Caste-specific expressions and diverse roles of takeout genes in the termite Reticulitermes speratus
Abstract Acquisition of novel functions caused by gene duplication may be important for termite social evolution. To clarify this possibility, additional evidence is needed. An important example is takeout, encoding juvenile hormone binding protein. We identified 25 takeouts in the termite Reticulit...
| Main Authors: | , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Nature Portfolio
2023-05-01
|
| Series: | Scientific Reports |
| Online Access: | https://doi.org/10.1038/s41598-023-35524-7 |
| _version_ | 1797818004642201600 |
|---|---|
| author | Kokuto Fujiwara Akimi Karasawa Takumi Hanada Mutsuaki Tobo Tousuke Kaneko Mizuna Usui Kiyoto Maekawa |
| author_facet | Kokuto Fujiwara Akimi Karasawa Takumi Hanada Mutsuaki Tobo Tousuke Kaneko Mizuna Usui Kiyoto Maekawa |
| author_sort | Kokuto Fujiwara |
| collection | DOAJ |
| description | Abstract Acquisition of novel functions caused by gene duplication may be important for termite social evolution. To clarify this possibility, additional evidence is needed. An important example is takeout, encoding juvenile hormone binding protein. We identified 25 takeouts in the termite Reticulitermes speratus genome. RNA-seq revealed that many genes were highly expressed in specific castes. Two novel paralogs (RsTO1, RsTO2) were tandemly aligned in the same scaffold. Real-time qPCR indicated that RsTO1 and RsTO2 were highly expressed in queens and soldiers, respectively. Moreover, the highest RsTO1 expression was observed in alates during queen formation. These patterns were different from vitellogenins, encoding egg-yolk precursors, which were highly expressed in queens than alates. In situ hybridization showed that RsTO1 mRNA was localized in the alate-frontal gland, indicating that RsTO1 binds with secretions probably used for the defence during swarming flight. In contrast, increased RsTO2 expression was observed approximately 1 week after soldier differentiation. Expression patterns of geranylgeranyl diphosphate synthase, whose product functions in the terpenoid synthesis, were similar to RsTO2 expression. In situ hybridization indicated RsTO2-specific mRNA signals in the soldier-frontal gland. RsTO2 may interact with terpenoids, with a soldier-specific defensive function. It may provide additional evidence for functionalization after gene duplication in termites. |
| first_indexed | 2024-03-13T09:01:53Z |
| format | Article |
| id | doaj.art-abbb229b3ff246da8b7c59c890e73e44 |
| institution | Directory Open Access Journal |
| issn | 2045-2322 |
| language | English |
| last_indexed | 2024-03-13T09:01:53Z |
| publishDate | 2023-05-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Scientific Reports |
| spelling | doaj.art-abbb229b3ff246da8b7c59c890e73e442023-05-28T11:16:43ZengNature PortfolioScientific Reports2045-23222023-05-0113111310.1038/s41598-023-35524-7Caste-specific expressions and diverse roles of takeout genes in the termite Reticulitermes speratusKokuto Fujiwara0Akimi Karasawa1Takumi Hanada2Mutsuaki Tobo3Tousuke Kaneko4Mizuna Usui5Kiyoto Maekawa6Graduate School of Science and Engineering, University of Toyama, GofukuDepartment of Biology, Faculty of Science, University of Toyama, GofukuGraduate School of Science and Engineering, University of Toyama, GofukuGraduate School of Science and Engineering, University of Toyama, GofukuDepartment of Biology, Faculty of Science, University of Toyama, GofukuDepartment of Biology, Faculty of Science, University of Toyama, GofukuFaculty of Science, Academic Assembly, University of Toyama, GofukuAbstract Acquisition of novel functions caused by gene duplication may be important for termite social evolution. To clarify this possibility, additional evidence is needed. An important example is takeout, encoding juvenile hormone binding protein. We identified 25 takeouts in the termite Reticulitermes speratus genome. RNA-seq revealed that many genes were highly expressed in specific castes. Two novel paralogs (RsTO1, RsTO2) were tandemly aligned in the same scaffold. Real-time qPCR indicated that RsTO1 and RsTO2 were highly expressed in queens and soldiers, respectively. Moreover, the highest RsTO1 expression was observed in alates during queen formation. These patterns were different from vitellogenins, encoding egg-yolk precursors, which were highly expressed in queens than alates. In situ hybridization showed that RsTO1 mRNA was localized in the alate-frontal gland, indicating that RsTO1 binds with secretions probably used for the defence during swarming flight. In contrast, increased RsTO2 expression was observed approximately 1 week after soldier differentiation. Expression patterns of geranylgeranyl diphosphate synthase, whose product functions in the terpenoid synthesis, were similar to RsTO2 expression. In situ hybridization indicated RsTO2-specific mRNA signals in the soldier-frontal gland. RsTO2 may interact with terpenoids, with a soldier-specific defensive function. It may provide additional evidence for functionalization after gene duplication in termites.https://doi.org/10.1038/s41598-023-35524-7 |
| spellingShingle | Kokuto Fujiwara Akimi Karasawa Takumi Hanada Mutsuaki Tobo Tousuke Kaneko Mizuna Usui Kiyoto Maekawa Caste-specific expressions and diverse roles of takeout genes in the termite Reticulitermes speratus Scientific Reports |
| title | Caste-specific expressions and diverse roles of takeout genes in the termite Reticulitermes speratus |
| title_full | Caste-specific expressions and diverse roles of takeout genes in the termite Reticulitermes speratus |
| title_fullStr | Caste-specific expressions and diverse roles of takeout genes in the termite Reticulitermes speratus |
| title_full_unstemmed | Caste-specific expressions and diverse roles of takeout genes in the termite Reticulitermes speratus |
| title_short | Caste-specific expressions and diverse roles of takeout genes in the termite Reticulitermes speratus |
| title_sort | caste specific expressions and diverse roles of takeout genes in the termite reticulitermes speratus |
| url | https://doi.org/10.1038/s41598-023-35524-7 |
| work_keys_str_mv | AT kokutofujiwara castespecificexpressionsanddiverserolesoftakeoutgenesinthetermitereticulitermessperatus AT akimikarasawa castespecificexpressionsanddiverserolesoftakeoutgenesinthetermitereticulitermessperatus AT takumihanada castespecificexpressionsanddiverserolesoftakeoutgenesinthetermitereticulitermessperatus AT mutsuakitobo castespecificexpressionsanddiverserolesoftakeoutgenesinthetermitereticulitermessperatus AT tousukekaneko castespecificexpressionsanddiverserolesoftakeoutgenesinthetermitereticulitermessperatus AT mizunausui castespecificexpressionsanddiverserolesoftakeoutgenesinthetermitereticulitermessperatus AT kiyotomaekawa castespecificexpressionsanddiverserolesoftakeoutgenesinthetermitereticulitermessperatus |