Mutation is the ultimate source of genetic variation in natural populations and crops. To study mechanisms determining mutation rate variation within plant genomes, we analyzed 43,483 de novo germline single base substitutions in 1,504 fast neutron mutation lines of the model rice cultivar Kitaake (Oryza sativa ssp japonica) (from Li et al. 2017). We find that, like previously observed for de novo germline mutations in Arabidopsis. thaliana, mutation rates are significantly lower in genomic regions marked by H3K4me1, a histone modification found in the gene bodies of actively expressed genes in plants. We also observed conservation in rice for PDS5C, a cohesion cofactor involved in the homology-directed repair pathway that in A. thaliana binds to H3K4me1 via its Tudor domain. By examining existing ChIP-seq data for PDS5C in A. thaliana, we find that it localizes to genome regions marked by H3K4me1: regions of low mutation rates, coding regions, essential genes, constitutively expressed genes, and genes under stronger purifying selection, mirroring mutation biases observed in rice as well. We searched the A. thaliana proteome for genes containing similar Tudor domains and found that they are significantly enriched for DNA repair functions (p<1×10-11), including the mismatch repair MSH6 gene (in both rice and A. thaliana ), suggesting the potential for multiple DNA repair pathways to specifically target gene bodies and essential genes through H3K4me1 reading. These findings inspire further research to characterize mechanisms that localize DNA repair via histone interactions, leading to hypomutation in functionally constrained regions and potentially tuning the evolutionary trajectories of plant genomes.
Abstract‘Candidatus Methanophagales’ (ANME-1) is an order-level clade of archaea responsible for anaerobic methane oxidation in deep-sea sediments. The diversity, ecology and evolution of ANME-1 remain poorly understood. In this study, we use metagenomics on deep-sea hydrothermal samples to expand ANME-1 diversity and uncover the effect of virus–host dynamics. Phylogenetic analyses reveal a deep-branching, thermophilic family, ‘Candidatus Methanospirareceae’, closely related to short-chain alkane oxidizers. Global phylogeny and near-complete genomes show that hydrogen metabolism within ANME-1 is an ancient trait that was vertically inherited but differentially lost during lineage diversification. Metagenomics also uncovered 16 undescribed virus families so far exclusively targeting ANME-1 archaea, showing unique structural and replicative signatures. The expansive ANME-1 virome contains a metabolic gene repertoire that can influence host ecology and evolution through virus-mediated gene displacement. Our results suggest an evolutionary continuum between anaerobic methane and short-chain alkane oxidizers and underscore the effects of viruses on the dynamics and evolution of methane-driven ecosystems.
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