Environment-induced heritable variations are common in Arabidopsis thaliana.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
30 May 2024
30 May 2024
Historique:
received:
11
10
2023
accepted:
17
05
2024
medline:
31
5
2024
pubmed:
31
5
2024
entrez:
30
5
2024
Statut:
epublish
Résumé
Parental or ancestral environments can induce heritable phenotypic changes, but whether such environment-induced heritable changes are a common phenomenon remains unexplored. Here, we subject 14 genotypes of Arabidopsis thaliana to 10 different environmental treatments and observe phenotypic and genome-wide gene expression changes over four successive generations. We find that all treatments caused heritable phenotypic and gene expression changes, with a substantial proportion stably transmitted over all observed generations. Intriguingly, the susceptibility of a genotype to environmental inductions could be predicted based on the transposon abundance in the genome. Our study thus challenges the classic view that the environment only participates in the selection of heritable variation and suggests that the environment can play a significant role in generating of heritable variations.
Identifiants
pubmed: 38816460
doi: 10.1038/s41467-024-49024-3
pii: 10.1038/s41467-024-49024-3
doi:
Substances chimiques
DNA Transposable Elements
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
4615Subventions
Organisme : National Natural Science Foundation of China (National Science Foundation of China)
ID : 32371558
Organisme : National Natural Science Foundation of China (National Science Foundation of China)
ID : 32071485
Informations de copyright
© 2024. The Author(s).
Références
Hoffmann, A. A. & Sgrò, C. M. Climate change and evolutionary adaptation. Nature 470, 479–485 (2011).
pubmed: 21350480
doi: 10.1038/nature09670
Scheffers, B. R. et al. The broad footprint of climate change from genes to biomes to people. Science 354, aaf7671 (2016).
pubmed: 27846577
doi: 10.1126/science.aaf7671
Futuyma, D. J. & Kirkpatrick, M. Evolution. (Oxford University Press, 2017).
Agrawal, A. A., Laforsch, C. & Tollrian, R. Transgenerational induction of defences in animals and plants. Nature 401, 60–63 (1999).
doi: 10.1038/43425
Klosin, A., Casas, E., Hidalgo-Carcedo, C., Vavouri, T. & Lehner, B. Transgenerational transmission of environmental information in C. elegans. Science 356, 320–323 (2017).
pubmed: 28428426
doi: 10.1126/science.aah6412
Rechavi, O. et al. Starvation-induced transgenerational inheritance of small RNAs in C. elegans. Cell 158, 277–287 (2014).
pubmed: 25018105
pmcid: 4377509
doi: 10.1016/j.cell.2014.06.020
Yin, J., Zhou, M., Lin, Z., Li, Q. Q. & Zhang, Y.-Y. Transgenerational effects benefit offspring across diverse environments: a meta-analysis in plants and animals. Ecol. Lett. 22, 1976–1986 (2019).
pubmed: 31436014
doi: 10.1111/ele.13373
Galloway, L. F. Parental environmental effects on life history in the herbaceous plant Campanula americana. Ecology 82, 2781–2789 (2001).
doi: 10.2307/2679960
Latzel, V. et al. Parental environmental effects are common and strong, but unpredictable, in Arabidopsis thaliana. New Phytol. 237, 1014–1023 (2023).
pubmed: 36319609
doi: 10.1111/nph.18591
Alvarez, M., Bleich, A. & Donohue, K. Genotypic variation in the persistence of transgenerational responses to seasonal cues. Evolution 74, 2265–2280 (2020).
pubmed: 32383475
doi: 10.1111/evo.13996
Colicchio, J. Transgenerational effects alter plant defence and resistance in nature. J. Evol. Biol. 30, 664–680 (2017).
pubmed: 28102915
pmcid: 5382043
doi: 10.1111/jeb.13042
Groot, M. P. et al. Transgenerational effects of mild heat in Arabidopsis thaliana show strong genotype specificity that is explained by climate at origin. New Phytol. 215, 1221–1234 (2017).
pubmed: 28590553
doi: 10.1111/nph.14642
Munch, S. B. et al. A latitudinal gradient in thermal transgenerational plasticity and a test of theory. Proc. Royal Soc. B 288, 20210797 (2021).
doi: 10.1098/rspb.2021.0797
Gaudinier, A. & Blackman, B. K. Evolutionary processes from the perspective of flowering time diversity. New Phytol. 225, 1883–1898 (2020).
