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Conserved nuclear hormone receptors controlling a novel plastic trait target fast-evolving genes expressed in a single cell

Environment shapes development through a phenomenon called developmental plasticity. Deciphering its genetic basis has potential to shed light on the origin of novel traits and adaptation to environmental change. However, molecular studies are scarce, and little is known about molecular mechanisms a...

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Autores principales: Sieriebriennikov, Bogdan, Sun, Shuai, Lightfoot, James W., Witte, Hanh, Moreno, Eduardo, Rödelsperger, Christian, Sommer, Ralf J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7179942/
https://www.ncbi.nlm.nih.gov/pubmed/32282814
http://dx.doi.org/10.1371/journal.pgen.1008687
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author Sieriebriennikov, Bogdan
Sun, Shuai
Lightfoot, James W.
Witte, Hanh
Moreno, Eduardo
Rödelsperger, Christian
Sommer, Ralf J.
author_facet Sieriebriennikov, Bogdan
Sun, Shuai
Lightfoot, James W.
Witte, Hanh
Moreno, Eduardo
Rödelsperger, Christian
Sommer, Ralf J.
author_sort Sieriebriennikov, Bogdan
collection PubMed
description Environment shapes development through a phenomenon called developmental plasticity. Deciphering its genetic basis has potential to shed light on the origin of novel traits and adaptation to environmental change. However, molecular studies are scarce, and little is known about molecular mechanisms associated with plasticity. We investigated the gene regulatory network controlling predatory vs. non-predatory dimorphism in the nematode Pristionchus pacificus and found that it consists of genes of extremely different age classes. We isolated mutants in the conserved nuclear hormone receptor nhr-1 with previously unseen phenotypic effects. They disrupt mouth-form determination and result in animals combining features of both wild-type morphs. In contrast, mutants in another conserved nuclear hormone receptor nhr-40 display altered morph ratios, but no intermediate morphology. Despite divergent modes of control, NHR-1 and NHR-40 share transcriptional targets, which encode extracellular proteins that have no orthologs in Caenorhabditis elegans and result from lineage-specific expansions. An array of transcriptional reporters revealed co-expression of all tested targets in the same pharyngeal gland cell. Major morphological changes in this gland cell accompanied the evolution of teeth and predation, linking rapid gene turnover with morphological innovations. Thus, the origin of feeding plasticity involved novelty at the level of genes, cells and behavior.
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spelling pubmed-71799422020-05-05 Conserved nuclear hormone receptors controlling a novel plastic trait target fast-evolving genes expressed in a single cell Sieriebriennikov, Bogdan Sun, Shuai Lightfoot, James W. Witte, Hanh Moreno, Eduardo Rödelsperger, Christian Sommer, Ralf J. PLoS Genet Research Article Environment shapes development through a phenomenon called developmental plasticity. Deciphering its genetic basis has potential to shed light on the origin of novel traits and adaptation to environmental change. However, molecular studies are scarce, and little is known about molecular mechanisms associated with plasticity. We investigated the gene regulatory network controlling predatory vs. non-predatory dimorphism in the nematode Pristionchus pacificus and found that it consists of genes of extremely different age classes. We isolated mutants in the conserved nuclear hormone receptor nhr-1 with previously unseen phenotypic effects. They disrupt mouth-form determination and result in animals combining features of both wild-type morphs. In contrast, mutants in another conserved nuclear hormone receptor nhr-40 display altered morph ratios, but no intermediate morphology. Despite divergent modes of control, NHR-1 and NHR-40 share transcriptional targets, which encode extracellular proteins that have no orthologs in Caenorhabditis elegans and result from lineage-specific expansions. An array of transcriptional reporters revealed co-expression of all tested targets in the same pharyngeal gland cell. Major morphological changes in this gland cell accompanied the evolution of teeth and predation, linking rapid gene turnover with morphological innovations. Thus, the origin of feeding plasticity involved novelty at the level of genes, cells and behavior. Public Library of Science 2020-04-13 /pmc/articles/PMC7179942/ /pubmed/32282814 http://dx.doi.org/10.1371/journal.pgen.1008687 Text en © 2020 Sieriebriennikov et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Sieriebriennikov, Bogdan
Sun, Shuai
Lightfoot, James W.
Witte, Hanh
Moreno, Eduardo
Rödelsperger, Christian
Sommer, Ralf J.
Conserved nuclear hormone receptors controlling a novel plastic trait target fast-evolving genes expressed in a single cell
title Conserved nuclear hormone receptors controlling a novel plastic trait target fast-evolving genes expressed in a single cell
title_full Conserved nuclear hormone receptors controlling a novel plastic trait target fast-evolving genes expressed in a single cell
title_fullStr Conserved nuclear hormone receptors controlling a novel plastic trait target fast-evolving genes expressed in a single cell
title_full_unstemmed Conserved nuclear hormone receptors controlling a novel plastic trait target fast-evolving genes expressed in a single cell
title_short Conserved nuclear hormone receptors controlling a novel plastic trait target fast-evolving genes expressed in a single cell
title_sort conserved nuclear hormone receptors controlling a novel plastic trait target fast-evolving genes expressed in a single cell
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7179942/
https://www.ncbi.nlm.nih.gov/pubmed/32282814
http://dx.doi.org/10.1371/journal.pgen.1008687
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