Li Shuai, Tan Xin-Yang, He Zhen, Shen Chen, Li Ya-Li, Qin Lang, Zhao Chun-Qing, Luo Guang-Hua, Fang Ji-Chao, Ji Rui
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.
College of Plant Protection, Nanjing Agricultural University, Nanjing, China.
Insect Sci. 2025 Apr;32(2):530-550. doi: 10.1111/1744-7917.13401. Epub 2024 Jun 4.
N-methyladenosine (mA) is the most prevalent modification in cellular RNA which orchestrates diverse physiological and pathological processes during stress response. However, the differential mA modifications that cope with herbivore stress in resistant and susceptible crop varieties remain unclear. Here, we found that rice stem borer (RSB) larvae grew better on indica rice (e.g., MH63, IR64, Nanjing 11) than on japonica rice varieties (e.g., Nipponbare, Zhonghua 11, Xiushui 11). Then, transcriptome-wide mA profiling of representative resistant (Nipponbare) and susceptible (MH63) rice varieties were performed using a nanopore direct RNA sequencing approach, to reveal variety-specific mA modifications against RSB. Upon RSB infestation, mA methylation occurred in actively expressed genes in Nipponbare and MH63, but the number of methylation sites decreased across rice chromosomes. Integrative analysis showed that mA methylation levels were closely associated with transcriptional regulation. Genes involved in herbivorous resistance related to mitogen-activated protein kinase, jasmonic acid (JA), and terpenoid biosynthesis pathways, as well as JA-mediated trypsin protease inhibitors, were heavily methylated by mA, and their expression was more pronounced in RSB-infested Nipponbare than in RSB-infested MH63, which may have contributed to RSB resistance in Nipponbare. Therefore, dynamics of mA modifications act as the main regulatory strategy for expression of genes involved in plant-insect interactions, which is attributed to differential responses of resistant and susceptible rice varieties to RSB infestation. These findings could contribute to developing molecular breeding strategies for controlling herbivorous pests.
N-甲基腺苷（mA）是细胞RNA中最普遍的修饰，它在应激反应过程中协调各种生理和病理过程。然而，在抗性和敏感作物品种中应对食草动物胁迫的差异mA修饰仍不清楚。在这里，我们发现二化螟（RSB）幼虫在籼稻（如MH63、IR64、南京11）上比在粳稻品种（如日本晴、中华11、秀水11）上生长得更好。然后，使用纳米孔直接RNA测序方法对代表性抗性（日本晴）和敏感（MH63）水稻品种进行全转录组mA分析，以揭示针对RSB的品种特异性mA修饰。在RSB侵染后，日本晴和MH63中活跃表达的基因发生了mA甲基化，但水稻染色体上的甲基化位点数量减少。综合分析表明，mA甲基化水平与转录调控密切相关。参与丝裂原活化蛋白激酶、茉莉酸（JA）和萜类生物合成途径以及JA介导的胰蛋白酶蛋白酶抑制剂相关的抗草食性基因被mA高度甲基化，并且它们在受RSB侵染的日本晴中的表达比在受RSB侵染的MH63中更明显，这可能有助于日本晴对RSB的抗性。因此，mA修饰的动态变化是植物与昆虫相互作用相关基因表达的主要调控策略，这归因于抗性和敏感水稻品种对RSB侵染的不同反应。这些发现有助于制定控制草食性害虫的分子育种策略。
