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Caradec, C.

Publications and source records attributed to Caradec, C..

7 recordsLinked to original sources

Recurrent loss of crossover interference punctuates the recombination landscape across yeast species

Meiotic recombination is essential for the accurate chromosome segregation and the generation of genetic diversity through crossover and gene conversion events. Although this process has been studied extensively in a few selected model species, understanding how its properties vary across species remains limited. In this context, we first characterized the meiotic recombination landscape and properties of the Kluyveromyces lactis budding yeast. We then conducted a comprehensive analysis of 28,897 recombination events spanning 567 meioses in five budding yeast species including Saccharomyces cerevisiae, Saccharomyces paradoxus, Lachancea kluyveri, Lachancea waltii and K. lactis. We observed variations in the recombination landscapes and properties across these species. The Saccharomyces yeasts displayed higher recombination rates compared to the non-Saccharomyces yeasts. In addition, bona fide crossover interference and associated crossover homeostasis were found in the Saccharomyces species only. The evolutionarily conserved ZMM pathway, essential for generating interference-dependent crossovers, has undergone multiple losses throughout evolution, suggesting variations in the regulation of crossover formation. Finally, recombination hotspots, although highly conserved within the Saccharomyces yeasts are not conserved beyond the Saccharomyces genus. Overall, these results highlight great variability and evolution in the recombination landscape between species.

genomics↗

Pan-transcriptome reveals a large accessory genome contribution to gene expression variation in yeast

Gene expression is an essential step in the translation of genotypes into phenotypes. However, little is known about the transcriptome architecture and the underlying genetic effects at a species-level. Here, we generated and analyzed the pan-transcriptome of [~]1,000 yeast natural isolates across 4,977 core and 1,468 accessory genes. We found that the accessory genome is an underappreciated driver of the transcriptome divergence. Global gene expression patterns combined with population structure show that the heritable expression variation mainly lies within subpopulation-specific signatures, for which the accessory genes are overrepresented. Genome-wide association analyses consistently highlight that the accessory genes are associated with proportionally more variants with larger effect sizes, illustrating the critical role of the accessory genome on the transcriptional landscape within and between populations.

genomics↗

142 telomere-to-telomere assemblies reveal the genome structural landscape in Saccharomyces cerevisiae

As population genomics is transitioning from single reference genomes to pangenomes, major improvements in terms of genome contiguity, phylogenetic sampling, haplotype phasing and structural variant (SV) calling are required. Here, we generated the Saccharomyces cerevisiae Reference Assembly Panel (ScRAP) comprising 142 reference-quality genomes from strains of various geographic and ecological origins that faithfully represent the genomic diversity and complexity of the species. The ca. 4,800 non-redundant SVs we identified impact the expression of genes near the breakpoints and contribute to gene repertoire evolution through disruptions, duplications, fusions and horizontal transfers. We discovered frequent cases of complex aneuploidies, preferentially involving large chromosomes that underwent large SVs. We also characterized the evolutionary dynamics of complex genomic regions that classically remain unassembled in short read-based projects, including the 5 Ty families and the 32 individual telomeres. Overall, the ScRAP represents a crucial step towards establishing a high-quality, unified and complete S. cerevisiae pangenome.

genomics↗

Contrasting genomic evolution between domesticated and wild Kluyveromyces lactis yeast populations

The process of domestication has variable consequences on genome evolution leading to different phenotypic signatures. Access to the complete genome sequences of a large number of individuals makes it possible to explore the different facets of this domestication process. Here, we sought to explore the genome evolution of the Kluyveromyces lactis yeast species, a well-known species for its involvement in dairy processes but also present in natural environments. Using a combination of short and long-read sequencing strategies, we investigated the genomic variability of 41 Kluyveromyces lactis isolates and found that the overall genetic diversity of this species is very high ({pi} = 2.9 x 10-2) compared to other species such as Saccharomyces cerevisiae ({pi} = 3 x 10-3). However, the domesticated dairy population shows a reduced level of diversity ({pi} = 7 x 10-4), probably due to a domestication bottleneck. In addition, this entire population is characterized by the introgression of the LAC4 and LAC12 genes, responsible for lactose fermentation and coming from the closely related species, Kluyveromyces marxianus, as previously described. Our results also highlighted that the LAC4/LAC12 gene cluster was acquired through multiple and independent introgression events. Finally, we also identified several genes that could play a role in adaptation to dairy environments through copy number variation. These genes are involved in sugar consumption, flocculation and drug resistance, and may play a role in dairy processes. Overall, our study illustrates contrasting genomic evolution and sheds new light on the impact of domestication processes on it.

