A tuned orchestration of OG elicitor activity is crucial for maintaining the growth-defence trade-off in Arabidopsis

Microbes loosen and degrade the plant cell wall (CW) to promote their growth in planta. Several CW fragments released during colonization by microbes are recognized by Pattern Recognition Receptors as damage-associated molecular patterns (DAMPs) that trigger plant immunity. Typical CW DAMPs are the oligogalacturonides (OGs), oligomers of alpha-1,4-linked galacturonosyl residues. Accumulation of OGs in vivo is favored by the concomitant activity of microbial polygalacturonases (PGs) and their plant inhibitors (PGIPs). Transgenic Arabidopsis plants expressing a PGIP-PG chimera named “OG-machine” under inducible promoters release OGs on command that confer resistance to many microbes. However, over-accumulation of OGs in these plants also results in growth penalties (growth–defense trade-off) and may culminate in a deleterious hyper-immunity including cell death. This negative impact of the OG action may be prevented by a homeostatic control exerted by specific OG oxidases (OGOXs) that belong to the Berberine Bridge Enzyme-like (BBE-like) protein family. Through a reverse genetic approach we show that OGOXs play a crucial role in the homeostasis of OG levels in the apoplast and in dampening OG elicitor activity. Furthermore, expressing the OG machine in genetic backgrounds defective in key elements of plant immunity such as EDS1, RBOHD and JAR1 we show that the effects on growth and defense can be uncoupled. Our results suggest that a tuned orchestration of OG elicitor activity is crucial for maintaining the growth-defence trade-off in Arabidopsis.