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Gene Body Methylation Confers Transcription Robustness in Mangroves During Long-Term Stress Adaptation.

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.

SUBMITTER: Wang Y

PROVIDER: S-EPMC8493031 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Microbes are responsible for cycling carbon (C) through soils, and predicted changes in soil C stocks under climate change are highly sensitive to shifts in the mechanisms assumed to control the microbial physiological response to warming. Two mecha-nisms have been suggested to explain the long-term warming impact on microbial physiology: microbial thermal acclimation and changes in the quantity and quality of substrates available for microbial metabolism. Yet studies disentangling these two mechanisms are lacking. To resolve the drivers of changes in microbial physiology in response to long-term warming, we sampled soils from 13- and 28-year- old soil warming experiments in different seasons. We performed short-term laboratory incubations across a range of temperatures to measure the relationships between temperature sensitivity of physiology (growth, respiration, carbon use efficiency, and extracellular enzyme activity) and the chemical composition of soil organic matter. We observed apparent thermal acclimation of microbial respiration, but only in sum-mer, when warming had exacerbated the seasonally-induced, already small dissolved organic matter pools. Irrespective of warming, greater quantity and quality of soil carbon increased the extracellular enzymatic pool and its temperature sensitivity. We propose that fresh litter input into the system seasonally cancels apparent thermal acclimation of C-cycling processes to decadal warming. Our findings reveal that long-term warming has indirectly affected microbial physiology via reduced C availability in this system, implying that earth system models including these negative feedbacks may be best suited to describe long-term warming effects on these soils. Citation: Domeignoz-Horta LA, Pold G, Erb H, Sebag D, Verrecchia E, Northen T, Louie K, Eloe-Fadrosh E, Pennacchio C, Knorr MA, Frey SD, Melillo JM, DeAngelis KM. Substrate availability and not thermal acclimation controls microbial temperature sensitivity response to long-term warming. Glob Chang Biol. 2023 Mar;29(6):1574-1590. doi: 10.1111/gcb.16544. The work (proposal:https://doi.org/10.46936/10.25585/60001340) conducted by the U.S. Department of Energy Joint Genome Institute (https://ror.org/04xm1d337), a DOE Office of Science User Facility, is supported by the Office of Science of the U.S. Department of Energy operated under Contract No. DE-AC02-05CH11231.

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Gene Body Methylation Confers Transcription Robustness in Mangroves During Long-Term Stress Adaptation.

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