Complex Ancestries of Lager-Brewing Hybrids Were Shaped by Standing Variation in the Wild Yeast Saccharomyces eubayanus

AbstractA goal of speciation genetics is to understand how the genetic components underlying interspecific reproductive barriers originate within species. Unilateral incompatibility (UI) is a postmating prezygotic barrier in which pollen rejection in the female reproductive tract (style) occurs in only one direction of an interspecific cross. Natural variation in the strength of UI has been observed among populations within species in the wild tomato clade. In some cases, molecular loci underlying self-incompatibility (SI) are associated with this variation in UI, but the mechanistic connection between these intra- and inter-specific pollen rejection behaviors is poorly understood in most instances. We generated an F2 population between SI and SC genotypes of a single species, Solanum pennellii, to examine the genetic basis of intraspecific variation in the strength of UI against other species, and to determine whether loci underlying SI are genetically associated with this variation. We found that F2 individuals vary in the rate at which UI rejection occurs. One large effect QTL detected for this trait co-localized with the SI-determining S-locus. Moreover, individuals that expressed S-RNase—the S-locus protein involved in SI pollen rejection—in their styles had much more rapid UI responses compared to those without S-RNase protein. Our analysis shows that intraspecific variation at mate choice loci—in this case at loci that prevent self-fertilization—can contribute to variation in the strength of interspecific isolation, including postmating prezygotic barriers. Understanding the nature of such standing variation can provide insight into the accumulation of these barriers between diverging lineages.

Download Full-text

On the prospect of identifying adaptive loci in recently bottlenecked populations

10.1101/009456 ◽

2014 ◽

Author(s):

Yu-Ping Poh ◽

Vera S Domingues ◽

Hopi Hoekstra ◽

Jeffrey Jensen

Keyword(s):

Frequency Spectrum ◽

Population Genetic ◽

Null Model ◽

Large Parameter ◽

Independent Evidence ◽

Standing Variation ◽

In The Wild ◽

Site Frequency Spectrum ◽

Genomic Regions ◽

Large Parameter Space

Identifying adaptively important loci in recently bottlenecked populations?be it natural selection acting on a population following the colonization of novel habitats in the wild, or artificial selection during the domestication of a breed?remains a major challenge. Here we report the results of a simulation study examining the performance of available population-genetic tools for identifying genomic regions under selection. To illustrate our findings, we examined the interplay between selection and demography in two species of Peromyscus mice, for which we have independent evidence of selection acting on phenotype as well as functional evidence identifying the underlying genotype. With this unusual information, we tested whether population-genetic-based approaches could have been utilized to identify the adaptive locus. Contrary to published claims, we conclude that the use of the background site frequency spectrum as a null model is largely ineffective in bottlenecked populations. Results are quantified both for site frequency spectrum and linkage disequilibrium-based predictions, and are found to hold true across a large parameter space that encompasses many species and populations currently under study. These results suggest that the genomic footprint left by selection on both new and standing variation in strongly bottlenecked populations will be difficult, if not impossible, to find using current approaches.

Download Full-text

Mating in wild yeast: variable interest in sex after spore germination

10.1101/360289 ◽

2018 ◽

Cited By ~ 1

Author(s):

Allison W. McClure ◽

Katherine C. Jacobs ◽

Trevin R. Zyla ◽

Daniel J. Lew

Keyword(s):

Saccharomyces Cerevisiae ◽

Cell Cycle ◽

Information Processing ◽

Spore Germination ◽

Pheromone Production ◽

Wild Yeast ◽

Yeast Strains ◽

Processing Strategies ◽

In The Wild ◽

Cis And Trans

SummaryStudies of lab strains of Saccharomyces cerevisiae have uncovered signaling pathways involved in mating, including information processing strategies to optimize decisions to mate or to bud. However, lab strains are heterothallic (unable to self-mate) while wild yeast are homothallic. And while mating of lab strains is studied using cycling haploid cells, mating of wild yeast is thought to involve germinating spores. Thus, it was unclear whether lab strategies would be appropriate in the wild. Here, we have investigated the behaviors of several yeast strains derived from wild isolates. Following germination, these strains displayed large differences in their propensity to mate or to enter the cell cycle. The variable interest in sex following germination was correlated with differences in pheromone production, which were due to both cis- and trans-acting factors. Our findings suggest that yeast spores germinating in the wild may often enter the cell cycle and form microcolonies prior to engaging in mating.

