Ciliary adhesion and cilium-generated signaling during fertilization in Chlamydomonas

During fertilization in Chlamydomonas, binding between receptors (agglutinins) on the cilia of plus and minus gametes dynamically tethers the highly motile gametes together into large, swirling clusters of cells. The interacting gametes quickly shed their cell walls, pairs of plus and minus gametes within the clusters reorient by continually breaking and reforming ciliary attachments to bring their fusogenic apical ends into contact, and soon thereafter the two gametes fuse to form a quadriciliated cell. Binding between the receptor SAG1 on plus cilia and its cognate receptor SAD1 on minus cilia not only is responsible for ciliary adhesion, but also triggers a multistep signaling pathway that brings about the biochemical and morphological transformations of the two gametes. This chapter describes our current understanding of the cell biological and biochemical events that are triggered by SAG1-SAD1 interactions that make possible gamete fusion. At the heart of the transience of local ciliary attachments are the release of the SAG1 and SAD1 agglutinins from the ciliary surface in the form of ciliary membrane vesicles (ectosomes) and their replacement by one-way trafficking of stored agglutinins from the plasma membrane through the cytoplasm and onto the ciliary membrane. The signaling pathway activated by ciliary adhesion depends on coupling of SAG1-SAD1 binding to regulation of intraciliary protein phosphorylation and dephosphorylation and consequent regulation of one or more adenylyl cyclases to bring about the 15-fold increase in cellular cAMP required for gamete activation and cell fusion.