Phenotypic Diagnosis of Lineage and Differentiation During Sake Yeast Breeding

Sake yeast was developed exclusively in Japan. Its diversification during breeding remains largely uncharacterized. To evaluate the breeding processes of the sake lineage, we thoroughly investigated the phenotypes and differentiation of 27 sake yeast strains using high-dimensional, single-cell, morphological phenotyping. Although the genetic diversity of the sake yeast lineage is relatively low, its morphological diversity has expanded substantially compared to that of the Saccharomyces cerevisiae species as a whole. Evaluation of the different types of breeding processes showed that the generation of hybrids (crossbreeding) has more profound effects on cell morphology than the isolation of mutants (mutation breeding). Analysis of phenotypic robustness revealed that some sake yeast strains are more morphologically heterogeneous, possibly due to impairment of cellular network hubs. This study provides a new perspective for studying yeast breeding genetics and micro-organism breeding strategies.

[1]  Kevin L. Schneider,et al.  Inbreeding drives maize centromere evolution , 2016, Proceedings of the National Academy of Sciences.

[2]  Francis Galton,et al.  Natural inheritance. By Francis Galton. , 1889 .

[3]  Peter Langridge,et al.  Hybrid breeding in wheat: technologies to improve hybrid wheat seed production. , 2013, Journal of experimental botany.

[4]  Y. Hata,et al.  Breeding of a Sake Yeast with Improved Ethyl Caproate Productivity , 1991 .

[5]  K. Ouchi,et al.  Non-foaming Mutants of Sake Yeast : Their Physico-Chemical Characteristics , 1973 .

[6]  E. Fukusaki,et al.  Gas chromatography/mass spectrometry based component profiling and quality prediction for Japanese sake. , 2014, Journal of bioscience and bioengineering.

[7]  H. Shimizu,et al.  Saccharomyces cerevisiae and DNA microarray analyses: what did we learn from it for a better understanding and exploitation of yeast biotechnology? , 2010, Applied Microbiology and Biotechnology.

[8]  Sasha F. Levy,et al.  Network Hubs Buffer Environmental Variation in Saccharomyces cerevisiae , 2008, PLoS biology.

[9]  F. Klis,et al.  Identification of fungal cell wall mutants using susceptibility assays based on Calcofluor white and Congo red , 2006, Nature Protocols.

[10]  I. Kozone,et al.  Analysis of the biological activity of a novel 24-membered macrolide JBIR-19 in Saccharomyces cerevisiae by the morphological imaging program CalMorph. , 2012, FEMS yeast research.

[11]  Miguel C. Teixeira,et al.  Genome-Wide Identification of Saccharomyces cerevisiae Genes Required for Maximal Tolerance to Ethanol , 2009, Applied and Environmental Microbiology.

[12]  K. Abe,et al.  Reduced brain activity in female patients with non-alcoholic fatty liver disease as measured by near-infrared spectroscopy , 2017, PloS one.

[13]  B. Roberts,et al.  S. cerevisiae genes required for cell cycle arrest in response to loss of microtubule function , 1991, Cell.

[14]  K. Ito,et al.  Tolerance mechanism of the ethanol-tolerant mutant of sake yeast. , 2000, Journal of bioscience and bioengineering.

[15]  S. Elledge,et al.  The SAD1/RAD53 protein kinase controls multiple checkpoints and DNA damage-induced transcription in yeast. , 1994, Genes & development.

[16]  Justin C. Fay,et al.  Genomic Sequence Diversity and Population Structure of Saccharomyces cerevisiae Assessed by RAD-seq , 2013, G3: Genes, Genomes, Genetics.

[17]  K. Doi,et al.  Genetic variation in rice. , 2008, Current opinion in plant biology.

[18]  L. Hartwell,et al.  Mitotic checkpoint genes in budding yeast and the dependence of mitosis on DNA replication and repair. , 1994, Genes & development.

[19]  K. Ouchi,et al.  Non-foaming Mutants of Sake Yeasts Selection by Cell Agglutination Method and by Froth Flotation Method , 1971 .

[20]  D. Greig,et al.  Heterosis in hybrids within and between yeast species , 2017, Journal of evolutionary biology.

[21]  Elena Deza,et al.  Encyclopedia of Distances , 2014 .

[22]  Y. Ohya,et al.  Ethanol fermentation driven by elevated expression of the G1 cyclin gene CLN3 in sake yeast. , 2011, Journal of bioscience and bioengineering.

[23]  D. Axelrod,et al.  Inheritance and regression toward the mean in heterogeneous cell populations , 1991, Cell proliferation.

[24]  Hidetoshi Shimodaira,et al.  Pvclust: an R package for assessing the uncertainty in hierarchical clustering , 2006, Bioinform..

[25]  Robert P. Davey,et al.  Population genomics of domestic and wild yeasts , 2008, Nature.

[26]  M. Groenen,et al.  Whole-genome sequence analysis reveals differences in population management and selection of European low-input pig breeds , 2014, BMC Genomics.

[27]  秋山 裕一,et al.  Saké : the essence of 2000 years of Japanese wisdom gained from brewing alcoholic beverages from rice , 2010 .

[28]  Y. Ohya,et al.  Single-cell phenomics in budding yeast , 2015, Molecular biology of the cell.

[29]  Leonid Kruglyak,et al.  Comprehensive polymorphism survey elucidates population structure of Saccharomyces cerevisiae , 2009, Nature.

[30]  J. Crow,et al.  Wright and Fisher on Inbreeding and Random Drift , 2010, Genetics.