Download Full-text

Estimating the fitness effects of new mutations in the wild yeast Saccharomyces paradoxus

Genome Biology and Evolution ◽

10.1093/gbe/evv112 ◽

2015 ◽

Cited By ~ 6

Author(s):

V. Koufopanou ◽

S. Lomas ◽

I. J. Tsai ◽

A. Burt

Keyword(s):

Saccharomyces Paradoxus ◽

Fitness Effects ◽

Wild Yeast ◽

In The Wild ◽

New Mutations

Download Full-text

Unique Brewing-Relevant Properties of a Strain of Saccharomyces jurei Isolated From Ash (Fraxinus excelsior)

Frontiers in Microbiology ◽

10.3389/fmicb.2021.645271 ◽

2021 ◽

Vol 12 ◽

Author(s):

Mathias Hutzler ◽

Maximilian Michel ◽

Oliver Kunz ◽

Tiina Kuusisto ◽

Frederico Magalhães ◽

...

Keyword(s):

Fraxinus Excelsior ◽

Lag Phase ◽

Tropical Fruit ◽

Ethyl Hexanoate ◽

Wild Yeast ◽

Saccharomyces Pastorianus ◽

Application Potential ◽

Maltose Utilization ◽

Saccharomyces Eubayanus ◽

High Level

The successful application of Saccharomyces eubayanus and Saccharomyces paradoxus in brewery fermentations has highlighted the potential of wild Saccharomyes yeasts for brewing, and prompted investigation into the application potential of other members of the genus. Here, we evaluate, for the first time, the brewing potential of Saccharomyces jurei. The newly isolated strain from an ash tree (Fraxinus excelsior) in Upper Bavaria, Germany, close to the river Isar, was used to ferment a 12°P wort at 15°C. Performance was compared directly with that of a reference lager strain (TUM 34/70) and the S. eubayanus type strain. Both wild yeast rapidly depleted simple sugars and thereafter exhibited a lag phase before maltose utilization. This phase lasted for 4 and 10 days for S. eubayanus and S. jurei, respectively. S. eubayanus utilized fully the available maltose but, consistent with previous reports, did not use maltotriose. S. jurei, in contrast, utilized approximately 50% of the maltotriose available, making this the first report of maltotriose utilization in a wild Saccharomyces species. Maltotriose use was directly related to alcohol yield with 5.5, 4.9, and 4.5% ABV produced by Saccharomyces pastorianus, S. jurei, and S. eubayanus. Beers also differed with respect to aroma volatiles, with a high level (0.4 mg/L) of the apple/aniseed aroma ethyl hexanoate in S. jurei beers, while S. eubayanus beers had a high level of phenylethanol (100 mg/L). A trained panel rated all beers as being of high quality, but noted clear differences. A phenolic spice/clove note was prominent in S. jurei beer. This was less pronounced in the S. eubayanus beers, despite analytical levels of 4-vinylguaiacol being similar. Tropical fruit notes were pronounced in S. jurei beers, possibly resulting from the high level of ethyl hexanoate. Herein, we present results from the first intentional application of S. jurei as a yeast for beer fermentation (at the time of submission) and compare its fermentation performance to other species of the genus. Results indicate considerable potential for S. jurei application in brewing, with clear advantages compared to other wild Saccharomyces species.

Download Full-text

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

10.1101/709535 ◽

2019 ◽

Cited By ~ 1

Author(s):

Quinn K. Langdon ◽

David Peris ◽

Juan I. Eizaguirre ◽

Dana A. Opulente ◽

Kelly V. Buh ◽

...

