Higher eukaryotes sense microbes through the perception of pathogen-associated molecular patterns (PAMPs). Arabidopsis plants detect a variety of PAMPs including conserved domains of bacterial flagellin and of bacterial EF-Tu. Here, we show that flagellin and EF-Tu activate a common set of signaling events and defense responses but without clear synergistic effects. Treatment with either PAMP results in increased binding sites for both PAMPs. We used this finding in a targeted reverse-genetic approach to identify a receptor kinase essential for EF-Tu perception, which we called EFR. Nicotiana benthamiana, a plant unable to perceive EF-Tu, acquires EF-Tu binding sites and responsiveness upon transient expression of EFR. Arabidopsis efr mutants show enhanced susceptibility to the bacterium Agrobacterium tumefaciens, as revealed by a higher efficiency of T-DNA transformation. These results demonstrate that EFR is the EF-Tu receptor and that plant defense responses induced by PAMPs such as EF-Tu reduce transformation by Agrobacterium.
Plants sense potential microbial invaders by using patternrecognition receptors to recognize pathogen-associated molecular patterns (PAMPs) 1 . In Arabidopsis thaliana, the leucine-rich repeat receptor kinases flagellin-sensitive 2 (FLS2) (ref.2) and elongation factor Tu receptor (EFR) (ref.3) act as pattern-recognition receptors for the bacterial PAMPs flagellin 4 and elongation factor Tu (EF-Tu) (ref. 5) and contribute to resistance against bacterial pathogens. Little is known about the molecular mechanisms that link receptor activation to intracellular signal transduction. Here we show that BAK1 (BRI1-associated receptor kinase 1), a leucinerich repeat receptor-like kinase that has been reported to regulate the brassinosteroid receptor BRI1 (refs 6,7), is involved in signalling by FLS2 and EFR. Plants carrying bak1 mutations show normal flagellin binding but abnormal early and late flagellintriggered responses, indicating that BAK1 acts as a positive regulator in signalling. The bak1-mutant plants also show a reduction in early, but not late, EF-Tu-triggered responses. The decrease in responses to PAMPs is not due to reduced sensitivity to brassinosteroids. We provide evidence that FLS2 and BAK1 form a complex in vivo, in a specific ligand-dependent manner, within the first minutes of stimulation with flagellin. Thus, BAK1 is not only associated with developmental regulation through the plant hormone receptor BRI1 (refs 6,7), but also has a functional role in PRR-dependent signalling, which initiates innate immunity.PAMPs have key roles as activators of the innate immune response in animals 8 and, analogously, as 'general elicitors' of defence responses in plants [1][2][3][4][5][9][10][11] . We have previously characterized FLS2 and EFR as the pattern-recognition receptors (PRRs) for flagellin (represented by a 22-amino-acid peptide, flg22) and for EF-Tu (represented by the peptides elf18 and elf26, which correspond to its amino terminus), respectively 2-5,10 . Flagellin and EF-Tu rapidly induce a common set of Arabidopsis genes for leucine-rich repeat receptor-like kinases (LRR-RLKs), including FLS2 and EFR themselves 3,11 . This led to the assumption that some of these PAMPinduced LRR-RLKs might encode additional components of PAMP perception or signalling. Using a reverse genetic approach, we tested a collection of insertional mutants in these LRR-RLKs (previously used for identification of the EFR gene 3 ) for responsiveness to flg22 and found that two mutants with insertions in the LRR-RLK gene At4g33430 have reduced sensitivity to flg22 in seedling growth assays (Fig. 1a,b). In more than 10 repetitions of seedling growth assays with these mutants, we always observed a clear reduction (but never a complete loss) of sensitivity to flg22 and flg22-related peptides. By contrast, the mutants seemed to be as sensitive as the wild type to treatment with elf18 in more than five seedling growth assays (Fig. 1b and data not shown).
Plants and animals recognize microbial invaders by detecting pathogen-associated molecular patterns (PAMPs) such as flagellin. However, the importance of flagellin perception for disease resistance has, until now, not been demonstrated. Here we show that treatment of plants with flg22, a peptide representing the elicitor-active epitope of flagellin, induces the expression of numerous defence-related genes and triggers resistance to pathogenic bacteria in wild-type plants, but not in plants carrying mutations in the flagellin receptor gene FLS2. This induced resistance seems to be independent of salicylic acid, jasmonic acid and ethylene signalling. Wild-type and fls2 mutants both display enhanced resistance when treated with crude bacterial extracts, even devoid of elicitor-active flagellin, indicating the existence of functional perception systems for PAMPs other than flagellin. Although fls2 mutant plants are as susceptible as the wild type when bacteria are infiltrated into leaves, they are more susceptible to the pathogen Pseudomonas syringae pv. tomato DC3000 when it is sprayed on the leaf surface. Thus, flagellin perception restricts bacterial invasion, probably at an early step, and contributes to the plant's disease resistance.
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