Loading…
Restoring fertility in yeast hybrids: Breeding and quantitative genetics of beneficial traits
Hybrids between species can harbor a combination of beneficial traits from each parent and may exhibit hybrid vigor, more readily adapting to new harsher environments. Interspecies hybrids are also sterile and therefore an evolutionary dead end unless fertility is restored, usually via auto-polyploi...
Saved in:
Published in: | Proceedings of the National Academy of Sciences - PNAS 2021-09, Vol.118 (38), p.1-12 |
---|---|
Main Authors: | , , , , , , , , |
Format: | Article |
Language: | English |
Subjects: | |
Citations: | Items that this one cites Items that cite this one |
Online Access: | Get full text |
Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
cited_by | cdi_FETCH-LOGICAL-c443t-e2cab6dc4340f4474e6d63b9c02708f3cd2d08a155329a8a5cb57ab369401f623 |
---|---|
cites | cdi_FETCH-LOGICAL-c443t-e2cab6dc4340f4474e6d63b9c02708f3cd2d08a155329a8a5cb57ab369401f623 |
container_end_page | 12 |
container_issue | 38 |
container_start_page | 1 |
container_title | Proceedings of the National Academy of Sciences - PNAS |
container_volume | 118 |
creator | Naseeb, Samina Visinoni, Federico Hu, Yue Roberts, Alex J. Hinks Maslowska, Agnieszka Walsh, Thomas Smart, Katherine A. Louis, Edward J. Delneri, Daniela |
description | Hybrids between species can harbor a combination of beneficial traits from each parent and may exhibit hybrid vigor, more readily adapting to new harsher environments. Interspecies hybrids are also sterile and therefore an evolutionary dead end unless fertility is restored, usually via auto-polyploidisation events. In the Saccharomyces genus, hybrids are readily found in nature and in industrial settings, where they have adapted to severe fermentative conditions. Due to their hybrid sterility, the development of new commercial yeast strains has so far been primarily conducted via selection methods rather than via further breeding. In this study, we overcame infertility by creating tetraploid intermediates of Saccharomyces interspecies hybrids to allow continuous multigenerational breeding. We incorporated nuclear and mitochondrial genetic diversity within each parental species, allowing for quantitative genetic analysis of traits exhibited by the hybrids and for nuclear–mitochondrial interactions to be assessed. Using pooled F12 generation segregants of different hybrids with extreme phenotype distributions, we identified quantitative trait loci (QTLs) for tolerance to high and low temperatures, high sugar concentration, high ethanol concentration, and acetic acid levels. We identified QTLs that are species specific, that are shared between species, as well as hybrid specific, in which the variants do not exhibit phenotypic differences in the original parental species. Moreover, we could distinguish between mitochondria-type–dependent and – independent traits. This study tackles the complexity of the genetic interactions and traits in hybrid species, bringing hybrids into the realm of full genetic analysis of diploid species, and paves the road for the biotechnological exploitation of yeast biodiversity. |
doi_str_mv | 10.1073/pnas.2101242118 |
format | article |
fullrecord | <record><control><sourceid>jstor_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_8463882</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><jstor_id>27075657</jstor_id><sourcerecordid>27075657</sourcerecordid><originalsourceid>FETCH-LOGICAL-c443t-e2cab6dc4340f4474e6d63b9c02708f3cd2d08a155329a8a5cb57ab369401f623</originalsourceid><addsrcrecordid>eNpVkF1LwzAUhoMobk6vvVIKetvt5LPpjSDDLxgIotchTdMtY2tn0gn996ZsTr3KxXnOm_c8CF1iGGPI6GRT6zAmGDBhBGN5hIYYcpwKlsMxGgKQLJWMsAE6C2EJADmXcIoGlHEsCZZDdPtmQ9t4V8-TyvrWrVzbJa5OOqtDmyy6wrsynKOTSq-Cvdi_I_Tx-PA-fU5nr08v0_tZahijbWqJ0YUoDaMMKsYyZkUpaJGbWANkRU1JSpAac05JrqXmpuCZLqjIGeBKEDpCd7vczbZY29LYuvV6pTberbXvVKOd-j-p3ULNmy8lmaBS9gE3-wDffG7jZWrZbH0dOyvCM0FFFk1FarKjjG9C8LY6_IBB9VpVr1X9ao0b13-LHfgfjxG42gHL3uZhHu_OuOAZ_QYQDXzD</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2576367012</pqid></control><display><type>article</type><title>Restoring