Nanodomain-localized formin gates symbiotic microbial entry in legume and solanaceous plants.

Abstract

Colonization of plant roots by symbionts requires substantial morphodynamic reorganization. Examples are actin-scaffolded microcompartments called infection pockets formed during root nodule symbiosis (RNS) by legumes. We demonstrate that the actin-binding formin SYFO2 is indispensable for rhizobial infection in <i>Medicago truncatula</i>, where it drives actin polymerization in phase-separated and symbiosis-specific nanodomains. SYFO2 also regulates symbiotically active arbuscules formed during mycorrhizal symbiosis in plants outside the nodulating clade, indicating that it was additionally recruited to promote rhizobial infections in legumes. As part of our aim to enable nitrogen fixation in nonlegumes, we activated endogenous <i>SYFO2</i> by stably introducing the RNS master regulator NODULE INCEPTION (NIN) into the natural nonhost tomato. This demonstrates the possibility of recruiting arbuscular mycorrhizae-related genes into an engineered nodulation-specific pathway.