Rice false smut virulence protein subverts host chitin perception and signaling at lemma and palea for floral infection

Author:

Li Guo-Bang12ORCID,Liu Jie1ORCID,He Jia-Xue1ORCID,Li Gao-Meng1ORCID,Zhao Ya-Dan1ORCID,Liu Xiao-Ling1ORCID,Hu Xiao-Hong13ORCID,Zhang Xin1ORCID,Wu Jin-Long1ORCID,Shen Shuai1ORCID,Liu Xin-Xian1ORCID,Zhu Yong1ORCID,He Feng4ORCID,Gao Han5ORCID,Wang He1ORCID,Zhao Jing-Hao1ORCID,Li Yan1ORCID,Huang Fu1ORCID,Huang Yan-Yan1ORCID,Zhao Zhi-Xue1ORCID,Zhang Ji-Wei1ORCID,Zhou Shi-Xin1ORCID,Ji Yun-Peng1ORCID,Pu Mei1ORCID,He Min1ORCID,Chen Xuewei1ORCID,Wang Jing1ORCID,Li Weitao2ORCID,Wu Xian-Jun2ORCID,Ning Yuese4ORCID,Sun Wenxian5ORCID,Xu Zheng-Jun2ORCID,Wang Wen-Ming1ORCID,Fan Jing16ORCID

Affiliation:

1. State Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Sichuan Agricultural University , Chengdu 611130 , China

2. Rice Research Institute, Sichuan Agricultural University , Chengdu 611130 , China

3. Ecological Security and Protection Key Laboratory of Sichuan Province, Mianyang Normal University , Mianyang 621023 , China

4. State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences , Beijing 100193 , China

5. College of Plant Protection and the Ministry of Agriculture Key Laboratory of Pest Monitoring and Green Management, China Agricultural University , Beijing 100193 , China

6. Yazhouwan National Laboratory , Sanya 572024 , China

Abstract

Abstract The flower-infecting fungus Ustilaginoidea virens causes rice false smut, which is a severe emerging disease threatening rice (Oryza sativa) production worldwide. False smut not only reduces yield, but more importantly produces toxins on grains, posing a great threat to food safety. U. virens invades spikelets via the gap between the 2 bracts (lemma and palea) enclosing the floret and specifically infects the stamen and pistil. Molecular mechanisms for the U. virens–rice interaction are largely unknown. Here, we demonstrate that rice flowers predominantly employ chitin-triggered immunity against U. virens in the lemma and palea, rather than in the stamen and pistil. We identify a crucial U. virens virulence factor, named UvGH18.1, which carries glycoside hydrolase activity. Mechanistically, UvGH18.1 functions by binding to and hydrolyzing immune elicitor chitin and interacting with the chitin receptor CHITIN ELICITOR BINDING PROTEIN (OsCEBiP) and co-receptor CHITIN ELICITOR RECEPTOR KINASE1 (OsCERK1) to impair their chitin-induced dimerization, suppressing host immunity exerted at the lemma and palea for gaining access to the stamen and pistil. Conversely, pretreatment on spikelets with chitin induces a defense response in the lemma and palea, promoting resistance against U. virens. Collectively, our data uncover a mechanism for a U. virens virulence factor and the critical location of the host–pathogen interaction in flowers and provide a potential strategy to control rice false smut disease.

Funder

National Natural Science Foundation of China

Sichuan Applied Fundamental Research Foundation

Natural Science Foundation of Sichuan Province

Technology Research and Development Program of Sichuan Province

Publisher

Oxford University Press (OUP)

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