Centromere scission drives chromosome shuffling and reproductive isolation

Abstract

<jats:title>Abstract</jats:title><jats:p>A fundamental characteristic of eukaryotic organisms is the generation of genetic variation via sexual reproduction. Conversely, significant large-scale genome structure variations could hamper sexual reproduction, causing reproductive isolation and promote speciation. The underlying processes behind large-scale genome rearrangements are not well understood and include chromosome translocations involving centromeres. Recent genomic studies in the <jats:italic>Cryptococcus</jats:italic> species complex revealed that chromosome translocations generated via centromere recombination have reshaped the genomes of different species. In this study, multiple DNA double-strand breaks (DSBs) were generated via the CRISPR/Cas9 system at centromere-specific retrotransposons in the human fungal pathogen <jats:italic>Cryptococcus neoformans</jats:italic>. The resulting DSBs were repaired in a complex manner, leading to the formation of multiple inter-chromosomal rearrangements and new telomeres, similar to chromothripsis-like events. The newly generated strains harboring chromosome translocations exhibited normal vegetative growth but failed to undergo successful sexual reproduction with the parental wild-type strain. One of these strains failed to produce any spores, while another produced ∼3% viable progeny. The germinated progeny exhibited aneuploidy for multiple chromosomes and showed improved fertility with both parents. All chromosome translocation events were accompanied without any detectable change in gene sequences and thus, suggest that chromosomal translocations alone may play an underappreciated role in the onset of reproductive isolation and speciation.</jats:p>

Chromosomal rearrangements with stable repertoires of genes and transposable elements in an invasive forest-pathogenic fungus

“…This process has been described in several Eukaryotes, and especially in fungi (e.g. Hou et al 2014, Yadav et al 2020). Double break strands may occur during episodic stresses, for example during some specific recombination events (Yadav et al 2020), and have been described under laboratory conditions (e.g.…”

“…Hou et al 2014, Yadav et al 2020). Double break strands may occur during episodic stresses, for example during some specific recombination events (Yadav et al 2020), and have been described under laboratory conditions (e.g. Dunham et al 2002), and also under natural conditions (e.g.…”

“…The recent identification of changes in epigenetic marks between C. parasitica strains along the European gradient of colonization (Vukovic et al 2019) provide more rationale for investigating the role of these mechanisms in the putative adaptation of the species to these new environments. Another important consequence of these chromosomal rearrangements is the impact on the success of sexual reproduction between these genomes, and the raise of putative pre-zygotic barriers, leading to incipient speciation (Hou et al 2014, Yadav et al 2020). Inter-chromosomal translocations lead to abnormal segregation of homologous chromosomes during meiosis (Kistler and Miao 1992), and possible acquisition of an incomplete repertoire of genes in the progenies of parents with different karyotypes (Yadav et al 2020).…”

“…Another important consequence of these chromosomal rearrangements is the impact on the success of sexual reproduction between these genomes, and the raise of putative pre-zygotic barriers, leading to incipient speciation (Hou et al 2014, Yadav et al 2020). Inter-chromosomal translocations lead to abnormal segregation of homologous chromosomes during meiosis (Kistler and Miao 1992), and possible acquisition of an incomplete repertoire of genes in the progenies of parents with different karyotypes (Yadav et al 2020). Pre-zygotic barriers involving these rearrangements may actually explain the limited number of intermediate genotypes among the predominant genetic lineages observed in south-western Europe, and despite the regular presence of the two mating types within populations (e.g.…”

“…fungi and oomycetes) have generally small genome sizes, present a large diversity of lifestyles, and many are easy to manipulate in laboratory. These general characteristics make them especially interesting to study genomic evolution in eukaryotes and molecular mechanisms involved in genetic adaptation (Raffaele and Kamoun 2012, Chang et al 2013, Wang et al 2020, Yadav et al 2020). For example, fungal genomic studies have investigated gene repertory associated with specific lifestyles (e.g.…”