DNA Methylation Can Mediate Local Adaptation and Response to Climate Change in the Clonal Plant Fragaria vesca: Evidence From a European-Scale Reciprocal Transplant Experiment

. 2022 ; 13 () : 827166. [epub] 20220228

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid35295625

The ongoing climate crisis represents a growing threat for plants and other organisms. However, how and if plants will be able to adapt to future environmental conditions is still debated. One of the most powerful mechanisms allowing plants to tackle the changing climate is phenotypic plasticity, which can be regulated by epigenetic mechanisms. Environmentally induced epigenetic variation mediating phenotypic plasticity might be heritable across (a)sexual generations, thus potentially enabling rapid adaptation to climate change. Here, we assessed whether epigenetic mechanisms, DNA methylation in particular, enable for local adaptation and response to increased and/or decreased temperature of natural populations of a clonal plant, Fragaria vesca (wild strawberry). We collected ramets from three populations along a temperature gradient in each of three countries covering the southern (Italy), central (Czechia), and northern (Norway) edges of the native European range of F. vesca. After clonal propagation and alteration of DNA methylation status of half of the plants via 5-azacytidine, we reciprocally transplanted clones to their home locality and to the other two climatically distinct localities within the country of their origin. At the end of the growing season, we recorded survival and aboveground biomass as fitness estimates. We found evidence for local adaptation in intermediate and cold populations in Italy and maladaptation of plants of the warmest populations in all countries. Plants treated with 5-azacytidine showed either better or worse performance in their local conditions than untreated plants. Application of 5-azacytidine also affected plant response to changed climatic conditions when transplanted to the colder or warmer locality than was their origin, and the response was, however, country-specific. We conclude that the increasing temperature will probably be the limiting factor determining F. vesca survival and distribution. DNA methylation may contribute to local adaptation and response to climatic change in natural ecosystems; however, its role may depend on the specific environmental conditions. Since adaptation mediated by epigenetic variation may occur faster than via natural selection on genetic variants, epigenetic adaptation might to some degree help plants in keeping up with the ongoing environmental crisis.

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Ågren J., Schemske D. W. (2012). Reciprocal transplants demonstrate strong adaptive differentiation of the model organism Arabidopsis thaliana in its native range. New Phytol. 194, 1112–1122. doi: 10.1111/j.1469-8137.2012.04112.x, PMID: PubMed DOI

Ahmed I., Sarazin A., Bowler C., Colot V., Quesneville H. (2011). Genome-wide evidence for local DNA methylation spreading from small RNA-targeted sequences in Arabidopsis. Nucleic Acids Res. 39, 6919–6931. doi: 10.1093/nar/gkr324, PMID: PubMed DOI PMC

Akimoto K., Katakami H., Kim H. J., Ogawa E., Sano C. M., Wada Y., et al. . (2007). Epigenetic inheritance in rice plants. Ann. Bot. 100, 205–217. doi: 10.1093/aob/mcm110, PMID: PubMed DOI PMC

Alpert P., Stuefer J. F. (1997). “Division of labour in clonal plants.” in The ecology and evolution of clonal plants. eds. de Kroon H., Groenendael J. (Leiden: Backhuys Publishers; ), 137–154.

Anastasiadi D., Venney C. J., Bernatchez L., Wellenreuther M. (2021). Epigenetic inheritance and reproductive mode in plants and animals. Trends Ecol. Evol. 36, 1124–1140. doi: 10.1016/j.tree.2021.08.006, PMID: PubMed DOI

Anderson J. T., Wadgymar S. M. (2020). Climate change disrupts local adaptation and favours upslope migration. Ecol. Lett. 23, 181–192. doi: 10.1111/ele.13427, PMID: PubMed DOI

Bates D., Mächler M., Bolker B. M., Walker S. C. (2015). Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48. doi: 10.18637/jss.v067.i01 DOI

Birami B., Gattmann M., Heyer A. G., Grote R., Arneth A., Ruehr N. K. (2018). Heat waves alter carbon allocation and increase mortality of aleppo pine under dry conditions. Front. For. Glob. Chang. 1:8. doi: 10.3389/ffgc.2018.00008 DOI

Boonjing P., Masuta Y., Nozawa K., Kato A., Ito H. (2020). The effect of zebularine on the heat-activated retrotransposon ONSEN in Arabidopsis thaliana and Vigna angularis. Genes Genet. Syst. 95, 165–172. doi: 10.1266/ggs.19-00046, PMID: PubMed DOI

