behav 5(8):995–998

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Butenko Y, Ohad N (2011) Polycomb-group mediated epigenetic mechanisms through plant evolution. Biochim Biophys Acta 1809(8):395–406

    Article  CAS  PubMed  Google Scholar 

  • Cairney J, Pullman GS (2007) The cellular and molecular biology of conifer embryogenesis. New Phytol 176(3):511–536

    Article  CAS  PubMed  Google Scholar 

  • Chen M, Lv S, Meng Y (2010) Epigenetic performers in plants. Dev Growth Diff 52(6):555–566

    Article  CAS  Google Scholar 

  • Consortium GO (2004) The Gene Ontology (GO) database and informatics resource. Nucleic Acids Res 32(suppl 1):D258–D261

    Article  Google Scholar 

  • Dormling I, Johnsen Ø (1992) Effects of the parental environment on full-sib families of Pinus sylvestris. Can J For Res 22(1):88–100

    Article  Google Scholar 

  • Eveland AL, McCarty DR, Koch KE (2008) Transcript profiling by 3′-untranslated region sequencing resolves expression of gene families. Plant Physiol 146(1):32–44

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Feil R, Fraga MF (2012) Epigenetics and the environment: emerging patterns and implications. Nat Rev Gen 13(2):97–109

    CAS  Google Scholar 

  • Greenwood MS, Hutchison KW (1996) Genetic aftereffects of increased temperature in Larix. In: Hom J, Birdsey R, O’Brian K (eds) Proceedings of the 1995 Meeting of the Northern Global Change Program, vol 214. USDA Forest Service Report, Radnor, pp 56–62

    Google Scholar 

  • Grimanelli D, Roudier F (2013) Epigenetics and development in plants: green light to convergent innovations. In: Edith H (ed) Current topics in developmental biology, vol 104. Academic, New York, pp 189–222

  • Gupta PK, Durzan DZ (1985) Shoot multiplication from mature trees of Douglas-fir (Pseudotsuga menziesii) and sugar pine (Pinus lambertiana). Plant Cell Rep 4:177–179

    Article  CAS  PubMed  Google Scholar 

  • He G, Elling AA, Deng XW (2011) The epigenome and plant development. Annu Rev Plant Biol 62(1):411–435

    Article  CAS  PubMed  Google Scholar 

  • Heo JB, Sung S (2011) Encoding memory of winter by noncoding RNAs. Epigenetics 6(5):544–547

    Article  CAS  PubMed  Google Scholar 

  • Huang H-R, Yan P-C, Lascoux M, Ge X-J (2012) Flowering time and transcriptome variation in Capsella bursa-pastoris (Brassicaceae). New Phytol 194:676–689

    Article  CAS  PubMed  Google Scholar 

  • Huff JT, Zilberman D (2012) Regulation of biological accuracy, precision, and memory by plant chromatin organization. Curr Opin Genet Dev 22(2):132–138

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Johnsen Ø, Kvaalen H, Yakovlev IA, Dæhlen OG, Fossdal CG, Skrøppa T (2009) An epigenetic memory from time of embryo development affects climatic adaptation in Norway spruce. In: Gusta LV, Wisniewski ME, Tanino KK (eds) Plant cold hardiness. From the laboratory to the field. CABI, Wallingford, pp 99–107

    Chapter  Google Scholar 

  • Kaeppler SM, Kaeppler HF, Rhee Y (2000) Epigenetic aspects of somaclonal variation in plants. Plant Mol Biol 43(2):179–188

    Article  CAS  PubMed  Google Scholar 

  • Kelly L, Leitch I (2011) Exploring giant plant genomes with next-generation sequencing technology. Chromosome Res 19(7):939–953

    Article  CAS  PubMed  Google Scholar 

  • Kim SY, Zhu T, Sung ZR (2010) Epigenetic regulation of gene programs by EMF1 and EMF2 in Arabidopsis. Plant Physiol 152(2):516–528

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Kvaalen H, Daehlen OG, Rognstad AT, Grønstad B, Egertsdotter U (2005) Somatic embryogenesis for plant production of Abies lasiocarpa. Can J For Res 35:1053–1060

