YODA MAP3K kinase regulates plant immune responses conferring broad‐spectrum disease resistance

Abstract

Mitogen-activated protein kinases (MAPKs) cascades play essential roles in plants by transducing developmental cues and environmental signals into cellular responses. Among the latter are microbe-associated molecular patterns perceived by pattern recognition receptors (PRRs), which trigger immunity. We found that YODA (YDA) - a MAPK kinase kinase regulating several Arabidopsis developmental processes, like stomatal patterning - also modulates immune responses. Resistance to pathogens is compromised in yda alleles, whereas plants expressing the constitutively active YDA (CA-YDA) protein show broad-spectrum resistance to fungi, bacteria, and oomycetes with different colonization modes. YDA functions in the same pathway as ERECTA (ER) Receptor-Like Kinase, regulating both immunity and stomatal patterning. ER-YDA-mediated immune responses act in parallel to canonical disease resistance pathways regulated by phytohormones and PRRs. CA-YDA plants exhibit altered cell-wall integrity and constitutively express defense-associated genes, including some encoding putative small secreted peptides and PRRs whose impairment resulted in enhanced susceptibility phenotypes. CA-YDA plants show strong reprogramming of their phosphoproteome, which contains protein targets distinct from described MAPKs substrates. Our results suggest that, in addition to stomata development, the ER-YDA pathway regulates an immune surveillance system conferring broad-spectrum disease resistance that is distinct from the canonical pathways mediated by described PRRs and defense hormones.

Antagonistic interactions between two MAP kinase cascades in plant development and immune signaling

“…Consistent with enhanced flg22‐induced MAPK activation in YDA silencing lines, a partial loss‐of‐function mutant of YDA was recently reported to display slightly delayed but enhanced activation of MAPKs upon flg22 treatment . In the same study, a ΔN‐YDA line generated by crossing the ΔN‐YDA transgene in the L er background to Col‐0 background was also tested for flg22‐induced MAPK activation and resistance to pathogens.…”

“…Similarly, a kinase dead MAPKKK3 mutant does not affect the interaction between YDA and MKK5, suggesting that the kinase activities of YDA and MAPKKK3/MAPKKK5 are important for the competition for downstream MKKs. Consistent with enhanced flg22-induced MAPK activation in YDA silencing lines, a partial loss-of-function mutant of YDA was recently reported to display slightly delayed but enhanced activation of MAPKs upon flg22 treatment [36]. In the same study, a DN-YDA line generated by crossing the DN-YDA transgene in the Ler background to Col-0 background was also tested for flg22induced MAPK activation and resistance to pathogens.…”

Plant cell wall‐mediated immunity: cell wall changes trigger disease resistance responses

“…Remarkably, it was recently found that BAK1 and ER interact, and that they cooperate with other members of the ER pathway [ER‐like1 (ERL1) and ERL2, and the TOO MANY MOUTHS (TMM) RLP] in the regulation of innate immune response (Meng et al ., ; Jordá et al., 2016). Moreover, the YODA MAP3K functioning downstream of the ER–ERLs–TMM–BAK1 complex in the regulation of developmental processes like stomata patterning has also been found to be required for Arabidopsis broad‐spectrum disease resistance (Sopeña‐Torres et al ., ). Remarkably, yda11 and er‐105 mutants show similar cell wall modifications compared with wild‐type plants, as revealed by glycomics profiling (Sopeña‐Torres et al ., ).…”

“…Moreover, the YODA MAP3K functioning downstream of the ER–ERLs–TMM–BAK1 complex in the regulation of developmental processes like stomata patterning has also been found to be required for Arabidopsis broad‐spectrum disease resistance (Sopeña‐Torres et al ., ). Remarkably, yda11 and er‐105 mutants show similar cell wall modifications compared with wild‐type plants, as revealed by glycomics profiling (Sopeña‐Torres et al ., ). The over‐expression of a constitutively activated YODA protein ( CA‐YDA plants) results in broad‐spectrum disease resistance that is independent of canonical immune pathways (e.g.…”

“…CA‐YDA plants also show constitutive expression of genes encoding putative small secreted peptides (SSPs) and PRRs and altered cell wall composition. These SSPs and some carbohydrate‐derived ligands present in wall fractions of CA‐YDA plants have been suggested to function as novel DAMPs regulating the constitutive immune responses of CA‐YDA plants (Sopeña‐Torres et al ., ).…”