A Chimeric IDD4 Repressor Constitutively Induces Immunity in Arabidopsis via the Modulation of Salicylic Acid and Jasmonic Acid Homeostasis

INDETERMINATE DOMAIN (IDD)/BIRD proteins belong to a highly conserved plant-specific group of transcription factors with dedicated functions in plant physiology and development. Here, we took advantage of the chimeric repressor gene-silencing technology (CRES-T, SRDX) to widen our view on the role of IDD4/IMPERIAL EAGLE and IDD family members in plant immunity. The hypomorphic idd4SRDX lines are compromised in growth and show a robust autoimmune phenotype. Hormonal measurements revealed the concomitant accumulation of salicylic acid and jasmonic acid suggesting that IDDs are involved in regulating the metabolism of these biotic stress hormones. The analysis of immunity-pathways showed enhanced activation of immune MAP kinase-signaling pathways, the accumulation of hydrogen peroxide and spontaneous programmed cell death. The transcriptome of nonelicited idd4SRDX lines can be aligned to approximately 40% of differentially expressed genes (DEGs) in flg22-treated wild-type plants. The pattern of DEGs implies IDDs as pivotal repressors of flg22-dependent gene induction. Infection experiments showed the increased resistance of idd4SRDX lines to Pseudomonas syringae and Botrytis cinerea implying a function of IDDs in defense adaptation to hemibiotrophs and necrotrophs. Genome-wide IDD4 DNA-binding studies (DAP-SEQ) combined with DEG analysis of idd4SRDX lines identified IDD4-regulated functional gene clusters that contribute to plant growth and development. In summary, we discovered that the expression of idd4SRDX activates a wide range of defense-related traits opening up the possibility to apply idd4SRDX as a powerful tool to stimulate innate immunity in engineered crops.