pubmed: 31536639
doi: 10.1111/nph.16205
He, L. et al. DNA methylation-free Arabidopsis reveals crucial roles of DNA methylation in regulating gene expression and development. Nat. Commun. 13, 1335 (2022).
pubmed: 35288562
pmcid: 8921224
doi: 10.1038/s41467-022-28940-2
Roux, F., Touzet, P., Cuguen, J. & Le Corre, V. How to be early flowering: an evolutionary perspective. Trends Plant Sci. 11, 375–381 (2006).
pubmed: 16843035
doi: 10.1016/j.tplants.2006.06.006
Kim, D. H., Doyle, M. R., Sung, S. & Amasino, R. M. Vernalization: winter and the timing of flowering in plants. Annu. Rev. Cell Dev. Biol. 25, 277–299 (2009).
pubmed: 19575660
doi: 10.1146/annurev.cellbio.042308.113411
Searle, I. et al. The transcription factor FLC confers a flowering response to vernalization by repressing meristem competence and systemic signaling in Arabidopsis. Genes Dev. 20, 898–912 (2006).
pubmed: 16600915
pmcid: 1472290
doi: 10.1101/gad.373506
Ratcliffe, O. J., Nadzan, G. C., Reuber, T. L. & Riechmann, J. L. Regulation of flowering in Arabidopsis by an FLC homologue. Plant Physiol. 126, 122–132 (2001).
pubmed: 11351076
pmcid: 102287
doi: 10.1104/pp.126.1.122
Morgan, H. D., Sutherland, H. G. E., Martin, D. I. K. & Whitelaw, E. Epigenetic inheritance at the agouti locus in the mouse. Nat. Genet. 23, 314–318 (1999).
pubmed: 10545949
doi: 10.1038/15490
Ong-Abdullah, M. et al. Loss of Karma transposon methylation underlies the mantled somaclonal variant of oil palm. Nature 525, 533–537 (2015).
pubmed: 26352475
pmcid: 4857894
doi: 10.1038/nature15365
Ito, H. et al. An siRNA pathway prevents transgenerational retrotransposition in plants subjected to stress. Nature 472, 115–119 (2011).
pubmed: 21399627
doi: 10.1038/nature09861
Van’t Hof, A. E. et al. The industrial melanism mutation in British peppered moths is a transposable element. Nature 534, 102–105 (2016).
pubmed: 27251284
doi: 10.1038/nature17951
Schmidt, J. M. et al. Copy number variation and transposable elements feature in recent, ongoing adaptation at the Cyp6g1 locus. PLoS Genet. 6, e1000998 (2010).
pubmed: 20585622
pmcid: 2891717
doi: 10.1371/journal.pgen.1000998
Bourque, G. et al. Ten things you should know about transposable elements. Genome Biol. 19, 199 (2018).
pubmed: 30454069
pmcid: 6240941
doi: 10.1186/s13059-018-1577-z
Modzelewski, A. J. et al. A mouse-specific retrotransposon drives a conserved Cdk2ap1 isoform essential for development. Cell 184, 5541–5558.e5522 (2021).
pubmed: 34644528
pmcid: 8787082
doi: 10.1016/j.cell.2021.09.021
Kapusta, A. et al. Transposable elements are major contributors to the origin, fiversification, and regulation of vertebrate long noncoding RNAs. PLoS Genet. 9, e1003470 (2013).
pubmed: 23637635
pmcid: 3636048
doi: 10.1371/journal.pgen.1003470
Pastuzyn, E. D. et al. The neuronal gene Arc encodes a repurposed retrotransposon Gag protein that mediates intercellular RNA transfer. Cell 172, 275–288.e218 (2018).
pubmed: 29328916
pmcid: 5884693
doi: 10.1016/j.cell.2017.12.024
McClintock, B. The significance of responses of the genome to challenge. Science 226, 792–801 (1984).
pubmed: 15739260
doi: 10.1126/science.15739260
Baduel, P. et al. Genetic and environmental modulation of transposition shapes the evolutionary potential of Arabidopsis thaliana. Genome Biol. 22, 138 (2021).
pubmed: 33957946
pmcid: 8101250
doi: 10.1186/s13059-021-02348-5
Ho, E. K. H. et al. Engines of change: transposable element mutation rates are high and variable within Daphnia magna. PLoS Genet. 17, e1009827 (2021).
