Abstract
Whether induced epigenetic changes contribute to long-term adaptation remains controversial. Recent studies indicate that environmentally cued changes in gene body methylation (gbM) can facilitate acclimatization. However, such changes are often associated with genetic variation and their contribution to long-term stress adaptation remains unclear. Using whole-genome bisulfite sequencing, we examined evolutionary gains and losses of gbM in mangroves that adapted to extreme intertidal environments. We treated mangrove seedlings with salt stress, and investigated expression changes in relation with stress-induced or evolutionarily-acquired gbM changes. Evolution and function of gbM was compared with that of genetic variation. Mangroves gained much more gbM than their terrestrial relatives, mainly through convergent evolution. Genes that convergently gained gbM during evolution are more likely to become methylated in response to salt stress in species where they are normally not marked. Stress-induced and evolutionarily convergent gains of gbM both correlate with reduction in expression variation, conferring genome-wide expression robustness under salt stress. Moreover, convergent gbM evolution is uncoupled with convergent sequence evolution. Our findings suggest that transgenerational inheritance of acquired gbM helps environmental canalization of gene expression, facilitating long-term stress adaptation of mangroves in the face of a severe reduction in genetic diversity.
Highlights
Plants are constantly exposed to chronic or recurring environmental stresses across generations (Franks and Hoffmann, 2012; Lamke and Baurle, 2017)
Plant cytosine DNA methylation occurs in three sequence contexts: CG, CHG, and CHH (Henderson and Jacobsen, 2007)
Pairwise correlation analysis of the methylation levels among replicates showed good reproducibility in all three sequence contexts for all the mangrove species (Pearson’s correlation, r = 0.94–0.99, all P < 2.2 × 10−16; Supplementary Figure 2). Given their history of stress adaptation, we expected that mangroves have acquired more methylated CG sites than their non-mangrove relatives since environmental stress is known to accelerate the accumulation of epimutations (Jiang et al, 2014)
Summary
Plants are constantly exposed to chronic or recurring environmental stresses across generations (Franks and Hoffmann, 2012; Lamke and Baurle, 2017). Environmentally-induced epigenetic changes such as DNA methylation and small RNAs may contribute to phenotypic variations by modifying gene expression. As a mechanism connecting the genome to its environment, epigenetics plays a dual role in variability by either increasing plasticity or suppressing variation. The heritable epigenetic responses, known as stress memory, may increase transgenerational phenotypic plasticity (Kinoshita and Seki, 2014; He and Li, 2018; TurgutKara et al, 2020). Increased variability might increase fitness and enable rapid adaptation to environmental fluctuations (Mirouze and Paszkowski, 2011; Wibowo et al, 2016; Chang et al, 2020). Epigenetics is often appreciated for its contribution to acclimation (Richards et al, 2017; Li et al, 2018; Liew et al, 2018).
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