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HO diversity across the 1,011 genomes. The circle diameter is proportional to the number of strains. The red circle comprises 93 strains and represents the inactive form of HO present in most laboratory strains. The green circle comprises 307 strains carrying the active HO sequence. The blue circles contain strains for which HO functionality is unknown. However, all truncated forms of HO are likely heterothallic
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The budding yeast, Saccharomyces cerevisiae, has served as a model for nearly a century to understand the principles of the eukaryotic life cycle. The canonical life cycle of S. cerevisiae comprises a regular alternation between haploid and diploid phases. Haploid gametes generated by sporulation are expected to quickly restore the diploid phase ma...
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Anther culture is an important biotechnological tool for quick recovery of fixed breeding lines with unique gene combinations that might otherwise disappear in the course of an extended series of segregating generations in conventional breeding methods in rice. The haploid microspores in culture or the resultant haploid plants are converted to doub...
Citations
... Thus during mating by sibling spores a predetermined polarity program initially overrides pheromone signaling. Notably, many natural isolates of S. cerevisiae are unable to switch mating types (Fischer et al., 2021) and for many isolates competent to switch, mating between sibling spores is the default event upon germination (McClure et al., 2018). Hence whereas the mating process in S. cerevisiae has been almost exclusively studied using vegetative haploid cells, mating between sibling spores is much more common in nature and likely drove evolution of the underlying polarity pathways, yet it remains largely unexplored. ...
The yeast Saccharomyces cerevisiae buds at sites pre-determined by cortical landmarks deposited during prior budding. During mating between haploid cells in the lab, external pheromone cues override the cortical landmarks to drive polarization and cell fusion. By contrast, in haploid gametes (called spores) produced by meiosis, a pre-determined polarity site drives initial polarized morphogenesis independent of mating partner location. Spore membranes are made de novo so existing cortical landmarks were unknown, as were the mechanisms by which the spore polarity site is made and how it works. We find that the landmark canonically required for distal budding, Bud8, stably marks the spore polarity site along with Bud5, a GEF for the GTPase Rsr1 that canonically links cortical landmarks to the conserved Cdc42 polarity machinery. Cdc42 and other GTPase regulators arrive at the site during its biogenesis, after spore membrane closure but apparently at the site where membrane synthesis began, and then these factors leave, pointing to the presence of discrete phases of maturation. Filamentous actin may be required for initial establishment of the site, but thereafter Bud8 accumulates independent of actin filaments. These results suggest a distinct polarization mechanism that may provide insights into gamete polarization in other organisms.
SIGNIFICANCE STATEMENT
Dormant budding yeast spores possess a single, stable cortical site that marks the location where polarized growth occurs upon dormancy exit. It was not known how the site forms or which molecules comprise it.
Using fluorescently tagged proteins in living cells undergoing sporulation, the authors found proteins canonically involved in polarization of non-spore cells arriving at the polarity site in a choreographed manner and required for site function.
These findings point to a distinct polarity mechanism from non-spore cells and raise new questions about polarity protein interactions with membranes that may be applicable to gametogenesis in other organisms.
... Mating occurs only between haploid cells of compatible mating types, a with ⍺. Most natural S. cerevisiae isolates are diploid (Peter et al., 2018), and in most cases a haploid spore of either haploid mating type is able to switch mating types (Fischer et al., 2021). Subsequent mating with a daughter cell of opposite mating type provides an efficient route for an isolated spore to return to diploidy. ...
... In strains capable of mating-type switching ("homothallic"), HO encodes an endonuclease that makes a single cut in the genome to initiate recombination-mediated exchange of alleles at the MAT locus (Strathern et al., 1982;Kostriken et al., 3 1983). Apparent loss-of-function ho alleles have been found frequently in other natural isolates (Katz Ezov et al., 2010;Fischer et al., 2021) and in strains used in wine-making (Mortimer, 2000). Since HO is not expressed in diploid cells (Jensen et al., 1983), any strain that is incapable of, or rarely undergoes, meiosis and/or sporulation would rarely or never express HO. ...
... Others previously noted the diversity of alleles of HO among the genome sequences of 1,011 S. cerevisiae isolates and the fact that many are predicted to be non-functional for mating-type switching (Peter et al., 2018;Fischer et al., 2021). We examined the geographical origin of those strains with respect to the HO allele of each. ...
