Genetics and Epigenetics of Mating Type Determination in Paramecium and Tetrahymena

Abstract

While sex is an ancient and highly conserved eukaryotic invention, self-incompatibility systems such as mating types or sexes appear to be derived limitations that show considerable evolutionary plasticity. Within a single class of ciliates, Paramecium and Tetrahymena species have long been known to present a wide variety of mating type numbers and modes of inheritance, but only recently have the genes involved been identified. Although similar transmembrane proteins mediate self/nonself recognition in both ciliates, the mechanisms of mating type determination differ widely, ranging from Mendelian systems to developmental nuclear differentiation, either stochastic or maternally inherited. The non-Mendelian systems rely on programmed editing of the germline genome that occurs during differentiation of the somatic nucleus, and they have co-opted different DNA recombination mechanisms-some previously unknown. Here we review the recent molecular advances and some remaining unsolved questions and discuss the possible implications of these diverse mechanisms for inbreeding/outbreeding balance regulation.

Evolutionary origins and impacts of genome architecture in ciliates

“…Despite the critical importance of accurate complex genome reorganization in the development of a new somatic genome in ciliates, the process itself remains susceptible to heritable changes (errors) linked with epigenetic processes and environmental conditions. For example, in P. tetraurelia , mating‐type determination involves the retention of a single 195 bp IES at the mating‐type locus, where the IES is retained in MT‐E (IES + ) and absent in MT‐O (IES – ) . When growing under optimal conditions, spontaneous switches in mating type from MT‐E to MT‐O occur in ∼1/3000 cells, whereas the opposite is much rarer, <1/50,000 cells .…”

“…[51][52][53][54][55] When growing under optimal conditions, spontaneous switches in mating type from MT-E to MT-O occur in ∼1/3000 cells, whereas the opposite is much rarer, <1/50,000 cells. 55 Environmental conditions (e.g., temperature differences) can strongly alter the above patterns of mating-type inheritance. Interestingly, when exposed to reduced temperatures (13°C), MT-O individuals predominantly maintain their mating type; however, the frequency of spontaneous switches from MT-O to MT-E, the difference being the retention of a single specific IES in MT-E (IES + ), increases dramatically with increasing temperature.…”

Identification of the first oomycete mating-type locus sequence in the grapevine downy mildew pathogen,Plasmopara viticola

“…Mating types, preventing mating between individuals carrying the same alleles, have evolved independently in many lineages of the tree of life, including fungi, ciliates, green algae and oomycetes (Billiard et al 2012;Sekimoto 2017;Orias et al 2017). Plants possess a molecular system called self-incompatibility, which enforces outcrossing and is analogous to mating type (Fujii et al 2016).…”

“…Given the fundamental importance of mating types in life cycles and evolution, their molecular determinism has been extensively studied, particularly in plants, fungi and ciliates. Mating types are controlled by a number of different mechanisms, even within these groups (Billiard et al 2012;Fujii et al 2016;Orias et al 2017).…”

Dynamics of the sex ratio in Tetrahymena thermophila

“…100 for Stylonychia mytilus (Ammermann 1982). Second, 84 the mechanisms of sex determination (SD) differ widely, ranging from Mendelian 85 systems to developmental nuclear differentiation, either stochastic or cytoplasmic 86 (Orias et al 2017). The well-studied ciliate, Tetrahymena thermophila, has seven 87 self-incompatible sexes (I-VII) that are determined by alleles at a single locus (mat).…”