Epigenetics in the context of histone modifications plays essential roles in gene regulation and has strong relevance to animal adaptation in rapidly changing environments. However, the kinetics of epigenetic inheritance in dynamic environments remains to be uncovered. We conducted a systematic analysis to investigate the plastic and elastic epigenetic properties of histone marks H3K4me3, H3K27me3, H4K20me1, H3K9me3, and H3K36me1 on C. elegans genome: F0 worms were cultured on agar plates, F1 in liquid, followed by F2 on agar. Transferring animals from agar to liquid presents a drastic environmental change. For example, due to the presence of a buoyant force in liquid, the nematodes experience only 1/8th of their ground weight. In addition, the animals move by crawling in agar and swimming in liquid. As expected, F0 and F1 worms showed altered chromosomal distributions for different histone marks, with varying degrees of overlapping regions (1% - 31%). Interestingly, the histone distributions in F2 animals were additionally associated with unique genes (0.2% - 51%) that are not common to F0 and F1. Bioinformatics analyses were conducted to correlate environmental change with the histone distributions. One particular finding is that H3K4me3 marks in F1 animals are strongly associated with locomotion genes that are not present in F0 and F2. The additional activated locomotion genes in F1 reflect an adaptive response to the change from agar to liquid environments. In another example, F1 and F2 animals displayed enriched H3K4me3 activation in genes related to adult life span compared to F0. Others have shown that C. elegans lifespan is doubled in liquid cultures. The fact that F2 generation retains this epigenetic memory remains unclear, but may closely resemble epigenetic mechanisms observed with multigenerational human studies on starvation. Transgenerational analysis (F0, F1, and F2) showed that the distribution of H3K4me3, H3K27me3, and H3K36me1 generally remained constant (epigenetic plasticity), while the other histone modifications displayed up to eight-fold change in the number of common genes regulated in three generations exposed to environmental changes (epigenetic elasticity). These results indicate that chemically distinct histone marks exhibit different kinetics across multigenerations that can be described as elastic and plastic (memory-forming).
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