Features of the natural life cycle of the budding yeast Saccharomyces cerevisiae were crucial to its domestication as a laboratory experimental model, especially the ability to maintain stable haploid clones and cross them at will to combine alleles via meiosis. Stable haploidy results from mutations in HO, which encodes an endonuclease required for haploid-specific mating-type switching. Previous studies found an unexpected diversity of HO alleles among natural isolates within a small geographic area. We developed a hands-on field and laboratory activity for middle school students in Denver, Colorado, USA to isolate wild yeast from oak bark, identify species via DNA sequencing, and sequence HO from S. cerevisiae isolates. We find limited HO diversity in North American oak isolates, pointing to efficient, continuous dispersal across the continent. By contrast, we isolated the dairy yeast, Kluyveromyces lactis, from a tree <10 m away and found that it represents a new population distinct from an oak population in an adjacent state, pointing to high genetic diversity. The outreach activity partnered middle school, high school, and university students in making scientific discoveries and can be adapted to other locations and natural yeast habitats. Indeed, a pilot sampling activity in southeast Texas yielded S. cerevisiae oak isolates with a new allele of HO and, from a nearby prickly pear cactus, a heat-tolerant isolate of Saccharomyces paradoxus.
... Yeast species in the Sacc harom ycotina can pr opa gate both thr ough mainl y mitosis and often meiosis, gener ating differ ent cell types (Herskowitz 1988, Fischer et al. 2021. We refer to this type of cellular mor phological v ariation as de v elopmental v aria-tion. ...
The ∼1 200 known species in subphylum Saccharomycotina are a highly diverse clade of unicellular fungi. During its lifecycle, a typical yeast exhibits multiple cell types with various morphologies; these morphologies vary across Saccharomycotina species. Here, we synthesize the evolutionary dimensions of variation in cellular morphology of yeasts across the subphylum, focusing on variation in cell shape, cell size, type of budding, and filament production. Examination of 332 representative species across the subphylum revealed that the most common budding cell shapes are ovoid, spherical, and ellipsoidal, and that their average length and width is 5.6 μm and 3.6 μm, respectively. 58.4% of yeast species examined can produce filamentous cells, and 87.3% of species reproduce asexually by multilateral budding, which does not require utilization of cell polarity for mitosis. Interestingly, ∼1.8% of species examined have not been observed to produce budding cells, but rather only produce filaments of septate hyphae and/or pseudohyphae. 76.9% of yeast species examined have sexual cycle descriptions, with most producing one to four ascospores that are most commonly hat-shaped (37.4%). Systematic description of yeast cellular morphological diversity and reconstruction of its evolution promises to enrich our understanding of the evolutionary cell biology of this major fungal lineage.
... Budding is a phenomenon studied intensively in yeasts, which are unicellular ascomycete or basidiomycete fungi in which growth occurs mainly from budding (Kurtzman, 2011). The most studied species that reproduces by budding is S. cerevisiae (Russell & Nurse, 1986) and molecular analysis of genes involved in the different stages of the budding process have been carried out (Fischer et al., 2021;Hartwell, 1971;Hartwell et al., 1974;Nurse, 1975;Perrino et al., 2021;Yu et al., 2006). The budding process occurs in asexual reproduction in this species. ...
Common bean anthracnose is one of the main fungal diseases that affect the crop. The
disease is caused by the fungus Colletotrichum lindemuthianum, anamorph, which has
wide variability as well as its teleomorph. Sexual reproduction is the main mechanism of
increasing genetic variability in fungi, therefore the study of morphological characteristics and their sexual structures are important. Homothallic strains of the pathogen have
shown the production of new ascospores via mitosis after the sexual cycle. As a result of
each mitotic division there are two ascospores with amygdaliform and/or allantoid morphology. In this work the characterization of this phenomenon is described as budding.
This is the first report on the occurrence of ascospore budding in the genus Colletotrichum.
The homothallic strain UFLA84-1 was used. Analyses of light microscopy, fluorescence
and high-resolution scanning electron microscopy were used for the description of the
budding process. Cytological analyses were carried out to estimate the dimension of
ascospores, budding percentage and colony type. The budding cycle is described in six
stages, and the complete process develops after the release of all ascospores from an
ascus. The ascospores from this process can present both morphologies and bud growth
can be apical or lateral. Sexual reproduction is a mechanism of genetic recombination
and the budding process increases the number of ascospores generated by meiosis and
may therefore represent an adaptive advantage of the pathogen.
... For example, Raynes et al. [29][30][31] found that the nature of selection on mutationrate modifiers in yeast depends on the size and structure of populations and is not frequency-dependent. Continued investigations into the reproductive behavior and population structure of yeast in the wild [32][33][34] will therefore be important for predicting mutation-rate evolution. ...
... Yeast strains and species can be hybridized in the lab as another way to study TE activity [87][88][89][90][91][92], as well as the mutation rate and spectrum generally [75, 93,94], revealing mutation-rate variation among genetic backgrounds. Yeast and their hybrids have also been used to identify genome-wide patterns of loss-of-heterozygosity mutations [33,44,75,[93][94][95], an important form of genome evolution in many populations. This is only a brief overview, but yeast has clearly become a critical model for studying the amazing diversity of mutation mechanisms. ...
