1.Merilä, J. & Hendry, A. P. Climate change, adaptation, and phenotypic plasticity: the problem and the evidence. Evol. Appl. 7, 1–14. https://doi.org/10.1111/eva.12137 (2014).Article
PubMed
PubMed Central
Google Scholar
2.Reusch, T. B. Climate change in the oceans: evolutionary versus phenotypically plastic responses of marine animals and plants. Evol. Appl. 7, 104–122. https://doi.org/10.1111/eva.12109 (2014).Article
PubMed
Google Scholar
3.Pazzaglia, J., Reusch, T. B., Terlizzi, A., Marín‐Guirao, L. & Procaccini, G. Phenotypic plasticity under rapid global changes: the intrinsic force for future seagrasses survival. Evol. Appl. (2021).4.Lopez-Maury, L., Marguerat, S. & Baehler, J. Tuning gene expression to changing environments: from rapid responses to evolutionary adaptation. Nat. Rev. Genet. 9, 583–593 (2008).CAS
PubMed
Article
Google Scholar
5.Mäkinen, H., Papakostas, S., Vøllestad, L. A., Leder, E. H. & Primmer, C. R. Plastic and evolutionary gene expression responses are correlated in European grayling (Thymallus thymallus) subpopulations adapted to different thermal environments. J. Hered. 107, 82–89 (2016).PubMed
Article
CAS
Google Scholar
6.Alonso, C., Pérez, R., Bazaga, P., Medrano, M. & Herrera, C. M. MSAP markers and global cytosine methylation in plants: a literature survey and comparative analysis for a wild-growing species. Mol. Ecol. Resour. 16, 80–90 (2016).CAS
PubMed
Article
Google Scholar
7.Jeremias, G. et al. Synthesizing the role of epigenetics in the response and adaptation of species to climate change in freshwater ecosystems. Mol. Ecol. 27, 2790–2806 (2018).PubMed
Article
Google Scholar
8.Nicotra, A. B. et al. Adaptive plasticity and epigenetic variation in response to warming in an Alpine plant. Ecol. Evol. 5, 634–647 (2015).PubMed
PubMed Central
Article
Google Scholar
9.Kelly, S., Panhuis, T. & Stoehr, A. (2012).10.Thorson, J. L. et al. Epigenetics and adaptive phenotypic variation between habitats in an asexual snail. Sci. Rep. 7, 1–11 (2017).CAS
Article
Google Scholar
11.Rey, O., Danchin, E., Mirouze, M., Loot, C. & Blanchet, S. Adaptation to global change: a transposable element–epigenetics perspective. Trends Ecol. Evol. 31, 514–526. https://doi.org/10.1016/j.tree.2016.03.013 (2016).Article
PubMed
Google Scholar
12.Law, J. A. & Jacobsen, S. E. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat. Rev. Genet. 11, 204–220 (2010).CAS
PubMed
PubMed Central
Article
Google Scholar
13.Zemach, A., McDaniel, I. E., Silva, P. & Zilberman, D. Genome-wide evolutionary analysis of eukaryotic DNA methylation. Science 328, 916–919 (2010).CAS
PubMed
Article
ADS
Google Scholar
14.Niederhuth, C. E. et al. Widespread natural variation of DNA methylation within angiosperms. Genome Biol. 17, 1–19 (2016).Article
CAS
Google Scholar
15.Zhang, X. et al. Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell 126, 1189–1201 (2006).CAS
Article
Google Scholar
16.Bewick, A. J. et al. On the origin and evolutionary consequences of gene body DNA methylation. Proc. Natl. Acad. Sci. 113, 9111–9116 (2016).CAS
PubMed
PubMed Central
Article
Google Scholar
17.Bewick, A. J. & Schmitz, R. J. Gene body DNA methylation in plants. Curr. Opin. Plant Biol. 36, 103–110 (2017).CAS
PubMed
PubMed Central
Article
Google Scholar
18.Sarda, S., Zeng, J., Hunt, B. G. & Yi, S. V. The evolution of invertebrate gene body methylation. Mol. Biol. Evol. 29, 1907–1916 (2012).CAS
