Knockout BR-C induces premature expression of E93 thus triggering adult differentiation under larval morphology

Chang Liu; Mian Zhi Wu; Zi Jing Zheng; Shu Ting Fan; Jin Fang Tan; Yaoyu Jiao; Subba Reddy Palli; Guan Heng Zhu

doi:10.1002/ps.8592

Knockout BR-C induces premature expression of E93 thus triggering adult differentiation under larval morphology

Chang Liu, Mian Zhi Wu, Zi Jing Zheng, Shu Ting Fan, Jin Fang Tan, Yaoyu Jiao, Subba Reddy Palli, Guan Heng Zhu

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

Abstract

BACKGROUND: Holometabolan pupal-specifier broad-complex (BR-C) and adult specifier ecdysone-induced protein 93F (E93) are essential for metamorphosis; however, their interaction and effects on programmed cell death and cell differentiation during pupation remain unclear. RESULTS: Here, multiple single-guide RNA (sgRNA)-mediated mosaic knockout of BR-C induced a deformed larva/pupa intermediate phenotype in Spodoptera frugiperda. Quantitative real-time polymerase chain reaction (qPCR) analysis showed that the adult specifier E93 was prematurely expressed in the BR-C mutants during the penultimate and last instar larval stages. Additionally, histological observation and TUNEL assay showed that apoptosis in the fat body and midgut was activated in the larval tissues; astonishingly, the adult midgut appeared in the pupae of BR-C mutants. CONCLUSION: Overall, the results demonstrated that the premature expression of E93 induced by lack of BR-C triggers adult differentiation during the larval stages, which revealed the inhibitory effect of BR-C on E93 during metamorphosis in S. frugiperda.

Original language	English
Pages (from-to)	1923-1933
Number of pages	11
Journal	Pest Management Science
Volume	81
Issue number	4
DOIs	https://doi.org/10.1002/ps.8592
State	Published - Apr 2025

Bibliographical note

Publisher Copyright:
© 2024 Society of Chemical Industry.

Funding

This study was supported by the National Natural Science Foundation of China (grant number: 32102190), partly and by the Guangdong Basic and Applied Basic Research Foundation (grant number: 2024A1515010682), by the Shenzhen Science and Technology Program (grant number: JCYJ20230807111216033), and by the Fundamental Research Funds for the Central University, Sun Yat-sen University (grant number: 24lgqb011). This study was supported by the National Natural Science Foundation of China (grant number: 32102190), partly and by the Guangdong Basic and Applied Basic Research Foundation (grant number: 2024A1515010682), by the Shenzhen Science and Technology Program (grant number: JCYJ20230807111216033), and by the Fundamental Research Funds for the Central University, Sun Yat\u2010sen University (grant number: 24lgqb011).

Funders	Funder number
Fundamental Research Funds for the Central Universities
National Natural Science Foundation of China (NSFC)	32102190
National Natural Science Foundation of China (NSFC)
Basic and Applied Basic Research Foundation of Guangdong Province	2024A1515010682
Basic and Applied Basic Research Foundation of Guangdong Province
Science, Technology and Innovation Commission of Shenzhen Municipality	JCYJ20230807111216033
Science, Technology and Innovation Commission of Shenzhen Municipality
Sun Yat-Sen University	24lgqb011
Sun Yat-Sen University

Keywords

CRISPR/Cas9
Spodoptera frugiperda
apoptosis
metamorphosis
sgRNA

ASJC Scopus subject areas

Agronomy and Crop Science
Insect Science

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10.1002/ps.8592

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title = "Knockout BR-C induces premature expression of E93 thus triggering adult differentiation under larval morphology",

