Disruption of the primary salicylic acid hydroxylases in rice enhances broad‐spectrum resistance against pathogens

• Published in: Plant, cell and environment cell and environment, 2022-07, Vol.45 (7), p.2211-2225
• Main Authors: Zhang, Yanjun, Yu, Qilu, Gao, Shilei, Yu, Ningning, Zhao, Li, Wang, Jinbin, Zhao, Jiangzhe, Huang, Peng, Yao, Linbo, Wang, Mo, Zhang, Kewei
• Format: Article
• Language: English
• Subjects: Acid resistance; crop yield; Dihydroxybenzoic acid; Disease Resistance; Gene Expression Regulation, Plant; Grain size; growth; hormones; Immunity; Mixed Function Oxygenases; Mutants; Oryza - metabolism; Oryza sativa; Pathogens; Plant Diseases; Plant immunity; Plant Proteins - genetics; Plant Proteins - metabolism; Reactive oxygen species; Rice; rice (Oryza sativa) agronomic traits; Rice fields; Salicylic Acid; Xanthomonas
• ISSN: 0140-7791; 1365-3040
• DOI: 10.1111/pce.14328

Salicylic acid (SA) is a crucial hormone involved in plant immunity. Rice (Oryza sativa) maintains high SA levels that are not induced by pathogens. However, the roles of SA in rice immunity and yield remain largely unknown. Here, we identified SA 5‐hydroxylases 1 (OsS5H1) and 2 (OsS5H2) as the primary enzymes engaged in catalysing SA to 2,5‐dihydroxybenzoic acid (2,5‐DHBA) in rice. SA levels were significantly increased in the oss5h mutants, while they were dramatically decreased in the OsS5H1 and OsS5H2 overexpression lines. The mutants were resistant, whereas the overexpression lines were susceptible to Pyricularia oryzae and Xanthomonas oryzae pv. Oryzae. Moreover, the pathogen‐associated molecular patterns‐triggered immunity responses, including reactive oxygen species burst and callose deposition, were enhanced in all the mutants and compromised in the overexpression lines. Quantification of the agronomic traits of the oss5h mutants grown in the paddy fields demonstrated that the grain number per panicle was decreased as the SA levels increased; however, the tiller number and grain size were enhanced, resulting in no significant yield penalty. Collectively, we reveal that mildly increasing SA content in rice can confer broad‐spectrum resistance without yield penalty and put new insights into the roles of SA in immunity and growth. Summary statement Disruption of rice (Oryza sativa) primary salicylic acid (SA) hydroxylase OsS5H1 and OsS5H2 by CRISPR/Cas9 technology mildly increases the SA levels and confers broad‐spectrum resistance to both blast fungus and blight bacteria pathogens without significantly affecting yield.