Stronger transgenerational plasticity in clonal compared to sexual offspring of Fragaria vesca: effects of drought, elevated temperature and CO2
Jazyk angličtina Země Velká Británie, Anglie Médium print
Typ dokumentu časopisecké články
Grantová podpora
GACR 23-04749S
Czech Science Foundation
RVO 67985939
Czech Science Foundation
Postdoctoral Fellowship
Czech Academy of Sciences
Erasmus+ Traineeship Program 2022/2023
e-INFRA CZ LM2018140
'e-Infrastruktura CZ'
Ministry of Education, Youth and Sports of the Czech Republic
PubMed
40568957
PubMed Central
PMC12464940
DOI
10.1093/aob/mcaf136
PII: 8174837
Knihovny.cz E-zdroje
- Klíčová slova
- Climate change adaptation, DNA methylation, clonal propagation, environmental stress adaptation, epigenetic inheritance, high temperatures and CO2, sexual reproduction, transgenerational plasticity, woodland strawberry (Fragaria vesca),
- MeSH
- atmosféra chemie MeSH
- DNA rostlinná MeSH
- fyziologická adaptace * genetika MeSH
- globální oteplování MeSH
- jahodník * genetika fyziologie MeSH
- klimatické změny MeSH
- metylace DNA MeSH
- období sucha MeSH
- oxid uhličitý analýza MeSH
- rozmnožování fyziologie MeSH
- teplota MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- DNA rostlinná MeSH
- oxid uhličitý MeSH
BACKGROUND AND AIMS: Climate change threatens plant species, potentially exceeding their adaptive capacities. Plants may adapt to rapid environmental changes through transgenerational plasticity (TGP), where adaptive traits are passed to their offspring via proteins, hormones and epigenetic modifications such as DNA methylation. The extent of TGP and its ecological implications may differ between sexual and clonal reproductive modes due to differences in the inheritance of DNA methylation and provisioning. However, it remains unclear whether TGP differs between these reproductive modes and the role of DNA methylation. Addressing this gap is crucial, as higher TGP in clonal propagation could compensate for low genetic variation and help these plants in adapting to rapid environmental changes. METHODS: We assessed the adaptive potential of woodland strawberry (Fragaria vesca), a widely distributed herb with both clonal and sexual reproduction, in response to environmental conditions expected by the end of the 21st century: a temperature rise of 4 °C, a 400 ppm rise in atmospheric CO2 and periodic droughts. We quantified ecologically relevant phenotypic traits and examined whole-genome DNA methylation patterns in parents and their clonal and sexual offspring. KEY RESULTS: We found evidence for TGP induced by the parental environment, with a stronger overall effect observed in clonal compared to sexual offspring. Specifically, parental exposure to current temperature and CO2 conditions prompted adaptive TGP, particularly in clonal offspring. Additionally, adaptive TGP was observed exclusively in clonal offspring in response to a combination of elevated parental temperature and drought conditions. Finally, we found a higher inheritance of DNA methylation marks in clonal than in sexual offspring. CONCLUSIONS: These results suggest that while TGP via DNA methylation can influence clonal plant adaptation to future conditions, it remains uncertain whether this influence will consistently result in adaptive outcomes. Moreover, TGP would probably be more important in clonal than in sexual reproduction.
Department of Botany Faculty of Science Charles University Prague 128 01 Czechia
Institute of Botany Czech Academy of Sciences Průhonice 252 43 Czechia
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Anastasiadi D, Venney CJ, Bernatchez L, Wellenreuther M. 2021. Epigenetic inheritance and reproductive mode in plants and animals. Trends in Ecology & Evolution 36: 1124–1140. doi: 10.1016/J.TREE.2021.08.006 PubMed DOI
Andrews S. 2010. FastQC: A Quality Control Tool for High Throughput Sequence Data. http://www.bioinformatics.babraham.ac.uk/projects/fastqc/ (10 July 2025).
AR5 Synthesis Report: Climate Change 2014—IPCC.