genomics↗

Evolution of quantitative trait locus hotspots in yeast species

Dissecting the genetic basis of complex trait remains a real challenge. The budding yeast Saccharomyces cerevisiae has become a model organism for studying quantitative traits, successfully increasing our knowledge in many aspects. However, the exploration of the genotype-phenotype relationship in non-model yeast species could provide a deeper insight into the genetic basis of complex traits. Here, we have studied this relationship in the Lachancea waltii species which diverged from the S. cerevisiae lineage prior to the whole-genome duplication. By performing linkage mapping analyses in this species, we identified 86 quantitative trait loci (QTL) affecting growth fitness in a large number of conditions. The distribution of these loci across the genome has revealed two major QTL hotspots. A first hotspot corresponds to a general fitness QTL, impacting a wide range of conditions. By contrast, the second hotspot highlighted a fitness trade-off with a disadvantageous allele for drug-free conditions which proved to be advantageous in the presence of several drugs. Finally, the comparison of the detected QTL in L. waltii with those which had been previously identified for the same traits in a closely related species, Lachancea kluyveri, clearly revealed the absence of interspecific conservation of these loci. Altogether, our results expand our knowledge on the variation of the QTL landscape across different yeast species.

genetics↗

Pervasive phenotypic impact of a large non-recombining introgressed region in yeast

To explore the origin of the diversity observed in natural populations, many studies have investigated the relationship between genotype and phenotype. In yeast species, especially in Saccharomyces cerevisiae, these studies are mainly conducted using recombinant offspring derived from two genetically diverse isolates, allowing to define the phenotypic effect of genetic variants. However, large genomic variants such as interspecies introgressions are usually overlooked even if they are known to modify the genotype-phenotype relationship. To have a better insight into the overall phenotypic impact of introgressions, we took advantage of the presence of a 1-Mb introgressed region, which lacks recombination and contains the mating-type determinant in the Lachancea kluyveri budding yeast. By performing linkage mapping analyses in this species, we identified a total of 89 loci affecting growth fitness in a large number of conditions and 2,187 loci affecting gene expression mostly grouped into two major hotspots, one being the introgressed region carrying the mating-type locus. Because of the absence of recombination, our results highlight the presence of a sexual dimorphism in a budding yeast for the first time. Overall, by describing the phenotype-genotype relationship in the L. kluyveri species, we expanded our knowledge on how genetic characteristics of large introgression events can affect the phenotypic landscape.

genetics↗

Variation Of The Meiotic Recombination Landscape And Properties Over A Broad Evolutionary Distance In Yeasts

Meiotic recombination is a major factor of genome evolution, deeply characterized in only a few model species, notably the yeast Saccharomyces cerevisiae. Consequently, little is known about variations of its properties across species. In this respect, we explored the recombination landscape of Lachancea kluyveri, a protoploid yeast species that diverged from the Saccharomyces genus more than 100 million years ago and we found striking differences with S. cerevisiae. These variations include a lower recombination rate, a higher frequency of chromosomes segregating without any crossover and the absence of recombination on the chromosome arm containing the sex locus. In addition, although well conserved within the Saccharomyces clade, the S. cerevisiae recombination hotspots are not conserved over a broader evolutionary distance. Finally and strikingly, we found evidence of frequent reversion of meiotic commitment to mitotic growth allowing allele shuffling without meiosis completion. Identification of this major but underestimated evolutionary phenomenon illustrates the relevance of exploring non-model species.\n\nAuthor summaryMeiotic recombination promotes accurate chromosome segregation and genetic diversity. To date, the mechanisms and rules lying behind recombination were dissected using model organisms such as the budding yeast Saccharomyces cerevisiae. To assess the conservation and variation of this process over a broad evolutionary distance, we explored the meiotic recombination landscape in Lachancea kluyveri, a budding yeast species that diverged from S. cerevisiae more than 100 million years ago. The meiotic recombination map we generated revealed that the meiotic recombination landscape and properties significantly vary across distantly related yeast species, supporting that recombination hotspots conservation across yeast species is likely associated to the conservation of synteny. Finally, the frequent meiotic reversions we observed led us to re-evaluate their evolutionary importance.

genomics↗