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

Tree Genetics and Genomes

Volumn 10, Issue 2, 2014, Pages 355-366

  Yakovlev, Igor A ^a   Lee, YeonKyeong ^b   Rotter, Björn ^c   Olsen, Jorunn E ^b   Skrøppa, Tore ^a   Johnsen, Øystein ^b   Fossdal, Carl Gunnar ^a  

^a NORWEGIAN INSTITUTE OF BIOECONOMY RESEARCH   (Norway)

^b NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

^c GENXPRO GMBH   (Germany)

Author keywords

Conifers; Embryogenesis; Epigenetic memory; Next generation (high throughput) sequencing; Picea abies; Transcriptome

Indexed keywords

EID: 84897027909     PISSN: 16142942     EISSN: 16142950     Source Type: Journal    
DOI: 10.1007/s11295-013-0691-z     Document Type: Article

References (59)

1. Ahmad A, Zhang Y, Cao X-F (2010) Decoding the epigenetic language of plant development. Mol Plant 3(4): 719-728.
2. Angel A, Song J, Dean C, Howard M (2011) A Polycomb-based switch underlying quantitative epigenetic memory. Nature 476(7358): 105-108.
3. Audic S, Claverie J-M (1997) The significance of digital gene expression profiles. Genome Res 7(10): 986-995.
4. 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.
5. Boyko A, Kovalchuk I (2010) Transgenerational response to stress in Arabidopsis thaliana. Plant Signal Behav 5(8): 995-998.
6. Butenko Y, Ohad N (2011) Polycomb-group mediated epigenetic mechanisms through plant evolution. Biochim Biophys Acta 1809(8): 395-406.
7. Cairney J, Pullman GS (2007) The cellular and molecular biology of conifer embryogenesis. New Phytol 176(3): 511-536.
8. Chen M, Lv S, Meng Y (2010) Epigenetic performers in plants. Dev Growth Diff 52(6): 555-566.
9. Consortium GO (2004) The Gene Ontology (GO) database and informatics resource. Nucleic Acids Res 32(suppl 1): D258-D261.
10. 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.
11. 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.
12. Feil R, Fraga MF (2012) Epigenetics and the environment: emerging patterns and implications. Nat Rev Gen 13(2): 97-109.
13. 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.
14. 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.
15. 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.
16. He G, Elling AA, Deng XW (2011) The epigenome and plant development. Annu Rev Plant Biol 62(1): 411-435.
17. Heo JB, Sung S (2011) Encoding memory of winter by noncoding RNAs. Epigenetics 6(5): 544-547.
18. 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.
19. Huff JT, Zilberman D (2012) Regulation of biological accuracy, precision, and memory by plant chromatin organization. Curr Opin Genet Dev 22(2): 132-138.
20. 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.
21. 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.
22. 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.
23. Kaeppler SM, Kaeppler HF, Rhee Y (2000) Epigenetic aspects of somaclonal variation in plants. Plant Mol Biol 43(2): 179-188.
24. Kelly L, Leitch I (2011) Exploring giant plant genomes with next-generation sequencing technology. Chromosome Res 19(7): 939-953.
25. Kim SY, Zhu T, Sung ZR (2010) Epigenetic regulation of gene programs by EMF1 and EMF2 in Arabidopsis. Plant Physiol 152(2): 516-528.
26. 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.
27. 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.
28. 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.
29. 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.
30. 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.
31. Metzker ML (2010) Sequencing technologies-the next generation. Nat Rev Genet 11(1): 31-46.
32. 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.
33. 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.
34. Olsen J (2010) Light and temperature sensing and signaling in induction of bud dormancy in woody plants. Plant Mol Biol 73(1): 37-47.
35. 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.
36. 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.
37. 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.
38. 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.
39. Saze H (2008) Epigenetic memory transmission through mitosis and meiosis in plants. Semin Cell Dev Biol 19(6): 527-536.
40. Schmidtling RC, Hipkins V (2004) The after-effects of reproductive environment in shortleaf pine. Forestry 77(4): 287-295.
41. Schmitz RJ, Zhang X (2011) High-throughput approaches for plant epigenomic studies. Curr Opin Plant Biol 14(2): 130-136.
42. 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.
43. 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.
44. 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.
45. 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.
46. 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.
47. Thellier M, Lüttge U (2013) Plant memory: a tentative model. Plant Biol 15(1): 1-12.
48. Torres TT, Metta M, Ottenwälder B, Schlötterer C (2008) Gene expression profiling by massively parallel sequencing. Genome Res 18(1): 172-177.
49. 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.
50. Vanyushin BF, Ashapkin VV (2011) DNA methylation in higher plants: past, present and future. Biochim Biophys Acta 1809(8): 360-368.
51. 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.
52. 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.
53. Wang Q-M, Wang L (2012) An evolutionary view of plant tissue culture: somaclonal variation and selection. Plant Cell Rep 31: 1535-1547.
54. Webber J, Ott P, Owens J, Binder W (2005) Elevated temperature during reproductive development affects cone traits and progeny performance in Picea glauca-engelmannii complex. Tree Physiol 25: 1219-1227.
55. 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.
56. 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.
57. 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.
58. Yakovlev IA, Fossdal CG, Johnsen Ø (2010) MicroRNAs, the epigenetic memory and climatic adaptation in Norway spruce. New Phytol 187(4): 1154-1169.
59. Zerbino DR, Birney E (2008) Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18(5): 821-829.