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

Satoshi Miyazaki,Yudai Masuoka,Kiyoto Maekawa,Shuji Shigenobu,Hiroki Gotoh,Teruyuki Niimi,Yoshinobu Hayashi,Keima Kai,Kokuto Fujiwara

doi:10.1038/s41598-021-95423-7

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.

Highlights

The sex determination gene doublesex encodes a transcription factor with two domains, oligomerization domain 1 (OD1) and OD2, and is present throughout insects
We exhaustively searched genome and transcriptome databases of the subsocial woodroach Cryptocercus punctulatus and seven termite species (Hodotermopsis sjostedti, Cryptotermes secundus, Reticulitermes speratus, Coptotermes formosanus, and Macrotermes natalensis, as well as Z. nevadensis and N. takasagoensis) for the OD1 and OD2 of dsx, and examined whether the searched sequences were dsx homologues based on molecular phylogeny and synteny
BLAST searches using the translated OD1 sequence of Blattella dsx (45 amino acids) as a query against genome and/or transcriptome databases of seven termite species and one Cryptocercus woodroach species, after which two to four OD1-containing sequences were hit in each species (Table 1)

Summary

Introduction

The sex determination gene doublesex (dsx) encodes a transcription factor with two domains, oligomerization domain 1 (OD1) and OD2, and is present throughout insects. OD1 is found among dsx and doublesex/mab-3 related transcription factor (DMRT) genes that are present among metazoans and involved in their sexual d evelopment[10,11], whereas OD2 is specific to dsx[12] They failed to obtain any evidence of the presence of dsx in several hemimetabolous insects, including termites (infraorder Isoptera or epifamily Termitoidae), a monophyletic group within the cockroaches (Blattodea)[13,14]. We exhaustively searched genome and transcriptome databases of the subsocial woodroach Cryptocercus punctulatus and seven termite species (Hodotermopsis sjostedti, Cryptotermes secundus, Reticulitermes speratus, Coptotermes formosanus, and Macrotermes natalensis, as well as Z. nevadensis and N. takasagoensis) for the OD1 and OD2 of dsx, and examined whether the searched sequences were dsx homologues based on molecular phylogeny and synteny. Based on the results obtained, we conclude that dsx regulation shifted from sex-specific splicing to male-specific transcription at an early stage of social evolution in termites

Methods

Results

Conclusion