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Evolutionary process of male-killing Wolbachia in tortricid moths

Research Project

Project/Area Number 21KK0105
Research Category

Fund for the Promotion of Joint International Research (Fostering Joint International Research (B))

Allocation TypeMulti-year Fund
Review Section Medium-sized Section 39:Agricultural and environmental biology and related fields
Research InstitutionTokyo University of Agriculture and Technology

Principal Investigator

Inoue Maki  東京農工大学, (連合)農学研究科(研究院), 教授 (80512590)

Co-Investigator(Kenkyū-buntansha) 新井 大  国立研究開発法人農業・食品産業技術総合研究機構, 生物機能利用研究部門, JSPS 特別研究員 (00912255)
神保 宇嗣  独立行政法人国立科学博物館, 標本資料センター, 副コレクションディレクター (10568281)
宮田 真衣  福井大学, 学術研究院工学系部門, 助教 (70946681)
Project Period (FY) 2021-10-07 – 2025-03-31
Project Status Completed (Fiscal Year 2024)
Budget Amount *help
¥18,980,000 (Direct Cost: ¥14,600,000、Indirect Cost: ¥4,380,000)
Fiscal Year 2024: ¥4,030,000 (Direct Cost: ¥3,100,000、Indirect Cost: ¥930,000)
Fiscal Year 2023: ¥5,720,000 (Direct Cost: ¥4,400,000、Indirect Cost: ¥1,320,000)
Fiscal Year 2022: ¥5,850,000 (Direct Cost: ¥4,500,000、Indirect Cost: ¥1,350,000)
Fiscal Year 2021: ¥3,380,000 (Direct Cost: ¥2,600,000、Indirect Cost: ¥780,000)
Keywords共生細菌 / 生殖操作 / 進化プロセス / 生物間相互作用 / ボルバキア
Outline of Research at the Start

最も有名な細胞内共生微生物のひとつであるボルバキアは、昆虫の40-60%に感染し、産雌性単為生殖、遺伝的オスのメス化、細胞質不和合、オス殺しといった宿主の繁殖操作のほか、宿主メスの適応度を上昇させるような宿主操作を行う。これはボルバキアが経卵巣伝播することから、メスの繁殖成功率を向上させ自身の垂直感染率を上げる戦略と考えられている。申請者らは、非モデル生物であるハマキガ科昆虫-ボルバキア-バクテリオファージ系を用いて、これまでに構築した国際共同研究体制をもとに、ボルバキアの重要な表現型の一つであるオス殺しの進化プロセスの解明を目的する。

Outline of Final Research Achievements

Wolbachia, a common endosymbiont in arthropods, can manipulate host reproduction, with male killing being a notable example. However, its evolutionary origin and mechanism remain unclear. This study investigated male-killing Wolbachia in the tea pest moth Homona magnanima. We established lines infected with two strains: wHm-t (male-killing) and wHm-c (non-male-killing). Comparative genome analysis identified a prophage region unique to wHm-t encoding homologs of known male-killing genes, suggesting phage-mediated evolution. Field and phylogenetic analyses showed wHm-t occurs only in Taiwanese populations, while wHm-c is widespread. Functional assays confirmed that the prophage-encoded Hm-oscar gene alone induces male killing, highlighting phage-driven acquisition of this trait.

Academic Significance and Societal Importance of the Research Achievements

本研究により、バクテリオファージが共生細菌における利己的な表現型の獲得に寄与することが示され、進化生物学的観点から極めて意義深い学術的成果が得られた。また、対象としたハマキガ科昆虫はチャ樹に限らず広範な植物を加害する。近年、Wolbachiaは衛生害虫の防除への応用が進められており、本研究で明らかとなったファージおよびオス殺し関連遺伝子は、特定の性を標的とした新たな害虫防除技術への応用的転回により、将来的に高い社会的意義を持つ。加えて、本研究を通じて構築された研究者間の国際的な交流は、アジア地域における相互理解の深化と将来的な研究・教育面での連携基盤の構築にもつながった。

Report

(5 results)
  • 2024 Annual Research Report   Final Research Report ( PDF )
  • 2023 Research-status Report
  • 2022 Research-status Report
  • 2021 Research-status Report
  • Research Products

    (39 results)

All 2025 2024 2023 2022 Other

All Int'l Joint Research (10 results) Journal Article (11 results) (of which Int'l Joint Research: 7 results,  Peer Reviewed: 11 results,  Open Access: 10 results) Presentation (17 results) (of which Int'l Joint Research: 7 results) Book (1 results)

