Maintaining heterokaryosis in pseudo-homothallic fungi

Abstract

Among all the strategies displayed by fungi to reproduce and propagate, some species have adopted a peculiar behavior called pseudo-homothallism. Pseudo-homothallic fungi are true heterothallics, i.e., they need 2 genetically-compatible partners to mate, but they produce self-fertile mycelium in which the 2 different nuclei carrying the compatible mating types are present. This lifestyle not only enables the fungus to reproduce without finding a compatible partner, but also to cross with any mate it may encounter. However, to be fully functional, pseudo-homothallism requires maintaining heterokaryosis at every stage of the life cycle. We recently showed that neither the structure of the mating-type locus nor hybrid-enhancing effect due to the presence of the 2 mating types accounts for the maintenance of heterokaryosis in the pseudo-homothallic fungus P. anserina. In this addendum, we summarize the mechanisms creating heterokaryosis in P. anserina and 2 other well-known pseudo-homothallic fungi, Neurospora tetrasperma and Agaricus bisporus. We also discuss mechanisms potentially involved in maintaining heterokaryosis in these 3 species.

Keywords: heterokaryosis; mating; mating type; podospora anserina; sex in fungi.

Figure 1.

Creation of mating type heterokaryosis during sexual reproduction in P. anserina, N. tetrasperma and A. bisporus. For the 3 species, at meiosis I, the spindles are aligned in the longitudinal axis of the ascus for P. anserina and N. tetrasperma or of the basidium for A. bisporus. (A) In P. anserina, the mating type locus undergoes 99% of SDS. (B) In meiosis II, the spindles are aligned and oriented in the same way as in meiosis I. (C) After meiosis, a post meiotic mitosis occurs for which the spindles are parallel and oriented across the ascus. (D) The ascospores are formed within the ascus, each one engulfing 2 non-sister nuclei. (E) About 1% of the asci show abnormal spore formation where 5 ascospores are present, 2 of them carrying only one nucleus. (F) In N. tetrasperma, the mating type locus undergoes FDS. (G) In meiosis II, the spindles are parallel and partially overlapping. This overlap leads to the same situation as in P. anserina after meiosis. (H) A post-meiotic mitosis takes place in the same way as in P. anserina and (I) the ascospores are also formed around 2 non-sister nuclei and rare 5-spored asci may be obtained. (J) In A. bisporus var. bisporus, the mating type locus likely undergoes FDS. (K) In meiosis II, the spindles may be in the diagonal of the basidium as depicted here or adopt other conformations. After meiosis, 2 non-sister nuclei migrate preferentially through the sterigamata to the basidiospores. This may be facilitated by the fact that the second meiotic division is not synchronous for the 2 nuclei issued from the first meiotic division. (L) The 4 nuclei undergo a post-meiotic mitosis into the basidiospores.