Prions are a common mechanism for phenotypic inheritance in wild yeasts

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 hi...

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Main Authors: Halfmann, Randal Arthur, Jarosz, Daniel F., Jones, Sandra K., Chang, Amelia, Lancaster, Alex K., Lindquist, Susan
Other Authors: Massachusetts Institute of Technology. Department of Biology
Format: Article
Language:en_US
Published: Nature Publishing Group 2014
Online Access:http://hdl.handle.net/1721.1/84950
https://orcid.org/0000-0003-1307-882X
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author Halfmann, Randal Arthur
Jarosz, Daniel F.
Jones, Sandra K.
Chang, Amelia
Lancaster, Alex K.
Lindquist, Susan
author2 Massachusetts Institute of Technology. Department of Biology
author_facet Massachusetts Institute of Technology. Department of Biology
Halfmann, Randal Arthur
Jarosz, Daniel F.
Jones, Sandra K.
Chang, Amelia
Lancaster, Alex K.
Lindquist, Susan
author_sort Halfmann, Randal Arthur
collection MIT
description 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.
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spelling mit-1721.1/849502021-09-13T13:55:28Z Prions are a common mechanism for phenotypic inheritance in wild yeasts Halfmann, Randal Arthur Jarosz, Daniel F. Jones, Sandra K. Chang, Amelia Lancaster, Alex K. Lindquist, Susan Massachusetts Institute of Technology. Department of Biology Whitehead Institute for Biomedical Research Halfmann, Randal Arthur Jarosz, Daniel F. Jones, Sandra K. Chang, Amelia Lancaster, Alex K. Lindquist, Susan 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. Howard Hughes Medical Institute (Investigator) G. Harold and Leila Y. Mathers Foundation Damon Runyon Cancer Research Foundation (HHMI fellow, DRG-1964-08) National Institutes of Health (U.S.) (NIH Pathway to independence award (K99 GM098600)) Howard Hughes Medical Institute (Exceptional Research Opportunities Program (EXROP)) 2014-02-14T16:18:34Z 2014-02-14T16:18:34Z 2012-02 Article http://purl.org/eprint/type/JournalArticle 0028-0836 1476-4687 http://hdl.handle.net/1721.1/84950 Halfmann, Randal, Daniel F. Jarosz, Sandra K. Jones, Amelia Chang, Alex K. Lancaster, and Susan Lindquist. “Prions are a common mechanism for phenotypic inheritance in wild yeasts.” Nature 482, no. 7385 (February 15, 2012): 363-368. https://orcid.org/0000-0003-1307-882X en_US http://dx.doi.org/10.1038/nature10875 Nature Article is made available in accordance with the publisher's policy and may be subject to US copyright law. Please refer to the publisher's site for terms of use. application/pdf Nature Publishing Group PMC
spellingShingle Halfmann, Randal Arthur
Jarosz, Daniel F.
Jones, Sandra K.
Chang, Amelia
Lancaster, Alex K.
Lindquist, Susan
Prions are a common mechanism for phenotypic inheritance in wild yeasts
title Prions are a common mechanism for phenotypic inheritance in wild yeasts
title_full Prions are a common mechanism for phenotypic inheritance in wild yeasts
title_fullStr Prions are a common mechanism for phenotypic inheritance in wild yeasts
title_full_unstemmed Prions are a common mechanism for phenotypic inheritance in wild yeasts
title_short Prions are a common mechanism for phenotypic inheritance in wild yeasts
title_sort prions are a common mechanism for phenotypic inheritance in wild yeasts
url http://hdl.handle.net/1721.1/84950
https://orcid.org/0000-0003-1307-882X
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