  • [Int'l Joint Research] Can Tho University(ベトナム)

    • Related Report
      2024 Annual Research Report
  • [Int'l Joint Research] 中国行政院農業委員會茶業改良場(中国)

    • Related Report
      2024 Annual Research Report
  • [Int'l Joint Research] Universitas Gadjah Mada(インドネシア)

    • Related Report
      2024 Annual Research Report
  • [Int'l Joint Research] 台湾茶業改良所(中国)

    • Related Report
      2023 Research-status Report
  • [Int'l Joint Research] ガジャマダ大学(インドネシア)

    • Related Report
      2023 Research-status Report
  • [Int'l Joint Research] カントー大学(ベトナム)

    • Related Report
      2023 Research-status Report
  • [Int'l Joint Research] 台湾茶業改良所(その他の国・地域)

    • Related Report
      2022 Research-status Report
  • [Int'l Joint Research] ガジャマダ大学(インドネシア)

    • Related Report
      2022 Research-status Report
  • [Int'l Joint Research] カントー大学(ベトナム)

    • Related Report
      2022 Research-status Report
  • [Int'l Joint Research] 西シドニー大学(オーストラリア)

    • Related Report
      2022 Research-status Report
  • [Journal Article] Evolution of Wolbachia male-killing mechanism within a host species2025

    • Author(s)
      Arai Hiroshi、Wijonarko Arman、Katsuma Susumu、Naka Hideshi、Kageyama Daisuke、Hornett Emily A.、Hurst Gregory D.D.
    • Journal Title

      Current Biology

      Volume: 35 Issue: 9 Pages: 2006-2018.e6

    • DOI

      10.1016/j.cub.2025.03.027

    • Related Report
      2024 Annual Research Report
    • Peer Reviewed / Open Access / Int'l Joint Research
  • [Journal Article] Prophage-encoded Hm-oscar gene recapitulates Wolbachia-induced male killing in the tea tortrix moth Homona magnanima2024

    • Author(s)
      Arai Hiroshi、Katsuma Susumu、Matsuda-Imai Noriko、Lin Shiou-Ruei、Inoue Maki N、Kageyama Daisuke
    • Journal Title

      eLife

      Volume: 13

    • DOI

      10.7554/elife.101101.1

    • Related Report
      2024 Annual Research Report
    • Peer Reviewed / Open Access / Int'l Joint Research
  • [Journal Article] Infection pattern of male-killing viruses alters phenotypes in the tea tortrix moth Homona magnanima2024

    • Author(s)
      Takamatsu Takumi、Arai Hiroshi、Itoh Yoshiyuki、Kozono Takuma、Wu Chien-Fu、Kitaura Kentaro、Moriyama Hiromitsu、Inoue Maki N.
    • Journal Title

      Heredity

      Volume: 134 Issue: 2 Pages: 120-128

    • DOI

      10.1038/s41437-024-00741-x

    • Related Report
      2024 Annual Research Report
    • Peer Reviewed / Open Access
  • [Journal Article] Genomic insights into Spiroplasma endosymbionts that induce male-killing and protective phenotypes in the pea aphid2024

    • Author(s)
      Arai Hiroshi、Legeai Fabrice、Kageyama Daisuke、Sugio Akiko、Simon Jean-Christophe
    • Journal Title

      FEMS Microbiology Letters

      Volume: 371

    • DOI

      10.1093/femsle/fnae027

    • Related Report
      2024 Annual Research Report
    • Peer Reviewed / Open Access / Int'l Joint Research
  • [Journal Article] Conserved infections and reproductive phenotypes of <i>Wolbachia</i> symbionts in Asian tortrix moths2024

    • Author(s)
      Arai Hiroshi、Ueda Masatoshi、Hirano Tatsuya、Akizuki Naoya、Lin Shiou‐Ruei、Hanh Duong Kieu、Widada Jaka、Rohman Muhammad Saifur、Nakai Madoka、Kunimi Yasuhisa、Vang Le Van、Wijonarko Arman、Inoue Maki N.
    • Journal Title

      Environmental Microbiology Reports

      Volume: 16 Issue: 1 Pages: 1-10

    • DOI

      10.1111/1758-2229.13219

    • Related Report
      2023 Research-status Report
    • Peer Reviewed / Open Access / Int'l Joint Research
  • [Journal Article] Combined actions of bacteriophage-encoded genes in Wolbachia-induced male lethality2023

