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Peris, D.

Publications and source records attributed to Peris, D..

15 recordsLinked to original sources

Mitochondrial inheritance as an important parameter for the rational design of synthetic yeast polyploids

Synthetic allopolyploidization is a powerful strategy for generating strains with novel industrially relevant traits. During the design of select, hybridize, evolved and learn cycle, the mitochondrial inheritance is considered neutral and most studies overcome their phenotypic impact. Here, we generated 168 synthetic allotetraploid strains representing all pairwise parental combinations of eight wild Saccharomyces species, and systematically controlled mitochondrial inheritance in these crosses. These allopolyploids were phenotyped across 31 environmental conditions relevant to biotechnology. In ~50% of all condition-strain combinations conditions, allotetraploids exhibited mid-parent heterosis. In approximately 25% of conditions, we found crosses with hybrid vigor, particularly in combinations involving Saccharomyces arboricola x Saccharomyces mikatae . However, allotetraploids were highly unstable and rapidly sporulated. Our analyses revealed that environmental conditions accounted for the largest effects, follow by its interaction with mitotype. However, mitotype alone showed small effects but significantly affected 42% of the tested conditions, underscoring the importance of mitochondrial inheritance as a key determinant of allopolyploid performance. These findings demonstrate that mitochondrial inheritance is a key, environment-dependent determinant of allopolyploid fitness and should be considered alongside nuclear genome composition in the rational design of industrial allopolyploid strains

microbiology↗

eIF5A is an indispensable protein for eukaryotic cells

eIF5A is an evolutionarily conserved protein found in all eukaryotes, and in Archaea and bacteria. It functions as a translation factor promoting ribosomal elongation, and it can also bind to genes in the nucleus and to mRNA. eIF5A is encoded by two paralogous genes in most eukaryotes, with one copy (TIF51A in yeast and EIF5A1 in humans) highly expressed and essential, and the other (TIF51B in yeast and EIF5A2 in humans) repressed in most cells and conditions. eIF5A is linked to viral infection, aging, diabetes and neurodevelopmental disorders. Whilst derepression of the duplicated silent gene EIF5A2 is associated with several cancers, promoting metastasis. To expand our knowledge of eIF5As function, we searched for suppressors of yeast temperature-sensitive mutants of TIF51A, which cannot grow at restrictive temperature. All suppressors contained mutations in the transcriptional repressors Rox1 and Mot3, resulting in the upregulation of the paralogous gene TIF51B. Next, we searched for suppressors of TIF51A temperature-sensitive mutants in yeast lacking the TIF51B gene. The frequency of suppression was 20-times lower and all suppressors were revertants or contained intragenic mutations in the Tif51A protein that conferred stability. Our results suggest that the duplicated eIF5A gene serves as a non-conventional backup system that rescues mutations in the first copy, but acting at the population level. Furthermore, our results expand our understanding of the repression mechanisms that keep the second eIF5A gene silent. Lastly, our results demonstrate that eIF5A is an indispensable protein in eukaryotic cells, whose function cannot be substituted by mutations in other proteins or pathways. Article summaryeIF5A is an evolutionary conserved protein encoded by two paralogous genes in eukaryotes: one highly expressed and essential, and the other silent. eIF5A promotes translation elongation, and its deficiency is linked to diabetes, aging and neurodevelopmental disorders; while derepression of the silent gene promotes metastatic cancers. We isolated suppressors of conditional mutants of the first eIF5A gene in yeast cells. Suppressors either up-regulated the second eIF5A gene or reverted first copy mutations, restoring eIF5A protein levels and survival. Our work deepens our understanding of the eIF5A paralogue gene repression, and demonstrates that eIF5A is an indispensable protein for eukaryotic cells.

genetics↗

Macroevolutionary dynamics of beetles reveal long-term coupling with vascular plant diversification

