Neofunctionalization of a second insulin receptor gene in the wing-dimorphic planthopper, Nilaparvata lugens.

A single insulin receptor (InR) gene has been identified and extensively studied in model species ranging from nematodes to mice. However, most insects possess additional copies of InR, yet the functional significance, if any, of alternate InRs is unknown. Here, we used the wing-dimorphic brown plan...

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Main Authors: Wen-Hua Xue, Nan Xu, Sun-Jie Chen, Xin-Yang Liu, Jin-Li Zhang, Hai-Jun Xu
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2021-06-01
Series:PLoS Genetics
Online Access:https://doi.org/10.1371/journal.pgen.1009653
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spelling doaj-a406c27de97a463e9ee29717b93baf312021-07-24T04:31:12ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042021-06-01176e100965310.1371/journal.pgen.1009653Neofunctionalization of a second insulin receptor gene in the wing-dimorphic planthopper, Nilaparvata lugens.Wen-Hua XueNan XuSun-Jie ChenXin-Yang LiuJin-Li ZhangHai-Jun XuA single insulin receptor (InR) gene has been identified and extensively studied in model species ranging from nematodes to mice. However, most insects possess additional copies of InR, yet the functional significance, if any, of alternate InRs is unknown. Here, we used the wing-dimorphic brown planthopper (BPH) as a model system to query the role of a second InR copy in insects. NlInR2 resembled the BPH InR homologue (NlInR1) in terms of nymph development and reproduction, but revealed distinct regulatory roles in fuel metabolism, lifespan, and starvation tolerance. Unlike a lethal phenotype derived from NlInR1 null, homozygous NlInR2 null mutants were viable and accelerated DNA replication and cell proliferation in wing cells, thus redirecting short-winged-destined BPHs to develop into long-winged morphs. Additionally, the proper expression of NlInR2 was needed to maintain symmetric vein patterning in wings. Our findings provide the first direct evidence for the regulatory complexity of the two InR paralogues in insects, implying the functionally independent evolution of multiple InRs in invertebrates.https://doi.org/10.1371/journal.pgen.1009653
collection DOAJ
language English
format Article
sources DOAJ
author Wen-Hua Xue
Nan Xu
Sun-Jie Chen
Xin-Yang Liu
Jin-Li Zhang
Hai-Jun Xu
spellingShingle Wen-Hua Xue
Nan Xu
Sun-Jie Chen
Xin-Yang Liu
Jin-Li Zhang
Hai-Jun Xu
Neofunctionalization of a second insulin receptor gene in the wing-dimorphic planthopper, Nilaparvata lugens.
PLoS Genetics
author_facet Wen-Hua Xue
Nan Xu
Sun-Jie Chen
Xin-Yang Liu
Jin-Li Zhang
Hai-Jun Xu
author_sort Wen-Hua Xue
title Neofunctionalization of a second insulin receptor gene in the wing-dimorphic planthopper, Nilaparvata lugens.
title_short Neofunctionalization of a second insulin receptor gene in the wing-dimorphic planthopper, Nilaparvata lugens.
title_full Neofunctionalization of a second insulin receptor gene in the wing-dimorphic planthopper, Nilaparvata lugens.
title_fullStr Neofunctionalization of a second insulin receptor gene in the wing-dimorphic planthopper, Nilaparvata lugens.
title_full_unstemmed Neofunctionalization of a second insulin receptor gene in the wing-dimorphic planthopper, Nilaparvata lugens.
title_sort neofunctionalization of a second insulin receptor gene in the wing-dimorphic planthopper, nilaparvata lugens.
publisher Public Library of Science (PLoS)
series PLoS Genetics
issn 1553-7390
1553-7404
publishDate 2021-06-01
description A single insulin receptor (InR) gene has been identified and extensively studied in model species ranging from nematodes to mice. However, most insects possess additional copies of InR, yet the functional significance, if any, of alternate InRs is unknown. Here, we used the wing-dimorphic brown planthopper (BPH) as a model system to query the role of a second InR copy in insects. NlInR2 resembled the BPH InR homologue (NlInR1) in terms of nymph development and reproduction, but revealed distinct regulatory roles in fuel metabolism, lifespan, and starvation tolerance. Unlike a lethal phenotype derived from NlInR1 null, homozygous NlInR2 null mutants were viable and accelerated DNA replication and cell proliferation in wing cells, thus redirecting short-winged-destined BPHs to develop into long-winged morphs. Additionally, the proper expression of NlInR2 was needed to maintain symmetric vein patterning in wings. Our findings provide the first direct evidence for the regulatory complexity of the two InR paralogues in insects, implying the functionally independent evolution of multiple InRs in invertebrates.
url https://doi.org/10.1371/journal.pgen.1009653
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