[31]  C. D'onofrio,et al.  Loss of genetic diversity as a signature of apricot domestication and diffusion into the Mediterranean Basin , 2012, BMC Plant Biology.

[32]  K. Kitamoto,et al.  Breeding research on sake yeasts in Japan: history, recent technological advances, and future perspectives. , 2013, Annual review of food science and technology.

[33]  Y. Ohya,et al.  Isolation of a spontaneous cerulenin-resistant sake yeast with both high ethyl caproate-producing ability and normal checkpoint integrity , 2015, Bioscience, biotechnology, and biochemistry.

[34]  Y. Ohya,et al.  Large-Scale Survey of Intraspecific Fitness and Cell Morphology Variation in a Protoploid Yeast Species , 2016, G3: Genes, Genomes, Genetics.

[35]  P. VanRaden,et al.  Mating programs including genomic relationships and dominance effects. , 2013, Journal of dairy science.

[36]  Achim Zeileis,et al.  Diagnostic Checking in Regression Relationships , 2015 .

[37]  M. Kanauchi.  SAKE Alcoholic Beverage Production in Japanese Food Industry , 2013 .

[38]  Y. Ohya,et al.  Dynamic changes in brewing yeast cells in culture revealed by statistical analyses of yeast morphological data. , 2014, Journal of bioscience and bioengineering.

[39]  Daniel A. Skelly,et al.  The 100-genomes strains, an S. cerevisiae resource that illuminates its natural phenotypic and genotypic variation and emergence as an opportunistic pathogen , 2015, Genome research.

[40]  Andrew W. Murray,et al.  Feedback control of mitosis in budding yeast , 1991, Cell.

[41]  S. Kubodera,et al.  Distribution of phenolic yeasts and production of phenolic off-flavors in wine fermentation. , 2000, Journal of bioscience and bioengineering.

[42]  Yoshikazu Ohya,et al.  Genetic Complexity and Quantitative Trait Loci Mapping of Yeast Morphological Traits , 2007, PLoS genetics.

[43]  Koji Okamoto,et al.  Enhancement of Ethanol Fermentation in Saccharomyces cerevisiae Sake Yeast by Disrupting Mitophagy Function , 2013, Applied and Environmental Microbiology.

[44]  R. Kunkee,et al.  The Effect of Nitrogen Deficiency and Sulfur-Containing Amino Acids on the Reduction of Sulfate to Hydrogen Sulfide by Wine Yeasts , 1994, American Journal of Enology and Viticulture.

[45]  Paolo Giudici,et al.  Biometric and Genetic Study on Acetic Acid Production for Breeding of Wine Yeast , 1992, American Journal of Enology and Viticulture.

[46]  J. Harwood,et al.  Factors affecting levels of genetic diversity in natural populations. , 1998, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[47]  M. Aigle,et al.  Inheritable nature of enological quantitative traits is demonstrated by meiotic segregation of industrial wine yeast strains. , 2004, FEMS yeast research.

[48]  O. Yamada,et al.  Statistical analysis of sake-preparation conditions and dimethyl trisulfide formation. , 2014, Journal of bioscience and bioengineering.

[49]  Shinsuke Ohnuki,et al.  Single-cell phenomics reveals intra-species variation of phenotypic noise in yeast , 2013, BMC Systems Biology.

[50]  Leif Andersson,et al.  Prehistoric genomes reveal the genetic foundation and cost of horse domestication , 2014, Proceedings of the National Academy of Sciences.

[51]  Taro L. Saito,et al.  High-dimensional and large-scale phenotyping of yeast mutants. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[52]  A. Couloux,et al.  A population genomics insight into the Mediterranean origins of wine yeast domestication , 2015, Molecular ecology.

[53]  K. Iwashita,et al.  The AWA1 Gene Is Required for the Foam-Forming Phenotype and Cell Surface Hydrophobicity of Sake Yeast , 2002, Applied and Environmental Microbiology.

[54]  W. M. Ingledew,et al.  Ethanol tolerance in yeasts. , 1986, Critical reviews in microbiology.

[55]  Korbinian Strimmer,et al.  APE: Analyses of Phylogenetics and Evolution in R language , 2004, Bioinform..

[56]  Y. Ohya,et al.  Unveiling nonessential gene deletions that confer significant morphological phenotypes beyond natural yeast strains , 2014, BMC Genomics.

[57]  Yoshikazu Ohya,et al.  Identification of a mutation causing a defective spindle assembly checkpoint in high ethyl caproate-producing sake yeast strain K1801 , 2016, Bioscience, biotechnology and biochemistry.

[58]  R. Rigby,et al.  Generalized Additive Models for Location Scale and Shape (GAMLSS) in R , 2007 .

[59]  Chikara Furusawa,et al.  Comprehensive phenotypic analysis for identification of genes affecting growth under ethanol stress in Saccharomyces cerevisiae. , 2009, FEMS yeast research.

[60]  P. Langridge,et al.  Validation of Bismuth-Containing Indicator Media for Predicting H2S-Producing Potential ofSaccharomyces cerevisiaeWine Yeasts Under Enological Conditions , 1995, American Journal of Enology and Viticulture.

[61]  T. Hothorn,et al.  Simultaneous Inference in General Parametric Models , 2008, Biometrical journal. Biometrische Zeitschrift.

[62]  Akira Nishimura,et al.  Whole-Genome Sequencing of Sake Yeast Saccharomyces cerevisiae Kyokai no. 7 , 2011, DNA research : an international journal for rapid publication of reports on genes and genomes.