    Article  Google Scholar 

  • Lister R, Gregory BD, Ecker JR (2009) Next is now: new technologies for sequencing of genomes, transcriptomes, and beyond. Curr Opin Plant Biol 12(2):107–118

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Matsumura H, Yoshida K, Luo S, Kimura E, Fujibe T, Albertyn Z, Barrero RA, Krüger DH, Kahl G, Schroth GP, Terauchi R (2010) High-throughput SuperSAGE for digital gene expression analysis of multiple samples using next generation sequencing. PLoS ONE 5(8):e12010

    Article  PubMed Central  PubMed  Google Scholar 

  • Matzke M, Mittelsten Scheid O (2006) Epigenetic regulation in plants. In: Allis CD, Jenuwein T, Reinberg D (eds) Epigenetics. Cold Spring Harbor Laboratory Press, New York, pp 167–189

    Google Scholar 

  • Metzker ML (2010) Sequencing technologies—the next generation. Nat Rev Genet 11(1):31–46

    Article  CAS  PubMed  Google Scholar 

  • Nicol-Benoît F, Le-Goff P, Le-Dréan Y, Demay F, Pakdel F, Flouriot G, Michel D (2012) Epigenetic memories: structural marks or active circuits? Cell Mol Life Sci 69(13):2189–2203

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Olsen J (2010) Light and temperature sensing and signaling in induction of bud dormancy in woody plants. Plant Mol Biol 73(1):37–47

    Article  CAS  PubMed  Google Scholar 

  • Rohde A, Ruttink T, Hostyn V, Sterck L, Van Driessche K, Boerjan W (2007) Gene expression during the induction, maintenance, and release of dormancy in apical buds of poplar. J Exp Bot 58(15–16):4047–4060

    Article  CAS  PubMed  Google Scholar 

  • Rozen S, Skaletsky HJ (2000) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (eds) Methods in molecular biology, vol 132, Bioinformatics methods and protocols. Humana, Totowa, pp 365–386

    Google Scholar 

  • Ruttink T, Arend M, Morreel K, Storme V, Rombauts S, Fromm J, Bhalerao RP, Boerjan W, Rohde A (2007) A molecular timetable for apical bud formation and dormancy induction in poplar. Plant Cell 19(8):2370–2390

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Saze H (2008) Epigenetic memory transmission through mitosis and meiosis in plants. Semin Cell Dev Biol 19(6):527–536

    Article  PubMed  Google Scholar 

  • Schmidtling RC, Hipkins V (2004) The after-effects of reproductive environment in shortleaf pine. Forestry 77(4):287–295

    Article  Google Scholar 

  • Schmitz RJ, Zhang X (2011) High-throughput approaches for plant epigenomic studies. Curr Opin Plant Biol 14(2):130–136

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Seffer I, Nemeth Z, Hoffmann G, Matics R, Seffer AG, Koller A (2013) Unexplored potentials of epigenetic mechanisms of plants and animals—theoretical considerations. Genet Epigenetics 5:23–41

    Google Scholar 

  • Skrøppa T, Kohmann K, Johnsen Ø, Steffenrem A, Edvardsen ØM (2007) Field performance and early test results of offspring from two Norway spruce seed orchards containing clones transferred to warmer climates. Can J For Res 37(3):515–522

    Article  Google Scholar 

  • Stasolla C, Bozhkov PV, Chu T-M, van Zyl L, Egertsdotter U, Suarez MF, Craig D, Wolfinger RD, Von Arnold S, Sederoff RR (2004) Variation in transcript abundance during somatic embryogenesis in gymnosperms. Tree Physiol 24(10):1073–1085

    Article  CAS  PubMed  Google Scholar 

  • Stoehr MU, L’Hirondelle SJ, Binder WD, Webber JE (1998) Parental environment aftereffects on germination, growth, and adaptive traits in selected spruce families. Can J For Res 28:418–426

    Article  Google Scholar 

  • Su P-H, Li H-m (2008) Arabidopsis stromal 70-kD heat shock proteins are essential for plant development and important for thermotolerance of germinating seeds. Plant Physiol 146(3):1231–1241

    Google Scholar 

  • Thellier M, Lüttge U (2013) Plant memory: a tentative model. Plant Biol 15(1):1–12

