Advertisement

Tree Genetics & Genomes

, 14:78 | Cite as

Narrow-sense heritability and PST estimates of DNA methylation in three Populus nigra L. populations under contrasting water availability

  • Mamadou Dia Sow
  • Vincent Segura
  • Sylvain Chamaillard
  • Véronique Jorge
  • Alain Delaunay
  • Clément Lafon-Placette
  • Régis Fichot
  • Patricia Faivre-Rampant
  • Marc Villar
  • Franck Brignolas
  • Stéphane Maury
Original Article
Part of the following topical collections:
  1. Complex Traits

Abstract

In a context of climate change and forest decline, a better understanding of the sources of tree flexibility involved in phenotypic plasticity and adaptation is needed. These last years, the role of epigenetics in the response to environmental variations has been established in several model plants at the genotype level but little is known at the level of natural populations grown in pedoclimatic sites. Here, we focused on three French natural populations of black poplar, a key pioneer tree from watersheds, planted in common garden and subjected to controlled variations of water availability. We estimated common genetic parameters such as narrow-sense heritability (h2), phenotypic differentiation index (PST), and the overall genetic differentiation index (FST) from genome-wide SNPs to evaluate the extent of epigenetic variations. Indeed, global DNA methylation levels from individuals exposed to drought or irrigated in a common garden were used. We found that the three populations were not distinguished by their levels of DNA methylation. However, a moderate drought was associated to a significant decrease in DNA methylation in the populations. Narrow-sense heritability and PST estimates of DNA methylation were similar to those found for biomass productivity. Heritability and PST were higher when trees were subjected to drought than in control condition. Negative genetic correlations between global DNA methylation and height or biomass were detected in drought condition only. Altogether, our data highlight that global DNA methylation acts as a genetic marker of natural population differentiation under drought stress in a pedoclimatic context.

Keywords

DNA methylation h2 PST FST Poplar Water availability 

Notes

Data archiving statement

The raw data containing the full list of genotypes, global DNA methylation levels, biomass, and height are included as Supplementary Table 1. The SNP data used in order to reconstruct genomic relationships between genotypes, within and between populations, and to estimate h2, PST, and FST for global DNA methylation are in Supplementary Tables 2 and 3.

Funding information

MDS obtained a PhD grant from the “Ministère de la Recherche et Enseignement Supérieur,” France. This work was funded by the “INRA DÉPARTEMENT EFPA,” France, with the project “PI EFPA-2010” and by the “Agence Nationale de la Recherche (ANR)” with the project “EPITREE” 2018-2021, ANR-17-CE32-0009-01, http://www6.inra.fr/epitree-project/.

Supplementary material

11295_2018_1293_MOESM1_ESM.xlsx (14 kb)
Supplementary Table 1 Global DNA methylation levels (Perc_mC) were calculated as mentioned in Zhu et al. (2013). The values of height and biomass were retrieved in Chamaillard et al. (2011). NOH for Nohèdes, RAM for Ramières and SPM for Saint-Pryvé Saint-Mesmin. WW and WD referred to irrigated and drought conditions, respectively. (XLSX 14 kb)
11295_2018_1293_MOESM2_ESM.xlsx (1.1 mb)
Supplementary Table 2 SNP genotypic data used to calculate h2, PST and FST estimates in the three geographical populations (NOH, RAM and SPM). These SNP were retrieved from Faivre-Rampant et al. 2016 and Le Paslier et al. 2016. The SNPs are denoted by SNP_IGA followed by the chromosome or scaffold number (V3.0 poplar; http://www.phytozome.net/poplar.php) and the base position within the scaffold. (XLSX 1112 kb)
11295_2018_1293_MOESM3_ESM.xlsx (150 kb)
Supplementary Table 3 Details of the SNP data. The types of SNP, locus, sequence or position are mentioned. The SNPs were assembled with the V3.0 of the poplar genome (http://www.phytozome.net/poplar.php). (XLSX 149 kb)

