Selection for robust metabolism in domesticated yeasts is driven by adaptation to Hsp90 stress.

Publisher: American Association for the Advancement of Science Country of Publication: United States NLM ID: 0404511 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1095-9203 (Electronic) Linking ISSN: 00368075 NLM ISO Abbreviation: Science Subsets: MEDLINE

Publication: : Washington, DC : American Association for the Advancement of Science
Original Publication: New York, N.Y. : [s.n.] 1880-

Adaptation, Physiological*/genetics ; Ethanol*/metabolism ; HSP90 Heat-Shock Proteins*/metabolism ; HSP90 Heat-Shock Proteins*/genetics ; Saccharomyces cerevisiae*/genetics ; Saccharomyces cerevisiae*/metabolism ; Saccharomyces cerevisiae Proteins*/metabolism ; Saccharomyces cerevisiae Proteins*/genetics ; Selection, Genetic* ; Fermentation*/genetics; Beer ; Bread ; Gene Duplication ; Metabolic Networks and Pathways/genetics ; Protein Folding ; Stress, Physiological/genetics

Protein folding both promotes and constrains adaptive evolution. We uncover this surprising duality in the role of the protein-folding chaperone heat shock protein 90 (Hsp90) in maintaining the integrity of yeast metabolism amid proteotoxic stressors within industrial domestication niches. Ethanol disrupts critical Hsp90-dependent metabolic pathways and exerts strong selective pressure for redundant duplications of key genes within these pathways, yielding the classical genomic signatures of beer and bread domestication. This work demonstrates a mechanism of adaptive canalization in an ecology of major economic importance and highlights Hsp90-dependent variation as an important source of phantom heritability in complex traits.

Update of: bioRxiv. 2023 Jul 21:2023.07.21.547572. doi: 10.1101/2023.07.21.547572.. (PMID: 37745611)

