RNA m6A Methylation Suppresses Insect Juvenile Hormone Degradation to Minimize Fitness Costs in Response to A Pathogenic Attack
Abstract Bioinsecticides and transgenic crops based on the bacterial pathogen Bacillus thuringiensis (Bt) can effectively control diverse agricultural insect pests, nevertheless, the evolution of resistance without obvious fitness costs has seriously eroded the sustainable use of these Bt products....
| Main Authors: | , , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Wiley
2024-02-01
|
| Series: | Advanced Science |
| Subjects: | |
| Online Access: | https://doi.org/10.1002/advs.202307650 |
| _version_ | 1797319244240650240 |
|---|---|
| author | Zhaojiang Guo Yang Bai Xinyi Zhang Le Guo Liuhong Zhu Dan Sun Kaiyue Sun Xudan Xu Xin Yang Wen Xie Shaoli Wang Qingjun Wu Neil Crickmore Xuguo Zhou Youjun Zhang |
| author_facet | Zhaojiang Guo Yang Bai Xinyi Zhang Le Guo Liuhong Zhu Dan Sun Kaiyue Sun Xudan Xu Xin Yang Wen Xie Shaoli Wang Qingjun Wu Neil Crickmore Xuguo Zhou Youjun Zhang |
| author_sort | Zhaojiang Guo |
| collection | DOAJ |
| description | Abstract Bioinsecticides and transgenic crops based on the bacterial pathogen Bacillus thuringiensis (Bt) can effectively control diverse agricultural insect pests, nevertheless, the evolution of resistance without obvious fitness costs has seriously eroded the sustainable use of these Bt products. Recently, it has been discovered that an increased titer of juvenile hormone (JH) favors an insect host (Plutella xylostella) to enhance fitness whilst resisting the Bt pathogen, however, the underlying regulatory mechanisms of the increased JH titer are obscure. Here, the involvement of N6‐methyladenosine (m6A) RNA modification in modulating the availability of JH in this process is defined. Specifically, it is found that two m6A methyltransferase subunit genes, PxMettl3 and PxMettl14, repress the expression of a key JH‐degrading enzyme JH esterase (JHE) to induce an increased JH titer, mitigating the fitness costs associated with a robust defense against the Bt pathogen. This study identifies an as‐yet uncharacterized m6A‐mediated epigenetic regulator of insect hormones for maintaining fitness during pathogen defense and unveils an emerging Bt resistance‐related m6A methylation atlas in insects, which further expands the functional landscape of m6A modification and showcases the pivotal role of epigenetic regulation in host‐pathogen interactions. |
| first_indexed | 2024-03-08T04:04:07Z |
| format | Article |
| id | doaj.art-da7be63f7785468baca143fe4977786b |
| institution | Directory Open Access Journal |
| issn | 2198-3844 |
| language | English |
| last_indexed | 2024-03-08T04:04:07Z |
| publishDate | 2024-02-01 |
| publisher | Wiley |
| record_format | Article |
| series | Advanced Science |
| spelling | doaj.art-da7be63f7785468baca143fe4977786b2024-02-09T08:26:35ZengWileyAdvanced Science2198-38442024-02-01116n/an/a10.1002/advs.202307650RNA m6A Methylation Suppresses Insect Juvenile Hormone Degradation to Minimize Fitness Costs in Response to A Pathogenic AttackZhaojiang Guo0Yang Bai1Xinyi Zhang2Le Guo3Liuhong Zhu4Dan Sun5Kaiyue Sun6Xudan Xu7Xin Yang8Wen Xie9Shaoli Wang10Qingjun Wu11Neil Crickmore12Xuguo Zhou13Youjun Zhang14State Key Laboratory of Vegetable Biobreeding Department of Plant Protection Institute of Vegetables and Flowers Chinese Academy of Agricultural Sciences Beijing 100081 ChinaState Key Laboratory of Vegetable Biobreeding Department of Plant Protection Institute of Vegetables and Flowers Chinese Academy of Agricultural Sciences Beijing 100081 ChinaState Key Laboratory of Vegetable Biobreeding Department of Plant Protection Institute of Vegetables and Flowers Chinese Academy of Agricultural Sciences Beijing 100081 ChinaState Key Laboratory of Vegetable Biobreeding Department of Plant Protection Institute of Vegetables and Flowers Chinese Academy of Agricultural Sciences Beijing 100081 ChinaState Key Laboratory of Vegetable Biobreeding Department of Plant Protection Institute of Vegetables and Flowers Chinese Academy of Agricultural Sciences Beijing 100081 ChinaState Key Laboratory of Vegetable Biobreeding Department of Plant Protection Institute of Vegetables and Flowers Chinese Academy of Agricultural Sciences Beijing 100081 ChinaState Key Laboratory of Vegetable Biobreeding Department of Plant Protection Institute of Vegetables and Flowers Chinese Academy of Agricultural Sciences Beijing 100081 ChinaState Key Laboratory of Vegetable Biobreeding Department of Plant Protection Institute of Vegetables and Flowers Chinese Academy of Agricultural Sciences Beijing 100081 ChinaState Key Laboratory of Vegetable Biobreeding Department of Plant Protection Institute of Vegetables and Flowers Chinese Academy of Agricultural Sciences Beijing 100081 ChinaState Key Laboratory of Vegetable Biobreeding Department of Plant Protection Institute of Vegetables and Flowers Chinese Academy of Agricultural Sciences Beijing 100081 ChinaState Key Laboratory of Vegetable Biobreeding Department of Plant Protection Institute of Vegetables and Flowers Chinese Academy of Agricultural Sciences Beijing 100081 ChinaState Key Laboratory of Vegetable Biobreeding Department of Plant Protection Institute of Vegetables