FRINK Linked Data Fragments server

Matches in SemOpenAlex for { <https://semopenalex.org/work/W2155505293> ?p ?o ?g. }

• W2155505293 endingPage "2071" @default.
• W2155505293 startingPage "2056" @default.
• W2155505293 abstract "Heterosis is a universal phenomenon that has major implications in evolution and is of tremendous agro-economic value. To study the molecular manifestations of heterosis and to find factors that maximize its strength, we implemented a large-scale proteomic experiment in yeast. We analyzed the inheritance of 1,396 proteins in 55 inter- and intraspecific hybrids obtained from Saccharomyces cerevisiae and S. uvarum that were grown in grape juice at two temperatures. We showed that the proportion of heterotic proteins was highly variable depending on the parental strain and on the temperature considered. For intraspecific hybrids, this proportion was higher at nonoptimal temperature. Unexpectedly, heterosis for protein abundance was strongly biased toward positive values in interspecific hybrids but not in intraspecific hybrids. Computer modeling showed that this observation could be accounted for by assuming concave relationships between protein abundances and their controlling factors, in line with the metabolic model of heterosis. These results point to nonlinear processes that could play a central role in heterosis. Heterosis is a universal phenomenon that has major implications in evolution and is of tremendous agro-economic value. To study the molecular manifestations of heterosis and to find factors that maximize its strength, we implemented a large-scale proteomic experiment in yeast. We analyzed the inheritance of 1,396 proteins in 55 inter- and intraspecific hybrids obtained from Saccharomyces cerevisiae and S. uvarum that were grown in grape juice at two temperatures. We showed that the proportion of heterotic proteins was highly variable depending on the parental strain and on the temperature considered. For intraspecific hybrids, this proportion was higher at nonoptimal temperature. Unexpectedly, heterosis for protein abundance was strongly biased toward positive values in interspecific hybrids but not in intraspecific hybrids. Computer modeling showed that this observation could be accounted for by assuming concave relationships between protein abundances and their controlling factors, in line with the metabolic model of heterosis. These results point to nonlinear processes that could play a central role in heterosis. Nonadditive inheritance in hybrids, whereby the phenotype of offspring is not the average of the parental phenotypes, is commonly observed in all species. For monogenic traits, the departure from additivity is called dominance (1.Mendel G. Versuche uber Pflanzenhybriden.Verh Naturforsch Ver Brunn. 1866; 4: 3-47Google Scholar) or overdominance if the phenotypic value of the hybrid is outside the range defined by the parental values (2.Hull F.H. Overdominance and corn breeding where hybrid seed is not feasible.Agronom. J. 1946; 38: 1100-1103Crossref Google Scholar). For polygenic traits, it is called heterosis. Heterosis is commonly associated to macroscopic traits, but it also applies to less integrated traits such as metabolite abundances (3.Lisec J. Römisch-Margl L. Nikoloski Z. Piepho H. Giavalisco P. Selbig J. Gierl A. Willmitzer L. Corn hybrids display lower metabolite variability and complex metabolite inheritance patterns.Plant J. 2011; 68: 326-336Crossref PubMed Scopus (69) Google Scholar, 4.Salinas F. Cubillos F.A. Soto D. Garcia V. Bergström A. Warringer J. Ganga M.A. Louis E.J. Liti G. Martinez C. The genetic basis of natural variation in oenological traits in Saccharomyces cerevisiae.PLoS ONE. 2012; 7: e49640Crossref PubMed Scopus (62) Google Scholar), fluxes and enzyme activities (5.Warner R.L. Hageman R.H. Dudley J.W. Lambert R.J. Inheritance of nitrate reductase activity in Zea mays L.Proc. Natl. Acad. Sci. U.S.A. 1969; 62: 785-792Crossref PubMed Scopus (33) Google Scholar, 6.Causse M. Rocher J.-P. Pelleschi S. Barrière Y. de Vienne D. Prioul J.-L. Sucrose phosphate synthase: An enzyme with heterotic activity correlated with maize growth.Crop Sci. 1995; 35: 995-1001Crossref Scopus (32) Google Scholar, 7.Fiévet J.B. Dillmann C. de Vienne D. Systemic properties of metabolic networks lead to an epistasis-based model for heterosis.Theor. Appl. Genet. 