Beetles (Coleoptera) represent the most species-rich group of organisms, yet the macroevolutionary processes underlying their exceptional diversification remain unresolved. Here, we estimated their origination and extinction dynamics as well as the potential drivers shaping these patterns, using Bayesian birth-death models applied to a comprehensive fossil occurrence dataset. We find that beetles have experienced low extinction rates and exhibited high resilience through major extinction events. Vascular plant diversities emerge as a key driver of beetle diversification, with origination rates positively correlated with angiosperms, and extinction rates negatively correlated, especially for Polyphaga, the most diverse beetle clade. Together, our results provide quantitative evidence that the angiosperm radiation not only promoted beetle origination, but also buffered them against extinction, illustrating how ecological interactions can shape macroevolution.

evolutionary biology↗

Reticulate evolution and rapid development of reproductive barriers upon secondary contact pose challenges for species delineation in a forest fungus

Reproductive barriers within morphospecies of the mushroom-forming fungi tend to be stronger between sympatric lineages, leading to speculation on whether they are being reinforced by selection against hybrids. In this study we use population genomic analyses together with in vitro crosses of a global sample of the wood decay fungus Trichaptum abietinum to investigate reproductive barriers within this morphotaxon and the processes that have shaped them. Our phylogeographic analyses show that the morphospecies is delimited into six major lineages, one in Asia, two in Europe, and three in North America. The two lineages present in Europe are interfertile and admixed, whereas our crosses show that the North American lineages are reproductively isolated. In Asia a more complex pattern appears, with partial intersterility between multiple sub-lineages that likely originated independently and more recently than the reproductive barriers in North America. We found pre-mating barriers in T. abietinum to be moderately correlated with genomic divergence, whereas fitness of the mated hybrids showed a strong positive correlation with increasing genomic divergence. Genome wide association analyses identified candidate genes with programmed cell death annotations, which are known to be involved in intersterility in distantly related fungi. Our demographic modelling and phylogenetic network analyses suggest that reproductive barriers in Trichaptum abietinum could have been reinforced upon secondary contact between lineages that diverged in allopatry during the Pleistocene glacial cycles. Our combination of experimental and genomic approaches demonstrate how T. abietinum is a tractable system for studying speciation mechanims.

evolutionary biology↗

The dual role of the angiosperm radiation on insect diversification

Most of the animal pollination is realized by insects, interactions between them and flowering plants have been hypothesized to be important drivers of diversification. Yet, there is weak support for coevolutionary diversification in plant-pollinator interactions. Macroevolutionary studies on insect and plant diversities support the hypothesis that angiosperms evolved after an insect diversity peak in the Early Cretaceous, suggesting that gymnosperm pollinators may have been accessible for angiosperms when they evolved. We examined fossil and phylogenetic evidence documenting this hypothesis and provide new clues on the impact of angiosperm radiation on insect diversification. Using the family-level fossil record of insects and a Bayesian process-based approach, we estimated diversification rates and the role of six different variables on insect macroevolutionary history. We found that, among the six tested variables, angiosperms had a dual role that has changed through time with an attenuation of insect extinction in the Cretaceous and a driver of insect origination in the Cenozoic. However, increasing insect diversity, spore plants and global temperature also showed strong positive correlation with both origination and extinction rates of insects, suggesting that different drivers had important effect on insect evolution, not just angiosperms, which would deserve further studies.

paleontology↗

Introgression between highly divergent fungal sister species

To understand how species evolve and adapt to changing environments, it is important to study gene flow and introgression due to their influence on speciation and radiation events. Here, we apply a novel experimental system for investigating these mechanisms using natural populations. The system is based on two fungal sister species with morphological and ecological similarities occurring in overlapping habitats. We examined introgression between these species by conducting whole genome sequencing of individuals from populations in North America and Europe. We assessed genome wide nucleotide divergence and performed crossing experiments to study reproductive barriers. We further used ABBA-BABA statistics together with a network analysis to investigate introgression, and conducted demographic modelling to gain insight into divergence times and introgression events. The results revealed that the species are highly divergent and incompatible in vitro. Despite this, small regions of introgression were scattered throughout the genomes and one introgression event likely involves a ghost population (extant or extinct). This study demonstrates that introgression can be found among divergent species and that population histories can be studied without collections of all the populations involved. Moreover, the experimental system is shown to be a useful tool for research on reproductive isolation in natural populations.