fertility in yeast hybrids: Breeding and quantitative genetics of beneficial traits</title><source>Open Access: PubMed Central</source><source>JSTOR Archival Journals and Primary Sources Collection</source><creator>Naseeb, Samina ; Visinoni, Federico ; Hu, Yue ; Roberts, Alex J. Hinks ; Maslowska, Agnieszka ; Walsh, Thomas ; Smart, Katherine A. ; Louis, Edward J. ; Delneri, Daniela</creator><creatorcontrib>Naseeb, Samina ; Visinoni, Federico ; Hu, Yue ; Roberts, Alex J. Hinks ; Maslowska, Agnieszka ; Walsh, Thomas ; Smart, Katherine A. ; Louis, Edward J. ; Delneri, Daniela</creatorcontrib><description>Hybrids between species can harbor a combination of beneficial traits from each parent and may exhibit hybrid vigor, more readily adapting to new harsher environments. Interspecies hybrids are also sterile and therefore an evolutionary dead end unless fertility is restored, usually via auto-polyploidisation events. In the Saccharomyces genus, hybrids are readily found in nature and in industrial settings, where they have adapted to severe fermentative conditions. Due to their hybrid sterility, the development of new commercial yeast strains has so far been primarily conducted via selection methods rather than via further breeding. In this study, we overcame infertility by creating tetraploid intermediates of Saccharomyces interspecies hybrids to allow continuous multigenerational breeding. We incorporated nuclear and mitochondrial genetic diversity within each parental species, allowing for quantitative genetic analysis of traits exhibited by the hybrids and for nuclear–mitochondrial interactions to be assessed. Using pooled F12 generation segregants of different hybrids with extreme phenotype distributions, we identified quantitative trait loci (QTLs) for tolerance to high and low temperatures, high sugar concentration, high ethanol concentration, and acetic acid levels. We identified QTLs that are species specific, that are shared between species, as well as hybrid specific, in which the variants do not exhibit phenotypic differences in the original parental species. Moreover, we could distinguish between mitochondria-type–dependent and – independent traits. This study tackles the complexity of the genetic interactions and traits in hybrid species, bringing hybrids into the realm of full genetic analysis of diploid species, and paves the road for the biotechnological exploitation of yeast biodiversity.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.2101242118</identifier><identifier>PMID: 34518218</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Acetic acid ; Acetic Acid - metabolism ; Biodiversity ; Biological Sciences ; Breeding ; Cold Temperature ; Diploids ; Ethanol ; Ethanol - metabolism ; Evolution ; Exploitation ; Fermentation - genetics ; Fertility ; Gene mapping ; Genetic analysis ; Genetic diversity ; Genetic Variation - genetics ; Genetics ; Genome, Fungal - genetics ; Hybrid vigor ; Hybrids ; Infertility ; Intermediates ; Low temperature ; Mitochondria ; Mitochondria - genetics ; Phenotype ; Phenotypes ; Quantitative genetics ; Quantitative trait loci ; Quantitative Trait Loci - genetics ; Saccharomyces ; Saccharomyces - genetics ; Species ; Species diversity ; Sterility ; Sugars - metabolism ; Yeast ; Yeasts</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2021-09, Vol.118 (38), p.1-12</ispartof><rights>Copyright © 2021 the Author(s). Published by PNAS.