2010; 120: 463-473Crossref PubMed Scopus (34) Google Scholar), mRNA, and protein amounts (8.Mohayeji M. Capriotti A.L. Cavaliere C. Piovesana S. Samperi R. Stampachiacchiere S. Toorchi M. Lagana A. Heterosis profile of sunflower leaves: A label free proteomics approach.J. Proteomics. 2014; 99: 101-110Crossref PubMed Scopus (29) Google Scholar). The concept of heterosis is not universally shared and depends on the scientific communities. Strictly speaking, heterosis is defined as the superiority of the hybrid over the mean parental value (mid-parent heterosis, MPH1.Mendel G. Versuche uber Pflanzenhybriden.Verh Naturforsch Ver Brunn. 1866; 4: 3-47Google Scholar) or over its parent exhibiting the highest value (best-parent heterosis, BPH). This definition and the associated terminology are historical and come from the fact that heterosis was commonly associated to traits such as growth rate, biomass, size, yield, or fertility, for which higher values are beneficial. However, lower values can also occur (e.g. (9.Zörgö E. Gjuvsland A. Cubillos F.A. Louis E.J. Liti G. Blomberg A. Omholt S.W. Warringer J. Life history shapes trait heredity by promoting accumulation of loss-of-function alleles in yeast.Mol. Biol. Evol. 2012; 29: 1781-1789Crossref PubMed Scopus (57) Google Scholar)). The definition of heterosis has therefore been broadened to include also the cases where the hybrid is below the mean parental value (negative MPH) or below its parent exhibiting the lowest value (worst-parent heterosis, WPH). In this paper, we will adopt this second definition, motivated by its lack of presumption about whether the changes observed in hybrids are beneficial or detrimental. Heterosis has fascinated scientists and breeders for more than 100 years. It has major implications in evolution and domestication of crop plants (10.Rieseberg L.H. Baird S.J. Gardner K.A. Hybridization, introgression, and linkage evolution.Plant Mol. Biol. 2000; 42: 205-224Crossref PubMed Scopus (193) Google Scholar, 11.Lippman Z.B. Zamir D. Heterosis: Revisiting the magic.Trends Genet. 2007; 23: 60-66Abstract Full Text Full Text PDF PubMed Scopus (412) Google Scholar), and it has been exploited since the 1930s in plant breeding to produce hybrids of high agronomic value (12.Crow J.F. 90 years ago: The beginning of hybrid maize.Genetics. 1998; 148: 923-928Crossref PubMed Google Scholar). In this context, heterosis has proven to efficiently accelerate the process of selection for various crops (reviewed in (13.Duvick D.N. Heterosis: Feeding People and Protecting Natural Resources.In The Genetics and Exploitation of Heterosis in Crops. 1999; : 19-29Google Scholar)). Heterosis is opposite to inbreeding depression, that is supposed to be predominantly caused by the homozygosity of deleterious recessive alleles (14.Charlesworth D. Willis J.H. The genetics of inbreeding depression.Nat. Rev. Genet. 2009; 10: 783-796Crossref PubMed Scopus (1175) Google Scholar). Heterosis can provide a heterozygote advantage by buffering against these alleles and confers genetic plasticity to adapt to environmental changes (11.Lippman Z.B. Zamir D. Heterosis: Revisiting the magic.Trends Genet. 2007; 23: 60-66Abstract Full Text Full Text PDF PubMed Scopus (412) Google Scholar). Given the importance of heterosis for agriculture and because it is an intriguing phenomenon, many studies have focused on the understanding of its genetic and molecular bases (11.Lippman Z.B. Zamir D. Heterosis: Revisiting the magic.Trends Genet. 2007; 23: 60-66Abstract Full Text Full Text PDF PubMed Scopus (412) Google Scholar, 15.Sprague G.F. Heterosis in maize: Theory and practice.Heterosis. 1983; : 47-70Crossref Google Scholar, 16.Tsaftaris S.A. Molecular aspects of heterosis in plants.Physiol. Plant. 