Bossdorf O., Arcuri D., Richards C. L., Pigliucci M. (2010). Experimental alteration of DNA methylation affects the phenotypic plasticity of ecologically relevant traits in Arabidopsis thaliana. Evol. Ecol. 24, 541–553. doi: 10.1007/s10682-010-9372-7 DOI

Botero C. A., Weissing F. J., Wright J., Rubenstein D. R. (2015). Evolutionary tipping points in the capacity to adapt to environmental change. Proc. Natl. Acad. Sci. 112, 184–189. doi: 10.1073/pnas.1408589111, PMID: PubMed DOI PMC

Brady S. P., Bolnick D. I., Angert A. L., Gonzalez A., Barrett R. D. H., Crispo E., et al. . (2019). Causes of maladaptation. Evol. Appl. 12, 1229–1242. doi: 10.1111/eva.12844, PMID: PubMed DOI PMC

Carlson S. M., Cunningham C. J., Westley P. A. H. (2014). Evolutionary rescue in a changing world. Trends Ecol. Evol. 29, 521–530. doi: 10.1016/j.tree.2014.06.005, PMID: PubMed DOI

Chano V., Domínguez-Flores T., Hidalgo-Galvez M. D., Rodríguez-Calcerrada J., Pérez-Ramos I. M. (2021). Epigenetic responses of hare barley (Hordeum murinum subsp. leporinum) to climate change: an experimental, trait-based approach. Heredity 126, 748–762. doi: 10.1038/s41437-021-00415-y PubMed DOI PMC

Chevin L.-M., Collins S., Lefèvre F. (2013). Phenotypic plasticity and evolutionary demographic responses to climate change: taking theory out to the field. Funct. Ecol. 27, 967–979. doi: 10.1111/j.1365-2435.2012.02043.x DOI

Ci D., Song Y., Tian M., Zhang D. (2015). Methylation of miRNA genes in the response to temperature stress in Populus simonii. Front. Plant Sci. 6:921. doi: 10.3389/fpls.2015.00921, PMID: PubMed DOI PMC

Cornes R. C., van der Schrier G., van den Besselaar E. J. M., Jones P. D. (2018). An ensemble version of the E-OBS temperature and precipitation data sets. J. Geophys. Res. Atmos. 123, 9391–9409. doi: 10.1029/2017JD028200 DOI

Darrow G. M. (1966). The strawberry. History, breeding and physiology. New York: Holt, Rinehart & Winston.

Dobrowski S. Z., Abatzoglou J., Swanson A. K., Greenberg J. A., Mynsberge A. R., Holden Z. A., et al. . (2013). The climate velocity of the contiguous United States during the 20th century. Glob. Chang. Biol. 19, 241–251. doi: 10.1111/gcb.12026, PMID: PubMed DOI

Dodd R. S., Douhovnikoff V. (2016). Adjusting to global change through clonal growth and epigenetic variation. Front. Ecol. Evol. 4:86. doi: 10.3389/fevo.2016.00086 DOI

Dubin M. J., Zhang P., Meng D., Remigereau M. S., Osborne E. J., Paolo Casale F., et al. . (2015). DNA methylation in Arabidopsis has a genetic basis and shows evidence of local adaptation. elife 4:e05255. doi: 10.7554/eLife.05255, PMID: PubMed DOI PMC

Ebeling S. K., Stöcklin J., Hensen I., Auge H. (2011). Multiple common garden experiments suggest lack of local adaptation in an invasive ornamental plant. J. Plant Ecol. 4, 209–220. doi: 10.1093/jpe/rtr007 DOI

Fan H. H., Wei J., Li T. C., Li Z. P., Guo N., Cai Y. P., et al. . (2013). DNA methylation alterations of upland cotton (Gossypium hirsutum) in response to cold stress. Acta Physiol. Plant. 35, 2445–2453. doi: 10.1007/s11738-013-1278-x DOI

Feng S., Jacobsen S. E., Reik W. (2010). Epigenetic reprogramming in plant and animal development. Science 330, 622–627. doi: 10.1126/science.1190614, PMID: PubMed DOI PMC

Germino M. J., Moser A. M., Sands A. R. (2019). Adaptive variation, including local adaptation, requires decades to become evident in common gardens. Ecol. Appl. 29:e01842. doi: 10.1002/eap.1842 PubMed DOI

González A. P. R., Chrtek J., Dobrev P. I., Dumalasova V., Fehrer J., Mraz P., et al. . (2016). Stress-induced memory alters growth of clonal offspring of white clover (Trifolium repens). Am. J. Bot. 103, 1567–1574. doi: 10.3732/ajb.1500526, PMID: PubMed DOI

