Triparental inheritance inDictyostelium

Abstract

Sex promotes the recombination and reassortment of genetic material and is prevalent across eukaryotes. In social amoebae sex involves a promiscuous mixing of cytoplasm before zygotes consume the majority of cells.We report here the first genomewide characterisation of meiotic progeny in Dictyostelium discoideum. We find that recombination occurs at high frequency in pairwise crosses between all three mating types, despite the absence of the SPO11 enzyme that is normally required to initiate crossover formation. In crosses involving three strains, transient fusions involving more than two gametes frequently lead to triparental inheritance, with recombined nuclear haplotypes inherited from two parents and the mitochondrial genome from a third. Cells that do not contribute genetically to the Dictyostelium zygote nucleus thereby have a stake in the next haploid generation. We suggest that this lateral transfer helps to enforce cooperation in this confictual system.

Cooperation and conflict in the social amoeba Dictyostelium discoideum

“…The sex-determining locus is known and the presence of three different mating types has been confirmed (Bloomfield et al, 2010). A recent study has revealed an interesting mode of triparental inheritance in lab crosses involving more than two gametes, where two parents contribute to the nuclear genome and the mitochondrial genome comes from the third (Bloomfield et al, 2018). Much is still unknown about the sexual cycle, and it provides a rich area for future study.…”

Sex and macrocyst formation in Dictyostelium

“…When gametes prepared in this way are mixed with gametes of another mating type, fusion begins within minutes (Saga et al, 1983). Remarkably, fusion is so extensive that large syncytia containing tens or hundreds of haploid nuclei are often formed (Bloomfield et al, 2019;Ishida et al, 2005;Saga et al, 1983). These large cells can persist for several hours; gradually they break apart (Fig.…”

“…First, each species (at least in the genus Dictyostelium as recently redefined (Sheikh et al, 2018)) often has more than two mating types, perhaps resulting from selection to increase the probability of sexual compatibility between conspecific cells that encounter each other at the initiation of sex (Bloomfield, 2011). Second, there appears to be no block to multiple fusion of gametes during zygosis: tens or hundreds of gametes can fuse together over a period of several hours before measurable nuclear fusion occurs, allowing mixture of cytoplasms and exchange of mitochondria (Bloomfield et al, 2019;Ishida et al, 2005;Saga et al, 1983). Third, meiosis occurs in the absence of the key Spo11 enzyme, which has a very widely conserved essential function in initiating meiotic recombination in other sexual eukaryotes (Bloomfield, 2016;Bloomfield, 2018a;Bloomfield et al, 2019;Malik et al, 2007).…”

“…Second, there appears to be no block to multiple fusion of gametes during zygosis: tens or hundreds of gametes can fuse together over a period of several hours before measurable nuclear fusion occurs, allowing mixture of cytoplasms and exchange of mitochondria (Bloomfield et al, 2019;Ishida et al, 2005;Saga et al, 1983). Third, meiosis occurs in the absence of the key Spo11 enzyme, which has a very widely conserved essential function in initiating meiotic recombination in other sexual eukaryotes (Bloomfield, 2016;Bloomfield, 2018a;Bloomfield et al, 2019;Malik et al, 2007). This review will discuss recent progress in understanding these critical aspects of dictyostelid biology, and raise the questions that remain outstanding.…”

The past, present and future of Dictyostelium as a model system

“…Multiple knockout mutants can be created by Cre/LoxP-mediated recombination (Faix et al, 2004, Linkner et al, 2012, thus facilitating analysis of gene families or gene networks. Recombination or para-sexual complementation is possible only with a few selected strains (Bloomfield et al, 2019), but mutants may be generally rescued by introducing the gene of interest in wild type or mutated form. In addition to its use for disrupting genes by homologous recombination, restriction enzyme mediated integration (REMI) has been used for suppression genetics (Shaulsky et al, 1996).…”