1995; 94: 362-370Crossref Scopus (70) Google Scholar, 17.Tsaftaris A.S. Kafka M. Mechanisms of heterosis in crop plants.J. Crop Prod. 1997; 1: 95-111Crossref Scopus (37) Google Scholar, 18.Birchler J.A. Auger D.L. Riddle N.C. In search of the molecular basis of heterosis.Plant Cell. 2003; 15: 2236-2239Crossref PubMed Scopus (368) Google Scholar, 19.Hochholdinger F. Hoecker N. Towards the molecular basis of heterosis.Trends Plant Sci. 2007; 12: 427-432Abstract Full Text Full Text PDF PubMed Scopus (251) Google Scholar, 20.Birchler J.A. Yao H. Chudalayandi S. Vaiman D. Veitia R.A. Heterosis.Plant Cell. 2010; 22: 2105-2112Crossref PubMed Scopus (340) Google Scholar, 21.Chen Z.J. Molecular mechanisms of polyploidy and hybrid vigor.Trends Plant Sci. 2010; 15: 57-71Abstract Full Text Full Text PDF PubMed Scopus (411) Google Scholar, 22.Baranwal V.K. Mikkilineni V. Zehr U.B. Tyagi A.K. Kapoor S. Heterosis: Emerging ideas about hybrid vigour.J. Exp. Bot. 2012; 63: 6309-6314Crossref PubMed Scopus (103) Google Scholar, 23.Kaeppler S. Heterosis: Many genes, many mechanisms—End the search for an undiscovered unifying theory.ISRN Bot. 2012; 2012: 1-12Crossref Google Scholar, 24.Chen Z.J. Genomic and epigenetic insights into the molecular bases of heterosis.Nat. Rev. Genet. 2013; 14: 471-482Crossref PubMed Scopus (337) Google Scholar, 25.Schnable P.S. Springer N.M. Progress toward understanding heterosis in crop plants.Annu. Rev. Plant Biol. 2013; 64: 71-88Crossref PubMed Scopus (280) Google Scholar). Three nonexclusive hypotheses based on genetic effects are classically put forward to explain heterosis. First, the dominance hypothesis attributes heterosis to complementation: In the hybrid, the recessive alleles are masked by dominant and generally favorable alleles (26.Davenport C.B. Degeneration, albinism and inbreeding.Science. 1908; 28: 454-455Crossref PubMed Scopus (210) Google Scholar, 27.Bruce A.B. The Mendelian theory of heredity and the augmentation of vigor.Science. 1910; 32: 627-628Crossref PubMed Scopus (261) Google Scholar). Second, the overdominance hypothesis assumes that heterosis is inherent to the heterozygous state (2.Hull F.H. Overdominance and corn breeding where hybrid seed is not feasible.Agronom. J. 1946; 38: 1100-1103Crossref Google Scholar, 28.Crow J.F. Alternative hypotheses of hybrid vigor.Genetics. 1948; 33: 477-487Crossref PubMed Google Scholar). Third, the epistasis hypothesis proposes that heterosis is due to intergenic interactions created in the hybrid (29.Richey F.D. Mock-dominance and hybrid vigor.Science. 1942; 96: 280-281Crossref PubMed Scopus (39) Google Scholar, 30.Powers L. An expansion of Jones's theory for the explanation of heterosis.Am Nat. 1944; 78: 275-280Crossref Google Scholar). Scientists have long sought a unifying theory to account for heterosis, but it is now commonly admitted that this phenomenon likely arises from the combination of several genetic mechanisms, the relative effects of which vary according to the trait, the cross, or the species (23.Kaeppler S. Heterosis: Many genes, many mechanisms—End the search for an undiscovered unifying theory.ISRN Bot. 2012; 2012: 1-12Crossref Google Scholar, 25.Schnable P.S. Springer N.M. Progress toward understanding heterosis in crop plants.Annu. Rev. Plant Biol. 2013; 64: 71-88Crossref PubMed Scopus (280) Google Scholar). These genetic effects are consistent with the factors known to maximize the occurrence of heterosis. When compiling the results obtained so far across numerous studies, it appears that heterosis is of greatest magnitude for highly integrated, and hence polygenic, traits such as crop yield (23.Kaeppler S. Heterosis: Many genes, many mechanisms—End the search for an undiscovered unifying theory.ISRN Bot. 2012; 2012: 1-12Crossref Google Scholar, 31.Becker H.C. Pflanzenzuumlchtung.UTB, Eugen Ulmer Verlag, Stuttgart, Germany. 1993; : 1-368Google Scholar); it is larger in allogamous than in autogamous species (31.Becker H.C. Pflanzenzuumlchtung.UTB, Eugen Ulmer Verlag, Stuttgart, Germany. 1993; : 1-368Google Scholar); it requires genetic divergence between parents; and interspecific crosses commonly produce higher levels of heterosis (21.Chen Z.J. Molecular mechanisms of polyploidy and hybrid vigor.Trends Plant Sci. 2010; 15: 57-71Abstract Full Text Full Text PDF PubMed Scopus (411) Google Scholar, 24.Chen Z.J. Genomic and epigenetic insights into the molecular bases of heterosis.Nat. Rev. Genet. 2013; 14: 471-482Crossref PubMed Scopus (337) Google Scholar, 32.East E.M. Heterosis.Genetics. 