abstract = "BACKGROUND: Holometabolan pupal-specifier broad-complex (BR-C) and adult specifier ecdysone-induced protein 93F (E93) are essential for metamorphosis; however, their interaction and effects on programmed cell death and cell differentiation during pupation remain unclear. RESULTS: Here, multiple single-guide RNA (sgRNA)-mediated mosaic knockout of BR-C induced a deformed larva/pupa intermediate phenotype in Spodoptera frugiperda. Quantitative real-time polymerase chain reaction (qPCR) analysis showed that the adult specifier E93 was prematurely expressed in the BR-C mutants during the penultimate and last instar larval stages. Additionally, histological observation and TUNEL assay showed that apoptosis in the fat body and midgut was activated in the larval tissues; astonishingly, the adult midgut appeared in the pupae of BR-C mutants. CONCLUSION: Overall, the results demonstrated that the premature expression of E93 induced by lack of BR-C triggers adult differentiation during the larval stages, which revealed the inhibitory effect of BR-C on E93 during metamorphosis in S. frugiperda.",

keywords = "CRISPR/Cas9, Spodoptera frugiperda, apoptosis, metamorphosis, sgRNA",

author = "Chang Liu and Wu, \{Mian Zhi\} and Zheng, \{Zi Jing\} and Fan, \{Shu Ting\} and Tan, \{Jin Fang\} and Yaoyu Jiao and Palli, \{Subba Reddy\} and Zhu, \{Guan Heng\}",

note = "Publisher Copyright: {\textcopyright} 2024 Society of Chemical Industry.",

year = "2025",

month = apr,

doi = "10.1002/ps.8592",

language = "English",

volume = "81",

pages = "1923--1933",

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AU - Liu, Chang

AU - Wu, Mian Zhi

AU - Zheng, Zi Jing

AU - Fan, Shu Ting

AU - Tan, Jin Fang

AU - Jiao, Yaoyu

AU - Palli, Subba Reddy

AU - Zhu, Guan Heng

PY - 2025/4

Y1 - 2025/4

N2 - BACKGROUND: Holometabolan pupal-specifier broad-complex (BR-C) and adult specifier ecdysone-induced protein 93F (E93) are essential for metamorphosis; however, their interaction and effects on programmed cell death and cell differentiation during pupation remain unclear. RESULTS: Here, multiple single-guide RNA (sgRNA)-mediated mosaic knockout of BR-C induced a deformed larva/pupa intermediate phenotype in Spodoptera frugiperda. Quantitative real-time polymerase chain reaction (qPCR) analysis showed that the adult specifier E93 was prematurely expressed in the BR-C mutants during the penultimate and last instar larval stages. Additionally, histological observation and TUNEL assay showed that apoptosis in the fat body and midgut was activated in the larval tissues; astonishingly, the adult midgut appeared in the pupae of BR-C mutants. CONCLUSION: Overall, the results demonstrated that the premature expression of E93 induced by lack of BR-C triggers adult differentiation during the larval stages, which revealed the inhibitory effect of BR-C on E93 during metamorphosis in S. frugiperda.

AB - BACKGROUND: Holometabolan pupal-specifier broad-complex (BR-C) and adult specifier ecdysone-induced protein 93F (E93) are essential for metamorphosis; however, their interaction and effects on programmed cell death and cell differentiation during pupation remain unclear. RESULTS: Here, multiple single-guide RNA (sgRNA)-mediated mosaic knockout of BR-C induced a deformed larva/pupa intermediate phenotype in Spodoptera frugiperda. Quantitative real-time polymerase chain reaction (qPCR) analysis showed that the adult specifier E93 was prematurely expressed in the BR-C mutants during the penultimate and last instar larval stages. Additionally, histological observation and TUNEL assay showed that apoptosis in the fat body and midgut was activated in the larval tissues; astonishingly, the adult midgut appeared in the pupae of BR-C mutants. CONCLUSION: Overall, the results demonstrated that the premature expression of E93 induced by lack of BR-C triggers adult differentiation during the larval stages, which revealed the inhibitory effect of BR-C on E93 during metamorphosis in S. frugiperda.

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Knockout BR-C induces premature expression of E93 thus triggering adult differentiation under larval morphology

Abstract

Bibliographical note

Funding

Keywords

ASJC Scopus subject areas

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