Bird A. 2007. Perceptions of epigenetics. Nature 447: 396–398. doi: 10.1038/nature05913 PubMed DOI
Boyko A, Blevins T, Yao Y, et al. 2010. Transgenerational adaptation of Arabidopsis to stress requires DNA methylation and the function of dicer-like proteins. PLoS One 5: e9514. doi: 10.1371/journal.pone.0009514 PubMed DOI PMC
Burgess SC, Marshall DJ. 2014. Adaptive parental effects: the importance of estimating environmental predictability and offspring fitness appropriately. Oikos 123: 769–776. doi: 10.1111/OIK.01235 DOI
Calarco JP, Borges F, Donoghue MTA, et al. 2012. Reprogramming of DNA methylation in pollen guides epigenetic inheritance via small RNA. Cell 151: 194–205. doi: 10.1016/j.cell.2012.09.001 PubMed DOI PMC
Colicchio JM, Herman J. 2020. Empirical patterns of environmental variation favor adaptive transgenerational plasticity. Ecology and Evolution 10: 1648–1665. doi: 10.1002/ece3.6022 PubMed DOI PMC
Edger PP, VanBuren R, Colle M, et al. 2018. Single-molecule sequencing and optical mapping yields an improved genome of woodland strawberry ( PubMed DOI PMC
Feng S, Jacobsen SE, Reik W. 2010. Epigenetic reprogramming in plant and animal development. Science (New York, N.Y.) 330: 622–627. doi: 10.1126/SCIENCE.1190614 PubMed DOI PMC
Herman JJ, Sultan SE. 2011. Adaptive transgenerational plasticity in plants: case studies, mechanisms, and implications for natural populations. Frontiers in Plant Science 2: 102. doi: 10.3389/fpls.2011.00102 PubMed DOI PMC
Ibañez VN, Quadrana L. 2023. Shaping inheritance: how distinct reproductive strategies influence DNA methylation memory in plants. Current Opinion in Genetics & Development 78: 102018. doi: 10.1016/J.GDE.2022.102018 PubMed DOI
Jühling F, Kretzmer H, Bernhart SH, Otto C, Stadler PF, Hoffmann S. 2016. Metilene: fast and sensitive calling of differentially methylated regions from bisulfite sequencing data. Genome Research 26: 256–262. doi: 10.1101/GR.196394.115 PubMed DOI PMC
Jung S, Lee T, Cheng C-H, et al. 2019. 15 years of GDR: new data and functionality in the genome database for Rosaceae. Nucleic Acids Research 47: D1137. doi: 10.1093/NAR/GKY1000 PubMed DOI PMC
Klimeš L. 1997. Clonal plant architecture: a comparative analysis of form and function. In: The ecology and evolution of clonal plants. Leiden (Netherlands): Backhuys Publishers, 1–29. [Preprint].
Kremer A, Ronce O, Robledo-Arnuncio JJ, et al. 2012. Long-distance gene flow and adaptation of forest trees to rapid climate change. Ecology Letters 15: 378–392. doi: 10.1111/J.1461-0248.2012.01746.X PubMed DOI PMC
Latzel V, Fischer M, Groot M, et al. 2023. Parental environmental effects are common and strong, but unpredictable, in PubMed DOI
Latzel V, Klimešová J. 2010. Transgenerational plasticity in clonal plants. Evolutionary Ecology 24: 1537–1543. doi: 10.1007/s10682-010-9385-2 DOI
Latzel V, Mizgur-Hribar D, Sammarco I, Janoušková M. 2025. Transgenerational effects of mycorrhiza are stronger in sexual than in clonal offspring of DOI
Lau JA, Peiffer J, Reich PB, Tiffin P. 2008. Transgenerational effects of global environmental change: long-term CO PubMed DOI
Levine MT, Feller IC. 2004. Effects of forest age and disturbance on population persistence in the understory herb, DOI
Li Y, Pi M, Gao Q, Liu Z, Kang C. 2019. Updated annotation of the wild strawberry PubMed DOI PMC
Lin X, Yin J, Wang Y, et al. 2024. Environment-induced heritable variations are common in PubMed DOI PMC
Loarie SR, Duffy PB, Hamilton H, Asner GP, Field CB, Ackerly DD. 2009. The velocity of climate change. Nature 462: 1052–1055. doi: 10.1038/nature08649 PubMed DOI
López M-E, Roquis D, Becker C, Denoyes B, Bucher E. 2022. DNA methylation dynamics during stress response in woodland strawberry ( PubMed DOI PMC
Martin M. 2011. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet:journal 17: 10–12. doi: 10.14806/ej.17.1.200 DOI
MethylDackel . no date. https://github.com/dpryan79/MethylDackel/ (10 July 2025).
Münzbergová Z, Hadincová V. 2017. Transgenerational plasticity as an important mechanism affecting response of clonal species to changing climate. Ecology and Evolution 7: 5236–5247. doi: 10.1002/ece3.3105 PubMed DOI PMC
Nicotra AB, Atkin OK, Bonser SP, et al. 2010. Plant phenotypic plasticity in a changing climate. Trends in Plant Science 15: 684–692. doi: 10.1016/j.tplants.2010.09.008 PubMed DOI
Nunn A, Can SN, Otto C, et al. 2021. EpiDiverse toolkit: a pipeline suite for the analysis of bisulfite sequencing data in ecological plant epigenetics. NAR Genomics and Bioinformatics 3: lqab106. doi: 10.1093/NARGAB/LQAB106 PubMed DOI PMC
Ou S, Su W, Liao Y, et al. 2019. Benchmarking transposable element annotation methods for creation of a streamlined, comprehensive pipeline. Genome Biology 20: 275. doi: 10.1186/S13059-019-1905-Y PubMed DOI PMC
‘Picard toolkit’ . 2018. Broad Institute. http://broadinstitute.github.io/picard/ (10 July 2025).
