N6-adenosine (m6A) mRNA methylation is required for Tribolium castaneum development and reproduction

Yaoyu Jiao; Subba Reddy Palli

doi:10.1016/j.ibmb.2023.103985

N⁶-adenosine (m⁶A) mRNA methylation is required for Tribolium castaneum development and reproduction

Yaoyu Jiao, Subba Reddy Palli

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

10 Scopus citations

Abstract

Gene expression is regulated at various levels, including post-transcriptional mRNA modifications, where m⁶A methylation is the most common modification of mRNA. The m⁶A methylation regulates multiple stages of mRNA processing, including splicing, export, decay, and translation. How m⁶A modification is involved in insect development is not well known. We used the red flour beetle, Tribolium castaneum, as a model insect to identify the role of m⁶A modification in insect development. RNA interference (RNAi)-mediated knockdown of genes coding for m⁶A writers (m⁶A methyltransferase complex, depositing m⁶A to mRNA) and readers (YTH-domain proteins, recognizing and executing the function of m⁶A) was conducted. Knockdown of most writers during the larval stage caused a failure of ecdysis during eclosion. The loss of m⁶A machinery sterilized both females and males by interfering with the functioning of reproductive systems. Females treated with dsMettl3, the main m⁶A methyltransferase, laid significantly fewer and reduced-size eggs than the control insects. In addition, the embryonic development in eggs laid by dsMettl3 injected females was terminated in the early stages. Knockdown studies also showed that the cytosol m⁶A reader, YTHDF, is likely responsible for executing the function of m⁶A modifications during insect development. These data suggest that m⁶A modifications are critical for T. castaneum development and reproduction.

Original language	English
Article number	103985
Journal	Insect Biochemistry and Molecular Biology
Volume	159
DOIs	https://doi.org/10.1016/j.ibmb.2023.103985
State	Published - Aug 2023

Bibliographical note

Publisher Copyright:
© 2023 Elsevier Ltd

Funding

Research reported in this publication was supported by the National Institute of General Medical Sciences of the National Institutes of Health under Award Number R01GM070559 and the National Institute of Food and Agriculture , US Department of Agriculture (under HATCH Project 2351177000 ). The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

Funders	Funder number
National Institutes of Health (NIH)	R01GM070559
National Institute of General Medical Sciences DP2GM119177 Sophie Dumont National Institute of General Medical Sciences
U.S. Department of Agriculture	2351177000
US Department of Agriculture National Institute of Food and Agriculture, Agriculture and Food Research Initiative

Keywords

Embryogenesis
Mettl3
Oogenesis
RNA modifications
Red flour beetle

ASJC Scopus subject areas

Biochemistry
Molecular Biology
Insect Science

Access to Document

10.1016/j.ibmb.2023.103985

Cite this

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title = "N6-adenosine (m6A) mRNA methylation is required for Tribolium castaneum development and reproduction",

abstract = "Gene expression is regulated at various levels, including post-transcriptional mRNA modifications, where m6A methylation is the most common modification of mRNA. The m6A methylation regulates multiple stages of mRNA processing, including splicing, export, decay, and translation. How m6A modification is involved in insect development is not well known. We used the red flour beetle, Tribolium castaneum, as a model insect to identify the role of m6A modification in insect development. RNA interference (RNAi)-mediated knockdown of genes coding for m6A writers (m6A methyltransferase complex, depositing m6A to mRNA) and readers (YTH-domain proteins, recognizing and executing the function of m6A) was conducted. Knockdown of most writers during the larval stage caused a failure of ecdysis during eclosion. The loss of m6A machinery sterilized both females and males by interfering with the functioning of reproductive systems. Females treated with dsMettl3, the main m6A methyltransferase, laid significantly fewer and reduced-size eggs than the control insects. In addition, the embryonic development in eggs laid by dsMettl3 injected females was terminated in the early stages. Knockdown studies also showed that the cytosol m6A reader, YTHDF, is likely responsible for executing the function of m6A modifications during insect development. These data suggest that m6A modifications are critical for T. castaneum development and reproduction.",

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author = "Yaoyu Jiao and Palli, \{Subba Reddy\}",

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year = "2023",

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doi = "10.1016/j.ibmb.2023.103985",

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AU - Palli, Subba Reddy

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N2 - Gene expression is regulated at various levels, including post-transcriptional mRNA modifications, where m6A methylation is the most common modification of mRNA. The m6A methylation regulates multiple stages of mRNA processing, including splicing, export, decay, and translation. How m6A modification is involved in insect development is not well known. We used the red flour beetle, Tribolium castaneum, as a model insect to identify the role of m6A modification in insect development. RNA interference (RNAi)-mediated knockdown of genes coding for m6A writers (m6A methyltransferase complex, depositing m6A to mRNA) and readers (YTH-domain proteins, recognizing and executing the function of m6A) was conducted. Knockdown of most writers during the larval stage caused a failure of ecdysis during eclosion. The loss of m6A machinery sterilized both females and males by interfering with the functioning of reproductive systems. Females treated with dsMettl3, the main m6A methyltransferase, laid significantly fewer and reduced-size eggs than the control insects. In addition, the embryonic development in eggs laid by dsMettl3 injected females was terminated in the early stages. Knockdown studies also showed that the cytosol m6A reader, YTHDF, is likely responsible for executing the function of m6A modifications during insect development. These data suggest that m6A modifications are critical for T. castaneum development and reproduction.

AB - Gene expression is regulated at various levels, including post-transcriptional mRNA modifications, where m6A methylation is the most common modification of mRNA. The m6A methylation regulates multiple stages of mRNA processing, including splicing, export, decay, and translation. How m6A modification is involved in insect development is not well known. We used the red flour beetle, Tribolium castaneum, as a model insect to identify the role of m6A modification in insect development. RNA interference (RNAi)-mediated knockdown of genes coding for m6A writers (m6A methyltransferase complex, depositing m6A to mRNA) and readers (YTH-domain proteins, recognizing and executing the function of m6A) was conducted. Knockdown of most writers during the larval stage caused a failure of ecdysis during eclosion. The loss of m6A machinery sterilized both females and males by interfering with the functioning of reproductive systems. Females treated with dsMettl3, the main m6A methyltransferase, laid significantly fewer and reduced-size eggs than the control insects. In addition, the embryonic development in eggs laid by dsMettl3 injected females was terminated in the early stages. Knockdown studies also showed that the cytosol m6A reader, YTHDF, is likely responsible for executing the function of m6A modifications during insect development. These data suggest that m6A modifications are critical for T. castaneum development and reproduction.

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