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Phase-specific expression of an insulin-like androgenic gland factor in a marine shrimp Lysmata wurdemanni: Implication for maintaining protandric simultaneous hermaphroditism

BACKGROUND: Shrimp in the genus Lysmata have a unique and rare sexual system referred to as protandric simultaneous hermaphroditism, whereby individuals mature first as male (male phase), and then the female function may also develop as the shrimp grow, so that the gonad is able to produce both eggs...

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Autores principales: Zhang, Dong, Sun, Min, Liu, Xin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5325528/
https://www.ncbi.nlm.nih.gov/pubmed/28235100
http://dx.doi.org/10.1371/journal.pone.0172782
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author Zhang, Dong
Sun, Min
Liu, Xin
author_facet Zhang, Dong
Sun, Min
Liu, Xin
author_sort Zhang, Dong
collection PubMed
description BACKGROUND: Shrimp in the genus Lysmata have a unique and rare sexual system referred to as protandric simultaneous hermaphroditism, whereby individuals mature first as male (male phase), and then the female function may also develop as the shrimp grow, so that the gonad is able to produce both eggs and sperms simultaneously, a condition called simultaneous hermaphroditism (euhermaphrodite phase). To date, the mechanisms of sex control in this sexual system still remain poorly understood. Many studies indicate that an insulin-like androgenic gland factor (IAG) is involved in controlling sex differentiation in gonochoric crustaceans, but its role in the protandric simultaneous hermaphrodite is still not clear. RESULTS: To determine whether an IAG is involved in sex control in the hermaphrodite, here we, for the first time, cloned the IAG gene cDNA sequence from Lysmata wurdemanni (termed Lw-IAG: L. wurdemanni insulin-like AG factor), a protandric simultaneous hermaphroditic shrimp. The IAG contains an open reading frame of 528 bp, corresponding to 176 amino acids, which consists of a signal peptide, B chain, C peptide, and A chain. The organization is similar to the IAGs found in other decapods. The IAG gene was expressed in both male and euhermaphrodite phases, but the expression level was significantly higher in the male phase than in the euhermaphrodite phase. Immunofluorescence analysis and Western Blotting revealed that the IAG protein was expressed in the androgenic gland, and its expression level was higher in the male phase than in the euhermaphrodite phase. CONCLUSIONS: Data presented here suggest that the IAG gene may be a factor controlling sex in the protandric simultaneous hermaphrodite, and that the euhermaphrodite phase is maintained by reduced gene expression, i.e., the presence of the androgenic gland (or the androgenic hormone it produces) completely inhibits ovarian development in the male phase, and incomplete degeneration of the androgenic gland in the euhermaphrodite phase results in simultaneous hermaphroditism. The findings presented in the current study can help to reveal how protandric simultaneous hermaphroditism evolved in crustaceans.
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spelling pubmed-53255282017-03-09 Phase-specific expression of an insulin-like androgenic gland factor in a marine shrimp Lysmata wurdemanni: Implication for maintaining protandric simultaneous hermaphroditism Zhang, Dong Sun, Min Liu, Xin PLoS One Research Article BACKGROUND: Shrimp in the genus Lysmata have a unique and rare sexual system referred to as protandric simultaneous hermaphroditism, whereby individuals mature first as male (male phase), and then the female function may also develop as the shrimp grow, so that the gonad is able to produce both eggs and sperms simultaneously, a condition called simultaneous hermaphroditism (euhermaphrodite phase). To date, the mechanisms of sex control in this sexual system still remain poorly understood. Many studies indicate that an insulin-like androgenic gland factor (IAG) is involved in controlling sex differentiation in gonochoric crustaceans, but its role in the protandric simultaneous hermaphrodite is still not clear. RESULTS: To determine whether an IAG is involved in sex control in the hermaphrodite, here we, for the first time, cloned the IAG gene cDNA sequence from Lysmata wurdemanni (termed Lw-IAG: L. wurdemanni insulin-like AG factor), a protandric simultaneous hermaphroditic shrimp. The IAG contains an open reading frame of 528 bp, corresponding to 176 amino acids, which consists of a signal peptide, B chain, C peptide, and A chain. The organization is similar to the IAGs found in other decapods. The IAG gene was expressed in both male and euhermaphrodite phases, but the expression level was significantly higher in the male phase than in the euhermaphrodite phase. Immunofluorescence analysis and Western Blotting revealed that the IAG protein was expressed in the androgenic gland, and its expression level was higher in the male phase than in the euhermaphrodite phase. CONCLUSIONS: Data presented here suggest that the IAG gene may be a factor controlling sex in the protandric simultaneous hermaphrodite, and that the euhermaphrodite phase is maintained by reduced gene expression, i.e., the presence of the androgenic gland (or the androgenic hormone it produces) completely inhibits ovarian development in the male phase, and incomplete degeneration of the androgenic gland in the euhermaphrodite phase results in simultaneous hermaphroditism. The findings presented in the current study can help to reveal how protandric simultaneous hermaphroditism evolved in crustaceans. Public Library of Science 2017-02-24 /pmc/articles/PMC5325528/ /pubmed/28235100 http://dx.doi.org/10.1371/journal.pone.0172782 Text en © 2017 Zhang 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
Zhang, Dong
Sun, Min
Liu, Xin
Phase-specific expression of an insulin-like androgenic gland factor in a marine shrimp Lysmata wurdemanni: Implication for maintaining protandric simultaneous hermaphroditism
title Phase-specific expression of an insulin-like androgenic gland factor in a marine shrimp Lysmata wurdemanni: Implication for maintaining protandric simultaneous hermaphroditism
title_full Phase-specific expression of an insulin-like androgenic gland factor in a marine shrimp Lysmata wurdemanni: Implication for maintaining protandric simultaneous hermaphroditism
title_fullStr Phase-specific expression of an insulin-like androgenic gland factor in a marine shrimp Lysmata wurdemanni: Implication for maintaining protandric simultaneous hermaphroditism
title_full_unstemmed Phase-specific expression of an insulin-like androgenic gland factor in a marine shrimp Lysmata wurdemanni: Implication for maintaining protandric simultaneous hermaphroditism
title_short Phase-specific expression of an insulin-like androgenic gland factor in a marine shrimp Lysmata wurdemanni: Implication for maintaining protandric simultaneous hermaphroditism
title_sort phase-specific expression of an insulin-like androgenic gland factor in a marine shrimp lysmata wurdemanni: implication for maintaining protandric simultaneous hermaphroditism
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5325528/
https://www.ncbi.nlm.nih.gov/pubmed/28235100
http://dx.doi.org/10.1371/journal.pone.0172782
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