Examining the Role of DNA Methylation in Transcriptomic Plasticity of Early Stage Sea Urchins: Developmental and Maternal Effects in a Kelp Forest Herbivore

Abstract

Gene expression plasticity can confer physiological plasticity in response to the environment. However, whether epigenetic marks contribute to the dynamics of gene expression is still not well described in most marine invertebrates. Here, we explored the extent and molecular basis of intra-and intergenerational plasticity in the purple sea urchin, Strongylocentrotus purpuratus, by examining relationships between changes in DNA methylation, transcription, and embryo spicule length. Adult urchins were conditioned in the lab for 4 months to treatments that represent upwelling (∼1200 µatm pCO 2 , 13 • C) and non-upwelling conditions (∼500 µatm pCO 2 , 17 • C). Embryos spawned from conditioned adults were reared in either the same adult treatment or the reciprocal condition. Maternal conditioning resulted in significantly differentially methylated CpG sites and differential gene expression in embryos, despite no evidence of maternal effects on embryo spicule length. In contrast, conditions experienced during development resulted in significant differences in embryo spicule length. Intragenerational plasticity in spicule length was strongly correlated to transcriptomic plasticity, despite low levels of intragenerational plasticity in CpG methylation. We find plasticity in DNA methylation and gene expression in response to different maternal environments and these changes have similarities across broad functional groups of genes; yet exhibit little overlap on a gene-by-gene basis. Our results suggest that different forms of environmentally induced plasticity are observable across different time scales and that DNA methylation dynamics may be uncoupled from fast transcriptional responses to the environment and whole organism traits. Overall, this study illuminates the extent to which environmental differences can induce both intraand intergenerational phenotypic plasticity in a common kelp forest herbivore.

Gene regulation by DNA methylation is contingent on chromatin accessibility during transgenerational plasticity in the purple sea urchin

“…CpG methylation is more abundant in S. purpuratus relative to most invertebrates, likely because of its phylogenetic position as a basal deuterostome (Regev, Lamb, & Jablonka, 1998). TGP linked to maternal effects have been observed in S. purpuratus for traits including egg protein content, larval body size, gene expression, and DNA methylation Strader et al, 2020;Strader, Wong, Kozal, Leach, & Hofmann, 2019;Wong, Johnson, Kelly, & Hofmann, 2018;Wong, Kozal, Leach, Hoshijima, & Hofmann, 2019) alongside similar observations in congeneric Strongylocentrotus spp. (Ding et al, 2019) and other urchin genera (Clark et al, 2019;Karelitz, Lamare, Patel, Gemmell, & Uthicke, 2019;Wong & Hofmann, 2021).…”

“…(Downey-Wall et al, 2020;Johnson, Sirovy, Casas, La Peyre, & Kelly, 2020), and arthropods (Bonasio et al, 2012;Gatzmann et al, 2018;Glastad, Gokhale, Liebig, & Goodisman, 2016;Kvist et al, 2018) with exceptions to this pattern evident in some species and cell types (de Mendoza et al, 2019;Flores et al, 2012;Wang, Song, et al, 2021). By contrast, inducible changes in invertebrate gene expression in response to environmental variation have frequently possessed insignificant relationships with differential GBM (Arsenault et al, 2018;Dixon et al, 2018;Downey-Wall et al, 2020;Strader et al, 2020). In some arthropods, molluscs, and nematodes, there is evidence that GBM aids in regulating alternative splicing and exon skipping (Flores et al, 2012;Gao et al, 2012;Li-Byarlay et al, 2013;Libbrecht, Oxley, Keller, & Kronauer, 2016;Song, Li, & Zhang, 2017).…”

“…To elucidate the gene regulatory roles of differential methylation during TGP, we quantified changes in DNA methylation, gene expression, and alternative splicing in prism larvae induced by maternal exposure to ecologically relevant, abiotic stress in S. purpuratus using data from Strader et al, 2020 initially exhibiting limited overlap between DM and DE genes and robust annotations of chromatin accessibility during the S. purpuratus prism stage (Kudtarkar & Cameron, 2017). We then modeled differential expression and splicing as functions of DM, genic feature type, and chromatin accessibility to test the hypothesis that invertebrate DNA methylation's regulatory role is contingent upon additional genomic and epigenomic factors and reveal epigenetic interactions influencing gene expression during TGP.…”

Gene Expression Changes after Parental Exposure to Metals in the Sea Urchin Affect Timing of Genetic Programme of Embryo Development

“…Recently, several lines of evidence suggested that maternal exposure to different conditions affected the DNA methylation status of the offspring [ 83 , 84 ]. In particular, several genes involved in mechanisms of transcriptional regulation, including DNA modification and metabolism, as well in protein ubiquitination, were identified as differentially methylated in the offspring.…”

Maternal effects in gene expression of interspecific coral hybrids

“…Several studies have reported maternal effects in gene expression including in a perennial herb (Videvall et al, 2016), coral (Dixon et al, 2015), pipefish (Beemelmanns & Roth, 2016) and stickleback (Metzger & Schulte, 2016;Mommer & Bell, 2014;Shama et al, 2016), and maternal environments have also been demonstrated to affect DNA methylation of sea urchin (Strader et al, 2020). Videvall et al (2016) showed that gene expression patterns were distinct between parental populations of 12-week-old seedling of the perennial herb Arabidopsis lyrata, and expression in intraspecific hybrids was frequently more similar to that of the maternal than paternal population.…”