1936; 21: 375-397Crossref PubMed Google Scholar). However, these general trends are not sufficient for a reliable prediction of heterosis, which is a major challenge for plant and animal breeding and for biotechnology. Future strategies for heterosis prediction will have to rely both on an accurate description of its manifestations and on the detailed knowledge of the factors that maximize its strength. To address these issues, we performed a large-scale study of heterosis by analyzing the inheritance of the abundance of a high number of proteins in an unprecedented number of yeast hybrids grown in two conditions. The proteomic level is particularly relevant to the large-scale study of heterosis because protein abundances are polygenic molecular traits (33.Damerval C. Maurice A. Josse J.M. de Vienne D. Quantitative trait loci underlying gene product variation: A novel perspective for analyzing regulation of genome expression.Genetics. 1994; 137: 289-301Crossref PubMed Google Scholar) that can be measured by high-throughput quantitative proteomics (34.Cox J. Mann M. Quantitative, high-resolution proteomics for data-driven systems biology.Annu. Rev. Biochem. 2011; 80: 273-299Crossref PubMed Scopus (531) Google Scholar, 35.Bantscheff M. Lemeer S. Savitski M.M. Kuster B. Quantitative mass spectrometry in proteomics: Critical review update from 2007 to the present.Anal. Bioanal. Chem. 2012; 404: 939-965Crossref PubMed Scopus (581) Google Scholar). Yeast has only rarely been used to study heterosis (9.Zörgö E. Gjuvsland A. Cubillos F.A. Louis E.J. Liti G. Blomberg A. Omholt S.W. Warringer J. Life history shapes trait heredity by promoting accumulation of loss-of-function alleles in yeast.Mol. Biol. Evol. 2012; 29: 1781-1789Crossref PubMed Scopus (57) Google Scholar, 36.Timberlake W.E. Frizzell M.A. Richards K.D. Gardner R.C. A new yeast genetic resource for analysis and breeding.Yeast. 2011; 28: 63-80Crossref PubMed Scopus (24) Google Scholar, 37.Lindegren C.C. Braham J.E. Calle J.D. Heterosis in Saccharomyces.Nature. 1953; 172: 800-802Crossref PubMed Scopus (3) Google Scholar, 38.Steinmetz L.M. Sinha H. Richards D.R. Spiegelman J.I. Oefner P.J. McCusker J.H. Davis R.W. Dissecting the architecture of a quantitative trait locus in yeast.Nature. 2002; 416: 326-330Crossref PubMed Scopus (424) Google Scholar, 39.Schaefke B. Emerson J.J. Wang T.-Y. Lu M.-Y. J. Hsieh L.-C. Li W.-H. Inheritance of gene expression level and selective constraints on trans- and cis-regulatory changes in yeast.Mol. Biol. Evol. 2013; 30: 2121-2133Crossref PubMed Scopus (54) Google Scholar, 40.Plech M. de Visser J.A. Korona R. Heterosis is prevalent among domesticated but not wild strains of Saccharomyces cerevisiae.Genes Genom. Genet. 2014; 4: 315-323Google Scholar, 41.Shapira R. Levy T. Shaked S. Fridman E. David L. Extensive heterosis in growth of yeast hybrids is explained by a combination of genetic models.Heredity. 2014; 113: 316-326Crossref PubMed Scopus (36) Google Scholar). Yet, it is amenable to large-scale laboratory experiments, and it is of major industrial interest for wine making. Hybrids with exceptional performances were reported in Saccharomyces cerevisiae (36.Timberlake W.E. Frizzell M.A. Richards K.D. Gardner R.C. A new yeast genetic resource for analysis and breeding.Yeast. 2011; 28: 63-80Crossref PubMed Scopus (24) Google Scholar, 38.Steinmetz L.M. Sinha H. Richards D.R. Spiegelman J.I. Oefner P.J. McCusker J.H. Davis R.W. Dissecting the architecture of a quantitative trait locus in yeast.Nature. 2002; 416: 326-330Crossref PubMed Scopus (424) Google Scholar, 42.Romano P. Soli M.G. Suzzi G. Grazia L. Zambonelli C. Improvement of a wine Saccharomyces cerevisiae strain by a breeding program.Appl. Environ. Microbiol. 1985; 50: 1064-1067Crossref PubMed Google Scholar, 43.Jolly N.P. Janse B.J.H. Rooyen T.J.V. Louw J.H. Hybridization and typing of yeasts used in sparkling wine fermentations.Am. J. Enol. Vitic. 1993; 44: 217-226Google Scholar), and several observations indicate that interspecific hybridization could be used in breeding to produce improved strains for wine making. For instance, many interspecific hybrids between S. cerevisiae and S. uvarum Beijerinck or S. kudriavzevii isolated in wine and natural environments showed important biotechnological potential, such as a better robustness than their parents (44.Belloch C. Orlic S. Barrio E. Querol A. Fermentative stress adaptation of hybrids within the Saccharomyces sensu stricto complex.Int. J. Food Microbiol. 