Formin-mediated bridging of cell wall, plasma membrane, and cytoskeleton in symbiotic infections of Medicago truncatula Graphical abstract Highlights d The SYMBIOTIC FORMIN 1 (SYFO1) specifically regulates symbiotic root hair curling d SYFO1 directly binds actin and polarizes in responding root hairs d SYFO1 induces membrane protrusions in cell-wall-devoid protoplasts d Cell wall association of SYFO1 is indispensable for its function in root hairs

Plant cell infections are tightly orchestrated by cell wall (CW) alterations, plasma membrane (PM) resident signalling processes and dynamic remodelling of the cytoskeleton. During root nodule symbiosis these processes result in morpho-dynamic responses including root hair swelling and curling, PM invagination and polar growth of a tubular infection structure, the infection thread (IT). However, the molecular details driving and guiding these PM remodelling events remain to be unravelled. Here, we studied a formin protein (SYFO1) in M. truncatula that is specifically induced during rhizobial infection. Phenotypical analysis of syfo1 mutants clearly indicates that the encoded protein is required for efficient rhizobial colonization of root hairs. SYFO1 itself creates a proteinaceous bridge between the CW and the polarized cytoskeleton. It binds to CW components via a proline-rich N-terminal segment, which is indispensable for its function. On the cytoplasmic side of the PM SYFO1 is associated with actin accumulations supporting the hypothesis that it contributes to cell polarization in vivo. This is further sustained by the fact that cell shape changes can be induced in a stimulus-dependent manner in root protoplasts expressing SYFO1. Taken together we provide evidence for the evolutionary re-wiring of a generic cytoskeleton modulator into a symbiosis-specific response.