References

  1. Allen CD, Macalady AK, Chenchouni H, Bachelet D, McDowell N, Vennetier M, Kitzberger T, Rigling A, Breshears DD, Hogg EH(T), Gonzalez P, Fensham R, Zhang Z, Castro J, Demidova N, Lim JH, Allard G, Running SW, Semerci A, Cobb N (2010) A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. For Ecol Manag 259:660–684.  https://doi.org/10.1016/j.foreco.2009.09.001 CrossRefGoogle Scholar
  2. Alonso C, Pérez R, Bazaga P, Herrera CM (2015) Global DNA cytosine methylation as an evolving trait: phylogenetic signal and correlated evolution with genome size in angiosperms. Front Genet 6.  https://doi.org/10.3389/fgene.2015.00004
  3. Alonso C, Pérez R, Bazaga P, Medrano M, Herrera CM (2016) MSAP markers and global cytosine methylation in plants: a literature survey and comparative analysis for a wild-growing species. Mol Ecol Resour 16:80–90.  https://doi.org/10.1111/1755-0998.12426 CrossRefPubMedGoogle Scholar
  4. Bewick AJ, Schmitz RJ (2017) Gene body DNA methylation in plants. Curr Opin Plant Biol 36:103–110.  https://doi.org/10.1016/j.pbi.2016.12.007 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bizet F, Bogeat-Triboulot MB, Montpied P, Christophe A, Ningre N, Cohen D, Hummel I (2015) Phenotypic plasticity toward water regime: response of leaf growth and underlying candidate genes in Populus. Physiol Plant 154:39–53.  https://doi.org/10.1111/ppl.12271 CrossRefPubMedGoogle Scholar
  6. Bradshaw AD (2006) Unravelling phenotypic plasticity—why should we bother? New Phytol 170:644–648.  https://doi.org/10.1111/j.1469-8137.2006.01761.x CrossRefPubMedGoogle Scholar
  7. 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 MT (2013) Epigenetic regulation of adaptive responses of forest tree species to the environment. Ecol Evol 3:399–415.  https://doi.org/10.1002/ece3.461 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bruce TJA, Matthes MC, Napier A, Pickett JA (2007) Stressful “memories” of plants: evidence and possible mechanisms. Plant Sci 173:603–608.  https://doi.org/10.1016/j.plantsci.2007.09.002 CrossRefGoogle Scholar
  9. Causevic A, Delaunay A, Ounnar S, Righezza M, Delmotte F, Brignolas F, Hagège D, Maury S (2005) DNA methylating and demethylating treatments modify phenotype and cell wall differentiation state in sugarbeet cell lines. Plant Physiol Biochem 43:681–691.  https://doi.org/10.1016/j.plaphy.2005.05.011 CrossRefPubMedGoogle Scholar
  10. Chamaillard S, Fichot R, Vincent-Barbaroux C, Bastien C, Depierreux C, Dreyer E, Villar M, Brignolas F (2011) Variations in bulk leaf carbon isotope discrimination, growth and related leaf traits among three Populus nigra L. populations. Tree Physiol 31:1076–1087.  https://doi.org/10.1093/treephys/tpr089 CrossRefPubMedGoogle Scholar
  11. Conde D, Le Gac AL, Perales M, Dervinis C, Kirst M, Maury S, González-Melendi P, Allona I (2017) Chilling-responsive DEMETER-LIKE DNA demethylase mediates in poplar bud break: role of active DNA demethylase in trees’ bud break. Plant Cell Environ.  https://doi.org/10.1111/pce.13019 CrossRefGoogle Scholar
  12. Cortijo S, Wardenaar R, Colome-Tatche M, Gilly A, Etcheverry M, Labadie K, Caillieux E, Hospital F, Aury JM, Wincker P, Roudier F, Jansen RC, Colot V, Johannes F (2014) Mapping the epigenetic basis of complex traits. Science 343:1145–1148.  https://doi.org/10.1126/science.1248127 CrossRefPubMedGoogle Scholar
