Differential innate immune signalling via Ca2+ sensor protein kinases

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Abstract
Plants and animals sense the invasion of pathogens using pattern recognition receptors that recognize diverse microbe-associated molecular patterns (MAMPs) and initiate innate immune responses. Early signalling events in the host include calcium influx, activation of mitogen-activated protein kinases (MAPKs), oxidative burst and transcriptional reprogramming. Boudsocq et al. use a functional genomic screen and genome-wide gene expression profiling in Arabidopsis to show that four calcium-dependent protein kinases (CDPKs) acting as Ca2+ sensors are the convergence points for diverse MAMPs and are critical for transcriptional reprogramming and oxidative burst in plants. Plants and animals sense intruding pathogens by using proteins that recognize diverse microbe-associated molecular patterns (MAMPs) and initiate innate immune responses. Early signalling responses in the host include calcium influx, an oxidative burst and transcriptional reprogramming. Here, four calcium-dependent protein kinases are described that function as calcium sensors, act as convergence points for various MAMPs, and are crucial for transcriptional reprogramming and oxidative burst in plants. Innate immunity represents the first line of inducible defence against microbial infection in plants and animals1,2,3. In both kingdoms, recognition of pathogen- or microbe-associated molecular patterns (PAMPs or MAMPs, respectively), such as flagellin, initiates convergent signalling pathways involving mitogen-activated protein kinase (MAPK) cascades and global transcriptional changes to boost immunity1,2,3,4. Although Ca2+ has long been recognized as an essential and conserved primary mediator in plant defence responses, how Ca2+ signals are sensed and relayed into early MAMP signalling is unknown5,6. Using a functional genomic screen and genome-wide gene expression profiling, here we show that four calcium-dependent protein kinases (CDPKs) are Ca2+-sensor protein kinases critical for transcriptional reprogramming in plant innate immune signalling. Unexpectedly, CDPKs and MAPK cascades act differentially in four MAMP-mediated regulatory programs to control early genes involved in the synthesis of defence peptides and metabolites, cell wall modifications and redox signalling. Transcriptome profile comparison suggests that CDPKs are the convergence point of signalling triggered by most MAMPs. Double, triple and quadruple cpk mutant plants display progressively diminished oxidative burst and gene activation induced by the 22-amino-acid peptide flg22, as well as compromised pathogen defence. In contrast to negative roles of calmodulin and a calmodulin-activated transcription factor in plant defence7,8, the present study reveals Ca2+ signalling complexity and demonstrates key positive roles of specific CDPKs in initial MAMP signalling.