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. 2008 Feb;3(2):116–118. doi: 10.4161/psb.3.2.4981

Brassinosteroid-independent functions of the BRI1-associated kinase BAK1/SERK3

Birgit Kemmerling 1,✉, Thorsten Nürnberger 1
PMCID: PMC2633997  PMID: 19704727

Abstract

Eukaryotes have evolved programmed cell death (PCD) mechanisms that play important roles in both, development and immunity.1–3 We demonstrated a requirement for the Arabidopsis thaliana leucine-rich repeat receptor-like kinase (LRR-RLK), BAK1/SERK3 (BRI1-Associated receptor Kinase 1/Somatic Embryogenesis Receptor Kinase 3) in regulating the containment of microbial infection-induced necrosis. BAK1-deficient plants showed constitutive expression of defense-related genes and developed spreading cell death upon infection by necrotizing pathogens that result in enhanced susceptibility to necrotrophic pathogens. This reaction was not inducible by exposition of bak1 mutants to general stresses but appeared to be solely inducible by necrotizing pathogen infection. BAK1 is known to interact with the brassinosteroid receptor, BRI1, and thereby facilitates plant growth and development in a brassinolide (BL)-dependent manner.4,5 Surprisingly, the cell death-related phenotype in bak1 mutants is brassinolide-independent. In this addendum we want to present recent new data on BAK1 and discuss its role as a general regulator in plant processes being as diverse as brassinosteroid signaling in development, perception of pathogen associated molecular patterns (PAMPs), and cell-death control in innate immunity.

Key words: LRR-RLK, cell-death control, immunity, brassinosteroids, BAK1, SERK3, BRI1, FLS2

Introduction

Several LRR-RLKs have been shown to serve roles in plant growth and development.4,5 For example, BRI1, the receptor for the plant steroid hormone, brassinolide (BL),6 is an LRR-RLK that forms heteromeric complexes with another LRR-RLK, the non-ligand binding co-receptor BAK1 (BRI1-associated receptor kinase 1).7,8 Furthermore, plant LRR-RLKs were shown to be pattern recognition receptors in PAMP-triggered immunity and resistance genes in cultivar-specific effector-triggered immunity.9–12 Microbial pattern recognition in animal innate immunity is also mediated through LRR transmembrane receptors that recruit receptor-associated kinases into complexes in a ligand-specific manner, suggesting conceptual and mechanistic similarities among non-self recognition systems from different kingdoms.10,13

The large number of Arabidopsis LRR-RLK genes and the fact that LRR-RLKs have been implicated in various aspects of plant immunity both suggest that various members of this protein family play roles in plant-pathogen interactions.9,10 We recently demonstrated that BAK1 negatively regulates microbial pathogen-induced cell death. Mutants impaired in BAK1 develop propagating lesions upon infection by necrotizing pathogens. However, unlike the growth defect of these plants the aberrant cell death response does not result from impaired brassinolide sensitivity. We propose that BAK1 serves regulatory functions in both, plant development and immunity, and that these activities differ in their steroid hormone requirement.14

BAK1 Function in Pathogen Induced Cell-Death Responses

The ATGenExpress initiative enabled us to perform a number of microarray experiments with PAMP and pathogen-triggered plant material. These assays revealed 49 genes of the LRR-receptor-like protein kinase family to be induced by at least one of the treatments. Transcription of the BAK1 gene was found to be induced by avirulent and nonpathogenic bacteria but not by virulent pathogens. This is a general feature of genes that are likely targeted by bacterial effector proteins for suppression of PAMP-triggered immunity.15

Pathogen assays revealed that bak1 mutants react to infection with necrotizing pathogens with unrestricted spreading cell-death, but do not show spontaneous cell death or enhanced cell-death reactions to abiotic stress induction by chemicals such as H2O2, paraquat or salicylic acid. Exogenous complementation with brassinolide rescued the growth defects of the mutants, but not the enhanced cell-death reactions and the enhanced susceptibility to necrotrophic fungi. Other BL-deficient and BL-insensitive mutants did not show enhanced symptom development and microarray data with pathogen- and BL-treated plants did not show any significant overlap leading to the suggestion that the pathogen-related phenotype of bak1 mutants is not due to their reduced BL-sensitivity. Further transcriptome analyses with the bak1 mutants compared to wildtype revealed that pathogenesis and cell-death-related genes like PR2 and 5 were already expressed at higher levels in untreated mutant plants.14

