EC1 body controls sperm cell reception via gamete pit formation.

Abstract

The remarkable efficiency of double fertilization in flowering plants depends on the precise delivery of immotile sperm cells to two female gametes1. Although sperm cells are rapidly released from the pollen tube, how they are accurately directed to their fertilization site has remained unknown. Here we identify a transient extracellular structure, termed the gamete pit, that forms at the egg cell-central cell (EC-CC) interface immediately after pollen tube discharge and serves as the landing site for sperm cells. Gamete pit formation is enabled by localized dissociation of the EC-CC interface, mediated by extracellular protein assemblies designated EC1 bodies. These structures contain extracellular deposits enriched in EGG CELL 1 (EC1) peptides2, including amyloid-like assemblies. Loss of EC1 bodies prevented gamete pit formation, causing sperm-cell backflow or catastrophic over-penetration of pollen tube contents into the central cell. Surprisingly, ectopic deposition of a heterologous amyloidogenic protein alleviated over-penetration and partially restored fertility. Our findings reveal a mechanism by which extracellular protein assemblies remodel the gamete interface for sperm-cell reception, uncover an unexpected structural role for the conserved gamete-activating peptide EC1, and establish protein-mediated cell-interface remodeling as a fundamental principle underlying double fertilization in flowering plants.