Keyword(s):

Genetic Diversity ◽

South America ◽

Phenotypic Diversity ◽

Isolation By Distance ◽

Genomic Diversity ◽

Whole Genome Sequence ◽

Phenotypic Data ◽

In The Wild ◽

Saccharomyces Eubayanus ◽

Brewing Yeasts

AbstractS. 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.

Download Full-text

Further support for aneuploidy tolerance in wild yeast and effects of dosage compensation on gene copy-number evolution

eLife ◽

10.7554/elife.14409 ◽

2016 ◽

Vol 5 ◽

Cited By ~ 15

Author(s):

Audrey P Gasch ◽

James Hose ◽

Michael A Newton ◽

Maria Sardi ◽

Mun Yong ◽

...

Keyword(s):

Dosage Compensation ◽

Copy Number ◽

Gene Copy Number ◽

Gene Copy ◽

Prior Work ◽

Gene Group ◽

Wild Yeast ◽

A Genome ◽

In The Wild ◽

Wild Strains

In our prior work by Hose et al., we performed a genome-sequencing survey and reported that aneuploidy was frequently observed in wild strains of S. cerevisiae. We also profiled transcriptome abundance in naturally aneuploid isolates compared to isogenic euploid controls and found that 10–30% of amplified genes, depending on the strain and affected chromosome, show lower-than-expected expression compared to gene copy number. In Hose et al., we argued that this gene group is enriched for genes subject to one or more modes of dosage compensation, where mRNA abundance is decreased in response to higher dosage of that gene. A recent manuscript by Torres et al. refutes our prior work. Here, we provide a response to Torres et al., along with additional analysis and controls to support our original conclusions. We maintain that aneuploidy is well tolerated in the wild strains of S. cerevisiae that we studied and that the group of genes enriched for those subject to dosage compensation show unique evolutionary signatures.

Download Full-text

Mating in wild yeast: delayed interest in sex after spore germination

Molecular Biology of the Cell ◽

10.1091/mbc.e18-08-0528 ◽

2018 ◽

Vol 29 (26) ◽

pp. 3119-3127 ◽

Cited By ~ 6

Author(s):

Allison W. McClure ◽

Katherine C. Jacobs ◽

Trevin R. Zyla ◽

Daniel J. Lew

Keyword(s):

Saccharomyces Cerevisiae ◽

Cell Cycle ◽

Information Processing ◽

Spore Germination ◽

Pheromone Production ◽

Wild Yeast ◽

Yeast Strains ◽

Processing Strategies ◽

In The Wild ◽

Cis And Trans

Studies of laboratory strains of Saccharomyces cerevisiae have uncovered signaling pathways involved in mating, including information-processing strategies to optimize decisions to mate or to bud. However, lab strains are heterothallic (unable to self-mate), while wild yeast are homothallic. And while mating of lab strains is studied using cycling haploid cells, mating of wild yeast is thought to involve germinating spores. Thus, it was unclear whether lab strategies would be appropriate in the wild. Here, we have investigated the behavior of several yeast strains derived from wild isolates. Following germination, these strains displayed large differences in their propensity to mate or to enter the cell cycle. The variable interest in sex following germination was correlated with differences in pheromone production, which were due to both cis- and trans-acting factors. Our findings suggest that yeast spores germinating in the wild may often enter the cell cycle and form microcolonies before engaging in mating.

Download Full-text

Unique brewing-relevant properties of a strain of Saccharomyces jurei isolated from ash (Fraxinus excelsior)

10.1101/2021.01.11.426216 ◽

2021 ◽

Author(s):

Mathias Hutzler ◽

Maximilian Michel ◽

Oliver Kunz ◽

Tiina Kuusisto ◽

Frederico Magalhães ◽

...