2008; 122: 188-195Crossref PubMed Scopus (153) Google Scholar, 45.Arroyo-López F.N. Orlić S. Querol A. Barrio E. Effects of temperature, pH and sugar concentration on the growth parameters of Saccharomyces cerevisiae, S. kudriavzevii and their interspecific hybrid.Int. J. Food Microbiol. 2009; 131: 120-127Crossref PubMed Scopus (150) Google Scholar, 46.Tronchoni J. Gamero A. Arroyo-López F.N. Barrio E. Querol A. Differences in the glucose and fructose consumption profiles in diverse Saccharomyces wine species and their hybrids during grape juice fermentation.Int. J. Food Microbiol. 2009; 134: 237-243Crossref PubMed Scopus (91) Google Scholar, 47.Gamero A. Tronchoni J. Querol A. Belloch C. Production of aroma compounds by cryotolerant Saccharomyces species and hybrids at low and moderate fermentation temperatures.J. Appl. Microbiol. 2013; 114: 1405-1414Crossref PubMed Scopus (75) Google Scholar). In addition, several wine strains empirically selected for their biotechnological properties proved to be interspecific hybrids (48.Borneman A.R. Desany B.A. Riches D. Affourtit J.P. Forgan A.H. Pretorius I.S. Egholm M. Chambers P.J. The genome sequence of the wine yeast VIN7 reveals an allotriploid hybrid genome with Saccharomyces cerevisiae and Saccharomyces kudriavzevii origins.FEMS Yeast Res. 2012; 12: 88-96Crossref PubMed Scopus (90) Google Scholar, 49.Erny C. Raoult P. Alais A. Butterlin G. Delobel P. Matei-Radoi F. Casaregola S. Legras J.L. Ecological success of a group of Saccharomyces cerevisiae/Saccharomyces kudriavzevii hybrids in the Northern European wine making environment.Appl. Environ. Microbiol. 2012; 78: 3256-3265Crossref PubMed Scopus (59) Google Scholar). For all these reasons, we chose to study heterosis for protein abundance in yeast strains from S. cerevisiae and S. uvarum, which are the two main species associated with grape juice fermentation (50.Masneuf-Pomarède I. Bely M. Marullo P. Lonvaud-Funel A. Dubourdieu D. Reassessment of phenotypic traits for Saccharomyces bayanus var. uvarum wine yeast strains.Int. J. Food Microbiol. 2010; 139: 79-86Crossref PubMed Scopus (81) Google Scholar). By using shotgun proteomics, we analyzed more than 1,300 proteins in an experimental design, including 11 parental strains of S. cerevisiae and S. uvarum and their 55 intra- and interspecific hybrids, which were grown at two temperatures to take into account adaptation differences between parental species (18 °C and 26 °C optimal for S. uvarum and S. cerevisiae, respectively (44.Belloch C. Orlic S. Barrio E. Querol A. Fermentative stress adaptation of hybrids within the Saccharomyces sensu stricto complex.Int. J. Food Microbiol. 2008; 122: 188-195Crossref PubMed Scopus (153) Google Scholar, 51.Kishimoto M. Goto S. Growth temperatures and electrophoretic karyotyping as tools for practical discrimination of Saccharomyces bayanus and Saccharomyces cerevisiae.J. Gen. Appl. Microbiol. 1995; 41: 239-247Crossref Scopus (39) Google Scholar, 52.Naumov G. Genetic identification of biological species in the Saccharomyces sensu stricto complex.J. Ind. Microbiol. Biotechnol. 1996; 17: 295-302Crossref Google Scholar)). We showed that heterosis for protein abundance was strongly biased toward positive values in interspecific hybrids but not in intraspecific hybrids, which, to our knowledge, has never been reported. We also showed that our experimental results were consistent with results obtained from modeling approaches assuming nonlinear relationships between protein abundances and their controlling factors. Four diploid S. uvarum strains, seven diploid S. cerevisiae strains, and their 55 hybrids produced from a half diallel design (53.Albertin W. da Silva T. Rigoulet M. Salin B. Masneuf-Pomarede I. de Vienne D. Sicard D. Bely M. Marullo P. The mitochondrial genome impacts respiration but not fermentation in interspecific Saccharomyces hybrids.PLoS ONE. 2013; 8: e75121Crossref PubMed Scopus (32) Google Scholar) were analyzed in this study. Parental strains were derived from strains isolated from different geographical locations and from either natural or food-processing origins (Table I): the S. cerevisiae strains were isolated from diverse media (distillery, enology, oak exudate) to maximize the genetic diversity within this species (54.Liti G. Carter D.M. Moses A.M. Warringer J. Parts L. James S.A. Davey R.P. Roberts I.N. Burt A. Koufopanou V. Tsai I.J. Bergman C.M. Bensasson D. O'Kelly M.J. van Oudenaarden A. Barton D.B. Bailes E. Nguyen A.N. Jones M. Quail M.A. Goodhead I. Sims S. Smith F. Blomberg A. Durbin R. Louis E.J. Population genomics of domestic and wild yeasts.Nature. 