Griffin P. T., Niederhuth C. E., Schmitz R. J. (2016). A comparative analysis of 5-azacytidine- and zebularine-induced DNA demethylation. G3 6, 2773–2780. doi: 10.1534/g3.116.030262, PMID: PubMed DOI PMC

Gugger P. F., Fitz-Gibbon S., Pellegrini M., Sork V. L. (2016). Species-wide patterns of DNA methylation variation in Quercus lobata and their association with climate gradients. Mol. Ecol. 25, 1665–1680. doi: 10.1111/mec.13563, PMID: PubMed DOI

Hammer K. J., Borum J., Hasler-Sheetal H., Shields E. C., Sand-Jensen K., Moore K. A. (2018). High temperatures cause reduced growth, plant death and metabolic changes in eelgrass Zostera marina. Mar. Ecol. Prog. Ser. 604, 121–132. doi: 10.3354/meps12740 DOI

Hauser M. T., Aufsatz W., Jonak C., Luschnig C. (2011). Transgenerational epigenetic inheritance in plants. Biochim. Biophys. Acta Gene Regul. Mech. 1809, 459–468. doi: 10.1016/j.bbagrm.2011.03.007, PMID: PubMed DOI PMC

Herden J., Eckert S., Stift M., Joshi J., Kleunen M. (2019). No evidence for local adaptation and an epigenetic underpinning in native and non-native ruderal plant species in Germany. Ecol. Evol. 9, 9412–9426. doi: 10.1002/ece3.5325, PMID: PubMed DOI PMC

Herrera C. M., Bazaga P. (2013). Epigenetic correlates of plant phenotypic plasticity: DNA methylation differs between prickly and nonprickly leaves in heterophyllous Ilex aquifolium (Aquifoliaceae) trees. Bot. J. Linn. Soc. 171, 441–452. doi: 10.1111/boj.12007 DOI

Herrera C. M., Bazaga P., Pérez R., Alonso C. (2021). Lifetime genealogical divergence within plants leads to epigenetic mosaicism in the shrub Lavandula latifolia (Lamiaceae). New Phytol. 231, 2065–2076. doi: 10.1111/nph.17257, PMID: PubMed DOI

Hoffmann A. A., Sgrò C. M. (2011). Climate change and evolutionary adaptation. Nature 470, 479–485. doi: 10.1038/nature09670 PubMed DOI

Hossain M. S., Kawakatsu T., Kim K. D., Zhang N., Nguyen C. T., Khan S. M., et al. . (2017). Divergent cytosine DNA methylation patterns in single-cell, soybean root hairs. New Phytol. 214, 808–819. doi: 10.1111/nph.14421, PMID: PubMed DOI

Johannes F., Schmitz R. J. (2019). Spontaneous epimutations in plants. New Phytol. 221, 1253–1259. doi: 10.1111/nph.15434, PMID: PubMed DOI

Kondo H., Miura T., Wada K. C., Takeno K. (2007). Induction of flowering by 5-azacytidine in some plant species: relationship between the stability of photoperiodically induced flowering and flower-inducing effect of DNA demethylation. Physiol. Plant. 131, 462–469. doi: 10.1111/j.1399-3054.2007.00965.x, PMID: PubMed DOI

Kuznetsova A., Brockhoff P. B., Christensen R. H. B. (2017). lmerTest package: tests in linear mixed effects models. J. Stat. Softw. 82, 1–26. doi: 10.18637/jss.v082.i13 DOI

Latzel V., Klimešová J. (2010). Transgenerational plasticity in clonal plants. Evol. Ecol. 24, 1537–1543. doi: 10.1007/s10682-010-9385-2 DOI

Latzel V., Rendina González A. P., Rosenthal J. (2016). Epigenetic memory as a basis for intelligent behavior in clonal plants. Front. Plant Sci. 7:1354. doi: 10.3389/fpls.2016.01354, PMID: PubMed DOI PMC

Leimu R., Fischer M. (2008). A meta-analysis of local adaptation in plants. PLoS One 3:e4010. doi: 10.1371/journal.pone.0004010, PMID: PubMed DOI PMC

Lenoir J., Gégout J. C., Guisan A., Vittoz P., Wohlgemuth T., Zimmermann N. E., et al. . (2010). Going against the flow: potential mechanisms for unexpected downslope range shifts in a warming climate. Ecography 33, 295–303. doi: 10.1111/j.1600-0587.2010.06279.x DOI

