A transgenerational endocrine signaling pathway in Crustacea.

Environmental signals to maternal organisms can result in developmental alterations in progeny. One such example is environmental sex determination in Branchiopod crustaceans. We previously demonstrated that the hormone methyl farnesoate could orchestrate environmental sex determination in the early...

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Main Authors: Gerald A LeBlanc, Ying H Wang, Charisse N Holmes, Gwijun Kwon, Elizabeth K Medlock
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2013-01-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC3629115?pdf=render
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spelling doaj-e514f8ed68a94ea2a6a27c08361c399a2020-11-25T00:42:28ZengPublic Library of Science (PLoS)PLoS ONE1932-62032013-01-0184e6171510.1371/journal.pone.0061715A transgenerational endocrine signaling pathway in Crustacea.Gerald A LeBlancYing H WangCharisse N HolmesGwijun KwonElizabeth K MedlockEnvironmental signals to maternal organisms can result in developmental alterations in progeny. One such example is environmental sex determination in Branchiopod crustaceans. We previously demonstrated that the hormone methyl farnesoate could orchestrate environmental sex determination in the early embryo to the male phenotype. Presently, we identify a transcription factor that is activated by methyl farnesoate and explore the extent and significance of this transgenerational signaling pathway.Several candidate transcription factors were cloned from the water flea Daphnia pulex and evaluated for activation by methyl farnesoate. One of the factors evaluated, the complex of two bHLH-PAS proteins, dappuMet and SRC, activated a reporter gene in response to methyl farnesoate. Several juvenoid compounds were definitively evaluated for their ability to activate this receptor complex (methyl farnesoate receptor, MfR) in vitro and stimulate male sex determination in vivo. Potency to activate the MfR correlated to potency to stimulate male sex determination of offspring (pyriproxyfen>methyl farnesoate>methoprene, kinoprene). Daphnids were exposed to concentrations of pyriproxyfen and physiologic responses determined over multiple generations. Survivial, growth, and sex of maternal organisms were not affected by pyriproxyfen exposure. Sex ratio among offspring (generation 2) were increasingly skewed in favor of males with increasing pyriproxyfen concentration; while, the number of offspring per brood was progressively reduced. Female generation 2 daphnids were reared to reproductive maturity in the absence of pyriproxyfen. Sex ratios of offspring (generation 3) were not affected in this pyriproxyfen lineage, however, the number of offspring per brood, again, was significantly reduced.Results reveal likely components to a hormone/receptor signaling pathway in a crustacean that orchestrates transgenerational modifications to important population metrics (sex ratios, fecundity of females). A model is provided that describes how these signaling processes can facilitate population sustainability under normal conditions or threaten sustainability when perturbed by environmental chemicals.http://europepmc.org/articles/PMC3629115?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Gerald A LeBlanc
Ying H Wang
Charisse N Holmes
Gwijun Kwon
Elizabeth K Medlock
spellingShingle Gerald A LeBlanc
Ying H Wang
Charisse N Holmes
Gwijun Kwon
Elizabeth K Medlock
A transgenerational endocrine signaling pathway in Crustacea.
PLoS ONE
author_facet Gerald A LeBlanc
Ying H Wang
Charisse N Holmes
Gwijun Kwon
Elizabeth K Medlock
author_sort Gerald A LeBlanc
title A transgenerational endocrine signaling pathway in Crustacea.
title_short A transgenerational endocrine signaling pathway in Crustacea.
title_full A transgenerational endocrine signaling pathway in Crustacea.
title_fullStr A transgenerational endocrine signaling pathway in Crustacea.
title_full_unstemmed A transgenerational endocrine signaling pathway in Crustacea.
title_sort transgenerational endocrine signaling pathway in crustacea.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2013-01-01
description Environmental signals to maternal organisms can result in developmental alterations in progeny. One such example is environmental sex determination in Branchiopod crustaceans. We previously demonstrated that the hormone methyl farnesoate could orchestrate environmental sex determination in the early embryo to the male phenotype. Presently, we identify a transcription factor that is activated by methyl farnesoate and explore the extent and significance of this transgenerational signaling pathway.Several candidate transcription factors were cloned from the water flea Daphnia pulex and evaluated for activation by methyl farnesoate. One of the factors evaluated, the complex of two bHLH-PAS proteins, dappuMet and SRC, activated a reporter gene in response to methyl farnesoate. Several juvenoid compounds were definitively evaluated for their ability to activate this receptor complex (methyl farnesoate receptor, MfR) in vitro and stimulate male sex determination in vivo. Potency to activate the MfR correlated to potency to stimulate male sex determination of offspring (pyriproxyfen>methyl farnesoate>methoprene, kinoprene). Daphnids were exposed to concentrations of pyriproxyfen and physiologic responses determined over multiple generations. Survivial, growth, and sex of maternal organisms were not affected by pyriproxyfen exposure. Sex ratio among offspring (generation 2) were increasingly skewed in favor of males with increasing pyriproxyfen concentration; while, the number of offspring per brood was progressively reduced. Female generation 2 daphnids were reared to reproductive maturity in the absence of pyriproxyfen. Sex ratios of offspring (generation 3) were not affected in this pyriproxyfen lineage, however, the number of offspring per brood, again, was significantly reduced.Results reveal likely components to a hormone/receptor signaling pathway in a crustacean that orchestrates transgenerational modifications to important population metrics (sex ratios, fecundity of females). A model is provided that describes how these signaling processes can facilitate population sustainability under normal conditions or threaten sustainability when perturbed by environmental chemicals.
url http://europepmc.org/articles/PMC3629115?pdf=render
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