pubmed: 34723969
pmcid: 8594854
doi: 10.1371/journal.pgen.1009827
Ratner, V. A., Zabanov, S. A., Kolesnikova, O. V. & Vasilyeva, L. A. Induction of the mobile genetic element Dm-412 transpositions in the Drosophila genome by heat shock treatment. Proc. Natl. Acad. Sci. USA. 89, 5650–5654 (1992).
pubmed: 1319068
pmcid: 49350
doi: 10.1073/pnas.89.12.5650
Strand, D. J. & McDonald, J. F. Copia is transcriptionally responsive to environmental stress. Nucleic Acids Res. 13, 4401–4410 (1985).
pubmed: 2409535
pmcid: 321795
doi: 10.1093/nar/13.12.4401
Aminetzach, Y. T., Macpherson, J. M. & Petrov, D. A. Pesticide resistance via transposition-mediated adaptive gene truncation in Drosophila. Science 309, 764–767 (2005).
pubmed: 16051794
doi: 10.1126/science.1112699
Chung, H. et al. Cis-regulatory elements in the Accord retrotransposon result in tissue-specific expression of the Drosophila melanogaster insecticide resistance gene Cyp6g1. Genetics 175, 1071–1077 (2007).
pubmed: 17179088
pmcid: 1840086
doi: 10.1534/genetics.106.066597
Pimpinelli, S. & Piacentini, L. Environmental change and the evolution of genomes: transposable elements as translators of phenotypic plasticity into genotypic variability. Funct. Ecol. 34, 428–441 (2020).
doi: 10.1111/1365-2435.13497
Kanazawa, A., Liu, B., Kong, F., Arase, S. & Abe, J. Adaptive evolution involving gene duplication and insertion of a novel Ty1/copia-like retrotransposon in soybean. J. Mol. Evol. 69, 164–175 (2009).
pubmed: 19629571
doi: 10.1007/s00239-009-9262-1
Liu, B. et al. Genetic redundancy in soybean photoresponses associated with duplication of the phytochrome A gene. Genetics 180, 995–1007 (2008).
pubmed: 18780733
pmcid: 2567397
doi: 10.1534/genetics.108.092742
Thieme, M. et al. Experimentally heat-induced transposition increases drought tolerance in Arabidopsis thaliana. New Phytol. 236, 182–194 (2022).
pubmed: 35715973
pmcid: 9544478
doi: 10.1111/nph.18322
Yu, A. et al. Roles of Hsp70s in stress responses of microorganisms, plants, and animals. BioMed Res. Int. 2015, 510319 (2015).
pubmed: 26649306
pmcid: 4663327
doi: 10.1155/2015/510319
Berka, M., Kopecká, R., Berková, V., Brzobohatý, B. & Černý, M. Regulation of heat shock proteins 70 and their role in plant immunity. J. Exp. Bot. 73, 1894–1909 (2022).
pubmed: 35022724
pmcid: 8982422
doi: 10.1093/jxb/erab549
Cappucci, U. et al. The Hsp70 chaperone is a major player in stress-induced transposable element activation. Proc. Natl. Acad. Sci. USA. 116, 17943–17950 (2019).
pubmed: 31399546
pmcid: 6731680
doi: 10.1073/pnas.1903936116
Piacentini, L. et al. Transposons, environmental changes, and heritable induced phenotypic variability. Chromosoma 123, 345–354 (2014).
pubmed: 24752783
pmcid: 4107273
doi: 10.1007/s00412-014-0464-y
Barrett, R. D. H. & Schluter, D. Adaptation from standing genetic variation. Trends Ecol. Evol. 23, 38–44 (2008).
pubmed: 18006185
doi: 10.1016/j.tree.2007.09.008
Bitter, M. C., Kapsenberg, L., Gattuso, J. P. & Pfister, C. A. Standing genetic variation fuels rapid adaptation to ocean acidification. Nat. Commun. 10, 5821 (2019).
pubmed: 31862880
pmcid: 6925106
doi: 10.1038/s41467-019-13767-1
Weaver, I. C. G. et al. Epigenetic programming by maternal behavior. Nat. Neurosci. 7, 847–854 (2004).
