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Research Project: Mining Collections of Wild Germplasm and Novel Defense Regulators for Enhanced Plant Defenses

Location: Plant Gene Expression Center

Title: Utilising natural diversity of kinases to rationally engineer interactions with the angiosperm immune receptor ZAR1

item DIPLOCK, NATHAN - University Of California Berkeley
item BAUDIN, MAEL - University Of California Berkeley
item Harden, Leslie - Les
item Silva, Christopher - Chris
item Erickson-Beltran, Melissa
item HASSAN, JANA - University Of California Berkeley
item Lewis, Jennifer

Submitted to: Plant, Cell & Environment
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/24/2023
Publication Date: 5/9/2023
Citation: Diplock, N., Baudin, M., Harden, L.A., Silva, C.J., Erickson-Beltran, M.L., Hassan, J.A., Lewis, J.D. 2023. Utilising natural diversity of kinases to rationally engineer interactions with the angiosperm immune receptor ZAR1. Plant, Cell & Environment. 46(7):2238-2254.

Interpretive Summary: Plant diseases significantly impact crop productivity and yield. Plants have immune systems that can defend them against different pathogens. Plants evolve over long time frames to recognize pathogens, which makes it very challenging for plants to recognize a new pathogen. Immune receptors commonly monitor critical host proteins for modification by plant pathogens. Immune receptors serve as a mousetrap, to initiate immune responses when the mouse (a pathogen) nibbles on the cheese (critical host proteins). We found that an immune receptor is able to monitor many different protein kinases in the plant, all of which are likely targeted by pathogens. We demonstrated that we could modify a protein kinase to improve its interaction with the immune receptor. This work will help design better immune receptors as more effective mousetraps for pathogens.

Technical Abstract: The highly conserved angiosperm immune receptor HOPZ-ACTIVATED RESISTANCE1 (ZAR1) recognizes the activity of diverse pathogen effector proteins by monitoring the ZED1-related kinase (ZRK) family. Understanding how ZAR1 achieves interaction specificity for ZRKs may allow for expansion of the ZAR1-kinase recognition repertoire to achieve novel pathogen recognition. We took advantage of the natural diversity of Arabidopsis thaliana kinases to probe the ZAR1-kinase interaction interface and found that ZAR1 can interact with most ZRKs, except ZRK7. We found evidence of alternative splicing of ZRK7, resulting in a protein that can interact with ZAR1. Despite high sequence conservation of ZAR1, interspecific ZAR1-ZRK pairings resulted in auto-activation of cell death. We showed that ZAR1 interacts with a greater diversity of kinases than previously thought, while still possessing the capacity for specificity in kinase interactions. Finally, using ZAR1-ZRK interaction data, we rationally increased ZRK10 interaction strength with ZAR1, demonstrating the feasibility of rational design of a ZAR1-interacting kinase. Overall, our findings advance our understanding of the rules governing the ZAR1 pathogen recognition system, with promising future directions for expanding ZAR1 immunodiversity.