Interactive Regulations of Dynamic Methylation and Transcriptional Responses to Recurring Environmental Stresses During Biological Invasions

Abstract

Deoxyribonucleic acid methylation and gene transcription have been proved as two underlying mechanisms involved in rapid plastic response to environmental stresses. However, it remains elusive on how DNA methylation regulates gene transcription under acute and recurring environmental challenges to form the stress memory, further contributing to invasion success during range expansions. Using a model invasive species Ciona robusta, we investigated the regulatory roles of DNA methylation on gene transcription and their contribution to the formation of stress memory at 30 genes under acute and recurring osmotic challenges simulated during the invasion process. We found the bimodal distribution of methylation level for the 68 mCpGs identified across all the genes after challenges, but only five sites were significantly correlated with the expression of their corresponding genes. These genes participated in the biological processes of Ca2+ transport and metabolism of lipid and proline. At the DNA methylation level, we found two early-responding and four tardy-responding sites of stress memory and these sites were functionally related to genes involved in the biosynthesis of proline, metabolism of lipid, and transport of taurine and Ca2+. At the transcriptional level, three tardy-responding and five early-responding memory genes were involved in the transport of ions, regulation of water channels, biosynthesis of taurine, and metabolism of lipid. Altogether, the findings here suggest that DNA methylation and gene transcription should work in concert to facilitate the formation of stress memory, thus further improving the performance of invaders under recurring environmental challenges during biological invasions.

Multidimensional plasticity jointly contributes to rapid acclimation to environmental challenges during biological invasions

“…Gene expression is among the most well-known molecular plastic traits, mainly because transcriptional regulations, which link genotypes and phenotypes, can be immediately induced to cope with environmental stresses during many ecological and evolutionary processes ( Fu et al 2021 ; Josephs 2021 ). Many studies have examined the roles of gene expression plasticity in organismal acclimation and adaptation to various environmental changes.…”

Complementary genomic and epigenomic adaptation to environmental heterogeneity

“…Recent advances have shown that epigenetic variation, particularly for the most commonly studied type in animals – DNA methylation – could not only change phenotypic outcomes but also contribute to evolutionary and adaptive potential of wild populations (Adrian‐Kalchhauser et al, 2020; Hu et al, 2019; Hu & Barrett, 2017). Unlike genetic variation, epigenetic variants can be directly influenced by environmental conditions and provide a faster route to respond to environmental change (Fu et al, 2021; Heckwolf et al, 2020; Richards et al, 2017; Verhoeven et al, 2016). Epigenetic changes can also facilitate evolution when stably transmitted across generations or by increasing genetic mutation rate (Schmid et al, 2018).…”

(Epi)genomic adaptation driven by fine geographical scale environmental heterogeneity after recent biological invasions

“…Therefore, adaptation solely based upon changes in allele frequencies of available genetic variation limits the capacity for wild populations to cope with novel or rapidly changing environments (Hu & Barrett, 2017). Epigenetic changes, such as DNA methylation, can regulate many biological processes such as gene expression to promote phenotypic plasticity without changing underlying genotypes (Fu, Huang, Chen, et al, 2021; Huang et al, 2017). This mechanism can provide a rapid pathway for fine‐tuning phenotypes and “buy time” for genetic adaptation to catch up under rapid environmental changes during the initial stages of colonization (Bogan et al, 2021; Heckwolf et al, 2020).…”