Knockout of a testis-specific gene cluster impairs male fertility in the fall armyworm, Spodoptera frugiperda

Pei Wang; Yuchen Zhao; Yalan Cheng; Siyu Tian; Yuxuan Bai; Junfeng Zuo; Subba Reddy Palli; Xien Chen

doi:10.1002/ps.8634

Knockout of a testis-specific gene cluster impairs male fertility in the fall armyworm, Spodoptera frugiperda

Pei Wang, Yuchen Zhao, Yalan Cheng, Siyu Tian, Yuxuan Bai, Junfeng Zuo, Subba Reddy Palli, Xien Chen

Research output: Contribution to journal › Article › peer-review

3 Scopus citations

Abstract

BACKGROUND: The function of some testis-specific genes (TSGs) in model insects have been studied, but their function in non-model insects remains largely unexplored. In the present study, we identified several TSGs in the fall armyworm (FAW), a significant agricultural pest, through comparative transcriptomic analysis. A testis-specific gene cluster (TSGC) comprising multiple functional genes and long non-coding RNAs was found. RESULTS: Quantitative PCR analysis validated the testis-specific expression of genes within this cluster across different developmental stages. Interspecies collinearity analysis indicated that this TSGC is conserved among lepidopterans. To elucidate the function of this TSGC, we employed the CRISPR/Cas9 gene-editing technique to generate loss-of-function mutants. Notably, the hatching rate of eggs produced by wild-type females mated with mutant males (approximately 30%) was substantially lower than that of eggs from wild-type females mated with wild-type males (approximately 80%). Additionally, a significant reduction in the size and number of sperm was observed in the testis of mutant males compared to wild-type males. CONCLUSION: Collectively, this study not only elucidates the role of the TSGC in supporting male fertility in the FAW, which provides valuable information for understanding the mechanism of male reproduction in insects, but also identifies potential target genes for the development of genetic control strategies against lepidopteran pests.

Original language	English
Pages (from-to)	2355-2363
Number of pages	9
Journal	Pest Management Science
Volume	81
Issue number	4
DOIs	https://doi.org/10.1002/ps.8634
State	Published - Apr 2025

Bibliographical note

Publisher Copyright:
© 2025 Society of Chemical Industry.

Funding

This study was supported by Start-up funding from Northwest A&F University (Z1013023011) to XC and the National Institute of General Medical Sciences of the National Institutes of Health under Award Number R01GM070559 and the US Department of Agriculture (under HATCH Project 2353057000) to SRP. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health or the US Department of Agriculture. This study was supported by Start\u2010up funding from Northwest A&F University (Z1013023011) to XC and the National Institute of General Medical Sciences of the National Institutes of Health under Award Number R01GM070559 and the US Department of Agriculture (under HATCH Project 2353057000) to SRP. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health or the US Department of Agriculture.

Funders	Funder number
National Institute of General Medical Sciences
Northwest Agriculture and Forestry University	Z1013023011
Northwest Agriculture and Forestry University
National Institutes of Health (NIH)	R01GM070559
National Institutes of Health (NIH)
U.S. Department of Agriculture	2353057000
U.S. Department of Agriculture

Keywords

CRISPR/Cas9
fall armyworm
male fertility
testis development
testis-specific gene cluster

ASJC Scopus subject areas

Agronomy and Crop Science
Insect Science

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10.1002/ps.8634

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title = "Knockout of a testis-specific gene cluster impairs male fertility in the fall armyworm, Spodoptera frugiperda",

