INDETERMINATE DOMAIN (IDD)/ BIRD proteins are a highly conserved plant-specific family of transcription factors which play multiple roles in plant development and physiology. Here, we show that mutation in IDD4/IMPERIAL EAGLE increases resistance to the hemi-biotrophic pathogen Pseudomonas syringae, indicating that IDD4 may act as a repressor of basal immune response and PAMP-triggered immunity. Furthermore, the idd4 mutant exhibits enhanced plant-growth indicating IDD4 as suppressor of growth and development. Transcriptome comparison of idd4 mutants and IDD4ox lines aligned to genome-wide IDD4 DNA-binding studies revealed major target genes related to defense and developmental-biological processes. IDD4 is a phospho-protein that interacts and becomes phosphorylated on two conserved sites by the MAP kinase MPK6. DNA-binding studies of IDD4 after flg22 treatment and with IDD4 phosphosite mutants show enhanced binding affinity to ID1 motif-containing promoters and its function as a transcriptional regulator. In contrast to the IDD4-phospho-dead mutant, the IDD4 phospho-mimicking mutant shows altered susceptibility to PstDC3000, salicylic acid levels and transcriptome reprogramming. In summary, we found that IDD4 regulates various hormonal pathways thereby coordinating growth and development with basal immunity.
Alternative splicing (AS) of pre-mRNAs in plants is an important mechanism of gene regulation in environmental stress tolerance but plant signals involved are essentially unknown. Pathogenassociated molecular pattern (PAMP)-triggered immunity (PTI) is mediated by mitogenactivated protein kinases and the majority of PTI defense genes are regulated by MPK3, MPK4 and MPK6. These responses have been mainly analyzed at the transcriptional level, however many splicing factors are direct targets of MAPKs. Here, we studied alternative splicing induced by the PAMP flagellin in Arabidopsis. We identified 506 PAMP-induced differentially alternatively spliced (DAS) genes. Although many DAS genes are targets of nonsense-mediated degradation (NMD), only 19% are potential NMD targets. Importantly, of the 506 PAMPinduced DAS genes, only 89 overlap with the set of 1849 PAMP-induced differentially expressed genes (DEG), indicating that transcriptome analysis does not identify most DAS 2 events. Global DAS analysis of mpk3, mpk4, and mpk6 mutants revealed that MPK4 is a key regulator of PAMP-induced differential splicing, regulating AS of a number of splicing factors and immunity-related protein kinases, such as the calcium-dependent protein kinase CPK28, the cysteine-rich receptor like kinases CRK13 and CRK29 or the FLS2 co-receptor SERK4/BKK1. These data suggest that MAP kinase regulation of splicing factors is a key mechanism in PAMPinduced AS regulation of PTI. Significance statementAlternative pre-mRNA splicing (AS) affects plant responses to environmental stresses. So far, however, the regulation of AS is little understood. Here, we studied AS induced by the pathogenassociated molecular pattern (PAMP) flagellin in Arabidopsis. We identified 506 differentially alternatively spliced (DAS) genes, 89 of which overlap with the 1849 DEG, indicating that the majority of DAS events go undetected by common transcriptome analysis. PAMP-triggered immunity is mediated by mitogen-activated protein kinases. Global DAS analysis of MAPK mutants revealed that MPK4 is a key regulator of AS by affecting splicing factors and a number of important protein kinases involved in immunity. Since PAMP-triggered phosphorylation of several splicing factors is directly mediated by MAPKs, we discovered a key mechanism of AS regulation. IntroductionPlants possess pattern recognition receptors that detect conserved pathogen-associated molecular patterns (PAMPs) and initiate PAMP-triggered immunity (PTI) (1). Successful pathogens deliver effectors to the plant apoplast and various intracellular compartments; these effectors suppress PTI and thereby facilitate invasion of the host. As a strategy to counter effectors, plants have evolved intracellular receptors with nucleotide-binding leucine-rich repeat domains that sense effectors and mediate effector-triggered immunity (2).The bacterial PAMP flg22, a conserved 22-amino-acid peptide derived from Pseudomonas syringae flagellin, has provided a powerful tool to decipher PAMP-induced signaling pathways and reveal...
INDETERMINATE-DOMAIN proteins (IDDs) belong to a diverse plant-specific family of transcriptional regulators that coordinate distinct functions during plant growth and development. The functions of several of these IDD members are transcriptionally regulated, but so far nothing is known about the regulation at the post-translational level in spite of the fact that post-translational modifications of these proteins have been reported in several large-scale proteomics studies. Recently, we showed that IDD4 is a repressor of basal immunity and its characteristic traits are predominantly determined by the phosphorylation at two distinct phosphorylation sites. This finding prompted us to comprehensively review phosphorylation of the various IDD members from the plethora of phosphoproteomics studies demonstrating the post-translational modification of IDDs at highly conserved sites under various experimental conditions. We reckon that the phosphorylation of IDDs is an underrated mechanistic aspect in their regulation and we postulate their importance in IDD/BIRD functioning.
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