A male-killing gene encoded by a symbiotic virus of Drosophila

Daisuke Kageyama (), Toshiyuki Harumoto, Keisuke Nagamine, Akiko Fujiwara, Takafumi N. Sugimoto, Akiya Jouraku, Masaru Tamura, Takehiro K. Katoh and Masayoshi Watada ()
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Daisuke Kageyama: National Agriculture and Food Research Organization
Toshiyuki Harumoto: Kyoto University, Yoshida-honmachi
Keisuke Nagamine: National Agriculture and Food Research Organization
Akiko Fujiwara: Gunma University
Takafumi N. Sugimoto: National Agriculture and Food Research Organization
Akiya Jouraku: National Agriculture and Food Research Organization
Masaru Tamura: National Institute of Health Sciences
Takehiro K. Katoh: Graduate School of Science and Engineering, Ehime University
Masayoshi Watada: Graduate School of Science and Engineering, Ehime University

Nature Communications, 2023, vol. 14, issue 1, 1-9

Abstract: Abstract In most eukaryotes, biparentally inherited nuclear genomes and maternally inherited cytoplasmic genomes have different evolutionary interests. Strongly female-biased sex ratios that are repeatedly observed in various arthropods often result from the male-specific lethality (male-killing) induced by maternally inherited symbiotic bacteria such as Spiroplasma and Wolbachia. However, despite some plausible case reports wherein viruses are raised as male-killers, it is not well understood how viruses, having much smaller genomes than bacteria, are capable of inducing male-killing. Here we show that a maternally inherited double-stranded RNA (dsRNA) virus belonging to the family Partitiviridae (designated DbMKPV1) induces male-killing in Drosophila. DbMKPV1 localizes in the cytoplasm and possesses only four genes, i.e., one gene in each of the four genomic segments (dsRNA1−dsRNA4), in contrast to ca. 1000 or more genes possessed by Spiroplasma or Wolbachia. We also show that a protein (designated PVMKp1; 330 amino acids in size), encoded by a gene on the dsRNA4 segment, is necessary and sufficient for inducing male-killing. Our results imply that male-killing genes can be easily acquired by symbiotic viruses through reassortment and that symbiotic viruses are hidden players in arthropod evolution. We anticipate that host-manipulating genes possessed by symbiotic viruses can be utilized for controlling arthropods.

Date: 2023
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DOI: 10.1038/s41467-023-37145-0

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