Jennifer F Pinello, Andrés Ferriño-Iriarte, Hibba Hussain, Meenakshi Tanwar, Sijil Puthur Vijayan, Tingting Guo, Pierre Legrand, Sujan Manikumar, Ruhama Demissie, Félix A Rey, William J Snell, Eduard Baquero
Species-specific adhesion of gametes is a prerequisite to cell fusion during fertilization, yet the underlying molecular mechanisms are not fully understood for any organism. In Chlamydomonas, the adhesion protein MAR1 chaperones the conserved fusogen HAP2 into a pre-fusion conformation on the mt- gamete and is the receptor for the adhesion protein FUS1 on the mt+ gamete. Here, we report the X-ray structure of the FUS1/MAR1 adhesion complex, showing that it forms a (FUS1/MAR1)2 dimer. We found that mutagenesis at the observed MAR1-FUS1 interface strongly impairs adhesion, and that recombinant, soluble MAR1 binds to FUS1 on activated mt+ gametes and completely blocks HAP2 triggering for fusion. These findings uncover the molecular architecture of a cell surface receptor complex whose formation is required to trigger the membrane-fusogenic conformational change of a eukaryotic class II membrane fusion protein.