Natural cryptic variation in epigenetic modulation of an embryonic gene regulatory network.

Autor: Ewe CK; Department of Molecular, Cellular, and Developmental Biology, University of California, Santa Barbara, CA 93117.; Neuroscience Research Institute, University of California, Santa Barbara, CA 93117., Torres Cleuren YN; Department of Molecular, Cellular, and Developmental Biology, University of California, Santa Barbara, CA 93117; yamila.cleuren@uib.no joel.rothman@lifesci.ucsb.edu.; Neuroscience Research Institute, University of California, Santa Barbara, CA 93117.; School of Biological Sciences, University of Auckland, Auckland 1010, New Zealand., Flowers SE; Department of Molecular, Cellular, and Developmental Biology, University of California, Santa Barbara, CA 93117.; Neuroscience Research Institute, University of California, Santa Barbara, CA 93117., Alok G; Department of Molecular, Cellular, and Developmental Biology, University of California, Santa Barbara, CA 93117.; Neuroscience Research Institute, University of California, Santa Barbara, CA 93117., Snell RG; Neuroscience Research Institute, University of California, Santa Barbara, CA 93117.; School of Biological Sciences, University of Auckland, Auckland 1010, New Zealand., Rothman JH; Department of Molecular, Cellular, and Developmental Biology, University of California, Santa Barbara, CA 93117; yamila.cleuren@uib.no joel.rothman@lifesci.ucsb.edu.; Neuroscience Research Institute, University of California, Santa Barbara, CA 93117.; School of Biological Sciences, University of Auckland, Auckland 1010, New Zealand.
Jazyk: angličtina
Zdroj: Proceedings of the National Academy of Sciences of the United States of America [Proc Natl Acad Sci U S A] 2020 Jun 16; Vol. 117 (24), pp. 13637-13646. Date of Electronic Publication: 2020 Jun 01.
DOI: 10.1073/pnas.1920343117
Abstrakt: Gene regulatory networks (GRNs) that direct animal embryogenesis must respond to varying environmental and physiological conditions to ensure robust construction of organ systems. While GRNs are evolutionarily modified by natural genomic variation, the roles of epigenetic processes in shaping plasticity of GRN architecture are not well understood. The endoderm GRN in Caenorhabditis elegans is initiated by the maternally supplied SKN-1/Nrf2 bZIP transcription factor; however, the requirement for SKN-1 in endoderm specification varies widely among distinct C. elegans wild isotypes, owing to rapid developmental system drift driven by accumulation of cryptic genetic variants. We report here that heritable epigenetic factors that are stimulated by transient developmental diapause also underlie cryptic variation in the requirement for SKN-1 in endoderm development. This epigenetic memory is inherited from the maternal germline, apparently through a nuclear, rather than cytoplasmic, signal, resulting in a parent-of-origin effect (POE), in which the phenotype of the progeny resembles that of the maternal founder. The occurrence and persistence of POE varies between different parental pairs, perduring for at least 10 generations in one pair. This long-perduring POE requires piwi-interacting RNA (piRNA) function and the germline nuclear RNA interference (RNAi) pathway, as well as MET-2 and SET-32, which direct histone H3K9 trimethylation and drive heritable epigenetic modification. Such nongenetic cryptic variation may provide a resource of additional phenotypic diversity through which adaptation may facilitate evolutionary changes and shape developmental regulatory systems.
Competing Interests: The authors declare no competing interest.
Databáze: MEDLINE