pubmed: 15220929
doi: 10.1038/nn1276
Wan, Q.-L. et al. Histone H3K4me3 modification is a transgenerational epigenetic signal for lipid metabolism in Caenorhabditis elegans. Nat. Commun. 13, 768 (2022).
pubmed: 35140229
pmcid: 8828817
doi: 10.1038/s41467-022-28469-4
Fanti, L., Piacentini, L., Cappucci, U., Casale, A. M. & Pimpinelli, S. Canalization by selection of de Novo induced mutations. Genetics 206, 1995–2006 (2017).
pubmed: 28576865
pmcid: 5560803
doi: 10.1534/genetics.117.201079
Feiner, N. Accumulation of transposable elements in Hox gene clusters during adaptive radiation of Anolis lizards. Proc. Biol. Sci. 283, 20161555 (2016).
Schrader, L. et al. Transposable element islands facilitate adaptation to novel environments in an invasive species. Nat. Commun. 5, 5495 (2014).
pubmed: 25510865
doi: 10.1038/ncomms6495
Pigliucci, M. Ecology and evolutionary biology of Arabidopsis. Arabidopsis Book 1, e0003 (2002).
pubmed: 22303188
pmcid: 3243336
doi: 10.1199/tab.0003
Durvasula, A. et al. African genomes illuminate the early history and transition to selfing in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA. 114, 5213–5218 (2017).
pubmed: 28473417
pmcid: 5441814
doi: 10.1073/pnas.1616736114
Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).
doi: 10.18637/jss.v067.i01
Fox, J. W., S. An R companion to applied regression. (SAGE, 2019).
Kuznetsova, A., Brockhoff, P. B. & Christensen, R. H. B. lmerTest package: tests in linear mixed effects models. J. Stat. Softw. 82, 1–26 (2017).
doi: 10.18637/jss.v082.i13
Hothorn, T., Bretz, F. & Westfall, P. Simultaneous inference in general parametric models. Biom. J. 50, 346–363 (2008).
pubmed: 18481363
doi: 10.1002/bimj.200810425
Kawakatsu, T. et al. Epigenomic diversity in a global collection of Arabidopsis thaliana accessions. Cell 166, 492–505 (2016).
pubmed: 27419873
pmcid: 5172462
doi: 10.1016/j.cell.2016.06.044
Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).
pubmed: 24695404
pmcid: 4103590
doi: 10.1093/bioinformatics/btu170
Pedersen, B. S., Eyring, K. R., De, S., Yang, I. V. & Schwartz, D. A. Fast and accurate alignment of long bisulfite-seq reads. Preprint at arXiv https://doi.org/10.48550/arXiv.1401.1129 (2014).
Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).
pubmed: 19505943
pmcid: 2723002
doi: 10.1093/bioinformatics/btp352
Quadrana, L. et al. The Arabidopsis thaliana mobilome and its impact at the species level. eLife 5, e15716 (2016).
pubmed: 27258693
pmcid: 4917339
doi: 10.7554/eLife.15716
Hadley, W. ggplot2: elegant graphics for data analysis. (Springer Cham, 2016).
Rio, D. C., Ares, M. Jr., Hannon, G. J. & Nilsen, T. W. Purification of RNA using TRIzol (TRI reagent). Cold Spring Harb. Protoc. 2010, pdb.prot5439 (2010).
pubmed: 20516177
doi: 10.1101/pdb.prot5439
Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21 (2013).
pubmed: 23104886
doi: 10.1093/bioinformatics/bts635
Pertea, G. & Pertea, M. GFF Utilities: GffRead and GffCompare. F1000Res. 9, 304 (2020). 304.
doi: 10.12688/f1000research.23297.1
Liao, Y., Smyth, G. K. & Shi, W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30, 923–930 (2014).
pubmed: 24227677
doi: 10.1093/bioinformatics/btt656
Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).
pubmed: 25516281
pmcid: 4302049
doi: 10.1186/s13059-014-0550-8
Yu, G. C., Wang, L. G., Han, Y. Y. & He, Q. Y. clusterProfiler: an R package for comparing biological themes among gene clusters. Omics 16, 284–287 (2012).
pubmed: 22455463
pmcid: 3339379
doi: 10.1089/omi.2011.0118
Lawrence, M. et al. Software for computing and annotating genomic ranges. PLoS Comput. Biol. 9, e1003118 (2013).
pubmed: 23950696
pmcid: 3738458
doi: 10.1371/journal.pcbi.1003118