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

Shuai Li; Xinyang Tan; Zhen He; Lei Jiang; Yali Li; Liu Yang; Ary A Hoffmann; Chunqing Zhao; Jichao Fang; Rui Ji

doi:10.1002/ps.8265

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

Pest Manag Sci. 2024 Oct;80(10):5364-5376. doi: 10.1002/ps.8265. Epub 2024 Jun 21.

Authors

Shuai Li^#¹, Xinyang Tan^#², Zhen He^#³, Lei Jiang⁴, Yali Li⁵, Liu Yang⁵, Ary A Hoffmann⁶, Chunqing Zhao², Jichao Fang^{1

2}, Rui Ji^{1

7}

Affiliations

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.

^# Contributed equally.

PMID: 39031631
DOI: 10.1002/ps.8265

Abstract

Background: N⁶-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.

Results: Here, 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.

Conclusion: The 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.

Keywords: brown planthopper; gene regulation; plant defensive pathways; plant growth; rice N6‐methyladenosine.

MeSH terms

Adenosine* / analogs & derivatives
Adenosine* / metabolism
Animals
Female
Gene Expression Profiling
Hemiptera* / genetics
Hemiptera* / growth & development
Hemiptera* / metabolism
Hemiptera* / physiology
Herbivory
Oryza* / genetics
Oryza* / growth & development
Oryza* / parasitology
Plant Defense Against Herbivory / genetics
Transcriptome*

Substances

N-methyladenosine
Adenosine