2009; 458: 337-341Crossref PubMed Scopus (1052) Google Scholar); the S. uvarum strains, originating from grape must or cider fermentation, were chosen to cover a wide part of the genetic diversity of the S. uvarum species (Masneuf-Pomarède, I., personal communication). For each original strain, one meiospore was isolated with a micromanipulator (Singer MSM Manual, Singer Instrument, Somerset, UK). All the original strains but Alcotec 24 were homothallic (HO/HO); therefore, fully homozygous diploid strains were spontaneously obtained by fusion of opposite mating type cells. For A24 (ho/ho), one isolated haploid meiospore was diploidized via transient expression of the HO endonuclease (55.Albertin W. Marullo P. Aigle M. Bourgais A. Bely M. Dillmann C. De Vienne D. Sicard D. Evidence for autotetraploidy associated with reproductive isolation in Saccharomyces cerevisiae: Towards a new domesticated species.J. Evol. Biol. 2009; 22: 2157-2170Crossref PubMed Scopus (50) Google Scholar). All strains were grown at 30 °C in YPD medium containing 1% yeast extract (Difco Laboratories, Detroit, MI), 1% bactopeptone (Difco), and 2% glucose, supplemented or not with 2% agar. When necessary, antibiotics were added at the following concentrations: 100 μg/ml for G418 (Sigma, L'Isle d'Abeau, France), and nourseothricin (Werner bioagent, Jena, Germany) and 300 μg/ml for hygromycin B (Sigma).Table IOrigin of parental strainsSpeciesParental strainsMonosporic derivateCollection/SupplieraISVV, http://www.oenologie.u-bordeaux2.fr/.Isolation originArea of originReferenceS. uvarumPM12U1ISVVGrape must fermentationJurançon, France(98.Naumov G.I. James S.A. Naumova E.S. Louis E.J. Roberts I.N. Three new species in the Saccharomyces sensu stricto complex: Saccharomyces cariocanus, Saccharomyces kudriavzevii and Saccharomyces mikatae.Int. J. Syst. Evol. Microbiol. 2000; 50: 1931-1942Crossref PubMed Scopus (245) Google Scholar)S. uvarumPJP3U2ISVVGrape must fermentationSancerre, France(98.Naumov G.I. James S.A. Naumova E.S. Louis E.J. Roberts I.N. Three new species in the Saccharomyces sensu stricto complex: Saccharomyces cariocanus, Saccharomyces kudriavzevii and Saccharomyces mikatae.Int. J. Syst. Evol. Microbiol. 2000; 50: 1931-1942Crossref PubMed Scopus (245) Google Scholar)S. uvarumBr6.2U3ADRIA NORMANDIECider fermentationNormandie, France(95.Gout J.-F. Duret L. Kahn D. Differential retention of metabolic genes following whole-genome duplication.Mol. Biol. Evol. 2009; 26: 1067-1072Crossref PubMed Scopus (31) Google Scholar)S. uvarumRC4–15U4ISVVGrape must fermentationAlsace, France(57.Masneuf-Pomarède I. Le Jeune C. Durrens P. Lollier M. Aigle M. Dubourdieu D. Molecular typing of wine yeast strains Saccharomyces bayanus var. uvarum using microsatellite markers.Syst. Appl. Microbiol. 2007; 30: 75-82Crossref PubMed Scopus (52) Google Scholar)S. cerevisiaeCLIB-294D1CIRM-LevuresDistilleryCognac, France(98.Naumov G.I. James S.A. Naumova E.S. Louis E.J. Roberts I.N. Three new species in the Saccharomyces sensu stricto complex: Saccharomyces cariocanus, Saccharomyces kudriavzevii and Saccharomyces mikatae.Int. J. Syst. Evol. Microbiol. 2000; 50: 1931-1942Crossref PubMed Scopus (245) Google Scholar)S. cerevisiaeAlcotec 24D2Hambleton BardDistilleryUK(100.Albertin W. Marullo P. Aigle M. Dillmann C. de Vienne D. Bely M. Sicard D. Population size drives industrial Saccharomyces cerevisiae alcoholic fermentation and is under genetic control.Appl. Environ. Microbiol. 2011; 77: 2772-2784Crossref PubMed Scopus (39) Google Scholar)S. cerevisiaeCLIB-328E1CIRM-LevuresEnologyUK(100.Albertin W. Marullo P. Aigle M. Dillmann C. de Vienne D. Bely M. Sicard D. Population size drives industrial Saccharomyces cerevisiae alcoholic fermentation and is under genetic control.Appl. Environ. Microbiol. 