Journal Article

A large gene family in fission yeast encodes spore killers that subvert Mendel’s law

Jiang, Zhao-Di, Zheng, Jin-Xin, Suo, Fang, Hu, Wen, He, Wan-Zhong, Du, Li-Lin

2017

Overview

Spore killers in fungi are selfish genetic elements that distort Mendelian segregation in their favor. It remains unclear how many species harbor them and how diverse their mechanisms are. Here, we discover two spore killers from a natural isolate of the fission yeast Schizosaccharomyces pombe. Both killers belong to the previously uncharacterized wtf gene family with 25 members in the reference genome. These two killers act in strain-background-independent and genome-location-independent manners to perturb the maturation of spores not inheriting them. Spores carrying one killer are protected from its killing effect but not that of the other killer. The killing and protecting activities can be uncoupled by mutation. The numbers and sequences of wtf genes vary considerably between S. pombe isolates, indicating rapid divergence. We propose that wtf genes contribute to the extensive intraspecific reproductive isolation in S. pombe, and represent ideal models for understanding how segregation-distorting elements act and evolve. During evolution, new species emerge when individuals from different populations of similar organisms no longer breed with each other, or when the offspring produced if they do breed are sterile. This process is known as “reproductive isolation” and, for over 100 years, evolutionary biologists have tried to better understand how this process happens. Animals, plants and fungi produce sex cells – known as gametes – when they are preparing to reproduce. These cells are made when cells containing two copies of every gene in the organism divide to produce new cells that each only have one copy of each gene. Therefore, a particular gene copy usually has a 50% chance of being carried by an individual gamete. There are genes that selfishly increase their chances of being transmitted to the next generation by destroying the gametes that do not carry them. These “gamete killer” genes reduce the fertility of the organism and lead to reproductive isolation. Fission yeast is a fungus that is widely used in research. There are different strains of fission yeast that are reproductively isolated from each other, but it is not known whether gamete killers are responsible for this isolation. To address this question, Hu et al. investigated the causes of reproductive isolation in fission yeast. The experiments identified two gamete killers, referred to as cw9 and cw27. Both genes belong to the wtf gene family. Each gene is believed to encode two different proteins, one that acts as a poison and one that acts as an antidote. The poison is capable of killing all gametes, but the antidote protects the cells that contain the gamete killer gene. Further experiments show that the antidote produced by one of the gamete killer genes cannot protect cells against the poison produced by the other gene. A separate study by Nuckolls et al. found that another member of the wtf family also acts as a gamete killer in fission yeast. Together, these findings shed new light on the causes of reproductive isolation, and will contribute to deeper understanding of speciation and evolution in general.

• Publisher: eLife Science Publications, Ltd,eLife Sciences Publications Ltd,eLife Sciences Publications, Ltd
• Subject: Chromosomes / Deoxyribonucleic acid / DNA / Fungi / Gene expression / Genes / Genes, Fungal / Genetic aspects / Genetic engineering / Genomes / Genomics and Evolutionary Biology / Laboratories / meiotic drive / Microbial Viability - drug effects / Observations / Phylogenetics / Poisons - metabolism / Reproductive isolation / Schizosaccharomyces - drug effects / Schizosaccharomyces - genetics / Schizosaccharomyces - metabolism / segregation distortion / Selection, Genetic / spore killer / Spores / Spores, Fungal - drug effects / Yeast / Yeasts (Fungi)