PubMed
Article
Google Scholar
19.Takuno, S. & Gaut, B. S. Body-methylated genes in Arabidopsis thaliana are functionally important and evolve slowly. Mol. Biol. Evol. 29, 219–227 (2012).CAS
PubMed
Article
Google Scholar
20.Takuno, S. & Gaut, B. S. Gene body methylation is conserved between plant orthologs and is of evolutionary consequence. Proc. Natl. Acad. Sci. 110, 1797–1802 (2013).CAS
PubMed
PubMed Central
Article
ADS
Google Scholar
21.Takuno, S., Ran, J.-H. & Gaut, B. S. Evolutionary patterns of genic DNA methylation vary across land plants. Nat. Plants 2, 1–7 (2016).Article
CAS
Google Scholar
22.Wendte, J. M. et al. Epimutations are associated with CHROMOMETHYLASE 3-induced de novo DNA methylation. Elife 8, e47891 (2019).CAS
PubMed
PubMed Central
Article
Google Scholar
23.Aceituno, F. F., Moseyko, N., Rhee, S. Y. & Gutiérrez, R. A. The rules of gene expression in plants: organ identity and gene body methylation are key factors for regulation of gene expression in Arabidopsis thaliana. BMC Genomics 9, 438 (2008).PubMed
PubMed Central
Article
CAS
Google Scholar
24.Elango, N., Hunt, B. G., Goodisman, M. A. & Soojin, V. Y. DNA methylation is widespread and associated with differential gene expression in castes of the honeybee, Apis mellifera. Proc. Natl. Acad. Sci. 106, 11206–11211 (2009).CAS
PubMed
PubMed Central
Article
ADS
Google Scholar
25.Gavery, M. R. & Roberts, S. B. DNA methylation patterns provide insight into epigenetic regulation in the Pacific oyster (Crassostrea gigas). BMC Genomics 11, 1–9 (2010).Article
CAS
Google Scholar
26.Zilberman, D., Gehring, M., Tran, R. K., Ballinger, T. & Henikoff, S. Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nat. Genet. 39, 61–69 (2007).CAS
PubMed
Article
Google Scholar
27.Coleman-Derr, D. & Zilberman, D. in Cold Spring Harbor symposia on quantitative biology. 147–154 (Cold Spring Harbor Laboratory Press).28.Kim, M. Y. & Zilberman, D. DNA methylation as a system of plant genomic immunity. Trends Plant Sci. 19, 320–326 (2014).CAS
PubMed
Article
Google Scholar
29.Muyle, A. & Gaut, B. S. Loss of gene body methylation in Eutrema salsugineum is associated with reduced gene expression. Mol. Biol. Evol. 36, 155–158 (2019).CAS
PubMed
Article
Google Scholar
30.Roberts, S. B. & Gavery, M. R. Is there a relationship between DNA methylation and phenotypic plasticity in invertebrates?. Front. Physiol. 2, 116 (2012).PubMed
PubMed Central
Article
Google Scholar
31.Dimond, J. L. & Roberts, S. B. Germline DNA methylation in reef corals: patterns and potential roles in response to environmental change. Mol. Ecol. 25, 1895–1904 (2016).CAS
PubMed
Article
Google Scholar
32.Dixon, G. B., Bay, L. K. & Matz, M. V. Bimodal signatures of germline methylation are linked with gene expression plasticity in the coral Acropora millepora. BMC Genomics 15, 1–11 (2014).Article
CAS
Google Scholar
33.Bird, A. P. DNA methylation and the frequency of CpG in animal DNA. Nucleic Acids Res. 8, 1499–1504 (1980).CAS
PubMed
PubMed Central
Article
Google Scholar
34.Sved, J. & Bird, A. The expected equilibrium of the CpG dinucleotide in vertebrate genomes under a mutation model. Proc. Natl. Acad. Sci. 87, 4692–4696 (1990).CAS
PubMed
PubMed Central
Article
ADS
Google Scholar
35.Suzuki, M. M., Kerr, A. R., De Sousa, D. & Bird, A. CpG methylation is targeted to transcription units in an invertebrate genome. Genome Res. 17, 625–631 (2007).CAS
