Alternative splicing as a key player in the fine-tuning of the immunity response in Arabidopsis

Abstract

Plants, like animals, are constantly exposed to abiotic and biotic stresses, which often inhibit plant growth and development, and cause tissue damage, disease, and even plant death. Efficient and timely response to stress requires appropriate co- and posttranscriptional reprogramming of gene expression. Alternative pre-mRNA splicing provides an important layer of this regulation by controlling the level of factors involved in stress response and generating additional protein isoforms with specific features. Recent high-throughput studies have revealed that several defence genes undergo alternative splicing that is often affected by pathogen infection. Despite extensive work, the exact mechanisms underlying these relationships are still unclear, but the contribution of alternative protein isoforms to the defence response and the role of regulatory factors, including components of the splicing machinery, have been established. Modulation of gene expression in response to stress includes alternative splicing, chromatin remodelling, histone modifications, and nucleosome occupancy. How these processes affect plant immunity is mostly unknown, but these facets open new regulatory possibilities. Here we provide an overview of the current state of knowledge and recent findings regarding the growing importance of alternative splicing in plant response to biotic stress.

Keywords: R genes; chromatin; co-transcriptional splicing; defence response; pathogen; plant immunity; spliceosome.

FIGURE 1

Most frequent types of simply alternative splicing events based on a high‐quality reference transcript dataset for Arabidopsis (AtRTD2).

FIGURE 2

Alternative splicing (AS) of CPK28 regulates plant immunity. The pathogen‐associated molecular pattern (PAMP)‐triggered immunity response triggered by flg22 is mediated by the pattern recognition receptor complex FLS2 and BAK1. FLS2 together with BAK1 phosphorylate the cytoplasmic kinase BIK1, which acts as a positive regulator of the FLS2 signalling pathway. BIK1 phosphorylates RBOHD (RESPIRATORY BURST OXIDASE HOMOLOGUE D) to regulate reactive oxygen species production. BIK1 also phosphorylates MPK4, one of the mitogen‐activated protein kinases that constitute the PAMP‐induced signalling cascade leading to the activation of transcription factors that control the expression of defence genes. MPK4 regulates AS of a number of pathogen response genes, splicing factors (SFs), transcription factors (TFs), cysteine‐rich receptor‐like kinases (CRKs), and RNA‐binding proteins (RBPs). CPK28 acts as a negative immunity regulator through the association and phosphorylation of BIK1, which facilitates its turnover, and also through the phosphorylation of E3 PUB25/26 ligases, which polyubiquitinate BIK1 for proteasome‐mediated degradation. In turn, CPK28 activity requires its autophosphorylation or transphosphorylation by BIK1 at Ser318. The synthesis of a full‐length active CPK28 involves canonical splicing of its pre‐mRNA, which is promoted by association of the phosphorylated RNA‐binding protein IRR. During activation induced by plant elicitor peptides (Peps), IRR is dephoshorylated and dissociates from CPK28, resulting in accumulation of the PTC‐containing intron retention (IR) variant that yields a truncated inactive protein, leading to BIK1 stabilization and consequently a stronger defence response.

FIGURE 3

Mechanism of ASCO long noncoding RNA (lncRNA) action. ASCO lncRNA interacts with nuclear speckle RNA‐binding proteins (NSRs) and two core components of the spliceosome, PRP8a and SmD1, to modulate the population of alternatively spliced isoforms.