Evolutionary transition of doublesex regulation from sex-specific splicing to male-specific transcription in termites

Abstract The sex determination gene doublesex (dsx) encodes a transcription factor with two domains, oligomerization domain 1 (OD1) and OD2, and is present throughout insects. Sex-specific Dsx splicing isoforms regulate the transcription of target genes and trigger sex differentiation in all Holomet...

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Main Authors: Satoshi Miyazaki, Kokuto Fujiwara, Keima Kai, Yudai Masuoka, Hiroki Gotoh, Teruyuki Niimi, Yoshinobu Hayashi, Shuji Shigenobu, Kiyoto Maekawa
Format: Article
Language:English
Published: Nature Publishing Group 2021-08-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-021-95423-7
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spelling doaj-be50abc93b3e49e7afb9492eb49206882021-08-08T11:22:02ZengNature Publishing GroupScientific Reports2045-23222021-08-0111111210.1038/s41598-021-95423-7Evolutionary transition of doublesex regulation from sex-specific splicing to male-specific transcription in termitesSatoshi Miyazaki0Kokuto Fujiwara1Keima Kai2Yudai Masuoka3Hiroki Gotoh4Teruyuki Niimi5Yoshinobu Hayashi6Shuji Shigenobu7Kiyoto Maekawa8Graduate School of Agriculture, Tamagawa UniversityGraduate School of Science and Engineering, University of ToyamaGraduate School of Science and Engineering, University of ToyamaGraduate School of Science and Engineering, University of ToyamaDepartment of Biological Science, Faculty of Science, Shizuoka UniversityDivision of Evolutionary Developmental Biology, National Institute for Basic BiologyDepartment of Biology, Keio UniversityDepartment of Basic Biology, School of Life Science, The Graduate University for Advanced Studies, SOKENDAIFaculty of Science, Academic Assembly, University of ToyamaAbstract The sex determination gene doublesex (dsx) encodes a transcription factor with two domains, oligomerization domain 1 (OD1) and OD2, and is present throughout insects. Sex-specific Dsx splicing isoforms regulate the transcription of target genes and trigger sex differentiation in all Holometabola examined to date. However, in some hemimetabolous insects, dsx is not spliced sexually and its sequence is less conserved. Here, to elucidate evolutionary changes in dsx in domain organisation and regulation in termites, we searched genome and/or transcriptome databases for the dsx OD1 and OD2 in seven termite species and their sister group (Cryptocercus woodroaches). Molecular phylogenetic and synteny analyses identified OD1 sequences of termites and C. punctulatus that clustered with dsx of Holometabola and regarded them as dsx orthologues. The Cryptocercus dsx orthologue containing OD2 was spliced sexually, as previously shown in other insects. However, OD2 was not found in all termite dsx orthologues. These orthologues were encoded by a single exon in three termites for which genome information is available; they were not alternatively spliced but transcribed in a male-specific manner in two examined species. Evolution of dsx regulation from sex-specific splicing to male-specific transcription may have occurred at an early stage of social evolution in termites.https://doi.org/10.1038/s41598-021-95423-7
collection DOAJ
language English
format Article
sources DOAJ
author Satoshi Miyazaki
Kokuto Fujiwara
Keima Kai
Yudai Masuoka
Hiroki Gotoh
Teruyuki Niimi
Yoshinobu Hayashi
Shuji Shigenobu
Kiyoto Maekawa
spellingShingle Satoshi Miyazaki
Kokuto Fujiwara
Keima Kai
Yudai Masuoka
Hiroki Gotoh
Teruyuki Niimi
Yoshinobu Hayashi
Shuji Shigenobu
Kiyoto Maekawa
Evolutionary transition of doublesex regulation from sex-specific splicing to male-specific transcription in termites
Scientific Reports
author_facet Satoshi Miyazaki
Kokuto Fujiwara
Keima Kai
Yudai Masuoka
Hiroki Gotoh
Teruyuki Niimi
Yoshinobu Hayashi
Shuji Shigenobu
Kiyoto Maekawa
author_sort Satoshi Miyazaki
title Evolutionary transition of doublesex regulation from sex-specific splicing to male-specific transcription in termites
title_short Evolutionary transition of doublesex regulation from sex-specific splicing to male-specific transcription in termites
title_full Evolutionary transition of doublesex regulation from sex-specific splicing to male-specific transcription in termites
title_fullStr Evolutionary transition of doublesex regulation from sex-specific splicing to male-specific transcription in termites
title_full_unstemmed Evolutionary transition of doublesex regulation from sex-specific splicing to male-specific transcription in termites
title_sort evolutionary transition of doublesex regulation from sex-specific splicing to male-specific transcription in termites
publisher Nature Publishing Group
series Scientific Reports
issn 2045-2322
publishDate 2021-08-01
description Abstract The sex determination gene doublesex (dsx) encodes a transcription factor with two domains, oligomerization domain 1 (OD1) and OD2, and is present throughout insects. Sex-specific Dsx splicing isoforms regulate the transcription of target genes and trigger sex differentiation in all Holometabola examined to date. However, in some hemimetabolous insects, dsx is not spliced sexually and its sequence is less conserved. Here, to elucidate evolutionary changes in dsx in domain organisation and regulation in termites, we searched genome and/or transcriptome databases for the dsx OD1 and OD2 in seven termite species and their sister group (Cryptocercus woodroaches). Molecular phylogenetic and synteny analyses identified OD1 sequences of termites and C. punctulatus that clustered with dsx of Holometabola and regarded them as dsx orthologues. The Cryptocercus dsx orthologue containing OD2 was spliced sexually, as previously shown in other insects. However, OD2 was not found in all termite dsx orthologues. These orthologues were encoded by a single exon in three termites for which genome information is available; they were not alternatively spliced but transcribed in a male-specific manner in two examined species. Evolution of dsx regulation from sex-specific splicing to male-specific transcription may have occurred at an early stage of social evolution in termites.
url https://doi.org/10.1038/s41598-021-95423-7
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