Li J., Huang Q., Sun M., Zhang T., Li H., Chen B., et al. . (2016). Global DNA methylation variations after short-term heat shock treatment in cultured microspores of Brassica napus cv. Topas. Sci. Rep. 6:38401. doi: 10.1038/srep38401, PMID: PubMed DOI PMC

Liu D., Peñuelas J., Ogaya R., Estiarte M., Tielbörger K., Slowik F., et al. . (2018). Species selection under long-term experimental warming and drought explained by climatic distributions. New Phytol. 217, 1494–1506. doi: 10.1111/nph.14925, PMID: PubMed DOI

Loarie S. R., Duffy P. B., Hamilton H., Asner G. P., Field C. B., Ackerly D. D. (2009). The velocity of climate change. Nature 462, 1052–1055. doi: 10.1038/nature08649, PMID: PubMed DOI

Lynn J. S., Klanderud K., Telford R. J., Goldberg D. E., Vandvik V. (2021). Macroecological context predicts species’ responses to climate warming. Glob. Chang. Biol. 27, 2088–2101. doi: 10.1111/gcb.15532, PMID: PubMed DOI

McNamara J. M., Dall S. R. X., Hammerstein P., Leimar O. (2016). Detection vs. selection: integration of genetic, epigenetic and environmental cues in fluctuating environments. Ecol. Lett. 19, 1267–1276. doi: 10.1111/ele.12663, PMID: PubMed DOI

Merilä J. (2012). Evolution in response to climate change: in pursuit of the missing evidence. BioEssays 34, 811–818. doi: 10.1002/bies.201200054, PMID: PubMed DOI

Merilä J., Hendry A. P. (2014). Climate change, adaptation, and phenotypic plasticity: the problem and the evidence. Evol. Appl. 7, 1–14. doi: 10.1111/eva.12137, PMID: PubMed DOI PMC

Midolo G., Wellstein C. (2020). Plant performance and survival across transplant experiments depend upon temperature and precipitation change along elevation. J. Ecol. 108, 2107–2120. doi: 10.1111/1365-2745.13387 DOI

Münzbergová Z., Latzel V., Šurinová M., Hadincová V. (2019). DNA methylation as a possible mechanism affecting ability of natural populations to adapt to changing climate. Oikos 128, 124–134. doi: 10.1111/oik.05591 DOI

Nicotra A. B., Atkin O. K., Bonser S. P., Davidson A. M., Finnegan E. J., Mathesius U., et al. . (2010). Plant phenotypic plasticity in a changing climate. Trends Plant Sci. 15, 684–692. doi: 10.1016/j.tplants.2010.09.008, PMID: PubMed DOI

Oksanen J., Blanchet F. Guillaume, Friendly Michael, Kindt Roeland, Legendre Pierre, McGlinn Dan, et al. . (2020). CRAN - Package vegan. Available at: https://cran.r-project.org/web/packages/vegan/index.html

Pan Y., Wang W., Zhao X., Zhu L., Fu B., Li Z. (2011). DNA methylation alterations of rice in response to cold stress. POJ 4, 364–369.

Platt A., Gugger P. F., Pellegrini M., Sork V. L. (2015). Genome-wide signature of local adaptation linked to variable CpG methylation in oak populations. Mol. Ecol. 24, 3823–3830. doi: 10.1111/mec.13230, PMID: PubMed DOI

Putnam R. C., Reich P. B. (2017). Climate and competition affect growth and survival of transplanted sugar maple seedlings along a 1700-km gradient. Ecol. Monogr. 87, 130–157. doi: 10.1002/ecm.1237 DOI

Puy J., Dvořáková H., Carmona C. P., de Bello F., Hiiesalu I., Latzel V. (2018). Improved demethylation in ecological epigenetic experiments: testing a simple and harmless foliar demethylation application. Methods Ecol. Evol. 9, 744–753. doi: 10.1111/2041-210X.12903 DOI

Rapacciuolo G., Maher S. P., Schneider A. C., Hammond T. T., Jabis M. D., Walsh R. E., et al. . (2014). Beyond a warming fingerprint: individualistic biogeographic responses to heterogeneous climate change in California. Glob. Chang. Biol. 20, 2841–2855. doi: 10.1111/gcb.12638, PMID: PubMed DOI PMC

R Core Team (2017). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. Available at: https://www.r-project.org/