  13. Covarrubias-Pazaran G (2016) Genome-assisted prediction of quantitative traits using the R package sommer. PLOS ONE 11:e0156744.  https://doi.org/10.1371/journal.pone.0156744 CrossRefPubMedPubMedCentralGoogle Scholar
  14. de Rigo D, Enescu CM, Durrant TH, Caudullo G (2016) Populus nigra in Europe: distribution, habitat, usage and threats. European atlas of forest tree species. Publ. Off. EU, Luxembourg, pp. e0182a4.Google Scholar
  15. Ding Y, Fromm M, Avramova Z (2012) Multiple exposures to drought ‘train’ transcriptional responses in Arabidopsis. Nat Commun 3:740.  https://doi.org/10.1038/ncomms1732 CrossRefPubMedGoogle Scholar
  16. Dubin MJ, Zhang P, Meng D, Remigereau MS, Osborne EJ, Casale FP, Drewe P, Kahles A, Jean G, Vilhjálmsson B (2015) DNA methylation in Arabidopsis has a genetic basis and shows evidence of local adaptation. Elife 4:e05255.  https://doi.org/10.7554/eLife.05255.001 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Faivre-Rampant P, Zaina G, Jorge V, Giacomello S, Segura V, Scalabrin S, Guérin V, De Paoli E, Aluome C, Viger M, Cattonaro F, Payne A, PaulStephenRaj P, Le Paslier MC, Berard A, Allwright MR, Villar M, Taylor G, Bastien C, Morgante M (2016) New resources for genetic studies in Populus nigra: genome-wide SNP discovery and development of a 12k Infinium array. Mol Ecol Resour 16:1023–1036.  https://doi.org/10.1111/1755-0998.12513 CrossRefPubMedGoogle Scholar
  18. Feil R, Fraga MF (2012) Epigenetics and the environment: emerging patterns and implications. Nat Rev Genet 13:97.  https://doi.org/10.1038/nrg3142 CrossRefPubMedGoogle Scholar
  19. Fichot R, Brignolas F, Cochard H, Ceulemans R (2015) Vulnerability to drought-induced cavitation in poplars: synthesis and future opportunities: drought-induced cavitation in poplars: a review. Plant Cell Environ 38:1233–1251.  https://doi.org/10.1111/pce.12491 CrossRefPubMedGoogle Scholar
  20. Fleta-Soriano E, Munné-Bosch S (2016) Stress memory and the inevitable effects of drought: a physiological perspective. Front Plant Sci 7:143.  https://doi.org/10.3389/fpls.2016.00143 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Garg R, Narayana Chevala V, Shankar R, Jain M (2015) Divergent DNA methylation patterns associated with gene expression in rice cultivars with contrasting drought and salinity stress response. Sci Rep 5:14922.  https://doi.org/10.1038/srep14922 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Goudet J, Jombart T (2015) Hierfstat: estimation and tests of hierarchical F-statistics. R package version 0.04–22. Retrieved from https://CRAN.R-project.org/package=hierfstat
  23. Gourcilleau D, Bogeat-Triboulot MB, Le Thiec D, Lafon-Placette C, Delaunay A, El-Soud WA, Brignolas F, Maury S (2010) DNA methylation and histone acetylation: genotypic variations in hybrid poplars, impact of water deficit and relationships with productivity. Ann For Sci 67:208.  https://doi.org/10.1051/forest/2009101 CrossRefGoogle Scholar
  24. Guarino F, Cicatelli A, Brundu G, Heinze B, Castiglione S (2015) Epigenetic Diversity of Clonal White Poplar (Populus alba L.) Populations: could methylation support the success of vegetative reproduction strategy? PLoS One 10.  https://doi.org/10.1371/journal.pone.0131480 CrossRefGoogle Scholar
