Unholy marriages and eternal triangles: how competition in the mushroom life cycle can lead to genomic conflict

Abstract

In the vast majority of sexual life cycles, fusion between single-celled gametes is directly followed by nuclear fusion, leading to a diploid zygote and a lifelong commitment between two haploid genomes. Mushroom-forming basidiomycetes differ in two key respects. First, the multicellular haploid mating partners are fertilized in their entirety, each cell being a gamete that simultaneously can behave as a female, i.e. contributing the cytoplasm to a zygote by accepting nuclei, and a male gamete, i.e. only donating nuclei to the zygote. Second, after gamete union, the two haploid genomes remain separate so that the main vegetative stage, the dikaryon, has two haploid nuclei per cell. Only when the dikaryon produces mushrooms, do the nuclei fuse to enter a short diploid stage, immediately followed by meiosis and haploid spore formation. So in basidiomycetes, gamete fusion and genome mixing (sex) are separated in time. The ‘living apart together’ of nuclei in the dikaryon maintains some autonomy for nuclei to engage in a relationship with a different nucleus. We show that competition among the two nuclei of the dikaryon for such ‘extramarital affairs’ may lead to genomic conflict by favouring genes beneficial at the level of the nucleus, but deleterious at that of the dikaryon.This article is part of the themed issue ‘Weird sex: the underappreciated diversity of sexual reproduction’.

Weird sex: the underappreciated diversity of sexual reproduction

“…At the same time, researchers sometimes use the same terminology but mean fundamentally different things. 'Male' and 'female' as used in fungal sex are fundamentally different beasts than conventional males and females [9,10].…”

“…This is a somewhat awkward state of affairs, but our pragmatic approach is to accept that seeking analogies can help. Features such as the 'malebiased' operational sex ratio of a population of monokaryons and dikaryons [7,10] can truly help link findings in studies on fungi to existing theory, even if that theory is based on the sex life of a multicellular gonochorist animal. Moreover, it would probably be parochial of us to reserve succinct terminology to be used only in contexts that are most familiar to us.…”

“…The topics addressed in this special issue range from very fundamental questions such as the evolutionary benefits [12] and the origin of sex [3,4,13] and mating types [6], to secondary consequences of sexual reproduction, such as sexual selection [5,11] and the increased scope for genetic conflict [8,10,14], and the cost of sex, either due to the production of males in anisogamous species or due to mate finding or mechanisms of meiosis [15].…”

“…While sexual reproduction in most organisms involves a syndrome of various characteristics (gamete fusion, nuclear fusion leading to ploidy change and meiosis), Vreeburg et al [10] describe that in basidiomycete fungi gamete fusion and genomic amalgamation usually are separated in time. This begs for a definition of sex that catches its very essence.…”

“…Or is it meiosis? According to Vreeburg et al [10], sex is 'the union of two haploid nuclei, each produced by meiosis, in due course followed by a reduction of the genome through meiosis', a slightly modified version of Dick's [16] definition. Genetic mixing and meiosis are thus crucial components of eukaryotic sex.…”