ZAR1: Guardian of plant kinases

Abstract

A key facet of innate immunity in plants entails the recognition of pathogen "effector" virulence proteins by host Nucleotide-Binding Leucine-Rich Repeat Receptors (NLRs). Among characterized NLRs, the broadly conserved ZAR1 NLR is particularly remarkable due to its capacity to recognize at least six distinct families of effectors from at least two bacterial genera. This expanded recognition spectrum is conferred through interactions between ZAR1 and a dynamic network of two families of Receptor-Like Cytoplasmic Kinases (RLCKs): ZED1-Related Kinases (ZRKs) and PBS1-Like Kinases (PBLs). In this review, we survey the history of functional studies on ZAR1, with an emphasis on how the ZAR1-RLCK network functions to trap diverse effectors. We discuss 1) the dynamics of the ZAR1-associated RLCK network; 2) the specificity between ZRKs and PBLs; and 3) the specificity between effectors and the RLCK network. We posit that the shared protein fold of kinases and the switch-like properties of their interactions make them ideal effector sensors, enabling ZAR1 to act as a broad spectrum guardian of host kinases.

Keywords: PBL; ZAR1; ZRK; arabidopsis; effector-triggered immunity; kinases; network; pseudokinases.

Figure 1

The dynamic ZAR1/kinase immune signaling network. (A) Parallels between the ZAR1/kinase (left) and hNLR/sNLR (right) immune signaling networks. ZAR1 and hNLRs play similar roles in A. thaliana ETI. Six effector families are indirectly recognized by ZAR1 through its interactions with ZRK (green hexagons) and PBL (diamonds) kinase sensors (Wang et al., 2015; Seto et al., 2017; Liu et al., 2019; Martel et al., 2020; Seto et al., 2021). Analogously, several distinct effector families are recognized by sNLRs, which go on to activate NRG1 and/or ADR1 hNLRs (only a subset are represented) (Bonardi et al., 2011; Dong et al., 2016; Castel et al., 2019; Wu et al., 2019). Like the ZAR1 resistosome, hNLRs oligomerize and localize to the cell membrane to form calcium-permeable channels. Solid lines represent physical interactions whereas dashed lines represent signaling dependencies, which may include physical interactions that have yet to be demonstrated. Other ETI components of the sNLR/hNLR network (e.g., EDS1, NDR1) have been omitted for simplicity. This panel is adapted from Martel et al., 2020 and Jubic et al., 2019. (B) ZRK-PBL interactions induced by the effectors AvrAC, HopF1r, and HopZ1a according to the results of Bastedo et al., 2019; Seto et al., 2021, and Martel et al., 2020. Grey lines represent physical interactions that occur in the absence of an effector, black lines represent physical interactions that are induced or strengthened by the presence of an effector, and red lines represent the ZRK-PBL interaction required for the ETI response to the given effector in A. thaliana. Shown are the ZRKs that have been demonstrated to interact with ZAR1 (Wang et al., 2015) and the PBLs that have been demonstrated to interact with ZRKs (Bastedo et al., 2019; Seto et al., 2021). For more information about effector nomenclature, refer to (Lindeberg et al., 2005).