    • Author(s)
      Arai Hiroshi、Anbutsu Hisashi、Nishikawa Yohei、Kogawa Masato、Ishii Kazuo、Hosokawa Masahito、Lin Shiou-Ruei、Ueda Masatoshi、Nakai Madoka、Kunimi Yasuhisa、Harumoto Toshiyuki、Kageyama Daisuke、Takeyama Haruko、Inoue Maki N.
    • Journal Title

      iScience

      Volume: 26 Issue: 6 Pages: 106842-106842

    • DOI

      10.1016/j.isci.2023.106842

    • Related Report
      2023 Research-status Report
    • Peer Reviewed / Open Access / Int'l Joint Research
  • [Journal Article] Diverse Molecular Mechanisms Underlying Microbe-Inducing Male Killing in the Moth Homona magnanima2023

    • Author(s)
      Arai Hiroshi、Takamatsu Takumi、Lin Shiou-Ruei、Mizutani Tetsuya、Omatsu Tsutomu、Katayama Yukie、Nakai Madoka、Kunimi Yasuhisa、Inoue Maki N.
    • Journal Title

      Applied and Environmental Microbiology

      Volume: 89 Issue: 5 Pages: 1-10

    • DOI

      10.1128/aem.02095-22

    • Related Report
      2022 Research-status Report
    • Peer Reviewed / Open Access / Int'l Joint Research
  • [Journal Article] Male-killing mechanisms vary between Spiroplasma species.2022

    • Author(s)
      Hiroshi Arai, Maki N. Inoue, Daisuke Kageyama
    • Journal Title

      Frontiers in Microbiology

      Volume: - Pages: 1075199-1075199

    • DOI

      10.3389/fmicb.2022.1075199

    • Related Report
      2022 Research-status Report
    • Peer Reviewed / Open Access
  • [Journal Article] Distinct effects of three Wolbachia strains on fitness and immune traits in Homona magnanima2022

    • Author(s)
      Masatoshi Ueda, Hiroshi Arai, Kazuki Masaike, Madoka Nakai, Maki N. Inoue
    • Journal Title

      Heredity

      Volume: - Issue: 1 Pages: 1-8

    • DOI

      10.1038/s41437-022-00574-6

    • Related Report
      2022 Research-status Report
    • Peer Reviewed
  • [Journal Article] Mass-rearing and molecular studies in Tortricidae pest insects2022

    • Author(s)
      Arai H, Ishitsubo Y, Nakai M, Inoue MN
    • Journal Title

      Journal of Visualized Experiments

      Volume: 181 Issue: 181

    • DOI

      10.3791/63737

    • Related Report
      2021 Research-status Report
    • Peer Reviewed / Open Access
  • [Journal Article] A simple method to disperse eggs from lepidopteran scalelike egg masses and to observe embryogenesis2022

    • Author(s)
      Arai H, Ishitsubo Y, Nakai M, Inoue MN
    • Journal Title

      Entomological Science

      Volume: 25 Issue: 1 Pages: 1-4

    • DOI

      10.1111/ens.12497

    • Related Report
      2021 Research-status Report
    • Peer Reviewed / Open Access / Int'l Joint Research
  • [Presentation] Host’s fitness and suppress of cytoplasmic incompatibility-inducing Wolbachia2025

    • Author(s)
      Takada I, Takamatsu T. Inoue MN
    • Organizer
      Wolbachia Conference 2025
    • Related Report
      2024 Annual Research Report
    • Int'l Joint Research
  • [Presentation] Endocrine system disorders caused by Osugoroshi virus infection2025

    • Author(s)
      Takamatsu T, Fukutani Y, Xie X, Inoue MN
    • Organizer
      Wolbachia Conference 2025
    • Related Report
      2024 Annual Research Report
    • Int'l Joint Research
  • [Presentation] Host Response to cytoplasmic incompatibility-inducing Wolbachia in Homona magnanima2025

    • Author(s)
      Inoue MN, Konishi K, Takamatsu T, Arai H
    • Organizer
      Wolbachia Conference 2025
    • Related Report
      2024 Annual Research Report
    • Int'l Joint Research
  • [Presentation] チャハマキにおける共生微生物Wolbachia排除の適応的意義2025

    • Author(s)
      高田伊織・高松巧・井上真紀
    • Organizer
      第69回日本応用動物昆虫学会
    • Related Report
      2024 Annual Research Report
  • [Presentation] オスゴロシウイルス感染による内分泌代謝異常の解析2025

