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
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
35295625
PubMed Central
PMC8919072
DOI
10.3389/fpls.2022.827166
Knihovny.cz E-zdroje
- Klíčová slova
- 5-azacytidine, adaptation, climate change, clonal plant, epigenetics, latitudinal gradient, survival,
- Publikační typ
- časopisecké články MeSH
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.
Department of Botany Faculty of Science Charles University Prague Czechia
Institute of Botany Czech Academy of Sciences Průhonice Czechia
Zobrazit více v PubMed
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
The evolutionary consequences of interactions between the epigenome, the genome and the environment