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.
Highlights
Nowadays, species constantly suffer from various environmental challenges derived from multiple interacting factors such as global climate change and frequent anthropogenic activities
By integrating the DNA methylation data and gene expression data of these candidate genes, we aim to study the regulatory roles of DNA methylation on gene transcription and further characterize how such regulatory relationships contribute to rapid response and formation of stress memory under recurring environmental stresses during successful invasions into different saline environments
21 out of 30 candidate genes were methylated and the rest nine genes were completely unmethylated, including genes encoding AQPs, ATPase Na+/K+ transporting subunit (NKA_subunit_α and NKA_subunit_β1β2), taurine transporter 1 (TAUT1), serine hydroxymethyltransferase 1 (SHMT1), and pyrroline-5-carboxylate reductase 1.1 (PYCR1.1), suggesting that the regulation of these genes was independent of DNA methylation (Figure 2; Supplementary Table 1)
Summary
Species constantly suffer from various environmental challenges derived from multiple interacting factors such as global climate change and frequent anthropogenic activities. Taking shippingmediated range expansions as an example, marine invaders adhered to the hull of shipping vessels or sucked into ballast tanks must endure severe environmental challenges during subsequent shipping voyages such as salinity and temperature fluctuations ∼15% and ∼20◦C, respectively (Briski et al, 2013). Such dramatic environmental fluctuations can be recurring during the whole shipping voyage such as during ballast water exchanges and environmental changes in trans-oceans (Ibrahim and El-Naggar, 2012; Gollasch and David, 2021). The underlying mechanisms of rapid environmental adaptation and assimilation still remain elusive
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