Inactivation of β-1,3-glucan synthase-like 5 confers broad-spectrum resistance to Plasmodiophora brassicae pathotypes in cruciferous plants
Yupo Wu, Chuanji Zhao, Yi Zhang, Cuicui Shen, Yuanyuan Zhang, Xiong Zhang, Lixia Gao, Lingyi Zeng, Qinglin Ke, Qin Li, Fan Liu, Junyan Huang, Li Ren, Yueying Liu, Hongtao Cheng, Chaobo Tong, Qiong Hu, Xiaohui Cheng, Yangdou Wei, Shengyi Liu, Lìjiāng Liú
Abstract
Clubroot disease, caused by the obligate intracellular rhizarian protist Plasmodiophora brassicae, is devastating to cruciferous crops worldwide. Widespread field P. brassicae pathotypes frequently overcome the pathotype-specific resistance of modern varieties, posing a challenge for durable control of this disease. Here a genome-wide association study of 3 years of data comprising field clubroot phenotyping of 244 genome-resequenced Brassica napus accessions identified a strong association of β-1,3-glucan synthase-like 5 (GSL5) with clubroot susceptibility. GSL5 was evolutionarily conserved, and inactivation of GSL5 by genome editing in Arabidopsis, B. napus, Brassica rapa and Brassica oleracea conferred broad-spectrum, high-level resistance to P. brassicae pathotypes without yield penalties in B. napus. GSL5 inactivation derepressed the jasmonic acid-mediated immunity during P. brassicae secondary infection, and this immune repression was possibly reinforced through stabilization of GSL5 by a P. brassicae effector, facilitating clubroot susceptibility. Our study provides durable resistance resources for cruciferous clubroot disease control and insights into plant resistance against intracellular eukaryotic phytopathogens.