In the context of climate changes, clarifying the causes underlying tree phenotypic plasticity and adaptation is crucial. Studies suggest a role of epigenetic mechanisms in response to external stimuli, raising the question whether such processes can promote acclimation of trees exposed to adverse climate conditions. Recently, we revealed an environmental epigenetic footprint in the shoot apical meristem (SAM) which could partially be transmitted mitotically, for several months, up until the winter-dormant bud in field conditions. Here, we extended our previous analysis to the leaves of the same P. deltoides×P. nigra clones. We aimed at estimating the range of developmentally, genetically, and environmentally induced variations on DNA methylation. We showed that only the first leaves emerging from the SAM displayed variations of DNA methylation under changing water conditions. We also found that these variations are genotype- and pedoclimatic site-dependent. Altogether, our data raised questions and perspectives on the direct acquisition, the maintenance of environmentally induced DNA methylation changes, and their mitotic transmission from the SAM to the first emerging leaves.

b Institute for Biology 3 University of Freiburg Freiburg Germany

c Department of Botany Charles University Prague Czech Republic

Laboratoire de Biologie des Ligneux et des Grandes Cultures EA1207 USC 1328 INRA Université d'Orléans Orléans France

Zobrazit více v PubMed

Allen CD, Macalady AK, Chenchouni H, Bachelet D, McDowell N, Vennetier M, Kitzberger T, Rigling A, Breshears DD, Hogg EH (Ted), et al. A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. For Ecol Manage. 2010;259:660–684. doi:10.1016/j.foreco.2009.09.001. DOI

IPCC 2014a. Climate change 2014: impacts, adaptation, and vulnerability. Part a: global and sectoral aspects. European environment agency [accessed 2018 December12] https://www.eea.europa.eu/data-and-maps/indicators/heating-degree-days/ipcc-2007-contribution-of-working.

Bräutigam K, Vining KJ, Lafon-Placette C, Fossdal CG, Mirouze M, Marcos JG, Fluch S, Fraga MF, Guevara MÁ, Abarca D, et al. Epigenetic regulation of adaptive responses of forest tree species to the environment. Ecol Evol. 2013;3:399–415. doi:10.1002/ece3.2013.3.issue-2. PubMed DOI PMC

Plomion C, Bastien C, Bogeat-Triboulot M-B, Bouffier L, Déjardin A, Duplessis S, Fady B, Heuertz M, Le Gac A-L, Le Provost G, et al. Forest tree genomics: 10 achievements from the past 10 years and future prospects. Ann For Sci. 2016;73:77–103. doi:10.1007/s13595-015-0488-3. DOI

Nicotra AB, Atkin OK, Bonser SP, Davidson AM, Finnegan EJ, Mathesius U, Poot P, Purugganan MD, Richards CL, Valladares F, et al. Plant phenotypic plasticity in a changing climate. Trends Plant Sci. 2010;15:684–692. doi:10.1016/j.tplants.2010.09.008. PubMed DOI

Rey O, Danchin E, Mirouze M, Loot C, Blanchet S.. Adaptation to global change: a transposable element–epigenetics perspective. Trends Ecol Evol. 2016;31:514–526. doi:10.1016/j.tree.2016.03.013. PubMed DOI

Richards CL, Alonso C, Becker C, Bossdorf O, Bucher E, Colomé-Tatché M, Durka W, Engelhardt J, Gaspar B, Gogol-Döring A, et al. Ecological plant epigenetics: evidence from model and non-model species, and the way forward. Ecol Lett. 2017;20:1576–1590. doi:10.1111/ele.12858. PubMed DOI

Tuskan GA, DiFazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A, et al. The genome of black cottonwood, populus trichocarpa (Torr. & Gray). Science. 2006;313:1596–1604. doi:10.1126/science.1128691. PubMed DOI

Jansson S, Douglas CJ. Populus: a model system for plant biology. Annu Rev Plant Biol. 2007;58:435–458. doi:10.1146/annurev.arplant.58.032806.103956. PubMed DOI