evolutionary biology↗

Macroevolutionary diversity of traits and genomes in the model yeast genus Saccharomyces

Species is the fundamental unit to quantify biodiversity. In recent years, the model yeast Saccharomyces cerevisiae has seen an increased number of studies related to its geographical distribution, population structure, and phenotypic diversity. However, seven additional species from the same genus have been less thoroughly studied, which has limited our understanding of the macroevolutionary leading to the diversification of this genus over the last 20 million years. Here, we report the geographies, hosts, substrates, and phylogenetic relationships for approximately 1,800 Saccharomyces strains, covering the complete genus with unprecedented breadth and depth. We generated and analyzed complete genome sequences of 163 strains and phenotyped 128 phylogenetically diverse strains. This dataset provides insights about genetic and phenotypic diversity within and between species and populations, quantifies reticulation and incomplete lineage sorting, and demonstrates how gene flow and selection have affected traits, such as galactose metabolism. These findings elevate the genus Saccharomyces as a model to understand biodiversity and evolution in microbial eukaryotes.

evolutionary biology↗

Dinosaur bonebed amber from an original swamp forest soil

Dinosaur bonebeds with amber content, yet scarce, offer a superior wealth and quality of data on ancient terrestrial ecosystems. However, the preserved palaeodiversity and/or taphonomic characteristics of these exceptional localities had hitherto limited their palaeobiological potential. Here we describe the amber from the Lower Cretaceous dinosaur bonebed of Arino (Teruel, Spain) using a multidisciplinary approach. Amber is found in both a root layer with amber strictly in situ and a litter layer namely composed of aerial pieces unusually rich in bioinclusions, encompassing 11 insect orders, arachnids, and a few plant and vertebrate remains, including a feather. Additional palaeontological data - charophytes, palynomorphs, ostracods- are provided. Arino arguably represents the most prolific and palaeobiologically diverse locality in which fossiliferous amber and a dinosaur bonebed have been found in association, and the only one known where the vast majority of the palaeontological assemblage suffered no or low-grade pre-burial transport. That has enabled unlocking unprecedentedly complete and reliable palaeoecological data out of two complementary windows of preservation from the same site.

paleontology↗

Long-term balancing selection in highly dynamic mating loci generates trans-species polymorphisms in fungi

Balancing selection, an evolutionary force that retains genetic diversity, has been detected in multiple genes and organisms, such as the sexual mating loci in fungi. However, to quantify the strength of balancing selection and define the mating-related genes require a large number of specimens. In tetrapolar basidiomycete fungi, sexual type is determined by two unlinked loci, MATA and MATB. Genes in both loci defines mating type identity, control successful mating and completion of the life cycle. These loci are usually highly diverse. Previous studies have speculated, based on culture crosses, that species of the non-model genus Trichaptum (Hymenochaetales, Basidiomycota) possess a tetrapolar mating system, with multiple alleles. Here, we sequenced a hundred and eighty specimens of three Trichaptum species. We characterized the chromosomal location of MATA and MATB, the molecular structure of MAT regions and their allelic richness. Our sequencing effort was sufficient to molecularly characterize multiple MAT alleles segregating before the speciation event of Trichaptum species. Our analyses suggested that long-term balancing selection has generated trans-species polymorphisms. Mating sequences were classified in different allelic classes based on an amino acid identity (AAI) threshold supported by phylogenetics. The inferred allelic information mirrored the outcome of in vitro crosses, thus allowing us to support the degree of allelic divergence needed for successful mating. Even with the high amount of divergence, key amino acids in functional domains are conserved. The observed allelic classes could potentially generate 14,560 different mating types. We conclude that the genetic diversity of mating in Trichaptum loci is due to long-term balancing selection, with limited recombination and duplication activity. Our large number of sequenced specimens highlighted the importance of sequencing multiple individuals from different species to detect the mating-related genes, the mechanisms generating diversity and the evolutionary forces maintaining them. Author summaryFungi have complex mating systems, and basidiomycete fungi can encode thousands of mating types. Individuals with the same mating type cannot mate. This sexual system has evolved to facilitate sexual mating, increasing the chances to recombine into advantageous allelic combination and prune deleterious alleles. We explored the genomes of hundred and eighty specimens, combined with experimental mating studies of selected specimens, from a non-model organism (Trichaptum). We characterized the genomic regions controlling sex. The mating ability of the specimens confirmed the role of the mating alleles observed in the genomic data. The detailed analyses of many specimens allowed us to observe gene duplication and rearrangements within the mating loci, increasing the diversity within these loci. We supported previous suggestions of balancing selection in this region, an evolutionary force that maintains genomic diversity. These results supports that our fungal specimens are prone to outcross, which might facilitate the adaptation to new conditions.

