Dual roles of methoprene-tolerant gene TaMet in male molting and female reproduction of the tomato leafminer, Tuta absoluta (meyrick)

The tomato leafminer (Tuta absoluta) is a highly destructive global quarantine pest. The methoprene-tolerant (Met) protein, a member of the bHLH/PAS family of transcription factors, forms complexes with other family members to transduce the juvenile hormone signal, which regulates insect growth and...

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Main Authors: Tingwei Zhang, Kai Xu, Deqian Liu, Hang Ma, Wenbiao Liu, Wenjia Yang
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-11-01
Series:Frontiers in Physiology
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Online Access:https://www.frontiersin.org/articles/10.3389/fphys.2024.1500391/full
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author Tingwei Zhang
Kai Xu
Deqian Liu
Hang Ma
Wenbiao Liu
Wenjia Yang
author_facet Tingwei Zhang
Kai Xu
Deqian Liu
Hang Ma
Wenbiao Liu
Wenjia Yang
author_sort Tingwei Zhang
collection DOAJ
description The tomato leafminer (Tuta absoluta) is a highly destructive global quarantine pest. The methoprene-tolerant (Met) protein, a member of the bHLH/PAS family of transcription factors, forms complexes with other family members to transduce the juvenile hormone signal, which regulates insect growth and development. However, the functions of the TaMet gene have rarely been studied in T. absoluta. Herein, we investigated the significance of TaMet in T. absoluta. Spatiotemporal expression analysis revealed that TaMet exhibited comparable expression patterns in males and females, with high expression levels during the early pupal and early adult stages. TaMet was predominantly expressed in the female ovary and male wing. TaMet knockdown impaired ovarian development in female adults, causing irregular arrangement and increased spacing of the egg epithelial cells in the ovary. Silencing TaMet also led to a 67.25% reduction in female spawning and a 67.21% decrease in the offspring hatching rate. Furthermore, the vitellogenin content was significantly diminished, and the expression levels of vitellogenin (Vg) and vitellogenin receptor (VgR) genes were significantly downregulated. In contrast, silencing TaMet in 3-day-old male pupae resulted in an 80% mortality rate and various phenotypic abnormalities, including body melanism, molting defects, and wing deformities. Moreover, the expression levels of wing development and chitin metabolism genes decreased significantly after knocking down TaMet. Our results indicate that TaMet plays a significant dual role in male molting and female reproduction of T. absoluta.
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publishDate 2024-11-01
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spelling doaj-art-fcf1cdd1671c4ccabb3be8d0e49d6dfd2024-11-14T15:23:09ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2024-11-011510.3389/fphys.2024.15003911500391Dual roles of methoprene-tolerant gene TaMet in male molting and female reproduction of the tomato leafminer, Tuta absoluta (meyrick)Tingwei Zhang0Kai Xu1Deqian Liu2Hang Ma3Wenbiao Liu4Wenjia Yang5Key Laboratory of Surveillance and Management of Invasive Alien Species in Guizhou Education Department, College of Biological and Environmental Engineering, Guiyang University, Guiyang, ChinaKey Laboratory of Surveillance and Management of Invasive Alien Species in Guizhou Education Department, College of Biological and Environmental Engineering, Guiyang University, Guiyang, ChinaKey Laboratory of Surveillance and Management of Invasive Alien Species in Guizhou Education Department, College of Biological and Environmental Engineering, Guiyang University, Guiyang, ChinaYunnan Yuantianhua Co., Ltd Research and Development Center, Kunming, ChinaYunnan Yuantianhua Co., Ltd Research and Development Center, Kunming, ChinaKey Laboratory of Surveillance and Management of Invasive Alien Species in Guizhou Education Department, College of Biological and Environmental Engineering, Guiyang University, Guiyang, ChinaThe tomato leafminer (Tuta absoluta) is a highly destructive global quarantine pest. The methoprene-tolerant (Met) protein, a member of the bHLH/PAS family of transcription factors, forms complexes with other family members to transduce the juvenile hormone signal, which regulates insect growth and development. However, the functions of the TaMet gene have rarely been studied in T. absoluta. Herein, we investigated the significance of TaMet in T. absoluta. Spatiotemporal expression analysis revealed that TaMet exhibited comparable expression patterns in males and females, with high expression levels during the early pupal and early adult stages. TaMet was predominantly expressed in the female ovary and male wing. TaMet knockdown impaired ovarian development in female adults, causing irregular arrangement and increased spacing of the egg epithelial cells in the ovary. Silencing TaMet also led to a 67.25% reduction in female spawning and a 67.21% decrease in the offspring hatching rate. Furthermore, the vitellogenin content was significantly diminished, and the expression levels of vitellogenin (Vg) and vitellogenin receptor (VgR) genes were significantly downregulated. In contrast, silencing TaMet in 3-day-old male pupae resulted in an 80% mortality rate and various phenotypic abnormalities, including body melanism, molting defects, and wing deformities. Moreover, the expression levels of wing development and chitin metabolism genes decreased significantly after knocking down TaMet. Our results indicate that TaMet plays a significant dual role in male molting and female reproduction of T. absoluta.https://www.frontiersin.org/articles/10.3389/fphys.2024.1500391/fullinvasive speciesTuta absolutaRNAifunctional differentiationreproductionmolting
spellingShingle Tingwei Zhang
Kai Xu
Deqian Liu
Hang Ma
Wenbiao Liu
Wenjia Yang
Dual roles of methoprene-tolerant gene TaMet in male molting and female reproduction of the tomato leafminer, Tuta absoluta (meyrick)
Frontiers in Physiology
invasive species
Tuta absoluta
RNAi
functional differentiation
reproduction
molting
title Dual roles of methoprene-tolerant gene TaMet in male molting and female reproduction of the tomato leafminer, Tuta absoluta (meyrick)
title_full Dual roles of methoprene-tolerant gene TaMet in male molting and female reproduction of the tomato leafminer, Tuta absoluta (meyrick)
title_fullStr Dual roles of methoprene-tolerant gene TaMet in male molting and female reproduction of the tomato leafminer, Tuta absoluta (meyrick)
title_full_unstemmed Dual roles of methoprene-tolerant gene TaMet in male molting and female reproduction of the tomato leafminer, Tuta absoluta (meyrick)
title_short Dual roles of methoprene-tolerant gene TaMet in male molting and female reproduction of the tomato leafminer, Tuta absoluta (meyrick)
title_sort dual roles of methoprene tolerant gene tamet in male molting and female reproduction of the tomato leafminer tuta absoluta meyrick
topic invasive species
Tuta absoluta
RNAi
functional differentiation
reproduction
molting
url https://www.frontiersin.org/articles/10.3389/fphys.2024.1500391/full
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