Marron N, Dreyer E, Boudouresque E, Delay D, Petit J-M, Delmotte FM, Brignolas F. Impact of successive drought and re-watering cycles on growth and specific leaf area of two Populus x canadensis (Moench) clones,‘Dorskamp’and ‘Luisa_Avanzo’. Tree Physiol. 2003;23:1225–1235. doi:10.1093/treephys/23.18.1225. PubMed DOI

Monclus R, Dreyer E, Villar M, Delmotte FM, Delay D, Petit J-M, Barbaroux C, Le Thiec D, Brechet C, Brignolas F. Impact of drought on productivity and water use efficiency in 29 genotypes of Populus deltoides x Populus nigra. New Phytol. 2006;169:765–777. doi:10.1111/nph.2006.169.issue-4. PubMed DOI

Fichot R, Brignolas F, Cochard H, Ceulemans R. Vulnerability to drought-induced cavitation in poplars: synthesis and future opportunities: drought-induced cavitation in poplars: a review. Plant Cell Environ. 2015;38:1233–1251. doi:10.1111/pce.12491. PubMed DOI

Hamanishi ET, Thomas BR, Campbell MM. Drought induces alterations in the stomatal development program in Populus. J Exp Bot. 2012;63:4959–4971. doi:10.1093/jxb/ers177. PubMed DOI PMC

Bizet F, Bogeat-Triboulot M-B, Montpied P, Christophe A, Ningre N, Cohen D, Hummel I. Phenotypic plasticity toward water regime: response of leaf growth and underlying candidate genes in Populus. Physiol Plant. 2015;154:39–53. doi:10.1111/ppl.2015.154.issue-1. PubMed DOI

Toillon J, Dallé E, Bodineau G, Berthelot A, Bastien J-C, Brignolas F, Marron N. Plasticity of yield and nitrogen removal in 56 Populus deltoides×P. nigra genotypes over two rotations of short-rotation coppice. For Ecol Manage. 2016;375:55–65. doi:10.1016/j.foreco.2016.05.023. DOI

Le Gac A-L, Lafon-Placette C, Chauveau D, Segura V, Delaunay A, Fichot R, Marron N, Le Jan I, Berthelot A, Bodineau G, et al. Winter-dormant shoot apical meristem in poplar trees shows environmental epigenetic memory. J Exp Bot. 2018;69:4821–4837. doi:10.1093/jxb/ery271. PubMed DOI PMC

Lafon-Placette C, Le Gac A-L, Chauveau D, Segura V, Delaunay A, Lesage-Descauses M-C, Hummel I, Cohen D, Jesson B, Le Thiec D, et al. Changes in the epigenome and transcriptome of the poplar shoot apical meristem in response to water availability affect preferentially hormone pathways. J Exp Bot. 2018;69:537–551. doi:10.1093/jxb/erx409. PubMed DOI

Vining KJ, Pomraning KR, Wilhelm LJ, Priest HD, Pellegrini M, Mockler TC, Freitag M, Strauss SH. Dynamic DNA cytosine methylation in the Populus trichocarpa genome: tissue-level variation and relationship to gene expression. BMC Genomics. 2012;13:27. doi:10.1186/1471-2164-13-27. PubMed DOI PMC

Lafon-Placette C, Faivre-Rampant P, Delaunay A, Street N, Brignolas F, Maury S. 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. 2013;197:416–430. doi:10.1111/nph.12026. PubMed DOI

Liang D, Zhang Z, Wu H, Huang C, Shuai P, Ye C-Y, Tang S, Wang Y, Yang L, Wang J, et al. Single-base-resolution methylomes of Populus trichocarpa reveal the association between DNA methylation and drought stress. BMC Genet. 2014;15:S9. doi:10.1186/1471-2156-15-S1-S9. PubMed DOI PMC

Guarino F, Cicatelli A, Brundu G, Heinze B, Castiglione S, Labra M. Epigenetic diversity of clonal white poplar (Populus alba L.) populations: could methylation support the success of vegetative reproduction strategy? PLoS One. 2015;10:e0131480. doi:10.1371/journal.pone.0131480. PubMed DOI PMC

Schönberger B, Chen X, Mager S, Ludewig U, Jeltsch A. Site-dependent differences in DNA methylation and their impact on plant establishment and phosphorus nutrition in Populus trichocarpa. PLoS One. 2016;11:e0168623. doi:10.1371/journal.pone.0168623. PubMed DOI PMC