Reich P. B., Sendall K. M., Rice K., Rich R. L., Stefanski A., Hobbie S. E., et al. . (2015). Geographic range predicts photosynthetic and growth response to warming in co-occurring tree species. Nat. Clim. Chang. 5, 148–152. doi: 10.1038/nclimate2497 DOI

Rendina González A. P., Preite V., Verhoeven K. J. F., Latzel V. (2018). Transgenerational effects and epigenetic memory in the clonal plant Trifolium repens. Front. Plant Sci. 9:1677. doi: 10.3389/fpls.2018.01677, PMID: PubMed DOI PMC

Richards E. J. (2006). Inherited epigenetic variation — revisiting soft inheritance. Nat. Rev. Genet. 7, 395–401. doi: 10.1038/nrg1834, PMID: PubMed DOI

Richards C. L., Schrey A. W., Pigliucci M. (2012). Invasion of diverse habitats by few Japanese knotweed genotypes is correlated with epigenetic differentiation. Ecol. Lett. 15, 1016–1025. doi: 10.1111/j.1461-0248.2012.01824.x, PMID: PubMed DOI

Ruiz-García L., Cervera M. T., Martínez-Zapater J. M. (2005). DNA methylation increases throughout Arabidopsis development. Planta 222, 301–306. doi: 10.1007/s00425-005-1524-6, PMID: PubMed DOI

Schulze J., Rufener R., Erhardt A., Stoll P. (2012). The relative importance of sexual and clonal reproduction for population growth in the perennial herb Fragaria vesca. Popul. Ecol. 54, 369–380. doi: 10.1007/s10144-012-0321-x DOI

Shi W., Chen X., Gao L., Xu C. Y., Ou X., Bossdorf O., et al. . (2019). Transient stability of epigenetic population differentiation in a clonal invader. Front. Plant Sci. 9:1851. doi: 10.3389/fpls.2018.01851, PMID: PubMed DOI PMC

Sobral M., Sampedro L., Neylan I., Siemens D., Dirzo R. (2021). Phenotypic plasticity in plant defense across life stages: Inducibility, transgenerational induction, and transgenerational priming in wild radish. Proc. Natl. Acad. Sci. 118:e2005865118. doi: 10.1073/pnas.2005865118, PMID: PubMed DOI PMC

Tang X., Wang Q., Huang X. (2018). Chilling-induced DNA Demethylation is associated with the cold tolerance of Hevea brasiliensis. BMC Plant Biol. 18:70. doi: 10.1186/s12870-018-1276-7, PMID: PubMed DOI PMC

Thiebaut F., Hemerly A. S., Ferreira P. C. G. (2019). A role for epigenetic regulation in the adaptation and stress responses of non-model plants. Front. Plant Sci. 10:246. doi: 10.3389/fpls.2019.00246, PMID: PubMed DOI PMC

Tíscar P. A., Lucas-Borja M. E., Candel-Pérez D. (2018). Lack of local adaptation to the establishment conditions limits assisted migration to adapt drought-prone Pinus nigra populations to climate change. For. Ecol. Manag. 409, 719–728. doi: 10.1016/j.foreco.2017.12.014 DOI

Verhoeven K. J. F., Preite V. (2014). Epigenetic variation in asexually reproducing organisms. Evolution 68, 644–655. doi: 10.1111/evo.12320, PMID: PubMed DOI

Visser M. E. (2008). Keeping up with a warming world; assessing the rate of adaptation to climate change. Proc. R. Soc. B Biol. Sci. 275, 649–659. doi: 10.1098/rspb.2007.0997, PMID: PubMed DOI PMC

Zhang Y.-Y., Fischer M., Colot V., Bossdorf O. (2013). Epigenetic variation creates potential for evolution of plant phenotypic plasticity. New Phytol. 197, 314–322. doi: 10.1111/nph.12010, PMID: PubMed DOI

Zhang Y.-Y., Latzel V., Fischer M., Bossdorf O. (2018). Understanding the evolutionary potential of epigenetic variation: a comparison of heritable phenotypic variation in epiRILs, RILs, and natural ecotypes of Arabidopsis thaliana. Heredity 121, 257–265. doi: 10.1038/s41437-018-0095-9, PMID: PubMed DOI PMC

Zheng X., Levine D., Shen J., Gogarten S. M., Laurie C., Weir B. S. (2012). A high-performance computing toolset for relatedness and principal component analysis of SNP data. Bioinformatics 28, 3326–3328. doi: 10.1093/bioinformatics/bts606, PMID: PubMed DOI PMC

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