Date Published: January 24, 2019
Publisher: Public Library of Science
Author(s): Ronny Völz, Soon-Kap Kim, Jianing Mi, Anamika A. Rawat, Alaguraj Veluchamy, Kiruthiga G. Mariappan, Naganand Rayapuram, Jean-Michel Daviere, Patrick Achard, Ikram Blilou, Salim Al-Babili, Moussa Benhamed, Heribert Hirt, David Mackey.
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.
Plants and animals use pattern recognition receptors (PRRs) to rapidly activate defense signaling pathways and immune responses upon pathogen attack [1, 2]. PRR receptors and their associated signaling components possess a wide range of similarities in mammals, plants and invertebrates [3, 4]. Plant immunity relies on the recognition of pathogen-derived molecules in order to activate pattern-triggered immunity (PTI) and effector-triggered immunity (ETI) . PTI is initiated after the perception of pathogen-associated molecular patterns (PAMPs) of highly conserved pathogen components. FLAGELLIN22 (flg22), a 22 amino acid peptide from within bacterial flagellin protein, represents one important PAMP to trigger PTI in plants and is perceived by the plasma membrane-localized receptor FLAGELLIN-INSENSITIVE2 (FLS2) which associates with BRI1-ASSOCIATED RECEPTOR KINASE (BAK1) in order to rapidly stimulate two mitogen-activated protein kinase (MAPK) cascades. MAPK cascades consist of three sequentially activated kinase modules composed of a MAPK kinase kinase, a MAPK kinase and eventually a MAPK, thereby linking upstream signals to downstream targets. In Arabidopsis as well as throughout the plant kingdom, the MAPK orthologues of MPK3, MPK4 and MPK6 represent the final step in the two flg22-activated MAP kinase cascades and transmit signals to respective target proteins by phosphorylation [6, 7]. MPK3, MPK4 and MPK6 are required for full activation of defence genes . In particular, MPK3/MPK6 contributes to bacterial and fungal resistance  as well as to a multitude of developmental processes, including the regulation of plant architecture, seed, root  and stomatal formation . Furthermore, the MPK6 signaling module participates in nutrient signaling to influence nitrate assimilation, enhances phosphate acquisition and becomes activated upon iron deficiency . Recently, it was shown that MPK3/MPK6 exert essential functions in the induction of camalexin, the major phytoalexin in Arabidopsis, and promote the indole glucosinolate biosynthesis pathway . In addition, MPK3/MPK6 activation rapidly alters the expression of photosynthesis-related genes and inhibits photosynthesis, which promotes the accumulation of superoxide(O2) and hydrogen peroxide (H2O2), two major reactive oxygen species (ROS), in chloroplasts under light .
This work illustrates the involvement of the IDD family member 4 in the regulation of defense responses and in processes governing plant growth. IDD4 is embedded in widely-ramified regulatory pathways and exerts transcriptional control on key factors that shape and balance growth with defense.