New Insights into BAK1 Function as a General Regulator of Rlk-Mediated Signaling

Recently a number of publications provided insight into additional aspects of the function of BAK1. It was shown that bak1 mutants are less sensitive to the bacterial PAMP flg22.16 Chinchilla et al.16 demonstrated that the BAK1 protein is part of the FLS2 receptor complex that is involved in flagellin perception, but itself does not bind flagellin. Heese et al17 also detected BAK1 in a complex with FLS2 and showed that tobacco NbSerk3-silenced plants are less sensitive to other PAMPs like the oomycete-derived INF1 or a peptide of the bacterial cold shock protein CSP22, but not to fungal chitin. Interestingly, mutants impaired in FLS2 exhibit enhanced cell death responses to bacterial infection but do not show spreading cell death after necrotrophic fungal infection (our unpublished data). Chinchilla et al16 demonstrated that also the impairment of flg22-responses in bak1 mutants is independent of BL-signaling. We therefore conclude that the function of BAK1 in cell death control is both, independent of BL- and flg22-responses, indicating that BAK1 may serve multiple roles in development and plant immunity depending on the natureof of the interacting ligand-binding receptor. Double mutants with the closest homolog of BAK1/SERK3, the BKK1 or SERK4 gene, resulted in dwarf plants that show spontaneous cell-death and enhanced PR gene expression in a salicylic acid dependent manner18 suggesting that BAK1 and BKK1 have partially redundant but not identical functions in plant cell-death control.

Conclusions and Perspectives

Taken these data together, we conclude that BAK1 may act as a co-receptor for several RLKs thereby controlling various non-related processes such as development, cell death and PAMP-signaling in a stimulus-dependent manner (Fig. 1). Brassinosteroid and flagellin responses are only partially affected in bak1 mutants. It remains unclear if BAK1 operates only as an accessory component in receptor complexes or if BAK1 function is redundant with that of other coreceptors. Evidence from the Li lab shows that at least in growth and cell death regulation there is partial redundancy of BAK1/SERK3 and BKK1/SERK4.18 Furthermore, SERK3/BAK1 and SERK1 both interact with BRI1 to facilitate brassinosteroid signalling.19 The responses to the bacterial PAMP EF-Tu are less impaired in bak1 mutants than flg22 responses16 suggesting that other/additional members of the SERK family might interact with the corresponding receptor kinase EFR. A complex network of non-ligand binding receptor kinases appears to regulate ligand-binding receptor kinase signaling in plants.

Figure 1.

Figure 1

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Model of BAK1 function in different receptor complexes and signalling pathways.7,8,14,16–18

BAK1 is part of different receptor complexes. It remains to be determined if transphosphorylation is needed for signal transduction and if specificity is achieved by phosphorylation of specific targets or more general downstream components. For example, regulation of receptor-endocytosis in general could be one possible mechanism by which BAK1 might fullfill its broad function downstream of RLKs.16

In vitro and in vivo screens for protein complex partners of BAK1 are expected to reveal new ligand-binding receptors using BAK1 as a co-receptor as well as downstream components that will help to elucidate how signal specificity is maintained in various signal transduction pathways employing the same co-receptor BAK1.

Addendum to: The BRI1-associated kinase 1 BAK1 has a brassinolide-independent role in plant cell-death control. Kemmerling B, Schwedt A, Rodriguez P, Mazzotta S, Frank M, Qamar SA, Mngiste T, Betsuyaku S, Parker JE, Müssig C, Thomma BPHJ, Albrecht C, de Vries SC, Hirt H, Nürnberger T. Curr Biol. 2007;17:1116–1122.

Footnotes

Previously published online as a Plant Signaling & Behavior E-publication: www.landesbioscience.com/journals/psb/article/4981

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