Mutation is the origin of all genetic variation, good and bad. The mutation process can evolve in response to mutations, positive or negative selection, and genetic drift, but how these forces contribute to mutation-rate variation is an unsolved problem at the heart of genetics research. Mutations can be challenging to measure, but genome sequencing and other tools have allowed for the collection of larger and more detailed datasets, particularly in the yeast-model system. We review key hypotheses for the evolution of mutation rates and describe recent advances in understanding variation in mutational properties within and among yeast species. The multidimensional spectrum of mutations is increasingly recognized as holding valuable clues about how this important process evolves.
... In a diploid life cycle, organisms switch between a short haploid phase (usually restricted to unicellular gametes) and the prevailing diploid phase, only which is capable of mitotic growth. Such a life cycle occurs among diatoms, raphidophytes or budding yeasts; however, it is best known from animals, including humans [3][4][5][6]. A haploid life cycle is characterized by mitosis restricted to the haploid phase, which also lasts for most of the organism's lifespan, as the only diploid stage is a unicellular zygote. ...
Across eukaryotic organisms there is a great diversity of life cycles. This particularly applies to unicellular eukaryotes (protists), where the life cycles are still largely unexplored, although this knowledge is key to understanding their biology.
To detect the often inconspicuous transitions among life cycle stages, we focused at shifts in ploidy levels within strains of unicellular chrysophyte alga. Representatives of three genera (Chrysosphaerella, Ochromonas, and Synura) were analysed for nuclear DNA contents using a propidium iodide flow cytometry. Selected strains exhibiting ploidy level variation were also surveyed for DNA base composition (GC content) and cell size. Additionally, we tracked ploidy level changes in seven strains under long-term cultivation.
An alternation of two ploidy levels was revealed in the life cycle of chrysophytes with both life cycle stages capable of mitotic growth and long-term survival in cultivation. With the exception of a small increase in cell size with higher ploidy, both life cycle stages shared the same phenotype and also had highly similar genomic GC content. Further, we detected three ploidy levels in two Synura species (S. glabra, S. heteropora), where the highest ploidy (putatively 4x) most likely resulted from a polyploidization event.
Consequently, chrysophytes have a haploid-diploid life cycle with isomorphic life cycle stages. As far as we know, this is the first report of such life cycle strategy in unicellular algae. Life cycle stages and life stage transitions seem to be synchronized among all cells coexisting within a culture, possibly due to chemical signals. Particular life stages may be more successful under certain environmental conditions, for our studied strains the diploid stage prevailed in cultivation.
... This notion has not been abandoned after the early reports of its possible inadequacy (Kelly et al. 2012;Magwene 2014). Only after the completion of large and comprehensive surveys of strains derived from different geographical and ecological locations, an abundance of heterozygosity, and hence the potentially important role of mitotic LOH have been finally recognized (Peter et al. 2018;Fischer et al. 2021). Considering other and very different populations, those of human cancer cells, the meaning of LOH as a critical factor in the progression of tumors has been early understood and never questioned (Knudson 1971). ...
Former studies have established that loss of heterozygosity (LOH) can be a key driver of sequence evolution in unicellular eukaryotes and tissues of metazoans. However, little is known about whether the distribution of LOH events is largely random or forms discernible patterns across genomes. To initiate our experiments, we introduced selectable markers to both arms of all chromosomes of the budding yeast. Subsequent extensive assays, repeated over several genetic backgrounds and environments, provided a wealth of information on the genetic and environmental determinants of LOH. Three findings stand out. First, the number of LOH events per unit time was more than 25 times higher for growing than starving cells. Second, LOH was most frequent when regions of homology around a recombination site were identical, about a half-% sequence divergence was sufficient to reduce its incidence. Finally, the density of LOH events was highly dependent on the genome’s physical architecture. It was several-fold higher on short chromosomal arms than on long ones. Comparably large differences were seen within a single arm where regions close to a centromere were visibly less affected than regions close, though usually not strictly adjacent, to a telomere. We suggest that the observed uneven distribution of LOH events could have been caused not only by an uneven density of initial DNA damages. Location-depended differences in the mode of DNA repair, or its effect on fitness, were likely to operate as well.
... As S. cerevisiae practices mating type switching (secondary homothallism), the change of mating type gives rise to compatible cells within the same colony (referred to as haplo-selfing) (Wilson et al. 2015). Although this description implies that in nature S. cerevisiae cells would almost always exist as homozygous diploids, recent analysis of wild S. cerevisiae populations suggests that natural variation and environmental conditions may have an impact with frequencies of heterozygosity and outcrossing higher than hitherto appreciated (Fisher, Liti and Llorente 2021). The Saccharomyces preference for diplontic growth is an evolved trait whereas most other yeasts in the Saccharomycetaceae ordinarily grown as haplonts (Gerstein et al. 2006;Sherwood et al. 2014). ...
