Pichia sorbitophila, an Interspecies Yeast Hybrid, Reveals Early Steps of Genome Resolution After Polyploidization

Abstract

Polyploidization is an important process in the evolution of eukaryotic genomes, but ensuing molecular mechanisms remain to be clarified. Autopolyploidization or whole-genome duplication events frequently are resolved in resulting lineages by the loss of single genes from most duplicated pairs, causing transient gene dosage imbalance and accelerating speciation through meiotic infertility. Allopolyploidization or formation of interspecies hybrids raises the problem of genetic incompatibility (Bateson-Dobzhansky-Muller effect) and may be resolved by the accumulation of mutational changes in resulting lineages. In this article, we show that an osmotolerant yeast species, Pichia sorbitophila, recently isolated in a concentrated sorbitol solution in industry, illustrates this last situation. Its genome is a mosaic of homologous and homeologous chromosomes, or parts thereof, that corresponds to a recently formed hybrid in the process of evolution. The respective parental contributions to this genome were characterized using existing variations in GC content. The genomic changes that occurred during the short period since hybrid formation were identified (e.g., loss of heterozygosity, unilateral loss of rDNA, reciprocal exchange) and distinguished from those undergone by the two parental genomes after separation from their common ancestor (i.e., NUMT (NUclear sequences of MiTochondrial origin) insertions, gene acquisitions, gene location movements, reciprocal translocation). We found that the physiological characteristics of this new yeast species are determined by specific but unequal contributions of its two parents, one of which could be identified as very closely related to an extant Pichia farinosa strain.

Global deceleration of gene evolution following recent genome hybridizations in fungi

“…The uniparental gene losses of ribosomal subunit genes (Supplemental Fig. S4) are consistent with a previous study of a young Saccharomycetaceae hybrid (Louis et al 2012), in which uniparental losses of ribosomal RNA genes were detected. These observations may indicate a mechanism similar to nucleolar dominance, in which a hybrid genome epigenetically silences one parental set of ribosomal RNA genes.…”

“…Furthermore, in addition to the issue of globally increased gene dosage that is common between WGD and genome hybridization, a hybrid species has to resolve the issue of incompatible genes and proteins encoded by its two parental genomes. Recent analyses of several fungal hybrids have revealed mechanisms such as extensive loss of heterozygosity Louis et al 2012;Stukenbrock et al 2012) and gene expression reprogramming (Tirosh et al 2009) that may help hybrid genomes stabilize. Gene conversion, which is capable of homogenizing redundant paralogs (Takuno et al 2008;McGrath et al 2014), can also play a role in resolving incompatibility between the two parental genomes of a hybrid.…”

Nucleolar dominance and maternal control of 45S rDNA expression

“…Histone deacetylase Sir2 controls both E-pro transcription [39] and replication timing [47]. Uniparental loss of 45S rDNA was also reported in the allotetraploid grass Zingeria trichopoda [48], allotetraploid Tragopogon (Asteraceae) [49], and allopolyploid yeast Pichia sorbitophila [50]. All these observations from hybrid (allopolyploid) genomes suggest that parent-of-origin effects may be a pervasive feature of rDNA chromatin.…”

Evolutionary history of two divergent Dmrt1 genes reveals two rounds of polyploidy origins in gibel carp

“…Recent polyploids have been identified in fishes and amphibians (Choleva and Janko, 2013;Gui and Zhou, 2010;Otto, 2007;Song et al, 2012) and some diploidized tetraploid species have been demonstrated in some teleost fish lineages including cyprinids, catostomids, and salmonids (Allendorf and Thorgaard, 1984;Collares-Pereira et al, 2013;Gui and Zhou, 2010;Yang and Gui, 2004), but the two recent rounds of polyploidy have been documented only in the polyploid gibel carp. Recent genome-wide studies have confirmed that the problem of genetic incompatibility raised by polyploidy may be resolved by the accumulation of diverse mutational changes to form a stable chimerical and diploidized genome (Buggs et al, 2011;Chen and Ni, 2006;Louis et al, 2012;Tate et al, 2009). And, a lot of biogeographic and ecological investigations have revealed the close association between polyploidy occurrence and environmental change (Parisod et al, 2010;Wu et al, 2010).…”