2011; 77: 2772-2784Crossref PubMed Scopus (39) Google Scholar)S. cerevisiaeBO213E2LAFFORT OenologieEnologyFrance(101.Marullo P. Bely M. Masneuf-Pomarède I. Pons M. Aigle M. Dubourdieu D. Breeding strategies for combining fermentative qualities and reducing off-flavor production in a wine yeast model.FEMS Yeast Res. 2006; 6: 268-279Crossref PubMed Scopus (96) Google Scholar)S. cerevisiaeF10E4LAFFORT OenologieEnologyBordeaux, France(101.Marullo P. Bely M. Masneuf-Pomarède I. Pons M. Aigle M. Dubourdieu D. Breeding strategies for combining fermentative qualities and reducing off-flavor production in a wine yeast model.FEMS Yeast Res. 2006; 6: 268-279Crossref PubMed Scopus (96) Google Scholar)S. cerevisiaeVL3E5LAFFORT OenologieEnologyBordeaux, France(102.Marullo P. Mansour C. Dufour M. Albertin W. Sicard D. Bely M. Dubourdieu D. Genetic improvement of thermo-tolerance in wine Saccharomyces cerevisiae strains by a backcross approach.FEMS Yeast Res. 2009; 9: 1148-1160Crossref PubMed Scopus (56) Google Scholar)S. cerevisiaeYPS128W1SGRPForest, oak exudatePennsylvania, USA(54.Liti G. Carter D.M. Moses A.M. Warringer J. Parts L. James S.A. Davey R.P. Roberts I.N. Burt A. Koufopanou V. Tsai I.J. Bergman C.M. Bensasson D. O'Kelly M.J. van Oudenaarden A. Barton D.B. Bailes E. Nguyen A.N. Jones M. Quail M.A. Goodhead I. Sims S. Smith F. Blomberg A. Durbin R. Louis E.J. Population genomics of domestic and wild yeasts.Nature. 2009; 458: 337-341Crossref PubMed Scopus (1052) Google Scholar)ADRIA NORMANDIE, http://www.adria-normandie.comSGRP, http://www.sanger.ac.uk/research/projects/genomeinformatics/sgrp.html.CIRM-Levures, http://www.inra.fr/internet/Produits/cirmlevures.Hambleton Bard, http://www.hambletonbard.com.LAFFORT Œnologie, http://www.laffort.com.a ISVV, http://www.oenologie.u-bordeaux2.fr/. Open table in a new tab ADRIA NORMANDIE, http://www.adria-normandie.com SGRP, http://www.sanger.ac.uk/research/projects/genomeinformatics/sgrp.html. CIRM-Levures, http://www.inra.fr/internet/Produits/cirmlevures. Hambleton Bard, http://www.hambletonbard.com. LAFFORT Œnologie, http://www.laffort.com. Hybrid construction was performed as described in Albertin et al. (53.Albertin W. da Silva T. Rigoulet M. Salin B. Masneuf-Pomarede I. de Vienne D. Sicard D. Bely M. Marullo P. The mitochondrial genome impacts respiration but not fermentation in interspecific Saccharomyces hybrids.PLoS ONE. 2013; 8: e75121Crossref PubMed Scopus (32) Google Scholar). Briefly, the 11 diploid parental strains were transformed with a cassette containing the HO allele disrupted by a gene of resistance to either G418 (ho::KanR), hygromycin B (ho::HygR), or nourseothricin (ho::NatR). Strain transformation allowed conversion to heterothallism for the homothallic strains. Then the mating-type (MATa or MATalpha) of antibiotic-resistant monosporic clones was determined using testers of well-known mating type. For each cross, parental strains of opposite mating type were put in contact 2 to 6 h in YPD medium at room temperature and plated on YPD-agar containing the appropriate antibiotics. Ten independent hybrids per cross were recovered. After recurrent cultures on YPD-agar corresponding to ∼ 80 generations, the nuclear chromosomal stability of the hybrids was controlled by pulsed field electrophoresis (CHEF-DRIII, Bio-Rad, Marnes-La-Coquette, France) as well as homoplasmy (only one parental mitochondrial genome). One hybrid per cross was finally retained for further experiments. Two polymorphic microsatellites specific to S. cerevisiae (Sc-YFR038 and Sc-YML091 (56.Richards K.D. Goddard M.R. Gardner R.C. A database of microsatellite genotypes for Saccharomyces cerevisiae.Antonie Van Leeuwenhoek. 2009; 96: 355-359Crossref PubMed Scopus (61) Google Scholar)) and two specific to S. uvarum (locus 4 and 9 (57.Masneuf-Pomarède I. Le Jeune C. Durrens P. Lollier M. Aigle M. Dubourdieu D. Molecular typing of wine yeast strains Saccharomyces bayanus var. uvarum using microsatellite markers.Syst. Appl. Microbiol. 2007; 30: 75-82Crossref PubMed Scopus (52) Google Scholar)) were used to discriminate rapidly the hybrids from the parental strains. These four markers were amplified in a multiplex PCR reaction (95 °C for 5 min for initial denaturation step; 95 °C for 30 s, 55 °C for 90 s, and 72 °C for 60 s repeated 35 times; a final elongation step of 30 min at 60 °C). The PCR products were analyzed on an ABI3730 apparatus (A" @default.
