Spermine-mediated tight sealing of the Magnaporthe oryzae appressorial pore-rice leaf surface interface

Cellular adhesion mediates many important plant-microbe interactions. In the devastating blast fungus Magnaporthe oryzae¹, powerful glycoprotein-rich mucilage adhesives² cement melanized and pressurized dome-shaped infection cells-appressoria-to host rice leaf surfaces. Enormous internal turgor pressure is directed onto a penetration peg emerging from the unmelanized, thin-walled pore at the appressorial base^1-4, forcing it through the leaf cuticle where it elongates invasive hyphae in underlying epidermal cells⁵. Mucilage sealing around the appressorial pore facilitates turgor build-up², but the molecular underpinnings of mucilage secretion and appressorial adhesion are unknown. Here, we discovered an unanticipated and sole role for spermine in facilitating mucilage production by mitigating endoplasmic reticulum (ER) stress in the developing appressorium. Mutant strains lacking the spermine synthase-encoding gene SPS1 progressed through all stages of appressorial development, including penetration peg formation, but cuticle penetration was unsuccessful due to reduced appressorial adhesion, which led to solute leakage. Mechanistically, spermine neutralized off-target oxygen free radicals produced by NADPH oxidase-1 (Nox1)^3,6 that otherwise elicited ER stress and the unfolded protein response, thereby critically reducing mucilage secretion. Our study reveals that spermine metabolism via redox buffering of the ER underpins appressorial adhesion and rice cell invasion and provides insights into a process that is fundamental to host plant infection.