  25. Hamanishi ET, Thomas BR, Campbell MM (2012) Drought induces alterations in the stomatal development program in Populus. J Exp Bot 63:4959–4971.  https://doi.org/10.1093/jxb/ers177 CrossRefPubMedPubMedCentralGoogle Scholar
  26. IPCC (2014) Climate change 2014: impacts, adaptation, and vulnerability. Part a: global and sectoral aspects. Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge, New York: Cambridge University Press.Google Scholar
  27. Jansson S, Douglas CJ (2007) Populus: a model system for plant biology. Annu Rev Plant Biol 58:435–458.  https://doi.org/10.1146/annurev.arplant.58.032806.103956 CrossRefPubMedGoogle Scholar
  28. Kawakatsu T, Huang SC, Jupe F, Sasaki E, Schmitz RJ, Urich MA, Castanon R, Nery JR, Barragan C, He Y, Chen H, Dubin M, Lee CR, Wang C, Bemm F, Becker C, O’Neil R, O’Malley RC, Quarless DX, Schork NJ, Weigel D, Nordborg M, Ecker JR, Alonso-Blanco C, Andrade J, Becker C, Bemm F, Bergelson J, Borgwardt K, Chae E, Dezwaan T, Ding W, Ecker JR, Expósito-Alonso M, Farlow A, Fitz J, Gan X, Grimm DG, Hancock A, Henz SR, Holm S, Horton M, Jarsulic M, Kerstetter RA, Korte A, Korte P, Lanz C, Lee CR, Meng D, Michael TP, Mott R, Muliyati NW, Nägele T, Nagler M, Nizhynska V, Nordborg M, Novikova P, Picó FX, Platzer A, Rabanal FA, Rodriguez A, Rowan BA, Salomé PA, Schmid K, Schmitz RJ, Seren Ü, Sperone FG, Sudkamp M, Svardal H, Tanzer MM, Todd D, Volchenboum SL, Wang C, Wang G, Wang X, Weckwerth W, Weigel D, Zhou X (2016) Epigenomic diversity in a global collection of Arabidopsis thaliana accessions. Cell 166:492–505.  https://doi.org/10.1016/j.cell.2016.06.044 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Kooke R, Johannes F, Wardenaar R, Becker F, Etcheverry M, Colot V, Vreugdenhil D, Keurentjes JJ (2015) Epigenetic basis of morphological variation and phenotypic plasticity in Arabidopsis thaliana. Plant Cell 27:337–348.  https://doi.org/10.1105/tpc.114.133025 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Lafon-Placette C, Faivre-Rampant P, Delaunay A, Street N, Brignolas F, Maury S (2013) Methylome of DNase I sensitive chromatin in Populus trichocarpa shoot apical meristematic cells: a simplified approach revealing characteristics of gene-body DNA methylation in open chromatin state. New Phytol 197:416–430.  https://doi.org/10.1111/nph.12026 CrossRefPubMedGoogle Scholar
  31. Lafon-Placette C, Le Gac AL, Chauveau D, Segura V, Delaunay A, Lesage-Descauses MC, Hummel I, Cohen D, Jesson B, Le Thiec D, Bogeat-Triboulot MB, Brignolas F, Maury S (2018) Changes in the epigenome and transcriptome of the poplar shoot apical meristem in response to water availability affect preferentially hormone pathways. J Exp Bot 69(3):537–551.  https://doi.org/10.1093/jxb/erx409 CrossRefPubMedGoogle Scholar
  32. Lambé P, Mutambel HSN, Fouché JG, Deltour R, Foidart JM, Gaspar T (1997) DNA methylation as a key process in regulation of organogenic totipotency and plant neoplastic progression? In Vitro Cell Dev Biol Plant 33:155–162.  https://doi.org/10.1007/s11627-997-0015-9 CrossRefGoogle Scholar
  33. Lämke J, Bäurle I (2017) Epigenetic and chromatin-based mechanisms in environmental stress adaptation and stress memory in plants. Genome Biol 18.  https://doi.org/10.1186/s13059-017-1263-6