Evolution has provided a vast diversity of yeasts that play fundamental roles in nature and society. This diversity is not limited to genotypically homogenous species with natural interspecies hybrids and allodiploids that blur species boundaries frequently isolated. Thus, life-cycle and the nature of breeding systems have profound effects on genome variation, shaping heterozygosity, genotype diversity and ploidy level. The apparent enrichment of hybrids in industry-related environments suggests that hybridisation provides an adaptive route against stressors and creates interest in developing new hybrids for biotechnological uses. For example, in the Saccharomyces genus where regulatory circuits controlling cell-identity, mating competence and meiosis commitment have been extensively studied, this body of knowledge is being used to combine interesting traits into synthetic F1 hybrids, to by-pass F1 hybrid sterility, and to dissect complex phenotypes by bulk segregant analysis. Although there is less known about these aspects in other industrially-promising yeasts, advances in whole genome sequencing and analysis are changing this and new insights are being gained, especially in the food-associated genera Zygosaccharomyces and Kluyveromyces. We discuss this new knowledge and highlight how deciphering cell identity circuits in these lineages will contribute significantly to identify the genetic determinants underpinning complex phenotypes and open new avenues for breeding programmes.
... This wealth of whole-genome sequencing (WGS) data, most of which has been generated using short-read technologies, has provided insights critical to numerous aspects of S. cerevisiae biology including genome evolution, population diversity, and genotype-phenotype relationships 1,4-6 . Collectively, these survey-level genome investigations have demonstrated that this model organism has a complex and fascinating evolutionary history 7,8 , and have highlighted the tremendous genomic diversity that can exist within a single species 3,9,10 . Whereas short-read WGS data are ideal for assessing genomic heterozygosity and allelic variation between individuals, long-read sequencing approaches can reveal the structural architecture of the genome 11 . ...
The budding yeast Saccharomyces cerevisiae has been extensively characterized for many decades and is a critical resource for the study of numerous facets of eukaryotic biology. Recently, whole genome sequence analysis of over 1000 natural isolates of S. cerevisiae has provided critical insights into the evolutionary landscape of this species by revealing a population structure comprised of numerous genomically diverse lineages. These survey-level analyses have been largely devoid of structural genomic information, mainly because short read sequencing is not suitable for detailed characterization of genomic architecture. Consequently, we still lack a complete perspective of the genomic variation the exists within the species. Single molecule long read sequencing technologies, such as Oxford Nanopore and PacBio, provide sequencing-based approaches with which to rigorously define the structure of a genome, and have empowered yeast geneticists to explore this poorly described realm of eukaryotic genomics. Here, we present the comprehensive genomic structural analysis of a wild diploid isolate of S. cerevisiae, YJM311. We used long read sequence analysis to construct a haplotype-phased, telomere-to-telomere length assembly of the YJM311 genome and characterized the structural variations (SVs) therein. We discovered that the genome of YJM311 contains significant intragenomic structural variation, some of which imparts notable consequences to the genomic stability and developmental biology of the strain. Collectively, we outline a new methodology for creating accurate haplotype-phased genome assemblies and highlight how such genomic analyses can define the structural architectures of S. cerevisiae isolates. It is our hope that continued structural characterization of S. cerevisiae genomes, such as we have reported here for YJM311, will comprehensively advance our understanding of eukaryotic genome structure-function relationships, structural genomic diversity, and evolution.
... This provides an obvious direct route to polyploidization that can restore the fertility of sterile hybrids by whole-genome duplication 33,34 . RTG-driven polyploidization would produce a similar outcome to what is observed in plants, where polyploidization can result from the mating of endoreplicated gametes with an unreduced genome content 35 , and may help explain the abundance of yeast polyploids in nature 36 . LOH regions might be selected by adaptation under specific selective regimes 37-40 but may also be constrained by incompatibility between allele pairs located in different subgenomes 41 . ...
Hybrids between diverged lineages contain novel genetic combinations but an impaired meiosis often makes them evolutionary dead ends. Here, we explore to what extent an aborted meiosis followed by a return-to-growth (RTG) promotes recombination across a panel of 20 Saccharomyces cerevisiae and S. paradoxus diploid hybrids with different genomic structures and levels of sterility. Genome analyses of 275 clones reveal that RTG promotes recombination and generates extensive regions of loss-of-heterozygosity in sterile hybrids with either a defective meiosis or a heavily rearranged karyotype, whereas RTG recombination is reduced by high sequence divergence between parental subgenomes. The RTG recombination preferentially arises in regions with low local heterozygosity and near meiotic recombination hotspots. The loss-of-heterozygosity has a profound impact on sexual and asexual fitness, and enables genetic mapping of phenotypic differences in sterile lineages where linkage analysis would fail. We propose that RTG gives sterile yeast hybrids access to a natural route for genome recombination and adaptation.