INDETERMINATE-DOMAIN 4 (IDD4) coordinates immune responses with plant-growth in Arabidopsis thaliana

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. Author summary This work illustrates the involvement of the IDD family member 4 in the regulation of defense responses against hemibiotrophic pathogens and in processes governing plant growth. IDD4 is embedded in widely-ramified regulatory pathways and exerts transcriptional control of key factors that shape and balance growth with defense. Mutation in IDD4 and overexpression affect the plant shoot and root growth. At the same time, IDD4 acts as a repressor of innate immunity against the hemi-biotrophic pathogen Pst DC3000. IDD4 interacts with and is in vitro phosphorylated by the immune MAP kinase MPK6. Genome-wide IDD4 DNA-binding studies revealed subsets of direct targets contributing to various developmental processes and immunity. Chromatin-immunoprecipitation and DNA-shift experiments identified the ID1 motif as the prime target site of IDD4 and revealed that phospho-modifed IDD4 shows altered DNA binding ability and thereby gene expression and pathogen resistance. Overall, these results indicate that IDD4 links signal transduction to gene expression of genes involved in basal immunity and growth and development.