Apomixis in Eukaryotes: An Ancient Fair-Weather Alternative to Sex

A characteristic of eukaryotes is the production of epigenetically-reset cells that re‑initiate the life cycle, a process that generally involves sex, i.e., meiosis and syngamy. However, many eukaryotes produce epigenetically-reset gametes or gamete-like cells without meiosis, and these re‑initiate the life cycle without syngamy. This is called apomixis, and it occurs in all eukaryote kingdoms, e.g., in single-celled protists, fungi and algae and in both primitive and derived fungi, algae, diatoms, plants and animals. Primitive apomicts today include single-celled haplontic protists where apomixis cycles with sex in response to environmental cues. The fair-weather mode is apomixis, and sex occurs in response to metabolic stress. Similar environment-regulated sex-apomixis switching is found in taxa of all eukaryote kingdoms. Accordingly, we have hypothesized that apomixis is an epigenetically-regulated polyphenic alternative to sex that originated during eukaryogenesis where it cycled with sex in response to environmental cues. If this is correct, two major implications emerge. First, apomeiosis is more than unreduced gamete formation. It is “formation, without chromosome reduction, of parthenogenesis-competent gametes or gamete-like cells.” This definition unites all types of apomeiosis by a conserved, epigenetics-based apomixis-life-cycle mandate. Accordingly, it includes no meiosis, as in haplontic apomicts, and derived apomeiotic mechanisms where meiosis is either avoided, modified or nullified, as occurs in apospory, diplospory, apogamy, adventitious embryony and automictic parthenogenesis. The second major implication of our hypothesis is an absence of de novo-created (mutation-derived) apomixis genes. Instead, apomixis and sex use the same genes. Cyclical apomixis, where sex and apomixis alternate with seasons, is primitive, and obligate sex and obligate apomixis are derived. The latter may have evolved due to mechanisms of apomixis/sex switching being damaged during evolution.