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Facing constant challenges from various pathogens and pests, plants have evolved different strategies to defend themselves both locally and systemically. A global change in RNA metabolism is one of the necessary steps to mount a long-lasting immunity against present and future invasions.Arabidopsisserine/arginine-rich 45 (SR45) is an evolutionarily conserved RNA-binding protein that regulates multiple steps of RNA metabolism. Our prior study suggested that SR45 acts as a negative regulator of plant immunity. To better understand the molecular mechanism for SR45’s defense role, we examined the metabolic profile in both Col-0 andsr45-1. The results showed a significant accumulation of pipecolic acid (Pip), salicylic acid (SA), and other potential defense compounds insr45-1, indicating an increased systemic immunity. Thesr45–1mutant exhibited an elevated resistance to a wide range of biotrophic pathogen species and insensitivity to Pip, SA, and pathogen pretreatment. Between the two alternatively spliced isoforms, SR45.1 and SR45.2, SR45.1 seemed to be the culprit for the observed immune suppression. Upon examination of the transcriptome profile between Col-0 andsr45-1under either mock orPseudomonas syringae PmaDG3 challenge, we identified 1,125 genes as SR45-suppressed andPmaDG3-induced. Genes that function in SA biosynthesis and systemic acquired resistance were overrepresented, including those coding for WRKY, receptor-like kinases (RLKs), receptor-like proteins (RLPs), protein kinases, and TIR-NBS-LRR proteins. In addition, we identified significant alternative splicing activity in a list of genes due to eithersr45–1alone or bothsr45–1andPmaDG3 challenge. Among them, we characterized the effect of alternative splicing in two candidates,CBRLK1andSRF1. Interestingly, alternative splicing in both exhibited a switch between RLPs and RLKs in the predicted protein products. Overexpressing theirsr45–1dominant isoform in Col-0 led to a partial increase in immunity, suggesting the involvement of both alternative splicing events in SR45-conferred immune suppression. In summary, we hypothesize that SR45 regulates a subset of immune genes at either transcriptional or co-transcriptional pre-mRNA splicing levels to confer its function in systemic immune suppression.