</rights><rights>Copyright National Academy of Sciences Sep 21, 2021</rights><rights>Copyright © 2021 the Author(s). Published by PNAS. 2021</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c443t-e2cab6dc4340f4474e6d63b9c02708f3cd2d08a155329a8a5cb57ab369401f623</citedby><cites>FETCH-LOGICAL-c443t-e2cab6dc4340f4474e6d63b9c02708f3cd2d08a155329a8a5cb57ab369401f623</cites><orcidid>0000-0001-9840-7017 ; 0000-0003-1157-3608 ; 0000-0003-3599-5813 ; 0000-0001-8070-411X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/27075657$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/27075657$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,53791,53793,58238,58471</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34518218$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Naseeb, Samina</creatorcontrib><creatorcontrib>Visinoni, Federico</creatorcontrib><creatorcontrib>Hu, Yue</creatorcontrib><creatorcontrib>Roberts, Alex J. Hinks</creatorcontrib><creatorcontrib>Maslowska, Agnieszka</creatorcontrib><creatorcontrib>Walsh, Thomas</creatorcontrib><creatorcontrib>Smart, Katherine A.</creatorcontrib><creatorcontrib>Louis, Edward J.</creatorcontrib><creatorcontrib>Delneri, Daniela</creatorcontrib><title>Restoring fertility in yeast hybrids: Breeding and quantitative genetics of beneficial traits</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>Hybrids between species can harbor a combination of beneficial traits from each parent and may exhibit hybrid vigor, more readily adapting to new harsher environments. Interspecies hybrids are also sterile and therefore an evolutionary dead end unless fertility is restored, usually via auto-polyploidisation events. In the Saccharomyces genus, hybrids are readily found in nature and in industrial settings, where they have adapted to severe fermentative conditions. Due to their hybrid sterility, the development of new commercial yeast strains has so far been primarily conducted via selection methods rather than via further breeding. In this study, we overcame infertility by creating tetraploid intermediates of Saccharomyces interspecies hybrids to allow continuous multigenerational breeding. We incorporated nuclear and mitochondrial genetic diversity within each parental species, allowing for quantitative genetic analysis of traits exhibited by the hybrids and for nuclear–mitochondrial interactions to be assessed. Using pooled F12 generation segregants of different hybrids with extreme phenotype distributions, we identified quantitative trait loci (QTLs) for tolerance to high and low temperatures, high sugar concentration, high ethanol concentration, and acetic acid levels. We identified QTLs that are species specific, that are shared between species, as well as hybrid specific, in which the variants do not exhibit phenotypic differences in the original parental species. Moreover, we could distinguish between mitochondria-type–dependent and – independent traits. This study tackles the complexity of the genetic interactions and traits in hybrid species, bringing hybrids into the realm of full genetic analysis of diploid species, and paves the road for the biotechnological exploitation of yeast biodiversity.</description><subject>Acetic acid</subject><subject>Acetic Acid - metabolism</subject><subject>Biodiversity</subject><subject>Biological Sciences</subject><subject>Breeding</subject><subject>Cold Temperature</subject><subject>Diploids</subject><subject>Ethanol</subject><subject>Ethanol - metabolism</subject><subject>Evolution</subject><subject>Exploitation</subject><subject>Fermentation - genetics</subject><subject>Fertility</subject><subject>Gene mapping</subject><subject>Genetic analysis</subject><subject>Genetic diversity</subject><subject>Genetic Variation - genetics</subject><subject>Genetics</subject><subject>Genome, Fungal - genetics</subject><subject>Hybrid vigor</subject><subject>Hybrids</subject><subject>Infertility</subject><subject>Intermediates</subject><subject>Low temperature</subject><subject>Mitochondria</subject><subject>Mitochondria - genetics</subject><subject>Phenotype</subject><subject>Phenotypes</subject><subject>Quantitative genetics</subject><subject>Quantitative trait loci</subject><subject>Quantitative Trait Loci - genetics</subject><subject>Saccharomyces</subject><subject>Saccharomyces - genetics</subject><subject>Species</subject><subject>Species diversity</subject><subject>Sterility</subject><subject>Sugars - metabolism</subject><subject>Yeast</subject><subject>Yeasts</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><recordid>eNpVkF1LwzAUhoMobk6vvVIKetvt5LPpjSDDLxgIotchTdMtY2tn0gn996ZsTr3KxXnOm_c8CF1iGGPI6GRT6zAmGDBhBGN5hIYYcpwKlsMxGgKQLJWMsAE6C2EJADmXcIoGlHEsCZZDdPtmQ9t4V8-TyvrWrVzbJa5OOqtDmyy6wrsynKOTSq-Cvdi_I_Tx-PA-fU5nr08v0_tZahijbWqJ0YUoDaMMKsYyZkUpaJGbWANkRU1JSpAac05JrqXmpuCZLqjIGeBKEDpCd7vczbZY29LYuvV6pTberbXvVKOd-j-p3ULNmy8lmaBS9gE3-wDffG7jZWrZbH0dOyvCM0FFFk1FarKjjG9C8LY6_IBB9VpVr1X9ao0b13-LHfgfjxG42gHL3uZhHu_OuOAZ_QYQDXzD</recordid><startdate>20210921</startdate><enddate>20210921</enddate><creator>Naseeb, Samina</creator><creator>Visinoni, Federico</creator><creator>Hu, Yue</creator><creator>Roberts, Alex J. Hinks</creator><creator>Maslowska, Agnieszka</creator><creator>Walsh, Thomas</creator><creator>Smart, Katherine A.</creator><creator>Louis, Edward J.</creator><creator>Delneri, Daniela</creator><general>National Academy of Sciences</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-9840-7017</orcidid><orcidid>https://orcid.org/0000-0003-1157-3608</orcidid><orcidid>https://orcid.org/0000-0003-3599-5813</orcidid><orcidid>https://orcid.org/0000-0001-8070-411X</orcidid></search><sort><creationdate>20210921</creationdate><title>Restoring fertility in yeast hybrids</title><author>Naseeb, Samina ; Visinoni, Federico ; Hu, Yue ; Roberts, Alex J. Hinks ; Maslowska, Agnieszka ; Walsh, Thomas ; Smart, Katherine A. ; Louis, Edward J. ; Delneri, Daniela</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c443t-e2cab6dc4340f4474e6d63b9c02708f3cd2d08a155329a8a5cb57ab369401f623</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Acetic acid</topic><topic>Acetic Acid - metabolism</topic><topic>Biodiversity</topic><topic>Biological Sciences</topic><topic>Breeding</topic><topic>Cold Temperature</topic><topic>Diploids</topic><topic>Ethanol</topic><topic>Ethanol - metabolism</topic><topic>Evolution</topic><topic>Exploitation</topic><topic>Fermentation - genetics</topic><topic>Fertility</topic><topic>Gene mapping</topic><topic>Genetic analysis</topic><topic>Genetic diversity</topic><topic>Genetic Variation - genetics</topic><topic>Genetics</topic><topic>Genome, Fungal - genetics</topic><topic>Hybrid vigor</topic><topic>Hybrids</topic><topic>Infertility</topic><topic>Intermediates</topic><topic>Low temperature</topic><topic>Mitochondria</topic><topic>Mitochondria - genetics</topic><topic>Phenotype</topic><topic>Phenotypes</topic><topic>Quantitative genetics</topic><topic>Quantitative trait loci</topic><topic>Quantitative Trait Loci - genetics</topic><topic>Saccharomyces</topic><topic>Saccharomyces - genetics</topic><topic>Species</topic><topic>Species diversity</topic><topic>Sterility</topic><topic>Sugars - metabolism</topic><topic>Yeast</topic><topic>Yeasts</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Naseeb, Samina</creatorcontrib><creatorcontrib>Visinoni, Federico</creatorcontrib><creatorcontrib>Hu, Yue</creatorcontrib><creatorcontrib>Roberts, Alex J. Hinks</creatorcontrib><creatorcontrib>Maslowska, Agnieszka</creatorcontrib><creatorcontrib>Walsh, Thomas</creatorcontrib><creatorcontrib>Smart, Katherine A.</creatorcontrib><creatorcontrib>Louis, Edward J.</creatorcontrib><creatorcontrib>Delneri, Daniela</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Naseeb, Samina</au><au>Visinoni, Federico</au><au>Hu, Yue</au><au>Roberts, Alex J. Hinks</au><au>Maslowska, Agnieszka</au><au>Walsh, Thomas</au><au>Smart, Katherine A.</au><au>Louis, Edward J.</au><au>Delneri, Daniela</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Restoring fertility in yeast hybrids: Breeding and quantitative genetics of beneficial traits</atitle><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle><addtitle>Proc Natl Acad Sci U S A</addtitle><date>2021-09-21</date><risdate>2021</risdate><volume>118</volume><issue>38</issue><spage>1</spage><epage>12</epage><pages>1-12</pages><issn>0027-8424</issn><eissn>1091-6490</eissn><abstract>Hybrids between species can harbor a combination of beneficial traits from each parent and may exhibit hybrid vigor, more readily adapting to new harsher environments. Interspecies hybrids