PubMed
PubMed Central
Article
Google Scholar
36.Weber, M. et al. Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome. Nat. Genet. 39, 457–466 (2007).CAS
PubMed
Article
Google Scholar
37.Glastad, K., Hunt, B. G., Yi, S. & Goodisman, M. DNA methylation in insects: on the brink of the epigenomic era. Insect Mol. Biol. 20, 553–565 (2011).CAS
PubMed
Article
PubMed Central
Google Scholar
38.Aliaga, B., Bulla, I., Mouahid, G., Duval, D. & Grunau, C. Universality of the DNA methylation codes in Eucaryotes. Sci. Rep. 9, 1–11 (2019).CAS
Article
Google Scholar
39.Asselman, J., De Coninck, D. I., Pfrender, M. E. & De Schamphelaere, K. A. Gene body methylation patterns in Daphnia are associated with gene family size. Genome Biol Evol 8, 1185–1196 (2016).CAS
PubMed
PubMed Central
Article
Google Scholar
40.Park, J. et al. Comparative analyses of DNA methylation and sequence evolution using Nasonia genomes. Mol. Biol. Evol. 28, 3345–3354 (2011).CAS
PubMed
PubMed Central
Article
Google Scholar
41.Olsen, J. L. et al. The genome of the seagrass Zostera marina reveals angiosperm adaptation to the sea. Nature 530, 331–335. https://doi.org/10.1038/nature16548 (2016).CAS
Article
PubMed
ADS
Google Scholar
42.Costanza, R. et al. Changes in the global value of ecosystem services. Glob. Environ. Chang. 26, 152–158. https://doi.org/10.1016/j.gloenvcha.2014.04.002 (2014).Article
Google Scholar
43.Nordlund, L. M., Koch, E. W., Barbier, E. B. & Creed, J. C. Correction: Seagrass ecosystem services and their variability across genera and geographical regions. PLoS ONE 12, e0169942 (2017).PubMed
PubMed Central
Article
Google Scholar
44.Orth, R. J. et al. A global crisis for seagrass ecosystems. Bioscience 56, 987–996. https://doi.org/10.1641/0006-3568(2006)56[987:agcfse]2.0.co;2 (2006).Article
Google Scholar
45.Waycott, M. et al. Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proc. Natl. Acad. Sci. 106, 12377–12381. https://doi.org/10.1073/pnas.0905620106 (2009).Article
PubMed
PubMed Central
ADS
Google Scholar
46.Koch, M., Bowes, G., Ross, C. & Zhang, X. H. Climate change and ocean acidification effects on seagrasses and marine macroalgae. Glob. Change Biol. 19, 103–132. https://doi.org/10.1111/j.1365-2486.2012.02791.x (2013).Article
ADS
Google Scholar
47.Marbà, N. & Duarte, C. M. Mediterranean warming triggers seagrass (Posidonia oceanica) shoot mortality. Glob. Change Biol. 16, 2366–2375. https://doi.org/10.1111/j.1365-2486.2009.02130.x (2010).Article
ADS
Google Scholar
48.Thomson, J. A. et al. Extreme temperatures, foundation species, and abrupt ecosystem change: an example from an iconic seagrass ecosystem. Glob. Change Biol. 21, 1463–1474. https://doi.org/10.1111/gcb.12694 (2014).Article
ADS
Google Scholar
49.Maxwell, P. S. et al. Phenotypic plasticity promotes persistence following severe events: physiological and morphological responses of seagrass to flooding. J. Ecol. 102, 54–64 (2014).Article
Google Scholar
50.Marín-Guirao, L., Ruiz, J. M., Dattolo, E., Garcia-Munoz, R. & Procaccini, G. Physiological and molecular evidence of differential short-term heat tolerance in Mediterranean seagrasses. Sci. Rep. 6, 28615. https://doi.org/10.1038/srep28615 (2016).CAS
Article
PubMed
PubMed Central
ADS
Google Scholar
