The ZmWAKL–ZmWIK–ZmBLK1–ZmRBOH4 module provides quantitative resistance to gray leaf spot in maize

Authors: ZHONG, TAO - China Agriculture University; ZHU, MANG - China Agriculture University; ZHANG, QIANQIAN - China Agriculture University; ZHANG, YAN - China Agriculture University; DENG, SUINING - China Agriculture University; GUO, CHENYU - China Agriculture University; XU, LING - China Agriculture University; JIU, TINGTING - China Agriculture University; LI, YANCONG - China Agriculture University; BI, YAQI - China Agriculture University; FAN, XINGMING - China Agriculture University; Balint-Kurti, Peter; XU, MINGLIANG - China Agriculture University

Submitted to: Nature
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/8/2023
Publication Date: 1/18/2024
Citation: Zhong, T., Zhu, M., Zhang, Q., Zhang, Y., Deng, S., Guo, C., Xu, L., Jiu, T., Li, Y., Bi, Y., Fan, X., Balint Kurti, P.J., Xu, M. 2024. The ZmWAKL–ZmWIK–ZmBLK1–ZmRBOH4 module provides quantitative resistance to gray leaf spot in maize. Nature. 56:315-326. https://doi.org/10.1038/s41588-023-01644-z.
DOI: https://doi.org/10.1038/s41588-023-01644-z

Interpretive Summary: Gray leaf spot (GLS), caused by the fungal pathogens Cercospora zeae-maydis and Cercospora zeina, is a major global foliar disease of maize (Zea mays L.). In this study we have identified four proteins which work together to confer a moderate (or quantitative) level of resistance to GLS. These proteins include the protein that recognizes the pathogen (the “resistance protein”) and three other proteins with which it interacts to transmit the recognition signal and initiate the defense response. While several other quantitative resistance proteins for plant disease have been identified, this may the first time that the signal transduction and execution process has been characterized in such detail.

Technical Abstract: Gray leaf spot (GLS), caused by the fungal pathogens Cercospora zeae-maydis and Cercospora zeina, is a major foliar disease of maize worldwide (Zea mays L.). Here we demonstrate that ZmWAKL encoding cell-wall-associated receptor kinase-like protein is the causative gene at the major quantitative disease resistance locus against GLS. The ZmWAKLY protein, encoded by the resistance allele, can self-associate and interact with a leucine-rich repeat immune-related kinase ZmWIK on the plasma membrane. The ZmWAKLY/ZmWIK receptor complex interacts with and phosphorylates the receptor-like cytoplasmic kinase (RLCK) ZmBLK1, which in turn phosphorylates its downstream NADPH oxidase ZmRBOH4. Upon pathogen infection, ZmWAKLY phosphorylation activity is transiently increased, initiating immune signaling from ZmWAKLY, ZmWIK, ZmBLK1 to ZmRBOH4, ultimately triggering a reactive oxygen species burst. Our study thus uncovers the role of the maize ZmWAKL–ZmWIK–ZmBLK1–ZmRBOH4 receptor/signaling/executor module in perceiving the pathogen invasion, transducing immune signals, activating defense responses and conferring increased resistance to GLS.