  34. Lande R (2009) Adaptation to an extraordinary environment by evolution of phenotypic plasticity and genetic assimilation. J Evol Biol 22:1435–1446.  https://doi.org/10.1111/j.1420-9101.2009.01754.x CrossRefPubMedGoogle Scholar
  35. Latzel V, Allan E, Bortolini Silveira A, Colot V, Fischer M, Bossdorf O (2013) Epigenetic diversity increases the productivity and stability of plant populations. Nat Commun 4:2875.  https://doi.org/10.1038/ncomms3875 CrossRefPubMedGoogle Scholar
  36. Law JA, Jacobsen SE (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11:204–220.  https://doi.org/10.1038/nrg2719 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Le Paslier MC, Berard A, Chauveau A, Marquand E, Boland-Auge A, Eggen A, Brunel D, Faivre Rampant P (2016) Performance of a multi-species-plant Illumina beadchip. In: PAG XXIV—Plant and Animal Genome Conference. Presented at PAG XXIV—Plant and Animal Genome Conference, San Diego, USA, 01–09–01-13.Google Scholar
  38. Lehtonen PK, Laaksonen T, Artemyev AV, Belskii E, Both C, Bureš S, Bushuev AV, Krams I, Moreno J, Mägi M, Nord A, Potti J, Ravussin PA, Sirkiä PM, Saetre GP, Primmer CR (2009) Geographic patterns of genetic differentiation and plumage colour variation are different in the pied flycatcher (Ficedula hypoleuca). Mol Ecol 18:4463–4476.  https://doi.org/10.1111/j.1365-294X.2009.04364.x CrossRefPubMedGoogle Scholar
  39. Leinonen T, O’Hara RB, Cano JM, Merilä J (2008) Comparative studies of quantitative trait and neutral marker divergence: a meta-analysis: Q ST - F ST meta-analysis. J Evol Biol 21:1–17.  https://doi.org/10.1111/j.1420-9101.2007.01445.x CrossRefPubMedGoogle Scholar
  40. Liang D, Zhang Z, Wu H, Huang C, Shuai P, Ye CY, Tang S, Wang Y, Yang L, Wang J (2014) Single-base-resolution methylomes of Populus trichocarpa reveal the association between DNA methylation and drought stress, in: BMC Genetics. BioMed Central, p. S9.  https://doi.org/10.1186/1471-2156-15-S1-S9 CrossRefGoogle Scholar
  41. Maher B (2008) Personal genomes: the case of the missing heritability. Nature News 456:18–21.  https://doi.org/10.1038/456018a CrossRefGoogle Scholar
  42. Marron N, Dreyer E, Boudouresque E, Delay D, Petit JM, Delmotte FM, Brignolas F (2003) Impact of successive drought and re-watering cycles on growth and specific leaf area of two Populus\times canadensis (Moench) clones, ‘Dorskamp’ and ‘Luisa_Avanzo’. Tree Physiol 23:1225–1235.  https://doi.org/10.1093/treephys/23.18.1225 CrossRefPubMedGoogle Scholar
  43. Mauch-Mani B, Baccelli I, Luna E, Flors V (2017) Defense priming: an adaptive part of induced resistance. Annu Rev Plant Biol 68:485–512.  https://doi.org/10.1146/annurev-arplant-042916-041132 CrossRefPubMedGoogle Scholar
  44. Merilä J, Crnokrak P (2001) Comparison of genetic differentiation at marker loci and quantitative traits. J Evol Biol 14:892–903.  https://doi.org/10.1046/j.1420-9101.2001.00348.x CrossRefGoogle Scholar
  45. Meyer P (2015) Epigenetic variation and environmental change: Fig. 1. J Exp Bot 66:3541–3548.  https://doi.org/10.1093/jxb/eru502 CrossRefPubMedGoogle Scholar
  46. Mirouze M, Paszkowski J (2011) Epigenetic contribution to stress adaptation in plants. Curr Opin Plant Biol 14:267–274.  https://doi.org/10.1016/j.pbi.2011.03.004 CrossRefPubMedGoogle Scholar
