An ATPase promotes autophosphorylation of the pattern recognition receptor XA21 and inhibits XA21-mediated immunity

Abstract

Cell-surface pattern recognition receptors (PRRs) are key components of the innate immune response in animals and plants. These receptors typically carry or associate with non-RD kinases to control early events of innate immunity signaling. Despite their importance, the mode of regulation of PRRs is largely unknown. Here we show that the rice PRR, XA21, interacts with XA21 binding protein 24 (XB24), a previously undescribed ATPase. XB24 promotes autophosphorylation of XA21 through its ATPase activity. Rice lines silenced for Xb24 display enhanced XA21-mediated immunity, whereas rice lines overexpressing XB24 are compromised for immunity. XB24 ATPase enzyme activity is required for XB24 function. XA21 is degraded in the presence of the pathogen-associated molecular pattern Ax21 when XB24 is overexpressed. These results demonstrate a function for this large class of broadly conserved ATPases in PRR-mediated immunity.non-RD kinase | pathogen-associated molecular pattern | pattern recognition receptor | ATPase | rice I nnate immunity is the first line of defense against pathogen attack and is activated rapidly following infection. In contrast to the adaptive immune system that depends on somatic gene rearrangements for the generation of antigen receptors with random specificities, the innate immune system uses a set of defined receptors for recognition of pathogen-associated molecular patterns (PAMPs) (1).Cell-surface pattern recognition receptors (PRRs) are key components of the innate immune response in animals and plants (2-8).In animals, recognition of PAMPs at the cell surface is largely carried out by the Toll-like receptor (TLR) family that contains leucine-rich repeats (LRRs) in the extracellular domain and a Toll-interleukin receptor (TIR) intracellular domain (9). Although TLRs recognize diverse molecules, they activate a common signaling pathway via association with non-RD (arginine-aspartic acid) kinases to induce a core set of defense responses (10, 11). For example, TLRs 1, 3, 5, 6, 7, 8, and 9 function through interleukin-1 receptor-associated kinase (IRAK1), whereas TLR3 and TLR4 function through receptor interacting-protein 1 (RIP1). Both IRAK1 and RIP1 are non-RD kinases (10). In plants, cell-surface recognition of PAMPs is carried out by PRRs that carry non-RD IRAK kinases integral to the receptor (ca. 35 in Arabidopsis and 328 in rice) (10). For example, rice XA21, XA26, Arabidopsis flagellin sensitive 2 (FLS2), elongation factor-Tu receptor (EFR), and barley Rpg1 (conferring stem rust-resistance) all contain an intracellular non-RD Ser/Thr kinase (8,(12)(13)(14)(15).Non-RD kinases typically carry a cysteine or glycine (in place of the arginine) before the catalytic aspartate residue and control early events of innate immunity signaling in animals and plants (16). Whereas RD kinases are regulated by autophosphorylation of the activation segment-a centrally located loop that sits close to the catalytic center-non-RD kinases are not autophosphorylated in the activation segment (17). These results s...

Plant Innate Immunity: Perception of Conserved Microbial Signatures

“…Furthermore, there are vast differences within the plant kingdom. For example, genome analyses have revealed that rice has approximately 10 times as many non-RD RKs (328 non-RD RKs) as Arabidopsis (35 non-RD RKs) (31,48,178). It may be that the expansion of non-RD kinases in rice is representative of a divide between monocots and dicots.…”

“…Support for this hypothesis comes from recent results showing that the ATPase XB24 promotes XA21 autophosphorylation, holding it in a biologically inactive state. Only upon ligand binding does the ATPase disassociate, triggering XA21 activation (31).…”

Plasma Membrane Calcium ATPases Are Important Components of Receptor-Mediated Signaling in Plant Immune Responses and Development

“…This offers the possibility for molecular cross talk between different RKmediated signaling pathways, as recently demonstrated for brassinosteroid signaling negatively impacting flg22 responses (Albrecht et al, 2012;Belkhadir et al, 2012). At the molecular level, BAK1/SERK3 was shown to transphosphorylate BRI1 and EFR (Wang et al, 2008;Chen et al, 2010;Schwessinger et al, 2011). Moreover, BRI1, FLS2, and EFR can associate with other members of the SERK family, revealing some levels of functional redundancy (Albrecht et al, 2008;Roux et al, 2011).…”

Disease Resistance

“…The XB24/ATPase physically associates with the juxtamembrane motif of Xa21 and enhances Xa21 autophosphorylation that keeps the Xa21 protein in an inactive status [ 72 ]. Upon recognition of sulfated Ax21, the Xa21 kinase disassociates from XB24 and is activated, which results in the initiation of downstream defense responses.…”