genomics↗

Genomic diversity and global distribution of Saccharomyces eubayanus, the wild ancestor of hybrid lager-brewing yeasts

S. eubayanus, the wild, cold-tolerant parent of hybrid lager-brewing yeasts, has a complex and understudied natural history. The exploration of this diversity can be used both to develop new brewing applications and to enlighten our understanding of the dynamics of yeast evolution in the wild. Here, we integrate whole genome sequence and phenotypic data of 200 S. eubayanus strains, the largest collection to date. S. eubayanus has a multilayered population structure, consisting of two major populations that are further structured into six subpopulations. Four of these subpopulations are found exclusively in the Patagonian region of South America; one is found predominantly in Patagonia and sparsely in Oceania and North America; and one is specific to the Holarctic ecozone. S. eubayanus is most abundant and genetically diverse in Patagonia, where some locations harbor more genetic diversity than is found outside of South America. All but one subpopulation shows isolation-by-distance, and gene flow between subpopulations is low. However, there are strong signals of ancient and recent outcrossing, including two admixed lineages, one that is sympatric with and one that is mostly isolated from its parental populations. Despite S. eubayanus extensive genetic diversity, it has relatively little phenotypic diversity, and all subpopulations performed similarly under most conditions tested. Using our extensive biogeographical data, we constructed a robust model that predicted all known and a handful of additional regions of the globe that are climatically suitable for S. eubayanus, including Europe. We conclude that this industrially relevant species has rich wild diversity with many factors contributing to its complex distribution and biology.

genomics↗

Allododecaploid yeasts: synthetic hybrids of six species

Allopolyploidy generates diversity by increasing the number of copies and sources of chromosomes. Many of the best-known evolutionary radiations, crops, and industrial organisms are ancient or recent allopolyploids. Allopolyploidy promotes differentiation and facilitates adaptation to new environments, but the tools to test its limits are lacking. Here we develop an iterative method to combine the genomes of multiple budding yeast species, generating Saccharomyces allopolyploids of an unprecedented scale. Chromosomal instability and cell size increased dramatically as additional copies of the genome were added, but we were able to construct synthetic hybrids of up to six species. The six-species hybrids initially grew slowly, but they rapidly adapted when selection to a novel environment was applied, even as they retained traits from multiple species. These new synthetic yeast hybrids have potential applications for the study of polyploidy, genome stability, chromosome segregation, cancer, and bioenergy. One sentence summaryWe constructed six-species synthetic hybrids and showed that they were chromosomally unstable but able to adapt rapidly.

genetics↗

Mitochondria-encoded genes contribute to the evolution of heat and cold tolerance among Saccharomyces species

