Handling Editor: Swathi Arur
ABSTRACT
Formation of a zygote is coupled with extensive epigenetic reprogramming to enable appropriate inheritance of histone methylation and prevent developmental delays. In Caenorhabditis elegans, this reprogramming is mediated by the H3K4me2 demethylase SPR-5 and the H3K9 methyltransferase, MET-2. In contrast, the H3K36 methyltransferase MES-4 maintains H3K36me2/3 at germline genes between generations to facilitate re-establishment of the germline. To determine whether the MES-4 germline inheritance pathway antagonizes spr-5; met-2 reprogramming, we examined the interaction between these two pathways. We found that the developmental delay of spr-5; met-2 mutant progeny is associated with ectopic H3K36me3 and the ectopic expression of MES-4-targeted germline genes in somatic tissues. Furthermore, the developmental delay is dependent upon MES-4 and the H3K4 methyltransferase, SET-2. We propose that MES-4 prevents crucial germline genes from being repressed by antagonizing maternal spr-5; met-2 reprogramming. Thus, the balance of inherited histone modifications is necessary to distinguish germline versus soma and prevent developmental delay.
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Footnotes
Competing interests
The authors declare no competing or financial interests.
Author contributions
Conceptualization: B.S.C., T.W.L., D.J.K.; Methodology: B.S.C., T.W.L., D.J.K.; Software: D.A.M.; Validation: B.S.C., D.J.K.; Formal analysis: B.S.C., C.F.P., J.S.B., D.A.M., D.J.K.; Investigation: B.S.C., C.F.P., J.D.R., J.S.B., D.J.K.; Resources: B.S.C., D.J.K.; Data curation: B.S.C., D.A.M., D.J.K.; Writing - original draft: B.S.C.; Writing - review & editing: B.S.C., T.W.L., D.J.K.; Visualization: B.S.C., D.J.K.; Supervision: B.S.C., D.J.K.; Project administration: B.S.C., D.J.K.; Funding acquisition: B.S.C., D.J.K.
Funding
This work was funded by a Division of Integrative Organismal Systems grant to D.J.K. (NSF IOS1931697); T.W.L. and B.S.C. were supported by National Institutes of Health Fellowships in Research and Science Teaching IRACDA postdoctoral program (NIH K12GM00680-15); B.S.C. and J.D.R. were supported by the National Institutes of Health (NIH F32 GM126734-01 and NIH F31 HD100145, respectively). Deposited in PMC for release after 12 months.
Data availability
Raw and processed genomic data has been deposited in GEO under accession number GSE143839.
Supplementary information
Supplementary information available online at https://dev.biologists.org/lookup/doi/10.1242/dev.196600.supplemental
- Received August 31, 2020.
- Accepted January 4, 2021.
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