Integrative Biology Journals
JIPB

J Integr Plant Biol. ›› 2025, Vol. 67 ›› Issue (4): 1179-1195.DOI: 10.1111/jipb.13840

• Plant Biotic Interactions • Previous Articles    

Unveiling the role of microRNAs in nonhost resistance to Sclerotinia sclerotiorum: Rice-specific microRNAs attack the pathogen via cross-kingdom RNAi

Jiaqin Mei1,2,3†,*, Shuxian Yang1,2,3†, Yanxia Linghu1,2,3†, Yang Gao1,2,3,4, Yuxin Hu1,2,3, Wenjing Nie1,2,3, Yujie Zhang1,2,3, Lixuan Peng1,2,3, Yongzhi Wu1,2,3, Yijuan Ding1,2,3, Ruirui Luo1,2,3, Jingyan Liao1,2,3, Wei Qian1,2,3,*   

  1. 1. Integrative Science Center of Germplasm Creation in Western China (Chongqing) Science City & Southwest University, College of Agronomy and Biotechnology, Southwest University, Chongqing 400715, China;
    2. Academy of Agricultural Sciences, Southwest University, Chongqing 400715, China;
    3. State Cultivation Base of Crop Stress Biology for Southern Mountainous Land of Southwest University, Chongqing 400715, China;
    4. Shilou Bureau of Agriculture and Rural Affairs, Lvliang 033000, China
  • Received:2024-09-27 Accepted:2024-12-14 Online:2025-01-16 Published:2025-04-01
  • Contact: *Wei Qian (qianwei666@hotmail.com); Jiaqin Mei (jiaqinmay@163.com, Dr. Mei is fully responsible for the distribution of all material associated with this article in the manuscript)
  • About author:†These authors contributed equally to this work.
  • Supported by:
    National Natural Science Foundation of China (32072021 to J.M.), Chongqing Technology Innovation and Application Development Program (CSTB2023TIAD-KPX0038 to J.M.), Southwest University Fuling Academy Joint Construction Project (FLYJY202405 to J.M.) and Chongqing Graduate Student Research Innovation Project (CYB240121 to S.Y.).

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Abstract: The development of rapeseed with high resistance against the pathogen Sclerotinia sclerotiorum is impeded by the lack of effective resistance resources within host species. Unraveling the molecular basis of nonhost resistance (NHR) holds substantial value for resistance improvement in crops. In the present study, small RNA sequencing and transcriptome sequencing were carried out between rice (a nonhost species of S. sclerotiorum) and rapeseed during infection, revealing the involvement of rice miRNAs on translation-related processes in both rice and the pathogen. Specifically, rice-specific miRNAs with potential capability for cross-kingdom RNAi against S. sclerotiorum were explored, of which Os-miR169y was selected as a representative case to elucidate its role in resistance to S. sclerotiorum. The silence of Os-miR169y decreased the resistance level of rice to S. sclerotiorum, and heterologous expression of Os-miR169y in Arabidopsis and rapeseed significantly enhanced the host resistance. The dual-luciferase reporter assay indicates that Os-miR169y targets S. sclerotiorum 60S ribosomal protein L19 (SsRPL19). Overexpressing Os-miR169y (OEss-miR169y) and RNAi of SsRPL19 (RNAiss-RPL19) in S. sclerotiorum significantly impaired the growth and pathogenicity of the pathogen, while overexpressing SsRPL19 exhibited a contrast effect. Yeast-two-hybridization revealed an interlinking role of SsRPL19 with multiple large and small ribosomal subunits, indicating its important role in translation. Proteome sequencing detected a decreased amount of proteins in transformants OEss-miR169y and RNAiss-RPL19 and significant suppression on key metabolic pathways such as carbon and nitrogen metabolisms. Collectively, this study suggests that rice can secrete specific miRNAs to suppress genes essential for S. sclerotiorum, such as Os-miR169y, which targets and suppresses SsRPL19 and thus impairs protein synthesis in the pathogen. This study sheds light on the intrinsic mechanisms of rice NHR against S. sclerotiorum, and further demonstrates the potential of using nonhost-specific “pathogen-attacking” miRNAs in improving resistance in host species.

Key words: cross-kingdom, nonhost resistance, Os-miR169y, rapeseed, rice-specific miRNAs, Sclerotinia sclerotiorum

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