A conserved regulatory module regulates receptor kinase signaling in immunity and development

Abstract

Ligand recognition by cell-surface receptors underlies development and immunity in both animals and plants. Modulating receptor signaling is critical for appropriate cellular responses but the mechanisms ensuring this are poorly understood. Here, we show that signaling by plant receptors for pathogen-associated molecular patterns (PAMPs) in immunity and CLAVATA3/EMBRYO SURROUNDING REGION-RELATED peptides (CLEp) in development employ a similar regulatory module. In the absence of ligand, signaling is dampened through association with specific type-2C protein phosphatases (PP2Cs). Upon activation, PAMP and CLEp receptors phosphorylate divergent cytosolic kinases, which, in turn, phosphorylate the phosphatases, thereby promoting their release from the receptor complexes. Our work reveals a regulatory circuit shared between immune and developmental receptor signaling, which may have broader important implications for plant receptor kinase-mediated signaling in general.

Molecular mechanisms of early plant pattern-triggered immune signaling

“…Consistent with the importance of phosphorylation in activating RK-mediated immune signaling, phosphatases have been identified that directly interact with several such RKs. The PP2C isoforms XB15 and POLTERGEIST-LIKE 4 and 5 (PLL4 and 5) are homologs from rice and Arabidopsis that were identified as interactors of XA21 and Arabidopsis EFR, respectively, where they act as negative regulators of immunity (DeFalco et al, 2021;Holton et al, 2015;Park et al, 2008). Other PP2Cs have been identified that regulate CERK1 (Liu et al, 2018), while a PP2A complex was found to negatively regulate the activation of BAK1 (Segonzac et al, 2014).…”

“…RLCK-VII/PBLs, however, are highly active kinases and have been found to directly phosphorylate numerous substrate proteins to initiate PTI signaling (discussed below). Among RLCK-VII isoforms, BOTRYTIS-INDUCED KINASE 1 (BIK1) (Veronese et al, 2006) and its close homolog PBL1 have emerged as key convergent signaling hubs downstream of diverse PRR complexes (DeFalco et al, 2021;Kadota et al, 2014;Li et al, 2014;Liu et al, 2013;Lu et al, 2010;Monaghan et al, 2015;Ranf et al, 2014;Zhang et al, 2010). Activation of BIK1 relies on its phosphorylation, which can be rapidly detected upon PAMP perception (Lu et al, 2010;Zhang et al, 2010).…”

“…The PLL-type phosphatases PLL4 and PLL5 are negative regulators of EFR-mediated immune signaling and dissociate from the EFR complex upon elf18 perception (Holton et al, 2015). Recently, BIK1 was found to directly phosphorylate PLL4 at a cluster of conserved sites in its N terminus, which in turn decreases interaction with EFR and FLS2, providing a regulatory circuit that governs immune RK activation (DeFalco et al, 2021). Interestingly, this molecular circuitry is conserved in LRR-RK pathways that regulate growth and development, suggesting extensive overlap between the signaling pathways of immune and non-immune RKs, as also suggested for the SHEN-GHEN pathway regulating endodermal development (Fujita et al, 2020).…”

Control of Arabidopsis shoot stem cell homeostasis by two antagonistic CLE peptide signalling pathways

“…The CLV3 peptide is perceived by a leucine-rich-repeat (LRR) receptor kinase, CLAVATA1 (CLV1), which interacts with coreceptors of the CLAVATA3 INSENSITIVE RECEPTOR KINASES (CIK) 1-4 family (Clark et al, 1997;Cui et al, 2018). CLV1 activation involves autophoshorylation, interaction with membrane-associated and cytosolic kinases and phosphatases (Blümke et al, 2021;Defalco et al, 2021).…”

Control of Arabidopsis shoot stem cell homeostasis by two antagonistic CLE peptide signalling pathways

“…The CLV3 peptide is perceived by a leucin-rich-repeat (LRR) receptor kinase, CLAVATA1 (CLV1), which interacts with coreceptors of the CLAVATA3 INSENSITIVE RECEPTOR KINASES (CIK) 1-4 family (Clark et al, 1997; Cui et al, 2018). CLV1 activation involves autophoshorylation, interaction with membrane-associated and cytosolic kinases and phosphatases (Blümke et al, 2021; Defalco et al, 2021). Furthermore, heterotrimeric G-proteins and MAPKs have been implicated in this signal transduction cascade in maize and Arabidopsis (Betsuyaku et al, 2011; Bommert et al, 2013; Ishida et al, 2014; Lee et al, 2019).…”