are also sterile and therefore an evolutionary dead end unless fertility is restored, usually via auto-polyploidisation events. In the Saccharomyces genus, hybrids are readily found in nature and in industrial settings, where they have adapted to severe fermentative conditions. Due to their hybrid sterility, the development of new commercial yeast strains has so far been primarily conducted via selection methods rather than via further breeding. In this study, we overcame infertility by creating tetraploid intermediates of Saccharomyces interspecies hybrids to allow continuous multigenerational breeding. We incorporated nuclear and mitochondrial genetic diversity within each parental species, allowing for quantitative genetic analysis of traits exhibited by the hybrids and for nuclear–mitochondrial interactions to be assessed. Using pooled F12 generation segregants of different hybrids with extreme phenotype distributions, we identified quantitative trait loci (QTLs) for tolerance to high and low temperatures, high sugar concentration, high ethanol concentration, and acetic acid levels. We identified QTLs that are species specific, that are shared between species, as well as hybrid specific, in which the variants do not exhibit phenotypic differences in the original parental species. Moreover, we could distinguish between mitochondria-type–dependent and – independent traits. This study tackles the complexity of the genetic interactions and traits in hybrid species, bringing hybrids into the realm of full genetic analysis of diploid species, and paves the road for the biotechnological exploitation of yeast biodiversity.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>34518218</pmid><doi>10.1073/pnas.2101242118</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0001-9840-7017</orcidid><orcidid>https://orcid.org/0000-0003-1157-3608</orcidid><orcidid>https://orcid.org/0000-0003-3599-5813</orcidid><orcidid>https://orcid.org/0000-0001-8070-411X</orcidid><oa>free_for_read</oa></addata></record> |
fulltext | fulltext |
identifier | ISSN: 0027-8424 |
ispartof | Proceedings of the National Academy of Sciences - PNAS, 2021-09, Vol.118 (38), p.1-12 |
issn | 0027-8424 1091-6490 |
language | eng |
recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_8463882 |
source | Open Access: PubMed Central; JSTOR Archival Journals and Primary Sources Collection |
subjects | Acetic acid Acetic Acid - metabolism Biodiversity Biological Sciences Breeding Cold Temperature Diploids Ethanol Ethanol - metabolism Evolution Exploitation Fermentation - genetics Fertility Gene mapping Genetic analysis Genetic diversity Genetic Variation - genetics Genetics Genome, Fungal - genetics Hybrid vigor Hybrids Infertility Intermediates Low temperature Mitochondria Mitochondria - genetics Phenotype Phenotypes Quantitative genetics Quantitative trait loci Quantitative Trait Loci - genetics Saccharomyces Saccharomyces - genetics Species Species diversity Sterility Sugars - metabolism Yeast Yeasts |
title | Restoring fertility in yeast hybrids: Breeding and quantitative genetics of beneficial traits |
url | http://sfxeu10.hosted.exlibrisgroup.com/loughborough?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-24T16%3A18%3A15IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-jstor_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Restoring%20fertility%20in%20yeast%20hybrids:%20Breeding%20and%20quantitative%20genetics%20of%20beneficial%20traits&rft.jtitle=Proceedings%20of%20the%20National%20Academy%20of%20Sciences%20-%20PNAS&rft.au=Naseeb,%20Samina&rft.date=2021-09-21&rft.volume=118&rft.issue=38&rft.spage=1&rft.epage=12&rft.pages=1-12&rft.issn=0027-8424&rft.eissn=1091-6490&rft_id=info:doi/10.1073/pnas.2101242118&rft_dat=%3Cjstor_pubme%3E27075657%3C/jstor_pubme%3E%3Cgrp_id%3Ecdi_FETCH-LOGICAL-c443t-e2cab6dc4340f4474e6d63b9c02708f3cd2d08a155329a8a5cb57ab369401f623%3C/grp_id%3E%3Coa%3E%3C/oa%3E%3Curl%3E%3C/url%3E&rft_id=info:oai/&rft_pqid=2576367012&rft_id=info:pmid/34518218&rft_jstor_id=27075657&rfr_iscdi=true |