Berberine Bridge enzyme-like oxidases orchestrate homeostatic control and signaling of oligogalacturonides in defense and wounding

Plant immunity is triggered by endogenous elicitors known as damage-associated molecular patterns (DAMPs). Oligogalacturonides (OGs) are DAMPs released from the cell wall (CW) demethylated homogalacturonan during microbial colonization, mechanical or pest-provoked tissue damage, and physiological CW remodeling. Berberine Bridge Enzyme-like (BBE-l) proteins named OG oxidases (OGOXs) have been proposed to govern OGs homeostasis, which is necessary to avoid deleterious growth-affecting hyper-immunity and possible cell death. Using OGOX1 over-expressing lines and ogox1/2 double mutants, we show that these enzymes determine the levels of active OGs vs. inactive oxidized products (oxOGs). The ogox1/2-deficient plants have elevated levels of OGs, while plants overexpressing OGOX1 accumulate oxOGs. The balance between OGs and oxOGs affect disease resistance against Pseudomonas syringae pv tomato, Pectobacterium carotovorum, and Botrytis cinerea depending on the microbial capacity to respond to OGs and metabolize oxOGs. Gene expression upon plant infiltration with OGs reveals that OGOXs orchestrate OG signaling in defense as well as upon tissue damage, pointing to these enzymes as apoplastic players in immunity and tissue repair. TeaserOxidases control the homeostasis of oligogalacturonides in the cell wall and play a pivotal role in the plant immunity.