Over time, species evolve substantial phenotype differences. Yet, genetic analysis of these traits is limited by reproductive barriers to those phenotypes that distinguish closely related species. Here, we conduct a genome-wide non-complementation screen to identify genes that contribute to a major difference in thermal growth profile between two Saccharomyces species. S. cerevisiae is capable of growing at temperatures exceeding 40{degrees}C, whereas S. uvarum cannot grow above 33{degrees}C but outperforms S. cerevisiae at 4{degrees}C. The screen revealed only a single nuclear-encoded gene with a modest contribution to heat tolerance, but a large effect of the species mitochondrial DNA (mitotype). Furthermore, we found that, while the S. cerevisiae mitotype confers heat tolerance, the S. uvarum mitotype confers cold tolerance. Recombinant mitotypes indicate multiple genes contribute to thermal divergence. Mitochondrial allele replacements showed that divergence in the coding sequence of COX1 has a moderate effect on both heat and cold tolerance, but it does not explain the entire difference between the two mitochondrial genomes. Our results highlight a polygenic architecture for interspecific phenotypic divergence and point to the mitochondrial genome as an evolutionary hotspot for not only reproductive incompatibilities, but also thermal divergence in yeast.

evolutionary biology↗

Mitochondrial DNA and temperature tolerance in lager yeasts

A growing body of research suggests that the mitochondrial genome (mtDNA) is important for temperature adaptation. In the yeast genus Saccharomyces, species have diverged in temperature tolerance, driving their use in high or low temperature fermentations. Here we experimentally test the role of mtDNA in temperature tolerance in synthetic and industrial hybrids (Saccharomyces cerevisiae x Saccharomyces eubayanus, or Saccharomyces pastorianus), which cold-brew lager beer. We find that the relative temperature tolerances of hybrids correspond to the parent donating mtDNA, allowing us to modulate lager strain temperature preferences. The strong influence of mitotype on the temperature tolerance of otherwise identical hybrid strains provides support for the mitochondrial climactic adaptation hypothesis in yeasts and demonstrates how mitotype has influenced the world's most commonly fermented beverage.\n\nOne Sentence SummaryMitochondrial genome origin affects the temperature tolerance of synthetic and industrial lager-brewing yeast hybrids.

genetics↗

sppIDer: a species identification tool to investigate hybrid genomes with high-throughput sequencing

The genomics era has expanded our knowledge about the diversity of the living world, yet harnessing high-throughput sequencing data to investigate alternative evolutionary trajectories, such as hybridization, is still challenging. Here we present sppIDer, a pipeline for the characterization of interspecies hybrids and pure species,that illuminates the complete composition of genomes. sppIDer maps short-read sequencing data to a combination genome built from reference genomes of several species of interest and assesses the genomic contribution and relative ploidy of each parental species, producing a series of colorful graphical outputs ready for publication. As a proof-of-concept, we use the genus Saccharomyces to detect and visualize both interspecies hybrids and pure strains, even with missing parental reference genomes. Through simulation, we show that sppIDer is robust to variable reference genome qualities and performs well with low-coverage data. We further demonstrate the power of this approach in plants, animals, and other fungi. sppIDer is robust to many different inputs and provides visually intuitive insight into genome composition that enables the rapid identification of species and their interspecies hybrids. sppIDer exists as a Docker image, which is a reusable, reproducible, transparent, and simple-to-run package that automates the pipeline and installation of the required dependencies (https://github.com/GLBRC/sppIDer).

evolutionary biology↗

Evidence for loss and adaptive reacquisition of alcoholic fermentation in an early-derived fructophilic yeast lineage

Fructophily is a rare trait that consists in the preference for fructose over other carbon sources. Here we show that in a yeast lineage (the Wickerhamiella/Starmerella, W/S clade) formed by fructophilic species thriving in the floral niche, the acquisition of fructophily is part of a wider process of adaptation of central carbon metabolism to the high sugar environment. Coupling comparative genomics with biochemical and genetic approaches, we show that the alcoholic fermentation pathway was profoundly remodeled in the W/S clade, as genes required for alcoholic fermentation were lost and subsequently re-acquired from bacteria through horizontal gene transfer. We further show that the reinstated fermentative pathway is functional and that an enzyme required for sucrose assimilation is also of bacterial origin, reinforcing the adaptive nature of the genetic novelties identified in the W/S clade. This work shows how even central carbon metabolism can be remodeled by a surge of HGT events.

genomics↗