Global profiling of lysine-malonylated proteins in rice elucidates the immune-regulatory mechanisms of malonylation under herbivore or viral stresses

doi:10.1111/jipb.70050

• Research Article •

Global profiling of lysine-malonylated proteins in rice elucidates the immune-regulatory mechanisms of malonylation under herbivore or viral stresses

Shuai Li^1†, Xinyang Tan^2†, Lei Yang¹, Xiaolong Deng³, Miaomiao Li⁴, Lang Qin³, Liangxuan Qi¹, Jing Li¹, Guanghua Luo¹, Meng Yuan³, Yang Sun⁴, Chunqing Zhao², Kun Zhang³, Jichao Fang^{1,2 *}, Zhen He^{3,5 *} and Rui Ji^{1,2 *}

1. Institute of Plant Protection, Jiangsu Academy of Agricultural Sciences, Jiangsu Key Laboratory for Food and Safety‐State KeyLaboratory Cultivation Base of Ministry of Science and Technology, Nanjing 210014, China

2. State Key Laboratory of Agricultural and Forestry Biosecurity, College of Plant Protection, Nanjing Agricultural University, Nanjing210095, China

3. School of Plant Protection, Yangzhou University, Yangzhou 225009, China

4. School of Life Sciences, Anhui Normal University/Key Laboratory for Conservation and Use of Important Biological Resources ofAnhui Province, Wuhu 241000, China

5. Sanya National Academy of Southern Propagation, Chinese Academy of Agricultural Science, Sanya 572024, China†These authors contributed equally to this work.

*Correspondences: Jichao Fang (fangjc@jaas.ac.cn); Zhen He (hezhen@yzu.edu.cn); Rui Ji (jirui@jaas.ac.cn, Dr Ji is fully responsible forthe distribution of all materials associated with this article)

Received:2025-04-01 Accepted:2025-08-18 Online:2025-10-20
Supported by:
The authors gratefully acknowledge ?nancial support from the National Natural Science Foundation of China (Grant Nos.32302320, 32272485, 32572760), the National Key Research and Development Program of China (Grant No.2022YFD1700200), and the Earmarked Fund for China Agriculture Research System (Grant No. CARS‐01).

Abstract

Abstract: Lysine malonylation (K_mal), an evolutionarily conserved post-translational modification, serves as a critical regulator of cellular processes including transcriptional control, metabolic coordination, and enzyme activation. While K_mal sites have been mapped in rice (Oryza sativa L.) seeds, their dynamic regulation in rice responses to biotic stresses remains poorly characterized. Here, we reported a global profiling of lysine-malonylated proteins in rice leaf sheaths, and the changes in these proteins under herbivore (Nilaparvata lugens/Chilo suppressalis) or viral (rice stripe virus/rice black-streaked dwarf virus) stresses. Using affinity enrichment and proteomics, we identified 3,113 K_mal sites across 1,324 proteins in wild-type rice leaf sheaths, these data demonstrated that lysine-malonylated proteins are involved in diverse biological processes. K_mallevels were significantly upregulated following herbivore infestation or viral infection, with two herbivores inducing more pronounced changes than viruses infection, revealing stress-specific malonylation landscapes. K_mal preferentially targeted highly expressed proteins in energy metabolism (e.g., glycolysis and the tricarboxylic acid cycle) and photosynthesis, exhibiting an inverse correlation between hypermalonylation and protein abundance. Cleavage under targets and tagmentation analyses revealed K_mal-mediated chromatin remodeling through promoter occupancy at defense-related genes. In addition, the histone deacetylases OsHDA702-704, OsHDA711-713 were functionally characterized as key regulators mediating the erasure of specific malonylation marks in rice plants, with OsHDA711 knockout lines exhibiting enhanced resistance against both herbivore and virus infection. Our work establishes K_mal as a regulator in rice biotic immunity, uncovering novel insights into K_mal-mediated plant defense responses against herbivorous pests and viral pathogens. These findings identify potential genetic targets for developing rice varieties with broad-spectrum immunity to biotic stresses, enhancing crop resilience.

Key words: herbivore infestation, histone deacetylases, lysinemalonylation, regulatory, virus infection

Shuai Li, Xinyang Tan, Lei Yang, Xiaolong Deng, Miaomiao Li, Lang Qin, Liangxuan Qi, Jing Li, Guanghua Luo, Meng Yuan, Yang Sun, Chunqing Zhao, Kun Zhang, Jichao Fang, Zhen He, Rui Ji. Global profiling of lysine-malonylated proteins in rice elucidates the immune-regulatory mechanisms of malonylation under herbivore or viral stresses[J]. J Integr Plant Biol., DOI: 10.1111/jipb.70050.

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Global profiling of lysine-malonylated proteins in rice elucidates the immune-regulatory mechanisms of malonylation under herbivore or viral stresses

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