Late Male-Killing Viruses in Homona magnanima Identified as Osugoroshi Viruses, Novel Members of Partitiviridae

Late male-killing, a male-specific death after hatching, is a unique phenotype found in Homona magnanima, oriental tea tortrix. The male-killing agent was suspected to be an RNA virus, but details were unknown. We herein successfully isolated and identified the putative male-killing virus as Osugoro...

Full description

Bibliographic Details
Main Authors: Ryosuke Fujita, Maki N. Inoue, Takumi Takamatsu, Hiroshi Arai, Mayu Nishino, Nobuhiko Abe, Kentaro Itokawa, Madoka Nakai, Syun-ichi Urayama, Yuto Chiba, Michael Amoa-Bosompem, Yasuhisa Kunimi
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-01-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2020.620623/full
_version_ 1831524953665568768
author Ryosuke Fujita
Ryosuke Fujita
Maki N. Inoue
Takumi Takamatsu
Hiroshi Arai
Mayu Nishino
Nobuhiko Abe
Kentaro Itokawa
Madoka Nakai
Syun-ichi Urayama
Yuto Chiba
Michael Amoa-Bosompem
Yasuhisa Kunimi
author_facet Ryosuke Fujita
Ryosuke Fujita
Maki N. Inoue
Takumi Takamatsu
Hiroshi Arai
Mayu Nishino
Nobuhiko Abe
Kentaro Itokawa
Madoka Nakai
Syun-ichi Urayama
Yuto Chiba
Michael Amoa-Bosompem
Yasuhisa Kunimi
author_sort Ryosuke Fujita
collection DOAJ
description Late male-killing, a male-specific death after hatching, is a unique phenotype found in Homona magnanima, oriental tea tortrix. The male-killing agent was suspected to be an RNA virus, but details were unknown. We herein successfully isolated and identified the putative male-killing virus as Osugoroshi viruses (OGVs). The three RNA-dependent RNA polymerase genes detected were phylogenetically related to Partitiviridae, a group of segmented double-stranded RNA viruses. Purified dsRNA from a late male-killing strain of H. magnanima revealed 24 segments, in addition to the RdRps, with consensus terminal sequences. These segments included the previously found male-killing agents MK1068 (herein OGV-related RNA16) and MK1241 (OGV-related RNA7) RNAs. Ultramicroscopic observation of purified virions, which induced late male-killing in the progeny of injected moths, showed sizes typical of Partitiviridae. Mathematical modeling showed the importance of late male-killing in facilitating horizontal transmission of OGVs in an H. magnanima population. This study is the first report on the isolation of partiti-like virus from insects, and one thought to be associated with late male-killing, although the viral genomic contents and combinations in each virus are still unknown.
first_indexed 2024-12-16T15:41:18Z
format Article
id doaj.art-df2efe7e59104658a1aecd83a12b6bb4
institution Directory Open Access Journal
issn 1664-302X
language English
last_indexed 2024-12-16T15:41:18Z
publishDate 2021-01-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Microbiology
spelling doaj.art-df2efe7e59104658a1aecd83a12b6bb42022-12-21T22:25:59ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-01-011110.3389/fmicb.2020.620623620623Late Male-Killing Viruses in Homona magnanima Identified as Osugoroshi Viruses, Novel Members of PartitiviridaeRyosuke Fujita0Ryosuke Fujita1Maki N. Inoue2Takumi Takamatsu3Hiroshi Arai4Mayu Nishino5Nobuhiko Abe6Kentaro Itokawa7Madoka Nakai8Syun-ichi Urayama9Yuto Chiba10Michael Amoa-Bosompem11Yasuhisa Kunimi12Laboratory of Sanitary Entomology, Faculty of Agriculture, Kyushu University, Fukuoka, JapanDepartment of Medical Entomology, National Institute of Infectious Diseases, Tokyo, JapanDepartment of Applied Biological Science, Tokyo University of Agriculture and Technology, Fuchu, JapanDepartment of Applied Biological Science, Tokyo University of Agriculture and Technology, Fuchu, JapanDepartment of Applied Biological Science, Tokyo University of Agriculture and Technology, Fuchu, JapanDepartment of Applied Biological Science, Tokyo University of Agriculture and Technology, Fuchu, JapanDepartment of Applied Biological Science, Tokyo University of Agriculture and Technology, Fuchu, JapanPathogen Genomics Center, Natinal Institute of Infectious Diseases, Tokyo, JapanDepartment of Applied Biological Science, Tokyo University of Agriculture and Technology, Fuchu, JapanDepartment of Life and Environmental Sciences, University of Tsukuba, Tsukuba, JapanDepartment of Life and Environmental Sciences, University of Tsukuba, Tsukuba, JapanLaboratory of Sanitary Entomology, Faculty