Conde D, Le Gac A-L, Perales M, Dervinis C, Kirst M, Maury S, González-Melendi P, Allona I. Chilling-responsive DEMETER-LIKE DNA demethylase mediates in poplar bud break: role of active DNA demethylase in trees’ bud break. Plant Cell Environ. 2017;40:2236–2249. doi:10.1111/pce.v40.10. PubMed DOI

Sow MD, Segura V, Chamaillard S, Jorge V, Delaunay A, Lafon-Placette C, Fichot R, Faivre-Rampant P, Villar M, Brignolas F, et al. Narrow-sense heritability and PST estimates of DNA methylation in three Populus nigra L. populations under contrasting water availability. Tree Genet Genomes. 2018;14. doi:10.1007/s11295-018-1293-6. DOI

Gourcilleau D, Bogeat-Triboulot M-B, Thiec D, Lafon-Placette C, Delaunay A, El-Soud WA, Brignolas F, Maury S. DNA methylation and histone acetylation: genotypic variations in hybrid poplars, impact of water deficit and relationships with productivity. Ann For Sci. 2010;67:208. doi:10.1051/forest/2009101. DOI

Alonso C, Pérez R, Bazaga P, Herrera CM. Global DNA cytosine methylation as an evolving trait: phylogenetic signal and correlated evolution with genome size in angiosperms. Front Genet. 2015;6. doi:10.3389/fgene.2015.00360. PubMed DOI PMC

Trap-Gentil M-V, Hébrard C, Lafon-Placette C, Delaunay A, Hagège D, Joseph C, Brignolas F, Lefebvre M, Barnes S, Maury S. Time course and amplitude of DNA methylation in the shootapical meristem are critical points for bolting induction in sugar beet andbolting tolerance between genotypes. J Exp Bot. 2011;62:2585–2597. doi:10.1093/jxb/err025. PubMed DOI

Zhu R, Shevchenko O, Ma C, Maury S, Freitag M, Strauss SH. Poplars with a PtDDM1-RNAi transgene have reduced DNA methylation and show aberrant post-dormancy morphology. Planta. 2013;237:1483–1493. doi:10.1007/s00425-013-1858-4. PubMed DOI

Cohen D, Lo C-Z, Su S-Y, Kuo B-H, Hsiung CA, Lin C-Y. Comparative transcriptomics of drought responses in populus: a meta-analysis of genome-wide expression profiling in mature leaves and root apices across two genotypes. BMC Genomics. 2010;11:1–21. doi:10.1186/1471-2164-11-S4-S6. PubMed DOI PMC

Toillon J, Fichot R, Dallé E, Berthelot A, Brignolas F, Marron N. Planting density affects growth and water-use efficiency depending on site in Populus deltoides×P. nigra. For Ecol Manag. 2013;304:345–354. doi:10.1016/j.foreco.2013.05.017. DOI

Dong-Hwan K, Sung S. Genetic and epigenetic mechanisms underlying vernalization. Arabidopsis Book. 2014;12:e0171. PubMed PMC

Liu X, Xie C, Si H, Yang J. CRISPR/Cas9-mediated genome editing in plants. Methods. 2017;15:121–122. PubMed

Fan D, Liu T, Li C, Jiao B, Li S, Hou Y, Luo K. Efficient CRISPR/Cas9-mediated targeted mutagenesis in Populus in the first generation. Sci Rep. 2015;5:12217. doi:10.1038/srep12217. PubMed DOI PMC

Banta JA, Richards CL. Quantitative epigenetics and evolution. Heredity. 2018;121:210–224. doi:10.1038/s41437-018-0114-x. PubMed DOI PMC

Sow MD, Allona I, Ambroise C, Conde D, Fichot R,  Gribkova S, Jorge V, Le-Provost G, Pâques L, Plomion C, et al. Epigenetics in forest trees: state of the art and potential implications for breeding and management in a context of climate change. Adv Bot Res. 2018;88:387–453.

Epigenetics for Crop Improvement in Times of Global Change