• W2155505293 created "2016-06-24" @default.
• W2155505293 creator A5003510298 @default.
• W2155505293 creator A5025481159 @default.
• W2155505293 creator A5029281110 @default.
• W2155505293 creator A5029338630 @default.
• W2155505293 creator A5041009303 @default.
• W2155505293 creator A5064248958 @default.
• W2155505293 creator A5067462896 @default.
• W2155505293 creator A5074469185 @default.
• W2155505293 creator A5080752297 @default.
• W2155505293 creator A5085974608 @default.
• W2155505293 creator A5086667367 @default.
• W2155505293 creator A5090097111 @default.
• W2155505293 date "2015-08-01" @default.
• W2155505293 modified "2023-10-18" @default.
• W2155505293 title "A Systems Approach to Elucidate Heterosis of Protein Abundances in Yeast" @default.
• W2155505293 cites W144778757 @default.
• W2155505293 cites W1494644796 @default.
• W2155505293 cites W1760179322 @default.
• W2155505293 cites W1929718737 @default.
• W2155505293 cites W1966966655 @default.
• W2155505293 cites W1970679073 @default.
• W2155505293 cites W1970900633 @default.
• W2155505293 cites W1971941790 @default.
• W2155505293 cites W1982044721 @default.
• W2155505293 cites W1987286226 @default.
• W2155505293 cites W1990987722 @default.
• W2155505293 cites W1992338509 @default.
• W2155505293 cites W1994950943 @default.
• W2155505293 cites W1996366533 @default.
• W2155505293 cites W2002525133 @default.
• W2155505293 cites W2006078742 @default.
• W2155505293 cites W2010454461 @default.
• W2155505293 cites W2013784328 @default.
• W2155505293 cites W2014919994 @default.
• W2155505293 cites W2017115075 @default.
• W2155505293 cites W2018085822 @default.
• W2155505293 cites W2020891911 @default.
• W2155505293 cites W2022907022 @default.
• W2155505293 cites W2027974246 @default.
• W2155505293 cites W2028932438 @default.
• W2155505293 cites W2029690376 @default.
• W2155505293 cites W2032786198 @default.
• W2155505293 cites W2036640311 @default.
• W2155505293 cites W2037235640 @default.
• W2155505293 cites W2040470684 @default.
• W2155505293 cites W2040763402 @default.
• W2155505293 cites W2042586732 @default.
• W2155505293 cites W2043896568 @default.
• W2155505293 cites W2044816823 @default.
• W2155505293 cites W2052948442 @default.
• W2155505293 cites W2054624670 @default.
• W2155505293 cites W2054837796 @default.
• W2155505293 cites W2059198799 @default.
• W2155505293 cites W2060156800 @default.
• W2155505293 cites W2061338144 @default.
• W2155505293 cites W2062819607 @default.
• W2155505293 cites W2065035179 @default.
• W2155505293 cites W2068036331 @default.
• W2155505293 cites W2075502552 @default.
• W2155505293 cites W2075556644 @default.
• W2155505293 cites W2078396119 @default.
• W2155505293 cites W2080589621 @default.
• W2155505293 cites W2084621494 @default.
• W2155505293 cites W2085232591 @default.
• W2155505293 cites W2085707114 @default.
• W2155505293 cites W2085990577 @default.
• W2155505293 cites W2092594118 @default.
• W2155505293 cites W2094814523 @default.
• W2155505293 cites W2096719970 @default.
• W2155505293 cites W2097610171 @default.
• W2155505293 cites W2103682702 @default.
• W2155505293 cites W2104221859 @default.
• W2155505293 cites W2106074866 @default.
• W2155505293 cites W2106962907 @default.
• W2155505293 cites W2107035215 @default.
• W2155505293 cites W2110401774 @default.
• W2155505293 cites W2110876945 @default.
• W2155505293 cites W2114130270 @default.
• W2155505293 cites W2118229337 @default.
• W2155505293 cites W2119686333 @default.
• W2155505293 cites W2119894085 @default.
• W2155505293 cites W2121547736 @default.
• W2155505293 cites W2122560513 @default.
• W2155505293 cites W2126781759 @default.
• W2155505293 cites W2130006002 @default.
• W2155505293 cites W2131587346 @default.
• W2155505293 cites W2137683543 @default.
• W2155505293 cites W2137917513 @default.
• W2155505293 cites W2142437744 @default.
• W2155505293 cites W2142907337 @default.
• W2155505293 cites W2147295567 @default.
• W2155505293 cites W2149126429 @default.
• W2155505293 cites W2150461557 @default.
• W2155505293 cites W2151509612 @default.
• W2155505293 cites W2157643505 @default.
• W2155505293 cites W2158516833 @default.

• next