Combined actions of bacteriophage-encoded genes in Wolbachia-induced male lethality

Hiroshi Arai; Hisashi Anbutsu; Yohei Nishikawa; Masato Kogawa; Kazuo Ishii; Masahito Hosokawa; Shiou-Ruei Lin; Masatoshi Ueda; Madoka Nakai; Yasuhisa Kunimi; Toshiyuki Harumoto; Daisuke Kageyama; Haruko Takeyama; Maki N. Inoue

iScience (Jun 2023)

Combined actions of bacteriophage-encoded genes in Wolbachia-induced male lethality

Hiroshi Arai,
Hisashi Anbutsu,
Yohei Nishikawa,
Masato Kogawa,
Kazuo Ishii,
Masahito Hosokawa,
Shiou-Ruei Lin,
Masatoshi Ueda,
Madoka Nakai,
Yasuhisa Kunimi,
Toshiyuki Harumoto,
Daisuke Kageyama,
Haruko Takeyama,
Maki N. Inoue

Affiliations

Hiroshi Arai: United Graduate School of Agricultural Science, Tokyo University of Agriculture and Technology, 3-5-8 Saiwai, Fuchu, Tokyo 183-8509, Japan; National Agriculture and Food Research Organization (NARO), 1-2 Owashi, Tsukuba, Ibaraki 305-0851, Japan; Corresponding author
Hisashi Anbutsu: Computational Bio Big-Data Open Innovation Laboratory (CBBD-OIL), National Institute of Advanced Industrial Science and Technology (AIST), 3-4-1 Okubo, Shinjuku-ku, Tokyo 169-8555, Japan; Bioproduction Research Institute, AIST, 1-1-1 Higashi, Tsukuba, Ibaraki 305-8566, Japan; Research Organization for Nano and Life Innovation, Waseda University, 513 Wasedatsurumaki-cho, Shinjuku-ku, Tokyo 162-0041, Japan
Yohei Nishikawa: Computational Bio Big-Data Open Innovation Laboratory (CBBD-OIL), National Institute of Advanced Industrial Science and Technology (AIST), 3-4-1 Okubo, Shinjuku-ku, Tokyo 169-8555, Japan; Research Organization for Nano and Life Innovation, Waseda University, 513 Wasedatsurumaki-cho, Shinjuku-ku, Tokyo 162-0041, Japan
Masato Kogawa: Research Organization for Nano and Life Innovation, Waseda University, 513 Wasedatsurumaki-cho, Shinjuku-ku, Tokyo 162-0041, Japan
Kazuo Ishii: United Graduate School of Agricultural Science, Tokyo University of Agriculture and Technology, 3-5-8 Saiwai, Fuchu, Tokyo 183-8509, Japan
Masahito Hosokawa: Computational Bio Big-Data Open Innovation Laboratory (CBBD-OIL), National Institute of Advanced Industrial Science and Technology (AIST), 3-4-1 Okubo, Shinjuku-ku, Tokyo 169-8555, Japan; Research Organization for Nano and Life Innovation, Waseda University, 513 Wasedatsurumaki-cho, Shinjuku-ku, Tokyo 162-0041, Japan; Institute for Advanced Research of Biosystem Dynamics, Waseda Research Institute for Science and Engineering, Graduate School of Advanced Science and Engineering, Waseda University, 3-4-1 Okubo, Shinjuku-ku, Tokyo 169-8555, Japan; Department of Life Science and Medical Bioscience, Graduate School of Advanced Science and Engineering, Waseda University, 2-2 Wakamatsucho, Shinjuku-ku, Tokyo 162-8480, Japan
Shiou-Ruei Lin: Tea Research and Extension Station, 326011 Chung-Hsing RD, Yangmei, Taoyuan, Taiwan, R.O.C
Masatoshi Ueda: United Graduate School of Agricultural Science, Tokyo University of Agriculture and Technology, 3-5-8 Saiwai, Fuchu, Tokyo 183-8509, Japan
Madoka Nakai: United Graduate School of Agricultural Science, Tokyo University of Agriculture and Technology, 3-5-8 Saiwai, Fuchu, Tokyo 183-8509, Japan
Yasuhisa Kunimi: United Graduate School of Agricultural Science, Tokyo University of Agriculture and Technology, 3-5-8 Saiwai, Fuchu, Tokyo 183-8509, Japan
Toshiyuki Harumoto: Hakubi Center for Advanced Research, Kyoto University. Yoshida-honmachi, Sakyo-ku, Kyoto 606-8501, Japan; Graduate School of Biostudies, Kyoto University, Yoshida-Konoe-cho, Sakyo-ku, Kyoto 606-8501, Japan
Daisuke Kageyama: National Agriculture and Food Research Organization (NARO), 1-2 Owashi, Tsukuba, Ibaraki 305-0851, Japan
Haruko Takeyama: Computational Bio Big-Data Open Innovation Laboratory (CBBD-OIL), National Institute of Advanced Industrial Science and Technology (AIST), 3-4-1 Okubo, Shinjuku-ku, Tokyo 169-8555, Japan; Research Organization for Nano and Life Innovation, Waseda University, 513 Wasedatsurumaki-cho, Shinjuku-ku, Tokyo 162-0041, Japan; Institute for Advanced Research of Biosystem Dynamics, Waseda Research Institute for Science and Engineering, Graduate School of Advanced Science and Engineering, Waseda University, 3-4-1 Okubo, Shinjuku-ku, Tokyo 169-8555, Japan; Department of Life Science and Medical Bioscience, Graduate School of Advanced Science and Engineering, Waseda University, 2-2 Wakamatsucho, Shinjuku-ku, Tokyo 162-8480, Japan; Corresponding author
Maki N. Inoue: United Graduate School of Agricultural Science, Tokyo University of Agriculture and Technology, 3-5-8 Saiwai, Fuchu, Tokyo 183-8509, Japan; Corresponding author

Journal volume & issue: Vol. 26, no. 6
p. 106842

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Summary: Some Wolbachia endosymbionts induce male killing, whereby male offspring of infected females are killed during development; however, the origin and diversity of the underlying mechanisms remain unclear. In this study, we identified a 76 kbp prophage region specific to male-killing Wolbachia hosted by the moth Homona magnanima. The prophage encoded a homolog of the male-killing gene oscar in Ostrinia moths and the wmk gene that induces various toxicities in Drosophila melanogaster. Upon overexpressing these genes in D. melanogaster, wmk-1 and wmk-3 killed all males and most females, whereas Hm-oscar, wmk-2, and wmk-4 had no impact on insect survival. Strikingly, co-expression of tandemly arrayed wmk-3 and wmk-4 killed 90% of males and restored 70% of females, suggesting their conjugated functions for male-specific lethality. While the male-killing gene in the native host remains unknown, our findings highlight the role of bacteriophages in male-killing evolution and differences in male-killing mechanisms among insects.

Published in iScience

ISSN: 2589-0042 (Online)
Publisher: Elsevier
Country of publisher: United States
LCC subjects: Science
Website: http://www.cell.com/iscience/home

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