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

View ORCID ProfileSatoshi Miyazaki, Kokuto Fujiwara, Keima Kai, Yudai Masuoka, Hiroki Gotoh, Teruyuki Niimi, Yoshinobu Hayashi, Shuji Shigenobu, Kiyoto Maekawa
doi: https://doi.org/10.1101/2021.05.31.446247
Satoshi Miyazaki
1Graduate School of Agriculture, Tamagawa University, Machida, Tokyo 194-8610, Japan
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  • ORCID record for Satoshi Miyazaki
  • For correspondence: smiyazaki@agr.tamagawa.ac.jp kmaekawa@sci.u-toyama.ac.jp
Kokuto Fujiwara
2Faculty of Science, Academic Assembly, University of Toyama, Gofuku, Toyama, 930-8555, Japan
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Keima Kai
2Faculty of Science, Academic Assembly, University of Toyama, Gofuku, Toyama, 930-8555, Japan
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Yudai Masuoka
2Faculty of Science, Academic Assembly, University of Toyama, Gofuku, Toyama, 930-8555, Japan
3Institute of Agrobiological Sciences, NARO (National Agriculture and Food Research Organization), Tsukuba, Ibaraki 305-8634, Japan
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Hiroki Gotoh
4Department of Biological Science, Faculty of Science, Shizuoka University, Suruga-ku, Shizuoka, 422-8529, Japan
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Teruyuki Niimi
5Division of Evolutionary Developmental Biology, National Institute for Basic Biology, Okazaki, Aichi, 444-8585 Japan
6Department of Basic Biology, School of Life Science, The Graduate University for Advanced Studies, SOKENDAI, Okazaki, Aichi, 444-8585 Japan
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Yoshinobu Hayashi
7Department of Biology, Keio University, Yokohama, Kanagawa, 223-8521, Japan
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Shuji Shigenobu
6Department of Basic Biology, School of Life Science, The Graduate University for Advanced Studies, SOKENDAI, Okazaki, Aichi, 444-8585 Japan
8NIBB Research Core Facilities, National Institute for Basic Biology, Okazaki, Aichi, 444-8585 Japan
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Kiyoto Maekawa
2Faculty of Science, Academic Assembly, University of Toyama, Gofuku, Toyama, 930-8555, Japan
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  • For correspondence: smiyazaki@agr.tamagawa.ac.jp kmaekawa@sci.u-toyama.ac.jp
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Abstract

The sex determination gene doublesex (dsx), which encodes a transcription factor with two domains: oligomerisation domain 1 (OD1) and OD2, is conserved among insects. The sex-specific Dsx splicing isoforms regulate the transcription of target genes and trigger sex differentiation in all holometabolous insects examined to date. However, in some hemimetabolous insects, dsx is less conserved and not spliced sexually. Here, to elucidate evolutionary changes in dsx in the gene structure and its regulatory manner in termites, we searched genome and/or transcriptome databases for the OD1 and OD2 of dsx in six termite species and their sister group (woodroach). Molecular phylogenetic analysis identified OD1 sequences of termites and a woodroach clustered with dsx of holometabolous insects and regarded them as dsx orthologues. In the woodroach, a dsx orthologue containing OD2 was spliced sexually, as previously shown in other insects. However, OD2 were not found in all termite dsx orthologues. These orthologues were encoded by only a single exon in three termites with genome information; they were not alternatively spliced, but transcribed in a male-specific manner in two species examined. Evolution of dsx regulation from sex-specific splicing to male-specific transcription might be occurred at the early stage of social evolution in termites.

Competing Interest Statement

The authors have declared no competing interest.

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Posted May 31, 2021.
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Evolutionary transition of doublesex regulation in termites and cockroaches: from sex-specific splicing to male-specific transcription
Satoshi Miyazaki, Kokuto Fujiwara, Keima Kai, Yudai Masuoka, Hiroki Gotoh, Teruyuki Niimi, Yoshinobu Hayashi, Shuji Shigenobu, Kiyoto Maekawa
bioRxiv 2021.05.31.446247; doi: https://doi.org/10.1101/2021.05.31.446247
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Evolutionary transition of doublesex regulation in termites and cockroaches: from sex-specific splicing to male-specific transcription
Satoshi Miyazaki, Kokuto Fujiwara, Keima Kai, Yudai Masuoka, Hiroki Gotoh, Teruyuki Niimi, Yoshinobu Hayashi, Shuji Shigenobu, Kiyoto Maekawa
bioRxiv 2021.05.31.446247; doi: https://doi.org/10.1101/2021.05.31.446247

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