51.Sandoval-Gil, J. M., Ruiz, J. M., Marin-Guirao, L., Bernardeau-Esteller, J. & Sanchez-Lizaso, J. L. Ecophysiological plasticity of shallow and deep populations of the Mediterranean seagrasses Posidonia oceanica and Cymodocea nodosa in response to hypersaline stress. Mar. Environ. Res. 95, 39–61. https://doi.org/10.1016/j.marenvres.2013.12.011 (2014).CAS
Article
PubMed
Google Scholar
52.Franssen, S. et al. Transcriptomic resilience to global warming in the seagrass Zostera marina, a marine foundation species. Proc. Natl. Acad. Sci. USA 108, 19276–19281 (2011).CAS
PubMed
PubMed Central
Article
ADS
Google Scholar
53.Jueterbock, A. et al. Phylogeographic differentiation versus transcriptomic adaptation to warm temperatures in Zostera marina, a globally important seagrass. Mol. Ecol. 25, 5396–5411 (2016).CAS
PubMed
Article
Google Scholar
54.Marín-Guirao, L., Entrambasaguas, L., Dattolo, E., Ruiz, J. M. & Procaccini, G. Molecular mechanisms behind the physiological resistance to intense transient warming in an iconic marine plant. Front. Plant Sci. https://doi.org/10.3389/fpls.2017.01142 (2017).Article
PubMed
PubMed Central
Google Scholar
55.Lee, H. et al. The genome of a southern hemisphere seagrass species (Zostera muelleri). Plant Physiol. (2016).56.Greco, M., Chiappetta, A., Bruno, L. & Bitonti, M. B. Effects of light deficiency on genome methylation in Posidonia oceanica. Mar. Ecol. Prog. Ser. 473, 103–114 (2013).CAS
Article
ADS
Google Scholar
57.Greco, M., Chiappetta, A., Bruno, L. & Bitonti, M. B. In Posidonia oceanica cadmium induces changes in DNA methylation and chromatin patterning. J. Exp. Bot. 63, 695–709. https://doi.org/10.1093/jxb/err313 (2012).CAS
Article
PubMed
Google Scholar
58.Ruocco, M., De Luca, P., Marín-Guirao, L. & Procaccini, G. Differential leaf age-dependent thermal plasticity in the keystone seagrass Posidonia oceanica. Front. Plant Sci. https://doi.org/10.3389/fpls.2019.01556 (2019).Article
PubMed
PubMed Central
Google Scholar
59.Ruocco, M., Marín-Guirao, L. & Procaccini, G. Within- and among-leaf variations in photo-physiological functions, gene expression and DNA methylation patterns in the large-sized seagrass Posidonia oceanica. Mar. Biol. 166, 24. https://doi.org/10.1007/s00227-019-3482-8 (2019).CAS
Article
Google Scholar
60.Ruocco, M. et al. A king and vassals’ tale: Molecular signatures of clonal integration in Posidonia oceanica under chronic light shortage. J. Ecol. (2020).61.Jueterbock, A. et al. The seagrass methylome is associated with variation in photosynthetic performance among clonal shoots. Front. Plant Sci. 11 (2020).62.Marín-Guirao, L. et al. Carbon economy of Mediterranean seagrasses in response to thermal stress. Mar. Pollut. Bull. 135, 617–629 (2018).PubMed
Article
CAS
Google Scholar
63.Beca-Carretero, P. et al. Effects of an experimental heat wave on fatty acid composition in two Mediterranean seagrass species. Mar. Pollut. Bull. 134, 27–37 (2018).CAS
PubMed
Article
Google Scholar
64.Angers, B., Castonguay, E. & Massicotte, R. Environmentally induced phenotypes and DNA methylation: how to deal with unpredictable conditions until the next generation and after. Mol. Ecol. 19, 1283–1295 (2010).CAS
PubMed
Article
Google Scholar
65.Dubin, M. J. et al. DNA methylation in Arabidopsis has a genetic basis and shows evidence of local adaptation. Elife 4, e05255 (2015).PubMed
PubMed Central
Article
Google Scholar