  47. Monclus R, Dreyer E, Villar M, Delmotte FM, Delay D, Petit JM, Barbaroux C, Le Thiec D, Bréchet C, Brignolas F (2006) Impact of drought on productivity and water use efficiency in 29 genotypes of Populus deltoides × Populus nigra. New Phytol 169:765–777.  https://doi.org/10.1111/j.1469-8137.2005.01630.x CrossRefPubMedGoogle Scholar
  48. Nicotra AB, Atkin OK, Bonser SP, Davidson AM, Finnegan EJ, Mathesius U, Poot P, Purugganan MD, Richards CL, Valladares F, van Kleunen M (2010) Plant phenotypic plasticity in a changing climate. Trends Plant Sci 15:684–692.  https://doi.org/10.1016/j.tplants.2010.09.008 CrossRefPubMedGoogle Scholar
  49. Niederhuth CE, Bewick AJ, Ji L, Alabady MS, Kim KD, Li Q, Rohr NA, Rambani A, Burke JM, Udall JA, Egesi C, Schmutz J, Grimwood J, Jackson SA, Springer NM, Schmitz RJ (2016) Widespread natural variation of DNA methylation within angiosperms. Genome Biol 17.  https://doi.org/10.1186/s13059-016-1059-0
  50. Plomion C, Bastien C, Bogeat-Triboulot MB, Bouffier L, Déjardin A, Duplessis S, Fady B, Heuertz M, Le Gac AL, Le Provost G, Legué V, Lelu-Walter MA, Leplé JC, Maury S, Morel A, Oddou-Muratorio S, Pilate G, Sanchez L, Scotti I, Scotti-Saintagne C, Segura V, Trontin JF, Vacher C (2016) Forest tree genomics: 10 achievements from the past 10 years and future prospects. Ann For Sci 73:77–103.  https://doi.org/10.1007/s13595-015-0488-3 CrossRefGoogle Scholar
  51. Porebski S, Bailey LG, Baum BR (1997) Modification of a CTAB DNA extraction protocol for plants containing high polysaccharide and polyphenol components. Plant Mol Biol Report 15:8–15.  https://doi.org/10.1007/BF02772108 CrossRefGoogle Scholar
  52. Raj S, Bräutigam K, Hamanishi ET, Wilkins O, Thomas BR, Schroeder W, Mansfield SD, Plant AL, Campbell MM (2011) Clone history shapes Populus drought responses. Proc Natl Acad Sci 108:12521–12526.  https://doi.org/10.1073/pnas.1103341108 CrossRefPubMedGoogle Scholar
  53. Richards CL, Alonso C, Becker C, Bossdorf O, Bucher E, Colomé-Tatché M, Durka W, Engelhardt J, Gaspar B, Gogol-Döring A, Grosse I, van Gurp TP, Heer K, Kronholm I, Lampei C, Latzel V, Mirouze M, Opgenoorth L, Paun O, Prohaska SJ, Rensing SA, Stadler PF, Trucchi E, Ullrich K, Verhoeven KJF (2017) Ecological plant epigenetics: evidence from model and non-model species, and the way forward. Ecol Lett 20:1576–1590.  https://doi.org/10.1111/ele.12858 CrossRefPubMedGoogle Scholar
  54. Robertson M, Schrey A, Shayter A, Moss C, Richards C (2017) Genetic and epigenetic variation in Spartina alterniflora following the Deepwater Horizon oil spill. Evol Appl 10:792–801.  https://doi.org/10.1111/eva.12482 CrossRefPubMedPubMedCentralGoogle Scholar
  55. Schmitz RJ, Schultz MD, Urich MA, Nery JR, Pelizzola M, Libiger O, Alix A, McCosh RB, Chen H, Schork NJ, Ecker JR (2013) Patterns of population epigenomic diversity. Nature 495:193.  https://doi.org/10.1038/nature11968 CrossRefPubMedPubMedCentralGoogle Scholar
  56. Schönberger B, Chen X, Mager S, Ludewig U (2016) Site-dependent differences in DNA methylation and their impact on plant establishment and phosphorus nutrition in Populus trichocarpa. PLOS ONE 11:e0168623.  https://doi.org/10.1371/journal.pone.0168623 CrossRefPubMedPubMedCentralGoogle Scholar
  57. Seymour DK, Becker C (2017) The causes and consequences of DNA methylome variation in plants. Curr Opin Plant Biol 36:56–63.  https://doi.org/10.1016/j.pbi.2017.01.005 CrossRefPubMedGoogle Scholar