    • Author(s)
      高松巧・福谷洋介・謝肖男・井上真紀
    • Organizer
      第69回日本応用動物昆虫学会
    • Related Report
      2024 Annual Research Report
  • [Presentation] Male-killing virus disrupts endocrine system of host males2024

    • Author(s)
      Takamatsu T, Xie X, Inoue MN
    • Organizer
      ICE 2024
    • Related Report
      2024 Annual Research Report
    • Int'l Joint Research
  • [Presentation] 細胞質不和合を引き起こすボルバキアに対する宿主応答2024

    • Author(s)
      小西楓・高松巧・伊藤克彦・新井大・井上真紀
    • Organizer
      第68回日本応用動物昆虫学会
    • Related Report
      2023 Research-status Report
  • [Presentation] Wolbachia-induced male-killing and phage WO: genes, diversity of mechanisms, and evolution2023

    • Author(s)
      Arai H, Katsuma S, Matsuda-Imai N, Sasaki T, Anbutsu T, Wijinarko A, Lin SR, Inoue MN, Kageyama D
    • Organizer
      12th International Wolbachia Conference
    • Related Report
      2023 Research-status Report
    • Int'l Joint Research
  • [Presentation] Different infection patterns of the symbiotic microorganism Wolbachia in male and female of Homona magnanima2023

    • Author(s)
      Konishi K, Arai H, Takamatsu T, Ito K, Inoue MN
    • Organizer
      12th International Wolbachia Conference
    • Related Report
      2023 Research-status Report
    • Int'l Joint Research
  • [Presentation] Effect of late male-killing viruses infected in Homona magnanima2023

    • Author(s)
      Takamatsu T, Itoh Y, Sigeno R, Chien-Fu W, Kitaura K, Inoue MN
    • Organizer
      12th International Wolbachia Conference
    • Related Report
      2023 Research-status Report
    • Int'l Joint Research
  • [Presentation] 共生微生物Wolbachiaのチャハマキ雌雄で異なる感染パターン2022

    • Author(s)
      小西 楓・井上真紀
    • Organizer
      第79回昆虫病理研究会
    • Related Report
      2022 Research-status Report
  • [Presentation] オスゴロシウイルスから産生されるタンパク質の探索2022

    • Author(s)
      高松 巧・茂野 稜・伊藤喜之・井上真紀
    • Organizer
      第79回昆虫病理研究会
    • Related Report
      2022 Research-status Report
  • [Presentation] スゴロシウイルスの性状解析2022

    • Author(s)
      高松巧、伊藤喜之、茂野綾、呉建甫、北浦健太朗、井上真紀
    • Organizer
      第67回日本応用動物昆虫学会
    • Related Report
      2022 Research-status Report
  • [Presentation] 共生微生物Wolbachiaのチャハマキ雌雄で異なる感染パターン2022

    • Author(s)
      小西楓・新井大・高松巧・伊藤克彦・井上真紀
    • Organizer
      第67回日本応用動物昆虫学会
    • Related Report
      2022 Research-status Report
  • [Presentation] 異なるWolbachia株間で保存されていたオス殺しに関わるファージWO領域2022

    • Author(s)
      新井 大・Arman Wijonarko・Shiou-Ruei Lin・Le Van Vang・佐々木 哲彦・和多田 正義・井上 真紀・陰山 大輔
    • Organizer
      第67回日本応用動物昆虫学会
    • Related Report
      2022 Research-status Report
  • [Presentation] 共生微生物Wolbachia のチャハマキ雌雄で異なる感染パター ン2022

    • Author(s)
      小西 楓・新井 大・伊藤 克彦・井上 真紀
    • Organizer
      第66回日本応用動物昆虫学会
    • Related Report
      2021 Research-status Report
  • [Presentation] チャハマキのオスを殺す共生細菌Wolbachia から検出された2022

    • Author(s)
      新井 大・安佛 尚志・Lin Shiou-Ruei・春本 敏之・井上真紀・陰山 大輔
    • Organizer
      第66回日本応用動物昆虫学会
    • Related Report
      2021 Research-status Report
  • [Book] バイオロジカル・コントロール 第2版2022

    • Author(s)
      仲井 まどか、日本 典秀
    • Total Pages
      200
    • Publisher
      朝倉書店
    • ISBN
      9784254420463
    • Related Report
      2022 Research-status Report

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Published: 2021-10-22   Modified: 2026-01-16  

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