Keyword(s):

Fraxinus Excelsior ◽

Lag Phase ◽

Tropical Fruit ◽

Ethyl Hexanoate ◽

Wild Yeast ◽

Trained Panel ◽

Application Potential ◽

Maltose Utilization ◽

Saccharomyces Eubayanus ◽

High Level

AbstractThe successful application of Saccharomyces eubayanus and Saccharomyces paradoxus in brewery fermentations has highlighted the potential of wild yeast for brewing, and prompted investigation into the application potential of other members of the genus. Here, we evaluate, for the first time, the brewing potential of Saccharomyces jurei. The newly isolated strain from an ash tree (Fraxinus excelsior) in Upper Bavaria, Germany, close to the river Isar, was used to ferment a 12°P wort at 15°C. Performance was compared directly with that of a reference lager strain (TUM 34/70) and the S. eubayanus type strain. Both wild yeast rapidly depleted simple sugars and thereafter exhibited a lag phase before maltose utilization. This phase lasted for 4 and 10 days for S. eubayanus and S. jurei, respectively. S. eubayanus utilized fully the available maltose but, consistent with previous reports, did not use maltotriose. S. jurei, in contrast, utilized approx. 50% of the maltotriose available, making this the first report of maltotriose utilization in a wild Saccharomyces species. Maltotriose use was directly related to alcohol yield with 5.5, 4.9, and 4.5 % ABV produced by S. pastorianus, S. jurei and S. eubayanus. Beers also differed with respect to aroma volatiles, with a high level (0.4 mg/L) of the apple/aniseed aroma ethyl hexanoate in S. jurei beers, while S. eubayanus beers had a high level of phenylethanol (100 mg/L). A trained panel rated all beers as being of high quality, but noted clear differences. A phenolic spice/clove note was prominent in S. jurei beer. This was less pronounced in the S. eubayanus beers, despite analytical levels of 4-vinylguaiacol being similar. Tropical fruit notes were pronounced in S. jurei beers, possibly resulting from the high level of ethyl hexanoate. Herein, we present the successful results of the first intentional application of S. jurei as a yeast for beer fermentation known to us and compare its fermentation performance to other species of the genus. Results indicate considerable potential for S. jurei application in brewing, with clear advantages compared to other wild Saccharomyces species.

Download Full-text

Freeze-substituted fungal cells of Nectria haematococca: A comparison of the macroconidial walls of the adhesion-competent wild type with an adhesion-reduced mutant

Proceedings, annual meeting, Electron Microscopy Society of America ◽

10.1017/s0424820100160996 ◽

1990 ◽

Vol 48 (3) ◽

pp. 688-689

Author(s):

Thecan Caesar-Ton That ◽

Lynn Epstein

Keyword(s):

Freeze Substitution ◽

Uranyl Acetate ◽

Wild Type ◽

Nectria Haematococca ◽

Fruit Extract ◽

Dialysis Tubing ◽

Tube Emergence ◽

Contrast Microscopy ◽

In The Wild ◽

Freeze Damage

Nectria haematococca mating population I (anamorph, Fusarium solani) macroconidia attach to its host (squash) and non-host surfaces prior to germ tube emergence. The macroconidia become adhesive after a brief period of protein synthesis. Recently, Hickman et al. (1989) isolated N. haematococca adhesion-reduced mutants. Using freeze substitution, we compared the development of the macroconidial wall in the wild type in comparison to one of the mutants, LEI.Macroconidia were harvested at 1C, washed by centrifugation, resuspended in a dilute zucchini fruit extract and incubated from 0 - 5 h. During the incubation period, wild type macroconidia attached to uncoated dialysis tubing. Mutant macroconidia did not attach and were collected on poly-L-lysine coated dialysis tubing just prior to freezing. Conidia on the tubing were frozen in liquid propane at 191 - 193C, substituted in acetone with 2% OsO4 and 0.05% uranyl acetate, washed with acetone, and flat-embedded in Epon-Araldite. Using phase contrast microscopy at 1000X, cells without freeze damage were selected, remounted, sectioned and post-stained sequentially with 1% Ba(MnO4)2 2% uranyl acetate and Reynold’s lead citrate. At least 30 cells/treatment were examined.

Download Full-text