66.Kawakatsu, T. et al. Epigenomic diversity in a global collection of Arabidopsis thaliana accessions. Cell 166, 492–505 (2016).CAS
PubMed
PubMed Central
Article
Google Scholar
67.Smith, Z. D. & Meissner, A. DNA methylation: roles in mammalian development. Nat. Rev. Genet. 14, 204–220 (2013).CAS
PubMed
PubMed Central
Article
Google Scholar
68.Serres-Giardi, L., Belkhir, K., David, J. & Glémin, S. Patterns and evolution of nucleotide landscapes in seed plants. Plant Cell 24, 1379–1397 (2012).CAS
PubMed
PubMed Central
Article
Google Scholar
69.Tatarinova, T., Elhaik, E. & Pellegrini, M. Cross-species analysis of genic GC3 content and DNA methylation patterns. Genome Biol. Evol. 5, 1443–1456 (2013).CAS
PubMed
PubMed Central
Article
Google Scholar
70.Vining, K. J. et al. Dynamic DNA cytosine methylation in the Populus trichocarpa genome: tissue-level variation and relationship to gene expression. BMC Genomics 13, 27 (2012).CAS
PubMed
PubMed Central
Article
Google Scholar
71.Lyko, F. et al. The honey bee epigenomes: differential methylation of brain DNA in queens and workers. PLoS Biol 8, 1506 (2010).Article
CAS
Google Scholar
72.Cortijo, S., Aydin, Z., Ahnert, S. & Locke, J. C. Widespread inter-individual gene expression variability in Arabidopsis thaliana. Mol. Syst. Biol. 15, e8591 (2019).PubMed
PubMed Central
Article
Google Scholar
73.Procaccini, G., Olsen, J. L. & Reusch, T. B. H. Contribution of genetics and genomics to seagrass biology and conservation. J. Exp. Mar. Biol. Ecol. 350, 234–259. https://doi.org/10.1016/j.jembe.2007.05.035 (2007).CAS
Article
Google Scholar
74.Alberto, F. et al. Genetic differentiation and secondary contact zone in the seagrass Cymodocea nodosa across the Mediterranean-Atlantic transition region. J. Biogeogr. 35, 1279–1294 (2008).Article
Google Scholar
75.Becker, C. et al. Spontaneous epigenetic variation in the Arabidopsis thaliana methylome. Nature 480, 245–249 (2011).CAS
PubMed
PubMed Central
Article
ADS
Google Scholar
76.Schmitz, R. J. et al. Patterns of population epigenomic diversity. Nature 495, 193–198 (2013).CAS
PubMed
PubMed Central
Article
ADS
Google Scholar
77.Yi, S. V. Insights into epigenome evolution from animal and plant methylomes. Genome Biol. Evol. 9, 3189–3201 (2017).CAS
PubMed
PubMed Central
Article
Google Scholar
78.Jahnke, M. et al. Adaptive responses along a depth and a latitudinal gradient in the endemic seagrass Posidonia oceanica. Heredity https://doi.org/10.1038/s41437-018-0103-0 (2018).Article
PubMed
PubMed Central
Google Scholar
79.Tuya, F. et al. Biogeographical scenarios modulate seagrass resistance to small-scale perturbations. J. Ecol. 107, 1263–1275 (2019).Article
Google Scholar
80.Gao, G. et al. Comparison of the heat stress induced variations in DNA methylation between heat-tolerant and heat-sensitive rapeseed seedlings. Breed. Sci. 64, 125–133 (2014).CAS
PubMed
PubMed Central
Article
Google Scholar
81.Dowen, R. H. et al. Widespread dynamic DNA methylation in response to biotic stress. Proc. Natl. Acad. Sci. 109, E2183–E2191 (2012).CAS
PubMed
PubMed Central
Article
Google Scholar
82.Wada, Y., Miyamoto, K., Kusano, T. & Sano, H. Association between up-regulation of stress-responsive genes and hypomethylation of genomic DNA in tobacco plants. Mol. Genet. Genomics 271, 658–666 (2004).CAS
PubMed
Article
Google Scholar
