Transcriptome‐wide N6‐methyladenosine profiling reveals growth–defense trade‐offs in the response of rice to brown planthopper (Nilaparvata lugens) infestation

Author:

Li Shuai1ORCID,Tan Xinyang2ORCID,He Zhen3,Jiang Lei4,Li Yali5,Yang Liu5,Hoffmann Ary A.6,Zhao Chunqing2ORCID,Fang Jichao12,Ji Rui17

Affiliation:

1. Institute of Plant Protection, Jiangsu Academy of Agricultural Sciences, Jiangsu Key Laboratory for Food and Safety, State Key Laboratory Cultivation Base of Ministry of Science and Technology Nanjing China

2. College of Plant Protection Nanjing Agricultural University Nanjing China

3. School of Plant Protection Yangzhou University Yangzhou China

4. School of Plant Protection Anhui Agricultural University Hefei China

5. Wuhan Benagen Technology Company Limited Wuhan China

6. School of BioSciences, Bio21 Institute University of Melbourne Parkville Australia

7. School of Life Sciences Anhui Normal University/Key Laboratory for Conservation and Use of Important Biological Resources of Anhui Province Anhui China

Abstract

AbstractBACKGROUNDN6‐Methyladenosine (m6A) is a common messenger RNA (mRNA) modification that affects various physiological processes in stress responses. However, the role of m6A modifications in plants responses to herbivore stress remains unclear.RESULTSHere, we found that an infestation of brown planthopper (Nilaparvata lugens) female adults enhanced the resistance of rice to N. lugens. The m6A methylome analysis of N. lugens‐infested and uninfested rice samples was performed to explore the interaction between rice and N. lugens. The m6A methylation mainly occurred in genes that were actively expressed in rice following N. lugens infestation, while an analysis of the whole‐genomic mRNA distribution of m6A showed that N. lugens infestation caused an overall decrease in the number of m6A methylation sites across the chromosomes. The m6A methylation of genes involved in the m6A modification machinery and several defense‐related phytohormones (jasmonic acid and salicylic acid) pathways was increased in N. lugens‐infested rice compared to that in uninfested rice. In contrast, m6A modification levels of growth‐related phytohormone (auxin and gibberellin) biosynthesis‐related genes were significantly attenuated during N. lugens infestation, accompanied by the down‐regulated expression of these transcripts, indicating that rice growth was restricted during N. lugens attack to rapidly optimize resource allocation for plant defense. Integrative analysis of the differential patterns of m6A methylation and the corresponding transcripts showed a positive correlation between m6A methylation and transcriptional regulation.CONCLUSIONThe m6A modification is an important strategy for regulating the expression of genes involved in rice defense and growth during rice–N. lugens interactions. These findings provide new ideas for formulating strategies to control herbivorous pests. © 2024 Society of Chemical Industry.

Publisher

Wiley

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