Convergent increase in gene body methylation contributes to gene expression homeostasis in mangroves. Mangroves

Gene body methylation (gbM) is a common epigenetic modification in plants but its function remains unclear. One possibility is that gbM may help buffer gene expression variation. Mangroves have experienced convergent adaption to stressful coastal environments and are thus a good system to test the homeostatic role of gbM. Using whole-genome bisulfite sequencing, we compared gene body methylation patterns between three pairs of mangrove and non-mangrove species with rice as the outgroup. We found massive gains, with gain to loss ratio of ~6.8, of gbM specific to mangrove lineages. In contrast, the ratio is ~0.07 in non-mangroves. We estimate that ~1,100 genes exhibit convergent body methylation in mangrove genomes but only 13 genes in non-mangroves. Compared to control genes with no signature of convergent gbM acquisition, expression variation of mangrove-specific convergent gbM loci is reduced. This is true for expression variation between mangrove and non-mangrove pairs as well as in response to salt and UV-B stress. This reduction of expression variation is independent of gene length and excess of CG dinucleotide prevalence, but is associated with slow evolutionary rate. We found little overlap between the genes undergoing mangrove-specific convergent methylation gain and loci with signatures of convergent DNA sequence evolution. Our study demonstrates that convergent gene body methylation in mangroves plays a homeostatic role in stabilizing gene expression. GbM variation that is under selection is largely independent of genetic variation, highlighting the contribution of epigenetics to plant stress adaptation.