83.Yaish, M. W., Colasanti, J. & Rothstein, S. J. The role of epigenetic processes in controlling flowering time in plants exposed to stress. J. Exp. Bot. 62, 3727–3735 (2011).CAS
PubMed
Article
Google Scholar
84.Secco, D. et al. Stress induced gene expression drives transient DNA methylation changes at adjacent repetitive elements. Elife 4, e09343 (2015).PubMed Central
Article
PubMed
Google Scholar
85.Marín-Guirao, L., Entrambasaguas, L., Ruiz, J. M. & Procaccini, G. Heat-stress induced flowering can be a potential adaptive response to ocean warming for the iconic seagrass Posidonia oceanica. Mol. Ecol. 28, 2486–2501. https://doi.org/10.1111/mec.15089 (2019).Article
PubMed
Google Scholar
86.Nguyen, H. M. et al. Stress memory in seagrasses: first insight into the effects of thermal priming and the role of epigenetic modifications. Front. Plant Sci. 11, 494 (2020).PubMed
PubMed Central
Article
Google Scholar
87.Pikaard, C. S. & Scheid, O. M. Epigenetic regulation in plants. Cold Spring Harbor Perspect. Biol. 6, a019315 (2014).Article
CAS
Google Scholar
88.Yu, Y. et al. Cytosine methylation alteration in natural populations of Leymus chinensis induced by multiple abiotic stresses. PLoS ONE 8, e55772 (2013).CAS
PubMed
PubMed Central
Article
ADS
Google Scholar
89.Liu, R. & Lang, Z. The mechanism and function of active DNA demethylation in plants. J. Integr. Plant. Biol. 62, 148–159 (2020).CAS
PubMed
Article
Google Scholar
90.Xu, X. et al. A CRISPR-based approach for targeted DNA demethylation. Cell Discovery 2, 1–12 (2016).
Google Scholar
91.Arnaud-Haond, S. et al. Implications of extreme life span in clonal organisms: millenary clones in meadows of the threatened seagrass Posidonia oceanica. PLoS ONE 7, e30454. https://doi.org/10.1371/journal.pone.0030454 (2012).CAS
Article
PubMed
PubMed Central
ADS
Google Scholar
92.Mascaró, O., Romero, J. & Pérez, M. Seasonal uncoupling of demographic processes in a marine clonal plant. Estuar. Coast. Shelf Sci. 142, 23–31 (2014).Article
ADS
Google Scholar
93.Olesen, B., Enríquez, S., Duarte, C. M. & Sand-Jensen, K. Depth-acclimation of photosynthesis, morphology and demography of Posidonia oceanica and Cymodocea nodosa in the Spanish Mediterranean Sea. Mar. Ecol. Prog. Ser. 236, 89–97. https://doi.org/10.3354/meps236089 (2002).Article
ADS
Google Scholar
94.Ruocco, M. et al. Genomewide transcriptional reprogramming in the seagrass Cymodocea nodosa under experimental ocean acidification. Mol. Ecol. 26, 4241–4259. https://doi.org/10.1111/mec.14204 (2017).CAS
Article
PubMed
Google Scholar
95.Fraley, C. & Raftery, A. E. Model-based methods of classification: using the mclust software in chemometrics. J. Stat. Softw. 18, 1–13 (2007).Article
Google Scholar
96.R Core Team (ISBN 3-900051-07-0, 2012).97.Benaglia, T., Chauveau, D., Hunter, D., Young, D. mixtools: an R package for analyzing finite mixture models (2009).98.Langmead, B., Trapnell, C., Pop, M. & Salzberg, S. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25 (2009).PubMed
PubMed Central
Article
CAS
Google Scholar
99.Li, B. & Dewey, C. N. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformat. 12, 323 (2011).CAS
Article
Google Scholar
100.Robinson, M. D., McCarthy, D. J. & Smyth, G. K. edgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139–140. https://doi.org/10.1093/bioinformatics/btp616 (2010).CAS
Article
PubMed
PubMed Central
Google Scholar More