Temperature-dependent differential transcriptomes during formation of an epigenetic memory in Norway spruce embryogenesis
- 996 Downloads
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.
KeywordsConifers Picea abies Epigenetic memory Transcriptome Next-generation (high-throughput) sequencing Embryogenesis
Massive Analysis of cDNA Ends
“Cold” embryogenesis environment (18 °C or C in libraries definitions)
“Warm” embryogenesis environment (30 °C or W in libraries definitions)
Real-time reverse transcription polymerase chain reaction
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.
- Feil R, Fraga MF (2012) Epigenetics and the environment: emerging patterns and implications. Nat Rev Gen 13(2):97–109Google 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 56–62Google 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 189–222Google 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 99–107CrossRefGoogle 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):e12010PubMedCentralPubMedCrossRefGoogle 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 167–189Google 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 497:579–584PubMedCrossRefGoogle 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 365–386Google 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 5:23–41Google 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):1231–1241Google Scholar
- Wang Q-M, Wang L (2012) An evolutionary view of plant tissue culture: somaclonal variation and selection. Plant Cell Rep 31:1535–1547Google 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):2691–2699PubMedCrossRefGoogle Scholar