DNA methylation and gene transcription act cooperatively in driving the adaptation of a marine diatom to global change

Jiaofeng Wan, Yunyue Zhou, John Beardall, John A. Raven, Jiamin Lin, Jiali Huang, Yucong Lu, Shiman Liang, Mengcheng Ye, Mengting Xiao, Jingyuan Zhao, Xiaoying Dai, Jianrong Xia, Peng Jin (Lead / Corresponding author)

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    Abstract

    Genetic changes together with epigenetic modifications such as DNA methylation have been demonstrated to regulate many biological processes and thereby govern the response of organisms to environmental changes. However, how DNA methylation might act cooperatively with gene transcription and thereby mediate the long-term adaptive responses of marine microalgae to global change is virtually unknown. Here we performed a transcriptomic analysis, and a whole-genome bisulfite sequencing, along with phenotypic analysis of a model marine diatom Phaeodactylum tricornutum adapted for two years to high CO2 and/or warming conditions. Our results show that the methylated islands (peaks of methylation) mCHH were positively correlated with expression of genes in the sub-region of the gene body when the populations were grown under high CO2 or its combination with warming for ~2 years. We further identified the differentially expressed genes (DEGs) and hence the metabolic pathways in which they function, at the transcriptomics level in differentially methylated regions (DMRs). Although DEGs in DMRs contributed only 18-24% of the total DEGs, we found that those DEGs acted cooperatively with DNA methylation and then regulated key processes such as central carbon metabolism, amino acid metabolism, ribosome biogenesis, terpenoid backbone biosynthesis, and degradation of misfolded proteins. Taken together, by integrating transcriptomic, epigenetic and phenotypic analysis, our study provides evidence for DNA methylation acting cooperatively with gene transcription to contribute to the adaptation of microalgae to global changes.

    Original languageEnglish
    Pages (from-to)4259–4276
    Number of pages18
    JournalJournal of Experimental Botany
    Volume74
    Issue number14
    Early online date26 Apr 2023
    DOIs
    Publication statusPublished - 3 Aug 2023

    Keywords

    • DNA methylation
    • transcriptomics
    • global change
    • diatom
    • high CO2
    • warming
    • adaptation

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