title: Prions are a common mechanism for phenotypic inheritance in wild yeasts.
abstract: The self-templating conformations of yeast prion proteins act as epigenetic elements of inheritance. Yeast prions might provide a mechanism for generating heritable phenotypic diversity that promotes survival in fluctuating environments and the evolution of new traits. However, this hypothesis is highly controversial. Prions that create new traits have not been found in wild strains, leading to the perception that they are rare 'diseases' of laboratory cultivation. Here we biochemically test approximately 700 wild strains of Saccharomyces for [PSI(+)] or [MOT3(+)], and find these prions in many. They conferred diverse phenotypes that were frequently beneficial under selective conditions. Simple meiotic re-assortment of the variation harboured within a strain readily fixed one such trait, making it robust and prion-independent. Finally, we genetically screened for unknown prion elements. Fully one-third of wild strains harboured them. These, too, created diverse, often beneficial phenotypes. Thus, prions broadly govern heritable traits in nature, in a manner that could profoundly expand adaptive opportunities.
authors.affiliation: Whitehead Institute for Biomedical Research, 9 Cambridge Center, Cambridge, Massachusetts 02142, USA.
authors.forename: Randal
authors.initials: R
authors.lastname: Halfmann
authors.forename: Daniel F
authors.initials: DF
authors.lastname: Jarosz
authors.forename: Sandra K
authors.initials: SK
authors.lastname: Jones
authors.forename: Amelia
authors.initials: A
authors.lastname: Chang
authors.forename: Alex K
authors.initials: AK
authors.lastname: Lancaster
authors.forename: Susan
authors.initials: S
authors.lastname: Lindquist
mesh_terms: D005075:Biological Evolution; D002473:Cell Wall / Q000378:metabolism; D003593:Cytoplasm / Q000378:metabolism; D044127:Epigenesis, Genetic; D056726:Genetic Association Studies; D014644:Genetic Variation / Q000235:genetics; D005838:Genotype; D006360:Heat-Shock Proteins / Q000235:genetics / Q000378:metabolism; D007753:Laboratories; D008540:Meiosis; D010454:Peptide Termination Factors / Q000235:genetics / Q000378:metabolism; D010641:Phenotype; D011328:Prions / Q000235:genetics / Q000378:metabolism*; D012441:Saccharomyces cerevisiae / Q000145:classification* / Q000166:cytology / Q000235:genetics* / Q000378:metabolism; D029701:Saccharomyces cerevisiae Proteins / Q000235:genetics / Q000378:metabolism; D014157:Transcription Factors / Q000235:genetics / Q000378:metabolism
chemical_list: D006360:Heat-Shock Proteins; C112006:MOT3 protein, S cerevisiae; D010454:Peptide Termination Factors; D011328:Prions; C404807:RNQ1 protein, S cerevisiae; C068068:SUP35 protein, S cerevisiae; D029701:Saccharomyces cerevisiae Proteins; D014157:Transcription Factors; C070972:HsP104 protein, S cerevisiae