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

Plant Cell Environ. 2023 Jul;46(7):2238-2254. doi: 10.1111/pce.14603. Epub 2023 May 9.

Abstract

The highly conserved angiosperm immune receptor HOPZ-ACTIVATED RESISTANCE1 (ZAR1) recognises 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 the expansion of the ZAR1-kinase recognition repertoire to achieve novel pathogen recognition outside of model species. We took advantage of the natural diversity of Arabidopsis thaliana kinases to probe the ZAR1-kinase interaction interface and found that A. thaliana ZAR1 (AtZAR1) can interact with most ZRKs, except ZRK7. We found evidence of alternative splicing of ZRK7, resulting in a protein that can interact with AtZAR1. Despite high sequence conservation of ZAR1, interspecific ZAR1-ZRK pairings resulted in the autoactivation 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 AtZAR1-ZRK interaction data, we rationally increased ZRK10 interaction strength with AtZAR1, demonstrating the feasibility of the rational design of a ZAR1-interacting kinase. Overall, our findings advance our understanding of the rules governing ZAR1 interaction specificity, with promising future directions for expanding ZAR1 immunodiversity.

Keywords: Arabidopsis thaliana; NLR; Nicotiana benthamiana; Pseudomonas syringae; cell death; disease resistance; hypersensitive response; kinase; plant immunity; protein-protein interactions.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Arabidopsis Proteins* / metabolism
  • Arabidopsis* / metabolism
  • Carrier Proteins / metabolism
  • Magnoliopsida* / metabolism
  • Phosphotransferases / metabolism
  • Plant Diseases
  • Plant Immunity / physiology
  • Protein Kinases / metabolism
  • Pseudomonas syringae / physiology

Substances

  • Arabidopsis Proteins
  • Carrier Proteins
  • Phosphotransferases
  • ZAR1 protein, Arabidopsis
  • ZED1 protein, Arabidopsis
  • Protein Kinases