A cytoplasmic protein kinase in Chlamydomonas couples engagement of ciliary receptors to rapid cellular responses

Abstract

The principal function of the primary cilium is to convert cues from the extracellular milieu into changes in cyclic nucleotide concentration and cytoplasmic responses, but fundamental questions remain about the mechanisms of transmission of cilium-to-cytoplasm signals. During fertilization in Chlamydomonas reinhardtii, ciliary adhesion between plus and minus gametes triggers an immediate ~10-fold increase in cellular cAMP and activation for cell fusion. Here, we identify Gamete-Specific Protein Kinase (GSPK) as an essential link between cilary receptor engagement and gamete activation. The ciiary adhesion-induced increase in cAMP and cell fusion are severely impaired in gspk mutants but fusion is rescued by a cell-permeable form of cAMP, indicating that GSPK functions upstream of the cAMP increase. GSPK is cytoplasmic, and, remarkably, the entire cellular complement is phosphorylated in less than 60 seconds after ciliary contact. Thus, a cytoplasmic protein kinase rapidly converts a ciliary membrane cue into a global cellular response.