  58. Shen X, De Jonge J, Forsberg SKG, Pettersson ME, Sheng Z, Hennig L, Carlborg Ö (2014) Natural CMT2 variation is associated with genome-wide methylation changes and temperature seasonality. PLoS Genetics 10:e1004842.  https://doi.org/10.1371/journal.pgen.1004842 CrossRefPubMedPubMedCentralGoogle Scholar
  59. Song Y, Ci D, Tian M, Zhang D (2016) Stable methylation of a non-coding RNA gene regulates gene expression in response to abiotic stress in Populus simonii. J Exp Bot 67:1477–1492.  https://doi.org/10.1093/jxb/erv543 CrossRefPubMedGoogle Scholar
  60. Sork VL (2017) Genomic studies of local adaptation in natural plant populations. J Hered 109:3–15.  https://doi.org/10.1093/jhered/esx091 CrossRefPubMedGoogle Scholar
  61. Speed D, Hemani G, Johnson MR, Balding DJ (2012) Improved heritability estimation from genome-wide SNPs. Am J Hum Genet 91:1011–1021.  https://doi.org/10.1016/j.ajhg.2012.10.010 CrossRefPubMedPubMedCentralGoogle Scholar
  62. Sultan SE, Barton K, Wilczek AM (2009) Contrasting patterns of transgenerational plasticity in ecologically distinct congeners. Ecology 90:1831–1839.  https://doi.org/10.1890/08-1064.1 CrossRefPubMedGoogle Scholar
  63. Teyssier E, Bernacchia G, Maury S, How Kit A, Stammitti-Bert L, Rolin D, Gallusci P (2008) Tissue dependent variations of DNA methylation and endoreduplication levels during tomato fruit development and ripening. Planta 228:391–399.  https://doi.org/10.1007/s00425-008-0743-z CrossRefPubMedGoogle Scholar
  64. Teyssier C, Maury S, Beaufour M, Grondin C, Delaunay A, Le Metté C, Ader K, Cadene M, Label P, Lelu-Walter MA (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.  https://doi.org/10.1111/ppl.12081 CrossRefPubMedGoogle Scholar
  65. Toillon J, Dallé E, Bodineau G, Berthelot A, Bastien JC, Brignolas F, Marron N (2016) Plasticity of yield and nitrogen removal in 56 Populus deltoides × P. nigra genotypes over two rotations of short-rotation coppice. For Ecol Manag 375:55–65.  https://doi.org/10.1016/j.foreco.2016.05.023 CrossRefGoogle Scholar
  66. Trap-Gentil MV, Hébrard C, Lafon-Placette C, Delaunay A, Hagège D, Joseph C, Brignolas F, Lefebvre M, Barnes S, Maury S (2011) Time course and amplitude of DNA methylation in the shoot apical meristem are critical points for bolting induction in sugar beet and bolting tolerance between genotypes. J Exp Bot 62:2585–2597.  https://doi.org/10.1093/jxb/erq433 CrossRefPubMedGoogle Scholar
  67. Tuskan GA, DiFazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A, Schein J, Sterck L, Aerts A, Bhalerao RR, Bhalerao RP, Blaudez D, Boerjan W, Brun A, Brunner A, Busov V, Campbell M, Carlson J, Chalot M, Chapman J, Chen GL, Cooper D, Coutinho PM, Couturier J, Covert S, Cronk Q, Cunningham R, Davis J, Degroeve S, Dejardin A, dePamphilis C, Detter J, Dirks B, Dubchak I, Duplessis S, Ehlting J, Ellis B, Gendler K, Goodstein D, Gribskov M, Grimwood J, Groover A, Gunter L, Hamberger B, Heinze B, Helariutta Y, Henrissat B, Holligan D, Holt R, Huang W, Islam-Faridi N, Jones S, Jones-Rhoades M, Jorgensen R, Joshi C, Kangasjarvi J, Karlsson J, Kelleher C, Kirkpatrick R, Kirst M, Kohler A, Kalluri U, Larimer F, Leebens-Mack J, Leple JC, Locascio P, Lou Y, Lucas S, Martin F, Montanini B, Napoli C, Nelson DR, Nelson C, Nieminen K, Nilsson O, Pereda V, Peter G, Philippe R, Pilate G, Poliakov A, Razumovskaya J, Richardson P, Rinaldi C, Ritland K, Rouze P, Ryaboy D, Schmutz J, Schrader J, Segerman B, Shin H, Siddiqui A, Sterky F, Terry A, Tsai CJ, Uberbacher E, Unneberg P, Vahala J, Wall K, Wessler S, Yang G, Yin T, Douglas C, Marra M, Sandberg G, Van de Peer Y, Rokhsar D (2006) The genome of Black Cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604.  https://doi.org/10.1126/science.1128691 CrossRefPubMedGoogle Scholar