of Agriculture, Kyushu University, Fukuoka, JapanDepartment of Applied Biological Science, Tokyo University of Agriculture and Technology, Fuchu, JapanLate male-killing, a male-specific death after hatching, is a unique phenotype found in Homona magnanima, oriental tea tortrix. The male-killing agent was suspected to be an RNA virus, but details were unknown. We herein successfully isolated and identified the putative male-killing virus as Osugoroshi viruses (OGVs). The three RNA-dependent RNA polymerase genes detected were phylogenetically related to Partitiviridae, a group of segmented double-stranded RNA viruses. Purified dsRNA from a late male-killing strain of H. magnanima revealed 24 segments, in addition to the RdRps, with consensus terminal sequences. These segments included the previously found male-killing agents MK1068 (herein OGV-related RNA16) and MK1241 (OGV-related RNA7) RNAs. Ultramicroscopic observation of purified virions, which induced late male-killing in the progeny of injected moths, showed sizes typical of Partitiviridae. Mathematical modeling showed the importance of late male-killing in facilitating horizontal transmission of OGVs in an H. magnanima population. This study is the first report on the isolation of partiti-like virus from insects, and one thought to be associated with late male-killing, although the viral genomic contents and combinations in each virus are still unknown.https://www.frontiersin.org/articles/10.3389/fmicb.2020.620623/fullmale killingHomona magnanimaPartitiviridaehorizontal transmissioninsect virus
spellingShingle Ryosuke Fujita
Ryosuke Fujita
Maki N. Inoue
Takumi Takamatsu
Hiroshi Arai
Mayu Nishino
Nobuhiko Abe
Kentaro Itokawa
Madoka Nakai
Syun-ichi Urayama
Yuto Chiba
Michael Amoa-Bosompem
Yasuhisa Kunimi
Late Male-Killing Viruses in Homona magnanima Identified as Osugoroshi Viruses, Novel Members of Partitiviridae
Frontiers in Microbiology
male killing
Homona magnanima
Partitiviridae
horizontal transmission
insect virus
title Late Male-Killing Viruses in Homona magnanima Identified as Osugoroshi Viruses, Novel Members of Partitiviridae
title_full Late Male-Killing Viruses in Homona magnanima Identified as Osugoroshi Viruses, Novel Members of Partitiviridae
title_fullStr Late Male-Killing Viruses in Homona magnanima Identified as Osugoroshi Viruses, Novel Members of Partitiviridae
title_full_unstemmed Late Male-Killing Viruses in Homona magnanima Identified as Osugoroshi Viruses, Novel Members of Partitiviridae
title_short Late Male-Killing Viruses in Homona magnanima Identified as Osugoroshi Viruses, Novel Members of Partitiviridae
title_sort late male killing viruses in homona magnanima identified as osugoroshi viruses novel members of partitiviridae
topic male killing
Homona magnanima
Partitiviridae
horizontal transmission
insect virus
url https://www.frontiersin.org/articles/10.3389/fmicb.2020.620623/full
work_keys_str_mv AT ryosukefujita latemalekillingvirusesinhomonamagnanimaidentifiedasosugoroshivirusesnovelmembersofpartitiviridae
AT ryosukefujita latemalekillingvirusesinhomonamagnanimaidentifiedasosugoroshivirusesnovelmembersofpartitiviridae
AT makininoue latemalekillingvirusesinhomonamagnanimaidentifiedasosugoroshivirusesnovelmembersofpartitiviridae
AT takumitakamatsu latemalekillingvirusesinhomonamagnanimaidentifiedasosugoroshivirusesnovelmembersofpartitiviridae
AT hiroshiarai latemalekillingvirusesinhomonamagnanimaidentifiedasosugoroshivirusesnovelmembersofpartitiviridae
AT mayunishino latemalekillingvirusesinhomonamagnanimaidentifiedasosugoroshivirusesnovelmembersofpartitiviridae
AT nobuhikoabe latemalekillingvirusesinhomonamagnanimaidentifiedasosugoroshivirusesnovelmembersofpartitiviridae
AT kentaroitokawa latemalekillingvirusesinhomonamagnanimaidentifiedasosugoroshivirusesnovelmembersofpartitiviridae
AT madokanakai latemalekillingvirusesinhomonamagnanimaidentifiedasosugoroshivirusesnovelmembersofpartitiviridae
AT syunichiurayama latemalekillingvirusesinhomonamagnanimaidentifiedasosugoroshivirusesnovelmembersofpartitiviridae
AT yutochiba latemalekillingvirusesinhomonamagnanimaidentifiedasosugoroshivirusesnovelmembersofpartitiviridae
AT michaelamoabosompem latemalekillingvirusesinhomonamagnanimaidentifiedasosugoroshivirusesnovelmembersofpartitiviridae
AT yasuhisakunimi latemalekillingvirusesinhomonamagnanimaidentifiedasosugoroshivirusesnovelmembersofpartitiviridae