abstract = "BACKGROUND: The function of some testis-specific genes (TSGs) in model insects have been studied, but their function in non-model insects remains largely unexplored. In the present study, we identified several TSGs in the fall armyworm (FAW), a significant agricultural pest, through comparative transcriptomic analysis. A testis-specific gene cluster (TSGC) comprising multiple functional genes and long non-coding RNAs was found. RESULTS: Quantitative PCR analysis validated the testis-specific expression of genes within this cluster across different developmental stages. Interspecies collinearity analysis indicated that this TSGC is conserved among lepidopterans. To elucidate the function of this TSGC, we employed the CRISPR/Cas9 gene-editing technique to generate loss-of-function mutants. Notably, the hatching rate of eggs produced by wild-type females mated with mutant males (approximately 30\%) was substantially lower than that of eggs from wild-type females mated with wild-type males (approximately 80\%). Additionally, a significant reduction in the size and number of sperm was observed in the testis of mutant males compared to wild-type males. CONCLUSION: Collectively, this study not only elucidates the role of the TSGC in supporting male fertility in the FAW, which provides valuable information for understanding the mechanism of male reproduction in insects, but also identifies potential target genes for the development of genetic control strategies against lepidopteran pests.",

keywords = "CRISPR/Cas9, fall armyworm, male fertility, testis development, testis-specific gene cluster",

author = "Pei Wang and Yuchen Zhao and Yalan Cheng and Siyu Tian and Yuxuan Bai and Junfeng Zuo and Palli, \{Subba Reddy\} and Xien Chen",

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doi = "10.1002/ps.8634",

language = "English",

volume = "81",

pages = "2355--2363",

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AU - Wang, Pei

AU - Zhao, Yuchen

AU - Cheng, Yalan

AU - Tian, Siyu

AU - Bai, Yuxuan

AU - Zuo, Junfeng

AU - Palli, Subba Reddy

AU - Chen, Xien

PY - 2025/4

Y1 - 2025/4

N2 - BACKGROUND: The function of some testis-specific genes (TSGs) in model insects have been studied, but their function in non-model insects remains largely unexplored. In the present study, we identified several TSGs in the fall armyworm (FAW), a significant agricultural pest, through comparative transcriptomic analysis. A testis-specific gene cluster (TSGC) comprising multiple functional genes and long non-coding RNAs was found. RESULTS: Quantitative PCR analysis validated the testis-specific expression of genes within this cluster across different developmental stages. Interspecies collinearity analysis indicated that this TSGC is conserved among lepidopterans. To elucidate the function of this TSGC, we employed the CRISPR/Cas9 gene-editing technique to generate loss-of-function mutants. Notably, the hatching rate of eggs produced by wild-type females mated with mutant males (approximately 30%) was substantially lower than that of eggs from wild-type females mated with wild-type males (approximately 80%). Additionally, a significant reduction in the size and number of sperm was observed in the testis of mutant males compared to wild-type males. CONCLUSION: Collectively, this study not only elucidates the role of the TSGC in supporting male fertility in the FAW, which provides valuable information for understanding the mechanism of male reproduction in insects, but also identifies potential target genes for the development of genetic control strategies against lepidopteran pests.

AB - BACKGROUND: The function of some testis-specific genes (TSGs) in model insects have been studied, but their function in non-model insects remains largely unexplored. In the present study, we identified several TSGs in the fall armyworm (FAW), a significant agricultural pest, through comparative transcriptomic analysis. A testis-specific gene cluster (TSGC) comprising multiple functional genes and long non-coding RNAs was found. RESULTS: Quantitative PCR analysis validated the testis-specific expression of genes within this cluster across different developmental stages. Interspecies collinearity analysis indicated that this TSGC is conserved among lepidopterans. To elucidate the function of this TSGC, we employed the CRISPR/Cas9 gene-editing technique to generate loss-of-function mutants. Notably, the hatching rate of eggs produced by wild-type females mated with mutant males (approximately 30%) was substantially lower than that of eggs from wild-type females mated with wild-type males (approximately 80%). Additionally, a significant reduction in the size and number of sperm was observed in the testis of mutant males compared to wild-type males. CONCLUSION: Collectively, this study not only elucidates the role of the TSGC in supporting male fertility in the FAW, which provides valuable information for understanding the mechanism of male reproduction in insects, but also identifies potential target genes for the development of genetic control strategies against lepidopteran pests.

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Knockout of a testis-specific gene cluster impairs male fertility in the fall armyworm, Spodoptera frugiperda

Abstract

Bibliographical note

Funding

Keywords

ASJC Scopus subject areas

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