Meiotic Drive in Neurospora and Other Fungi

Abstract

When a gene complex called Spore killer is heterozygous, ascospores representing two of the four products of each meiosis are killed. Only those that receive the killer complex survive. This article reviews what is known of the mode of action of the Neurospora Spore killers, their chromosomal basis, and their occurrence in nature. Similar genes or gene com- plexes have been found in other fungi. An example from Podospora anserina is analyzed. The best-studied example of meiotic drive in fungi is Spore killer in Neuro- spora, which has much in common with the Segregation Distorter (SD) complex in Drosophila and the t complex in mice. The effects are manifested postmeioti- cally in all three systems, but the results of drive are seen most directly in Neuro- spora. With the SD complex and with the t haplotypes, it is necessary to produce a heterozygous male and then to obtain and analyze diploid progeny in order to assess the effects of that heterozygosity in the father. Electron microscopy of heterozygous SD crosses can be used to confirm that about half of the sperm deteriorate, but this procedure is far too demanding for routine use. In Neuro- spora, by contrast, Spore killer is manifested in ascospores that can be seen under low magnification with a dissecting microscope. These ascospores are the immediate products of meiosis; yet they differ from sperm in being themselves the progeny. In Neurospora crassa, each fertilization event in a cross results in a fruiting body within which haploid nuclei proliferate in dikaryotic fashion, producing many pairs of nuclei of opposite mating type that fuse and go into meiosis, each in a separate ascus. As with male meiosis in plants and animals, all four meiotic products normally survive. Each mature ascus normally contains eight viable black ascospores, which originated from the same meiosis (the four immediate meiotic products undergo an additional mitosis before ascospore walls enclose the eight daughter nuclei). The result is essentially four sets of identical twins. A feature of ascospore formation that is important for Spore killer is the timing of cell-wall formation. Meiosis and the postmeiotic mitosis occur in a common cytoplasm. No cell walls are present in the developing ascus until the ascospore walls are formed. (For a diagram of the Neurospora life cycle, see Perkins and Barry 1977; for an illustrated account of events in the ascus, see Raju 1980.) Spore killer was discovered because of its dramatic effect on the appearance of ascospores. Viable ascospores are black, but inviable ascospores remain small and unpigmented. When a Spore-killer strain is crossed with the standard wild