A General and Fundamental Molecular Bipolarity of the Sex Cell Contact Mechanism as Revealed by Tunicamycin and Bacitracin in Chlamydomonas

Abstract

Sex cell contact in isogamous dioecious Chlamydomonas species is caused by the interaction of special complementary glycoproteins, mating type substances (MTS), on the flagella of (+) and (-) gametes. Absent in vegetative cells, these glycoproteins are synthesized only after induction of the sexual phase. Their synthesis is sensitive to tunicamycin (TUM) and bacitracin (BAC), but in one sex only. These antibiotics are known to block N-glycosylation of proteins. The contact capacity in the sensitive sex is apparently bound to a ligand of carbohydrate nature, which is N-glycosidically linked to the polypeptide chain of the MTS. The demonstration reported here of a unilateral TUM-effect in another unrelated species, i.e., in all species studied so far, and of a unilateral bacitracin block to gametogenesis indicates the general occurrence of such a basic complementarity between two types of glycoproteins with differently linked contact-establishing ligands. The existence of such complementarity bears on several cell-physiological and evolutionary aspects of gamete copulation: (1) The asymmetrical bipolarity requires alternative and entirely different pathways of gametic differentiation and explains special cases of sex-limited inheritance. (2) In spite of the absence of morphological differences between a species' two gamete types and the sexual isolation between species, the sexes of isogamous incompatible taxa can be homologized according to whether the contact-causing ligand is N-glycosidically linked or not. (3) The basic asymmetrical complementarity stabilizes the sexual bipolarity in isogamous taxa; i.e., because glycoprotein synthesis is channeled early into alternative pathways, the evolution of multiple mating types is effectively prevented. On the molecular level, the fundamental asymmetry grants a gametic bipolarity as efficiently as a morphologically expressed gamete dimorphism does in anisogamous and oogamous species. (4) The data presented suggest a distinctive mode of speciation in these simply organized eukaryotes by mutative alterations of their MTS-systems. Future experiments will prove whether the postulated interaction between an N-glycosidically linked ligand and a ligand of another type holds true for all sex cell contact mechanisms, i.e., for other anisogamous or oogamous algae, for protozoa and fungi, and even for lower and higher plants and metazoans.