  68. Van Kleunen M, Fischer M (2005) Constraints on the evolution of adaptive phenotypic plasticity in plants. New Phytol 166:49–60.  https://doi.org/10.1111/j.1469-8137.2004.01296.x CrossRefPubMedGoogle Scholar
  69. Vaughn MW, Tanurdžić M, Lippman Z, Jiang H, Carrasquillo R, Rabinowicz PD, Dedhia N, McCombie WR, Agier N, Bulski A (2007) Epigenetic natural variation in Arabidopsis thaliana. PLoS Biol 5:e174.  https://doi.org/10.1371/journal.pbio.0050174 CrossRefPubMedPubMedCentralGoogle Scholar
  70. Verhoeven KJF, vonHoldt BM, Sork VL (2016) Epigenetics in ecology and evolution: what we know and what we need to know. Mol Ecol 25:1631–1638.  https://doi.org/10.1111/mec.13617 CrossRefPubMedGoogle Scholar
  71. Vining KJ, Pomraning KR, Wilhelm LJ, Priest HD, Pellegrini M, Mockler TC, Freitag M, Strauss SH (2012) Dynamic DNA cytosine methylation in the Populus trichocarpa genome: tissue-level variation and relationship to gene expression. BMC Genomics 13:27.  https://doi.org/10.1186/1471-2164-13-27 CrossRefPubMedPubMedCentralGoogle Scholar
  72. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358.  https://doi.org/10.2307/2408641 CrossRefPubMedGoogle Scholar
  73. Yakovlev I.A, 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.  https://doi.org/10.3389/fphys.2017.00674
  74. Yakovlev IA, Fossdal CG, Johnsen Ø (2010) MicroRNAs, the epigenetic memory and climatic adaptation in Norway spruce. New Phytol 187:1154–1169.  https://doi.org/10.1111/j.1469-8137.2010.03341.x CrossRefPubMedGoogle Scholar
  75. 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 180:132–139.  https://doi.org/10.1016/j.plantsci.2010.07.004 CrossRefPubMedGoogle Scholar
  76. 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 243:1237–1249.  https://doi.org/10.1007/s00425-016-2484-8 CrossRefPubMedGoogle Scholar
  77. Yong WS, Hsu FM, Chen PY (2016) Profiling genome-wide DNA methylation. Epigenetics Chromatin 9:26.  https://doi.org/10.1186/s13072-016-0075-3 CrossRefPubMedPubMedCentralGoogle Scholar
  78. Zhu R, Shevchenko O, Ma C, Maury S, Freitag M, Strauss SH (2013) Poplars with a PtDDM1-RNAi transgene have reduced DNA methylation and show aberrant post-dormancy morphology. Planta 237:1483–1493.  https://doi.org/10.1007/s00425-013-1858-4 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Mamadou Dia Sow
    • 1
  • Vincent Segura
    • 2
  • Sylvain Chamaillard
    • 1
  • Véronique Jorge
    • 2
  • Alain Delaunay
    • 1
  • Clément Lafon-Placette
    • 1
    • 3
  • Régis Fichot
    • 1
  • Patricia Faivre-Rampant
    • 4
  • Marc Villar
    • 2
  • Franck Brignolas
    • 1
  • Stéphane Maury
    • 1
  1. 1.LBLGC, INRA, Université d’Orléans, EA 1207 USC 1328OrleansFrance
  2. 2.BioForA, INRA, ONFOrleansFrance
  3. 3.Department of Botany, Charles UniversityPragueCzech Republic
  4. 4.INRA, US1279 EPGV, CEA-IG/CNGEvryFrance

Personalised recommendations