sept-1/zina-1 is an Ancient Toxin-Antidote System in Caenorhabditis elegans

The toxin-antidote (TA) systems, consisting of two tightly linked genes acting as a postzygotic distorter, are found in several eukaryotic organisms, including three androdioecious Caenorhabditis species. However, the evolutionary history of such TA systems remains poorly understood. We report an ancient C. elegans TA system identified in the highly divergent Hawaiian strain XZ1516. The maternal toxin SEPT-1 induces a rod-like larval arrest phenotype in progeny that do not carry the antidote ZINA-1, which has ten zinc finger motifs. Interestingly, zina-1 is pseudogenized in most non-Hawaiian strains, while sept-1 evolves from a toxic to a non-toxic form through sequence divergence. Phylogenetic studies found that sept-1/zina-1 is the most ancestral TA system among the three known ones, and its loss preceded the rise of sup-35/pha-1. These two maternal TAs do not coexist in the same strain but have overlaps with the paternal TA peel-1/zeel-1, which is the latest one to propagate.