and Flowers Chinese Academy of Agricultural Sciences Beijing 100081 ChinaSchool of Life Sciences University of Sussex Brighton BN1 9QG UKDepartment of Entomology University of Kentucky Lexington Kentucky 40546‐0091 USAState Key Laboratory of Vegetable Biobreeding Department of Plant Protection Institute of Vegetables and Flowers Chinese Academy of Agricultural Sciences Beijing 100081 ChinaAbstract Bioinsecticides and transgenic crops based on the bacterial pathogen Bacillus thuringiensis (Bt) can effectively control diverse agricultural insect pests, nevertheless, the evolution of resistance without obvious fitness costs has seriously eroded the sustainable use of these Bt products. Recently, it has been discovered that an increased titer of juvenile hormone (JH) favors an insect host (Plutella xylostella) to enhance fitness whilst resisting the Bt pathogen, however, the underlying regulatory mechanisms of the increased JH titer are obscure. Here, the involvement of N6‐methyladenosine (m6A) RNA modification in modulating the availability of JH in this process is defined. Specifically, it is found that two m6A methyltransferase subunit genes, PxMettl3 and PxMettl14, repress the expression of a key JH‐degrading enzyme JH esterase (JHE) to induce an increased JH titer, mitigating the fitness costs associated with a robust defense against the Bt pathogen. This study identifies an as‐yet uncharacterized m6A‐mediated epigenetic regulator of insect hormones for maintaining fitness during pathogen defense and unveils an emerging Bt resistance‐related m6A methylation atlas in insects, which further expands the functional landscape of m6A modification and showcases the pivotal role of epigenetic regulation in host‐pathogen interactions.https://doi.org/10.1002/advs.202307650Bacillus thuringiensishost‐pathogen interactionsjuvenile hormone esterasem6A modificationPlutella xylostella |
| spellingShingle | Zhaojiang Guo Yang Bai Xinyi Zhang Le Guo Liuhong Zhu Dan Sun Kaiyue Sun Xudan Xu Xin Yang Wen Xie Shaoli Wang Qingjun Wu Neil Crickmore Xuguo Zhou Youjun Zhang RNA m6A Methylation Suppresses Insect Juvenile Hormone Degradation to Minimize Fitness Costs in Response to A Pathogenic Attack Advanced Science Bacillus thuringiensis host‐pathogen interactions juvenile hormone esterase m6A modification Plutella xylostella |
| title | RNA m6A Methylation Suppresses Insect Juvenile Hormone Degradation to Minimize Fitness Costs in Response to A Pathogenic Attack |
| title_full | RNA m6A Methylation Suppresses Insect Juvenile Hormone Degradation to Minimize Fitness Costs in Response to A Pathogenic Attack |
| title_fullStr | RNA m6A Methylation Suppresses Insect Juvenile Hormone Degradation to Minimize Fitness Costs in Response to A Pathogenic Attack |
| title_full_unstemmed | RNA m6A Methylation Suppresses Insect Juvenile Hormone Degradation to Minimize Fitness Costs in Response to A Pathogenic Attack |
| title_short | RNA m6A Methylation Suppresses Insect Juvenile Hormone Degradation to Minimize Fitness Costs in Response to A Pathogenic Attack |
| title_sort | rna m6a methylation suppresses insect juvenile hormone degradation to minimize fitness costs in response to a pathogenic attack |
| topic | Bacillus thuringiensis host‐pathogen interactions juvenile hormone esterase m6A modification Plutella xylostella |
| url | https://doi.org/10.1002/advs.202307650 |
| work_keys_str_mv | AT zhaojiangguo rnam6amethylationsuppressesinsectjuvenilehormonedegradationtominimizefitnesscostsinresponsetoapathogenicattack AT yangbai rnam6amethylationsuppressesinsectjuvenilehormonedegradationtominimizefitnesscostsinresponsetoapathogenicattack AT xinyizhang rnam6amethylationsuppressesinsectjuvenilehormonedegradationtominimizefitnesscostsinresponsetoapathogenicattack AT leguo rnam6amethylationsuppressesinsectjuvenilehormonedegradationtominimizefitnesscostsinresponsetoapathogenicattack AT liuhongzhu rnam6amethylationsuppressesinsectjuvenilehormonedegradationtominimizefitnesscostsinresponsetoapathogenicattack AT dansun rnam6amethylationsuppressesinsectjuvenilehormonedegradationtominimizefitnesscostsinresponsetoapathogenicattack AT kaiyuesun rnam6amethylationsuppressesinsectjuvenilehormonedegradationtominimizefitnesscostsinresponsetoapathogenicattack AT xudanxu rnam6amethylationsuppressesinsectjuvenilehormonedegradationtominimizefitnesscostsinresponsetoapathogenicattack AT xinyang rnam6amethylationsuppressesinsectjuvenilehormonedegradationtominimizefitnesscostsinresponsetoapathogenicattack AT wenxie rnam6amethylationsuppressesinsectjuvenilehormonedegradationtominimizefitnesscostsinresponsetoapathogenicattack AT shaoliwang rnam6amethylationsuppressesinsectjuvenilehormonedegradationtominimizefitnesscostsinresponsetoapathogenicattack AT qingjunwu rnam6amethylationsuppressesinsectjuvenilehormonedegradationtominimizefitnesscostsinresponsetoapathogenicattack AT neilcrickmore rnam6amethylationsuppressesinsectjuvenilehormonedegradationtominimizefitnesscostsinresponsetoapathogenicattack AT xuguozhou rnam6amethylationsuppressesinsectjuvenilehormonedegradationtominimizefitnesscostsinresponsetoapathogenicattack AT youjunzhang rnam6amethylationsuppressesinsectjuvenilehormonedegradationtominimizefitnesscostsinresponsetoapathogenicattack |