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Sex-specific expression profiles of ecdysteroid biosynthesis and ecdysone response genes in extreme sexual dimorphism of the mealybug Planococcus kraunhiae (Kuwana)

Insect molting hormone (ecdysteroids) and juvenile hormone regulate molting and metamorphic events in a variety of insect species. Mealybugs undergo sexually dimorphic metamorphosis: males develop into winged adults through non-feeding, pupa-like stages called prepupa and pupa, while females emerge...

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Autores principales: Muramatsu, Miyuki, Tsuji, Tomohiro, Tanaka, Sayumi, Shiotsuki, Takahiro, Jouraku, Akiya, Miura, Ken, Vea, Isabelle Mifom, Minakuchi, Chieka
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7153872/
https://www.ncbi.nlm.nih.gov/pubmed/32282855
http://dx.doi.org/10.1371/journal.pone.0231451
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author Muramatsu, Miyuki
Tsuji, Tomohiro
Tanaka, Sayumi
Shiotsuki, Takahiro
Jouraku, Akiya
Miura, Ken
Vea, Isabelle Mifom
Minakuchi, Chieka
author_facet Muramatsu, Miyuki
Tsuji, Tomohiro
Tanaka, Sayumi
Shiotsuki, Takahiro
Jouraku, Akiya
Miura, Ken
Vea, Isabelle Mifom
Minakuchi, Chieka
author_sort Muramatsu, Miyuki
collection PubMed
description Insect molting hormone (ecdysteroids) and juvenile hormone regulate molting and metamorphic events in a variety of insect species. Mealybugs undergo sexually dimorphic metamorphosis: males develop into winged adults through non-feeding, pupa-like stages called prepupa and pupa, while females emerge as neotenic wingless adults. We previously demonstrated, in the Japanese mealybug Planococcus kraunhiae (Kuwana), that the juvenile hormone titer is higher in males than in females at the end of the juvenile stage, which suggests that juvenile hormone may regulate male-specific adult morphogenesis. Here, we examined the involvement of ecdysteroids in sexually dimorphic metamorphosis. To estimate ecdysteroid titers, quantitative RT-PCR analyses of four Halloween genes encoding for cytochrome P450 monooxygenases in ecdysteroid biosynthesis, i.e., spook, disembodied, shadow and shade, were performed. Overall, their expression levels peaked before each nymphal molt. Transcript levels of spook, disembodied and shadow, genes that catalyze the steps in ecdysteroid biosynthesis in the prothoracic gland, were higher in males from the middle of the second nymphal instar to adult emergence. In contrast, the expression of shade, which was reported to be involved in the conversion of ecdysone into 20-hydroxyecdysone in peripheral tissues, was similar between males and females. These results suggest that ecdysteroid biosynthesis in the prothoracic gland is more active in males than in females, although the final conversion into 20-hydroxyecdysone occurs at similar levels in both sexes. Moreover, expression profiles of ecdysone response genes, ecdysone receptor and ecdysone-induced protein 75B, were also analyzed. Based on these expression profiles, we propose that the changes in ecdysteroid titer differ between males and females, and that high ecdysteroid titer is essential for directing male adult development.
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spelling pubmed-71538722020-04-16 Sex-specific expression profiles of ecdysteroid biosynthesis and ecdysone response genes in extreme sexual dimorphism of the mealybug Planococcus kraunhiae (Kuwana) Muramatsu, Miyuki Tsuji, Tomohiro Tanaka, Sayumi Shiotsuki, Takahiro Jouraku, Akiya Miura, Ken Vea, Isabelle Mifom Minakuchi, Chieka PLoS One Research Article Insect molting hormone (ecdysteroids) and juvenile hormone regulate molting and metamorphic events in a variety of insect species. Mealybugs undergo sexually dimorphic metamorphosis: males develop into winged adults through non-feeding, pupa-like stages called prepupa and pupa, while females emerge as neotenic wingless adults. We previously demonstrated, in the Japanese mealybug Planococcus kraunhiae (Kuwana), that the juvenile hormone titer is higher in males than in females at the end of the juvenile stage, which suggests that juvenile hormone may regulate male-specific adult morphogenesis. Here, we examined the involvement of ecdysteroids in sexually dimorphic metamorphosis. To estimate ecdysteroid titers, quantitative RT-PCR analyses of four Halloween genes encoding for cytochrome P450 monooxygenases in ecdysteroid biosynthesis, i.e., spook, disembodied, shadow and shade, were performed. Overall, their expression levels peaked before each nymphal molt. Transcript levels of spook, disembodied and shadow, genes that catalyze the steps in ecdysteroid biosynthesis in the prothoracic gland, were higher in males from the middle of the second nymphal instar to adult emergence. In contrast, the expression of shade, which was reported to be involved in the conversion of ecdysone into 20-hydroxyecdysone in peripheral tissues, was similar between males and females. These results suggest that ecdysteroid biosynthesis in the prothoracic gland is more active in males than in females, although the final conversion into 20-hydroxyecdysone occurs at similar levels in both sexes. Moreover, expression profiles of ecdysone response genes, ecdysone receptor and ecdysone-induced protein 75B, were also analyzed. Based on these expression profiles, we propose that the changes in ecdysteroid titer differ between males and females, and that high ecdysteroid titer is essential for directing male adult development. Public Library of Science 2020-04-13 /pmc/articles/PMC7153872/ /pubmed/32282855 http://dx.doi.org/10.1371/journal.pone.0231451 Text en © 2020 Muramatsu 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
Muramatsu, Miyuki
Tsuji, Tomohiro
Tanaka, Sayumi
Shiotsuki, Takahiro
Jouraku, Akiya
Miura, Ken
Vea, Isabelle Mifom
Minakuchi, Chieka
Sex-specific expression profiles of ecdysteroid biosynthesis and ecdysone response genes in extreme sexual dimorphism of the mealybug Planococcus kraunhiae (Kuwana)
title Sex-specific expression profiles of ecdysteroid biosynthesis and ecdysone response genes in extreme sexual dimorphism of the mealybug Planococcus kraunhiae (Kuwana)
title_full Sex-specific expression profiles of ecdysteroid biosynthesis and ecdysone response genes in extreme sexual dimorphism of the mealybug Planococcus kraunhiae (Kuwana)
title_fullStr Sex-specific expression profiles of ecdysteroid biosynthesis and ecdysone response genes in extreme sexual dimorphism of the mealybug Planococcus kraunhiae (Kuwana)
title_full_unstemmed Sex-specific expression profiles of ecdysteroid biosynthesis and ecdysone response genes in extreme sexual dimorphism of the mealybug Planococcus kraunhiae (Kuwana)
title_short Sex-specific expression profiles of ecdysteroid biosynthesis and ecdysone response genes in extreme sexual dimorphism of the mealybug Planococcus kraunhiae (Kuwana)
title_sort sex-specific expression profiles of ecdysteroid biosynthesis and ecdysone response genes in extreme sexual dimorphism of the mealybug planococcus kraunhiae (kuwana)
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7153872/
https://www.ncbi.nlm.nih.gov/pubmed/32282855
http://dx.doi.org/10.1371/journal.pone.0231451
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