The Arabidopsis Leucine-Rich Repeat Receptor–Like Kinases BAK1/SERK3 and BKK1/SERK4 Are Required for Innate Immunity to Hemibiotrophic and Biotrophic Pathogens

Abstract

Recognition of pathogen-associated molecular patterns (PAMPs) by surface-localized pattern recognition receptors (PRRs) constitutes an important layer of innate immunity in plants. The leucine-rich repeat (LRR) receptor kinases EF-TU RECEPTOR (EFR) and FLAGELLIN SENSING2 (FLS2) are the PRRs for the peptide PAMPs elf18 and flg22, which are derived from bacterial EF-Tu and flagellin, respectively. Using coimmunoprecipitation and mass spectrometry analyses, we demonstrated that EFR and FLS2 undergo ligand-induced heteromerization in planta with several LRR receptor-like kinases that belong to the SOMATIC-EMBRYOGENESIS RECEPTOR-LIKE KINASE (SERK) family, including BRASSINOSTEROID INSENSITIVE1-ASSOCIATED KINASE1/SERK3 (BAK1/SERK3) and BAK1-LIKE1/SERK4 (BKK1/SERK4). Using a novel bak1 allele that does not exhibit pleiotropic defects in brassinosteroid and cell death responses, we determined that BAK1 and BKK1 cooperate genetically to achieve full signaling capability in response to elf18 and flg22 and to the damage-associated molecular pattern AtPep1. Furthermore, we demonstrated that BAK1 and BKK1 contribute to disease resistance against the hemibiotrophic bacterium Pseudomonas syringae and the obligate biotrophic oomycete Hyaloperonospora arabidopsidis. Our work reveals that the establishment of PAMP-triggered immunity (PTI) relies on the rapid ligand-induced recruitment of multiple SERKs within PRR complexes and provides insight into the early PTI signaling events underlying this important layer of plant innate immunity.

Cautionary Notes on the Use of C-Terminal BAK1 Fusion Proteins for Functional Studies

“…C-terminal BAK1 fusion proteins are often used in Arabidopsis and Nicotiana benthamiana to study the ability of BAK1 or derived variants to form a ligand-induced complex with FLS2 (Chinchilla et al, 2007;Heese et al, 2007;Shan et al, 2008;Lu et al, 2010Lu et al, , 2011Zhang et al, 2010;Roux et al, 2011;Schwessinger et al, 2011;Xiang et al, 2011). Using the transgenic lines described in Figure 1, we tested the ability of the different BAK1-tagged proteins to associate with FLS2 in response to flg22 treatment in coimmunoprecipitation experiments.…”

“…We tested the ability of the different BAK1 variants to complement the hyporesponsive phenotype of bak1-4 during FLS2-and EFR-mediated innate immune responses (Chinchilla et al, 2007;Heese et al, 2007;Shan et al, 2008;Ranf et al, 2011;Roux et al, 2011;Schwessinger et al, 2011). An early response triggered by flg22 and elf18 perception is the rapid production of reactive oxygen species (ROS) in an oxidative burst.…”

“…FLS2 and EFR heterooligomerize with other SERKs in addition to BAK1, including BKK1, which appears to act redundantly with BAK1 in FLS2-and EFR-mediated PTI signaling . Notably, the functional role of BAK1 seems more critical for PTI signaling than for BRI1-mediated responses, as bak1 mutants are strongly impaired in most flg22-and elf18-induced responses (Chinchilla et al, 2007;Heese et al, 2007;Shan et al, 2008;Ranf et al, 2011;Roux et al, 2011;Schwessinger et al, 2011), while the single mutants display only mild defects in BR-induced responses Nam and Li, 2002;Karlova et al, 2006;Albrecht et al, 2008).…”

Deciphering the Responses of Root Border-Like Cells of Arabidopsis and Flax to Pathogen-Derived Elicitors

“…9A). MAMP recognition generally triggers the activation of the salicylic acid pathway (Roux et al, 2011). An induction of SALICYLIC ACID INDUCTION DEFICIENT2 (SID2), one of the essential genes involved in salicylic acid biosynthesis, is observed already 1 h after flg22 application and is stronger at 3 h of treatment (Fig.…”

The Ankyrin-Repeat Transmembrane Protein BDA1 Functions Downstream of the Receptor-Like Protein SNC2 to Regulate Plant Immunity

“…Most of the known PAMP receptors, such as FLS2, EFR, and CERK1, belong to the receptor-like kinase family (Gómez-Gómez and Boller, 2000;Zipfel et al, 2006;Miya et al, 2007;Wan et al, 2008). The receptor-like kinase BAK1 functions as a coreceptor of FLS2 and EFR in the perception of bacterial flagellin and translation elongation factor EF-Tu (Chinchilla et al, 2007;Heese et al, 2007;Schulze et al, 2010;Roux et al, 2011). In rice (Oryza sativa), CERK1 functions together with the lysin motif (LysM) domain protein CEBiP to recognize the fungal cell wall component chitin (Shimizu et al, 2010).…”