Front Microbiol. 2018 Feb 22;9:288. (PMID: 29520259)
Yeast. 2002 Sep 15;19(12):1015-27. (PMID: 12210897)
J Agric Food Chem. 2014 Sep 24;62(38):9326-35. (PMID: 25174613)
Nat Commun. 2018 Mar 20;9(1):965. (PMID: 29559655)
Proc Natl Acad Sci U S A. 2002 Aug 6;99(16):10528-32. (PMID: 12082173)
Mol Cell Biol. 1995 Jul;15(7):3917-25. (PMID: 7791797)
Nat Commun. 2018 Jul 12;9(1):2690. (PMID: 30002370)
G3 (Bethesda). 2017 May 5;7(5):1475-1485. (PMID: 28292787)
Biol Direct. 2009 Nov 11;4:42. (PMID: 19906303)
Nat Rev Cancer. 2005 Oct;5(10):761-72. (PMID: 16175177)
Genes Dev. 2008 Nov 1;22(21):3064-75. (PMID: 18981482)
PLoS Genet. 2007 Jun;3(6):e93. (PMID: 17571922)
Genome Res. 2012 May;22(5):908-24. (PMID: 22369888)
Mol Biol Evol. 2022 Jun 2;39(6):. (PMID: 35234895)
Evolution. 1997 Apr;51(2):329-347. (PMID: 28565347)
Evolution. 2003 Sep;57(9):1959-72. (PMID: 14575319)
J Biol Chem. 2003 Nov 28;278(48):47441-8. (PMID: 14500708)
Nat Rev Genet. 2019 Jan;20(1):24-38. (PMID: 30385867)
Integr Comp Biol. 2022 Feb 5;61(6):2163-2179. (PMID: 34427654)
Nat Ecol Evol. 2022 Apr;6(4):448-460. (PMID: 35210580)
Annu Rev Cancer Biol. 2017 Mar;1:119-140. (PMID: 29399660)
Addiction. 2017 Jun;112(6):968-1001. (PMID: 28220587)
Nature. 2003 Jul 31;424(6948):549-52. (PMID: 12891357)
Proc Natl Acad Sci U S A. 2008 Feb 26;105(8):2969-74. (PMID: 18287064)
FEMS Microbiol Rev. 2007 Sep;31(5):535-69. (PMID: 17645521)
Proc Biol Sci. 2017 Aug 30;284(1861):. (PMID: 28835561)
Genetics. 1989 Jun;122(2):307-16. (PMID: 2548922)
BMC Evol Biol. 2008 Aug 11;8:231. (PMID: 18694497)
J Cell Biol. 2018 Nov 5;217(11):3809-3816. (PMID: 30131327)
Proc Natl Acad Sci U S A. 1993 Aug 1;90(15):7074-8. (PMID: 7688470)
Nat Genet. 2006 Aug;38(8):896-903. (PMID: 16845399)
Genetics. 2022 Nov 30;222(4):. (PMID: 36227141)
Genetics. 2008 May;179(1):331-43. (PMID: 18458105)
Nat Biotechnol. 1997 Dec;15(13):1351-7. (PMID: 9415886)
Genome Biol Evol. 2010;2:602-8. (PMID: 20660111)
Curr Biol. 2021 Feb 22;31(4):722-732.e5. (PMID: 33301710)
Nature. 1998 Nov 26;396(6709):336-42. (PMID: 9845070)
Proc Natl Acad Sci U S A. 2014 Dec 23;111(51):18297-302. (PMID: 25489079)
Nature. 1959 Jun 13;183(4676):1654-5. (PMID: 13666847)
Curr Biol. 2010 May 25;20(10):895-903. (PMID: 20471265)
Appl Microbiol. 1973 Sep;26(3):349-53. (PMID: 16349967)
Genome Biol Evol. 2016 Jun 03;8(5):1590-9. (PMID: 27189986)
Curr Genet. 2019 Dec;65(6):1287-1295. (PMID: 31076843)
Cell. 2017 Feb 23;168(5):856-866.e12. (PMID: 28215707)
Evolution. 1994 Oct;48(5):1478-1486. (PMID: 28568416)
Microb Cell Fact. 2011 Jan 28;10:4. (PMID: 21276210)
JAMA. 2003 Dec 10;290(22):2996-9. (PMID: 14665662)
Mol Syst Biol. 2015 Jan 21;11(1):773. (PMID: 25609648)
PLoS Genet. 2007 Mar 30;3(3):e43. (PMID: 17397257)
Nature. 2011 Dec 07;480(7376):250-3. (PMID: 22158248)
Nat Genet. 2005 Dec;37(12):1376-9. (PMID: 16273106)
Nat Commun. 2022 Oct 21;13(1):6271. (PMID: 36270993)
Semin Cell Dev Biol. 2019 Apr;88:21-35. (PMID: 29807130)
FEMS Yeast Res. 2015 May;15(3):. (PMID: 25725024)
Nat Rev Genet. 2004 Nov;5(11):826-37. (PMID: 15520792)
Genome Res. 2014 Nov;24(11):1830-41. (PMID: 25149527)
Science. 2005 Sep 30;309(5744):2185-9. (PMID: 16195452)
Curr Biol. 2019 May 20;29(10):R381-R393. (PMID: 31112692)
PLoS Biol. 2008 Nov 4;6(11):e264. (PMID: 18986213)
Crit Rev Food Sci Nutr. 2023;63(15):2447-2479. (PMID: 34523363)
Bioessays. 1997 Mar;19(3):257-62. (PMID: 9080776)
Nat Rev Genet. 2015 Aug;16(8):483-96. (PMID: 26184598)
PLoS Biol. 2005 Nov;3(11):e381. (PMID: 16248678)
Cell. 2004 Sep 17;118(6):675-85. (PMID: 15369668)
Semin Cell Dev Biol. 2019 Apr;88:67-79. (PMID: 29782925)
Q Rev Biol. 2005 Sep;80(3):287-316. (PMID: 16250465)
Mol Cell Biol. 1989 Sep;9(9):3919-30. (PMID: 2674684)
Mol Cell Biol. 2016 Apr 15;36(9):1412-24. (PMID: 26951197)
J Appl Microbiol. 2010 Jul;109(1):248-59. (PMID: 20070441)
PLoS Genet. 2013;9(8):e1003733. (PMID: 23990806)
Front Genet. 2020 Nov 11;11:584718. (PMID: 33262788)
Genome Biol Evol. 2016 Oct 5;8(9):2979-2991. (PMID: 27497316)
Bioessays. 2005 Feb;27(2):176-88. (PMID: 15666345)
PLoS Biol. 2012;10(12):e1001446. (PMID: 23239941)
Nature. 2002 Jun 6;417(6889):618-24. (PMID: 12050657)
Nature. 2002 May 23;417(6887):398. (PMID: 12024205)
Science. 2012 Jan 6;335(6064):82-5. (PMID: 22174126)
Cells. 2019 Jun 03;8(6):. (PMID: 31163702)
Proc Natl Acad Sci U S A. 2007 Feb 13;104(7):2307-12. (PMID: 17284612)
Proc Natl Acad Sci U S A. 2002 Aug 6;99(16):10229-30. (PMID: 12149521)
Nature. 1997 Jul 10;388(6638):167-71. (PMID: 9217155)
Cell. 2016 Sep 8;166(6):1397-1410.e16. (PMID: 27610566)
Nat Rev Genet. 2011 Mar;12(3):204-13. (PMID: 21331091)
Bioessays. 2000 Apr;22(4):372-80. (PMID: 10723034)
Annu Rev Genet. 2020 Nov 23;54:189-211. (PMID: 32867542)
Nat Commun. 2020 Jul 21;11(1):3664. (PMID: 32694532)
Science. 2013 Dec 13;342(6164):1372-5. (PMID: 24337296)
J Bacteriol. 1984 Mar;157(3):949-52. (PMID: 6321448)
Science. 2010 Dec 24;330(6012):1820-4. (PMID: 21205668)
J Exp Zool. 2000 Oct 15;288(3):242-83. (PMID: 11069142)
Curr Biol. 2016 Oct 24;26(20):2750-2761. (PMID: 27720622)
Front Microbiol. 2014 Feb 05;5:35. (PMID: 24550904)
Genes (Basel). 2022 Jan 26;13(2):. (PMID: 35205274)
Curr Protoc Microbiol. 2019 Sep;54(1):e91. (PMID: 31518063)

K22 CA222938 United States CA NCI NIH HHS; P30 CA125123 United States CA NCI NIH HHS; S10 RR024574 United States RR NCRR NIH HHS

3K9958V90M (Ethanol)
0 (HSP82 protein, S cerevisiae)
0 (HSP90 Heat-Shock Proteins)
0 (Saccharomyces cerevisiae Proteins)

Date Created: 20240725 Date Completed: 20240725 Latest Revision: 20250416

20250417

PMC11410103

10.1126/science.adi3048

39052788