    Article  CAS  PubMed  Google Scholar 

  • Torres TT, Metta M, Ottenwälder B, Schlötterer C (2008) Gene expression profiling by massively parallel sequencing. Genome Res 18(1):172–177

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Uddenberg D, Valladares S, Abrahamsson M, Sundström J, Sundås-Larsson A, Arnold S (2011) Embryogenic potential and expression of embryogenesis-related genes in conifers are affected by treatment with a histone deacetylase inhibitor. Planta 234(3):527–539

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Vanyushin BF, Ashapkin VV (2011) DNA methylation in higher plants: past, present and future. Biochim Biophys Acta 1809(8):360–368

    Article  CAS  PubMed  Google Scholar 

  • Vega-Bartol J, Santos R, Simões M, Miguel C (2013) Normalizing gene expression by quantitative PCR during somatic embryogenesis in two representative conifer species: Pinus pinaster and Picea abies. Plant Cell Rep 32(5):715–729

    Article  CAS  PubMed  Google Scholar 

  • Vestman D, Larsson E, Uddenberg D, Cairney J, Clapham D, Sundberg E, Sv A (2011) Important processes during differentiation and early development of somatic embryos of Norway spruce as revealed by changes in global gene expression. Tree Genet Genom 7(2):347–362

    Article  Google Scholar 

  • Wang Q-M, Wang L (2012) An evolutionary view of plant tissue culture: somaclonal variation and selection. Plant Cell Rep 31:1535–1547

    Google Scholar 

  • Webber J, Ott P, Owens J, Binder W (2005) Elevated temperature during reproductive development affects cone traits and progeny performance in Picea glaucaengelmannii complex. Tree Physiol 25:1219–1227

    Article  PubMed  Google Scholar 

  • Wiweger M, Farbos I, Ingouff M, Lagercrantz U, von Arnold S (2003) Expression of Chia4‐Pa chitinase genes during somatic and zygotic embryo development in Norway spruce (Picea abies): similarities and differences between gymnosperm and angiosperm class IV chitinases. J Exp Bot 54(393):2691–2699

    Article  CAS  PubMed  Google Scholar 

  • Yakovlev I, Fossdal CG, Skrøppa T, Olsen JE, Jahren AH, Johnsen Ø (2012) An adaptive epigenetic memory in conifers with important implications for seed production. Seed Sci Res 22(02):63–76

    Article  CAS  Google Scholar 

  • Yakovlev IA, Asante DKA, Fossdal CG, Junttila O, Johnsen Ø (2011) Differential gene expression related to an epigenetic memory affecting climatic adaptation in Norway spruce. Plant Sci 180(1):132–139

    Article  CAS  PubMed  Google Scholar 

  • Yakovlev IA, Fossdal CG, Johnsen Ø (2010) MicroRNAs, the epigenetic memory and climatic adaptation in Norway spruce. New Phytol 187(4):1154–1169

    Article  CAS  PubMed  Google Scholar 

  • Zerbino DR, Birney E (2008) Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18(5):821–829

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

The authors would like to thank Tone I. Melby (Norwegian University of Life Sciences) for assistance in RNA extraction and Anne E. Nilsen (Norwegian Forest and Landscape Institute) for valuable help during in vitro culturing. In addition, we would like to thank Ruth Jüngling and Nico Krezdorn (GenXPro GmbH) for conducting the sequencing and the initial bioinformatics processing of data. We express additional gratitude to Damien Vaisettes (Institut National Des Sciences Appliquees, France) for valuable technical help with primer testing and running qRT-PCRs. This work was supported by the Norwegian Research Council (FRIBIO Grant #191455/V40) and the EU FP7 project ProCoGen.

Data Archiving Statement

Unique transcripts from four libraries using Illumina-based MACE analysis were deposited to the SRA (Short Read Archive, NCBI) and got the following accession: PRJNA184229 and ID: 184229.

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Correspondence to Igor A. Yakovlev.

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Communicated by J. Dean

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Yakovlev, I.A., Lee, Y., Rotter, B. et al. Temperature-dependent differential transcriptomes during formation of an epigenetic memory in Norway spruce embryogenesis. Tree Genetics & Genomes 10, 355–366 (2014). https://doi.org/10.1007/s11295-013-0691-z

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