Differential Regulation of Two-Tiered Plant Immunity and Sexual Reproduction by ANXUR Receptor-Like Kinases

Abstract

Plants have evolved two tiers of immune receptors to detect infections: cell surface-resident pattern recognition receptors (PRRs) that sense microbial signatures and intracellular nucleotide binding domain leucine-rich repeat (NLR) proteins that recognize pathogen effectors. How PRRs and NLRs interconnect and activate the specific and overlapping plant immune responses remains elusive. A genetic screen for components controlling plant immunity identified ANXUR1 (ANX1), a malectin-like domain-containing receptor-like kinase, together with its homolog ANX2, as important negative regulators of both PRR- and NLR-mediated immunity in ANX1 constitutively associates with the bacterial flagellin receptor FLAGELLIN-SENSING2 (FLS2) and its coreceptor BRI1-ASSOCIATED RECEPTOR KINASE1 (BAK1). Perception of flagellin by FLS2 promotes ANX1 association with BAK1, thereby interfering with FLS2-BAK1 complex formation to attenuate PRR signaling. In addition, ANX1 complexes with the NLR proteins RESISTANT TO PSEUDOMONAS SYRINGAE2 (RPS2) and RESISTANCE TO P. SYRINGAE PV MACULICOLA1. ANX1 promotes RPS2 degradation and attenuates RPS2-mediated cell death. Surprisingly, a mutation that affects ANX1 function in plant immunity does not disrupt its function in controlling pollen tube growth during fertilization. Our study thus reveals a molecular link between PRR and NLR protein complexes that both associate with cell surface-resident ANX1 and uncovers uncoupled functions of ANX1 and ANX2 during plant immunity and sexual reproduction.

The common bean COK‐4 and the Arabidopsis FER kinase domain share similar functions in plant growth and defence

“…In addition, we observed that a lack of a functional FER, but not ANX1 or ANX2, resulted in altered plant defences against Pst DC3000 (Figs 2 and S2) when dip inoculated with high inoculum concentration [1 3 10 8 colony-forming units (CFU)/mL]. However, in a different experimental set-up (syringe infiltration with 5 3 10 4 CFU/mL), Mang et al (2017) observed that anx1-2 and anx2-2 leaves can support smaller bacterial populations than Col-0 leaves. Moreover, ANX1 may act as a negative regulator of immunity by interfering with FLS2-BAK1 formation under flagellin elicitation (Mang et al, 2017).…”

“…However, in a different experimental set‐up (syringe infiltration with 5 × 10 4 CFU/mL), Mang et al . () observed that anx1–2 and anx2‐ 2 leaves can support smaller bacterial populations than Col‐0 leaves. Moreover, ANX1 may act as a negative regulator of immunity by interfering with FLS2–BAK1 formation under flagellin elicitation (Mang et al ., ).…”

“…() observed that anx1–2 and anx2‐ 2 leaves can support smaller bacterial populations than Col‐0 leaves. Moreover, ANX1 may act as a negative regulator of immunity by interfering with FLS2–BAK1 formation under flagellin elicitation (Mang et al ., ). These recent studies indicate that other members of CrRLK1L could also be involved in plant immune responses.…”

“…1A). Arabidopsis ANX1 and ANX2 are highly expressed, but not exclusively (Mang et al, 2017), in mature pollen, whereas FER shows ubiquitous expression across all plant tissues ( Fig. S3A-C, see Supporting Information).…”

Early signalling mechanisms underlying receptor kinase-mediated immunity in plants

“…For example, two malectin-like RKs ANXUR1 (ANX1) and ANX2, which are receptors of RALF4 and RALF19, negatively regulate immune responses triggered by multiple patterns [18,19]. They constitutively associate with both FLS2 and BAK1, but interfere with flg22-induced FLS2-BAK1 complex formation to prevent excessive immune activation [19]. In the future, it will be interesting to test whether these negative regulatory components compete with positive regulatory components in the formation of PRR complexes.…”