Journal Article

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

Panstruga, Ralph, Beeckman, Tom, Mbengue, Malick, Robatzek, Silke, Altenbach, Denise, Häweker, Heidrun, Lozano-Duran, Rosa, Huettel, Bruno, Nitsch, Lisette, Njo, Maria Fransiska, dit Frey, Nicolas Frei, Borst, Jan Willem, Kwaaitaal, Mark

2012

Overview

Plasma membrane-resident receptor kinases (RKs) initiate signaling pathways important for plant immunity and development. In Arabidopsis (Arabidopsis thaliana), the receptor for the elicitor-active peptide epitope of bacterial flagellin, flg22, is encoded by FLAGELLIN SENSING2 (FLS2), which promotes plant immunity. Despite its relevance, the molecular components regulating FLS2-mediated signaling remain largely unknown. We show that plasma membrane ARABIDOPSIS-ALJTOINHIBITED Ca²⁺-ATPase (ACA8) forms a complex with FLS2 in planta. ACA8 and its closest homolog ACA10 are required for limiting the growth of virulent bacteria. One of the earliest flg22 responses is the transient increase of cytosolic Ca²⁺ ions, which is crucial for many of the well-described downstream responses (e.g. generation of reactive oxygen species and the transcriptional activation of defense-associated genes). Mutant aca8 aca10 plants show decreased flg22-induced Ca²⁺ and reactive oxygen species bursts and exhibit altered transcriptional reprogramming. In particular, mitogen-activated protein kinase-dependent flg22-induced gene expression is elevated, whereas calcium-dependent protein kinase-dependent flg22-induced gene expression is reduced. These results demonstrate that the fine regulation of Ca²⁺ fluxes across the plasma membrane is critical for the coordination of the downstream microbe-associated molecular pattern responses and suggest a mechanistic link between the FLS2 receptor complex and signaling kinases via the secondary messenger Ca²⁺. ACA8 also interacts with other RKs such as BRI1 and CLV1 known to regulate plant development, and both aca8 and aca10 mutants show morphological phenotypes, suggesting additional roles for ACA8 and ACA10 in developmental processes. Thus, Ca²⁺ ATPases appear to represent general regulatory components of RK-mediated signaling pathways.

• Publisher: American Society of Plant Biologists,Oxford University Press ; American Society of Plant Biologists
• Subject: Adenosine triphosphatases / Arabidopsis / Arabidopsis - enzymology / Arabidopsis - genetics / Arabidopsis - immunology / Arabidopsis - microbiology / Arabidopsis Proteins / Arabidopsis Proteins - genetics / Arabidopsis Proteins - immunology / Arabidopsis Proteins - metabolism / Arabidopsis thaliana / bacteria / Bacterial Proteins / Bacterial Proteins - immunology / bak1 / Biological and medical sciences / brassinosteroids / Ca2-transporting ATPase / Calcium / Calcium - metabolism / Calcium-Transporting ATPases / Calcium-Transporting ATPases - genetics / Calcium-Transporting ATPases - immunology / Calcium-Transporting ATPases - metabolism / Cell Membrane / Cell Membrane - enzymology / Cell Membrane - metabolism / Cell membranes / cell-death / Cytosol / Cytosol - metabolism / defense / enzymology / flagellin / Fluorescence / Fluorescence Resonance Energy Transfer / Fundamental and applied biological sciences. Psychology / gene activation / gene expression / Gene expression regulation / Gene Expression Regulation, Plant / Genes / genetics / immunity / immunology / innate immunity / ions / Life Sciences / metabolism / microbiology / molecular-patterns / mutants / nadph oxidase / Oligonucleotide Array Sequence Analysis / pathogenicity / pattern-recognition receptors / Phenotype / phosphotransferases (kinases) / plant development / Plant Immunity / Plant physiology and development / plant response / Plants / PLANTS INTERACTING WITH OTHER ORGANISMS / Plasma interactions / plasma membrane / Protein Interaction Mapping / Protein Kinases / Protein Kinases - metabolism / Pseudomonas syringae / Pseudomonas syringae - immunology / Pseudomonas syringae - pathogenicity / Reactive Oxygen Species / Receptors / Signal Transduction / Transcription, Genetic / transcriptional activation