Prezza N, Vezzi F, Käller M, Policriti A. 2016. Fast, accurate, and lightweight analysis of BS-treated reads with ERNE 2. BMC Bioinformatics 17: 69. doi: 10.1186/s12859-016-0910-3 PubMed DOI PMC
Puy J, Dvořáková H, Carmona CP, de Bello F, Hiiesalu I, Latzel V. 2018. Improved demethylation in ecological epigenetic experiments: testing a simple and harmless foliar demethylation application. Methods in Ecology and Evolution 9: 744–753. doi: 10.1111/2041-210X.12903 DOI
Quinlan AR, Hall IM. 2010. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics (Oxford, England) 26: 841–842. doi: 10.1093/BIOINFORMATICS/BTQ033 PubMed DOI PMC
R Core Team . 2024. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
Rendina González AP, Preite V, Verhoeven KJF, Latzel V. 2018. Transgenerational effects and epigenetic memory in the clonal plant PubMed DOI PMC
Richards EJ. 2006. Inherited epigenetic variation—revisiting soft inheritance. Nature Reviews: Genetics 7: 395–401. doi: 10.1038/nrg1834 PubMed DOI
Richards CL, Alonso C, Becker C, et al. 2017. Ecological plant epigenetics: evidence from model and non-model species, and the way forward. Ecology Letters 20: 1576–1590. doi: 10.1111/ELE.12858 PubMed DOI
Roach DA, Wulff RD. 1987. Maternal effects in plants. Annual Review of Ecology, Evolution, and Systematics 18: 209–235. doi: 10.1146/annurev.es.18.110187.001233 DOI
Rodríguez BD, Galanti D, Nunn A, et al. 2022. Epigenetic variation in the Lombardy poplar along climatic gradients is independent of genetic structure and persists across clonal reproduction. bioRxiv, p. 2022.11.17.516862. doi: 10.1101/2022.11.17.516862. DOI
Rossiter M. 1996. Incidence and consequences of inherited environmental effects. Annual Review of Ecology, Evolution, and Systematics 27: 451–476. doi: 10.1146/annurev.ecolsys.27.1.451 DOI
Sammarco I, Díez Rodríguez B, Galanti D, et al. 2024. DNA methylation in the wild: epigenetic transgenerational inheritance can mediate adaptation in clones of wild strawberry ( PubMed DOI
Sammarco I, Münzbergová Z, Latzel V. 2023. Response of PubMed DOI PMC
Schulze J, Rufener R, Erhardt A, Stoll P. 2012. The relative importance of sexual and clonal reproduction for population growth in the perennial herb DOI
Urrutia M, Bonet J, Arús P, Monfort A. 2015. A near-isogenic line (NIL) collection in diploid strawberry and its use in the genetic analysis of morphologic, phenotypic and nutritional characters. TAG: Theoretical and Applied Genetics: Theoretische Und Angewandte Genetik 128: 1261–1275. doi: 10.1007/S00122-015-2503-3 PubMed DOI
Van Groenendael JM, Klimeš L, Klimešová J, Hendriks RJJ. 1996. Comparative ecology of clonal plants. Philosophical Transactions of the Royal Society of London: Series B, Biological Sciences 351: 1331–1339. doi: 10.1098/RSTB.1996.0116 DOI
Wang Z, Xie L, Prather CM, Guo H, Han G, Ma C. 2018. What drives the shift between sexual and clonal reproduction of PubMed DOI PMC
Winkler E, Fischer M. 2022. The role of vegetative spread and seed dispersal for optimal life histories of clonal plants: a simulation study. In: Stuefer JF. ed. Ecology and evolutionary biology of clonal plants: proceedings of clone-2000. An International Workshop Held in Obergurgl, Austria, 20–25 August 2000. Springer Netherlands, 59–79. doi: 10.1007/978-94-017-1345-0_4 DOI
Wild J, Kopecký M, Macek M, Šanda M, Jankovec J, Haase T. 2019. Climate at ecologically relevant scales: a new temperature and soil moisture logger for long-term microclimate measurement. Agricultural and Forest Meteorology 268: 40–47. doi: 10.1016/J.AGRFORMET.2018.12.018 DOI
Wolf JB, Wade MJ. 2009. What are maternal effects (and what are they not)? Philosophical Transactions of the Royal Society B: Biological Sciences 364: 1107–1115. doi: 10.1098/rstb.2008.0238 PubMed DOI PMC
Ye D, Hu Y, Song M, et al. 2014. Clonality-climate relationships along latitudinal gradient across China: adaptation of clonality to environments. PLoS One 9: e94009. doi: 10.1371/JOURNAL.PONE.0094009 PubMed DOI PMC
Yu G, Wang L-G, Han Y, He Q-Y. 2012. clusterProfiler: an R package for comparing biological themes among gene clusters. Omics: A Journal of Integrative Biology 16: 284–287. doi: 10.1089/OMI.2011.0118 PubMed DOI PMC
Zemach A, Zilberman D. 2010. Evolution of eukaryotic DNA methylation and the pursuit of safer sex. Current Biology: CB 20: R780–R785. doi: 10.1016/J.CUB.2010.07.007 PubMed DOI
Zhang H, Lang Z, Zhu J-K. 2018. Dynamics and function of DNA methylation in plants. Nature Reviews: Molecular Cell Biology 19: 489–506. doi: 10.1038/s41580-018-0016-z PubMed DOI