Independent Evolution of Winner Traits without Whole Genome Duplication in Dekkera Yeasts
Dekkera yeasts have often been considered as alternative sources of ethanol production that could compete with S. cerevisiae. The two lineages of yeasts independently evolved traits that include high glucose and ethanol tolerance, aerobic fermentation, and a rapid ethanol fermentation rate. The Sacc...
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| description | Dekkera yeasts have often been considered as alternative sources of ethanol production that could compete with S. cerevisiae. The two lineages of yeasts independently evolved traits that include high glucose and ethanol tolerance, aerobic fermentation, and a rapid ethanol fermentation rate. The Saccharomyces yeasts attained these traits mainly through whole genome duplication approximately 100 million years ago (Mya). However, the Dekkera yeasts, which were separated from S. cerevisiae approximately 200 Mya, did not undergo whole genome duplication (WGD) but still occupy a niche similar to S. cerevisiae. Upon analysis of two Dekkera yeasts and five closely related non-WGD yeasts, we found that a massive loss of cis-regulatory elements occurred in an ancestor of the Dekkera yeasts, which led to improved mitochondrial functions similar to the S. cerevisiae yeasts. The evolutionary analysis indicated that genes involved in the transcription and translation process exhibited faster evolution in the Dekkera yeasts. We detected 90 positively selected genes, suggesting that the Dekkera yeasts evolved an efficient translation system to facilitate adaptive evolution. Moreover, we identified that 12 vacuolar H+-ATPase (V-ATPase) function genes that were under positive selection, which assists in developing tolerance to high alcohol and high sugar stress. We also revealed that the enzyme PGK1 is responsible for the increased rate of glycolysis in the Dekkera yeasts. These results provide important insights to understand the independent adaptive evolution of the Dekkera yeasts and provide tools for genetic modification promoting industrial usage. |
| doi_str_mv | 10.1371/journal.pone.0155140 |
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The two lineages of yeasts independently evolved traits that include high glucose and ethanol tolerance, aerobic fermentation, and a rapid ethanol fermentation rate. The Saccharomyces yeasts attained these traits mainly through whole genome duplication approximately 100 million years ago (Mya). However, the Dekkera yeasts, which were separated from S. cerevisiae approximately 200 Mya, did not undergo whole genome duplication (WGD) but still occupy a niche similar to S. cerevisiae. Upon analysis of two Dekkera yeasts and five closely related non-WGD yeasts, we found that a massive loss of cis-regulatory elements occurred in an ancestor of the Dekkera yeasts, which led to improved mitochondrial functions similar to the S. cerevisiae yeasts. The evolutionary analysis indicated that genes involved in the transcription and translation process exhibited faster evolution in the Dekkera yeasts. We detected 90 positively selected genes, suggesting that the Dekkera yeasts evolved an efficient translation system to facilitate adaptive evolution. Moreover, we identified that 12 vacuolar H+-ATPase (V-ATPase) function genes that were under positive selection, which assists in developing tolerance to high alcohol and high sugar stress. We also revealed that the enzyme PGK1 is responsible for the increased rate of glycolysis in the Dekkera yeasts. These results provide important insights to understand the independent adaptive evolution of the Dekkera yeasts and provide tools for genetic modification promoting industrial usage.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0155140</identifier><identifier>PMID: 27152421</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Adaptive systems ; Adenosine triphosphatase ; Alcohols ; Amino Acid Sequence ; Analysis ; Biological Evolution ; Biology and Life Sciences ; Dekkera ; Dekkera anomala ; Ethanol ; Evolution ; Evolutionary genetics ; Fermentation ; Fungal Proteins - chemistry ; Gene expression ; Genes ; Genetic aspects ; Genetic modification ; Genetically modified organisms ; Genetics ; Genome, Fungal ; Genomes ; Glucose tolerance ; Glycolysis ; H+-transporting ATPase ; Industrial applications ; Kinases ; Laboratories ; Mitochondria ; Molecular biology ; Ontology ; Physical Sciences ; Positive selection ; Proteins ; Regulatory sequences ; Reproduction (copying) ; Research and Analysis Methods ; Respiration ; Saccharomyces ; Saccharomyces cerevisiae ; Selection, Genetic ; Sequence Homology, Amino Acid ; Sugar ; Transcription ; Transcription (Genetics) ; Translation systems ; Yeast ; Yeasts ; Yeasts - genetics ; Zoology</subject><ispartof>PloS one, 2016-05, Vol.11 (5), p.e0155140-e0155140</ispartof><rights>COPYRIGHT 2016 Public Library of Science</rights><rights>2016 Guo et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2016 Guo et al 2016 Guo et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c725t-3b9c85ec4b545dd0c090aa506c8612ec618f4b3273850b23cd5f4d18d9d5918b3</citedby><cites>FETCH-LOGICAL-c725t-3b9c85ec4b545dd0c090aa506c8612ec618f4b3273850b23cd5f4d18d9d5918b3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4859550/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4859550/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79343,79344</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27152421$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Guo, Yi-Cheng</creatorcontrib><creatorcontrib>Zhang, Lin</creatorcontrib><creatorcontrib>Dai, Shao-Xing</creatorcontrib><creatorcontrib>Li, Wen-Xing</creatorcontrib><creatorcontrib>Zheng, Jun-Juan</creatorcontrib><creatorcontrib>Li, Gong-Hua</creatorcontrib><creatorcontrib>Huang, Jing-Fei</creatorcontrib><title>Independent Evolution of Winner Traits without Whole Genome Duplication in Dekkera Yeasts</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Dekkera yeasts have often been considered as alternative sources of ethanol production that could compete with S. cerevisiae. The two lineages of yeasts independently evolved traits that include high glucose and ethanol tolerance, aerobic fermentation, and a rapid ethanol fermentation rate. The Saccharomyces yeasts attained these traits mainly through whole genome duplication approximately 100 million years ago (Mya). However, the Dekkera yeasts, which were separated from S. cerevisiae approximately 200 Mya, did not undergo whole genome duplication (WGD) but still occupy a niche similar to S. cerevisiae. Upon analysis of two Dekkera yeasts and five closely related non-WGD yeasts, we found that a massive loss of cis-regulatory elements occurred in an ancestor of the Dekkera yeasts, which led to improved mitochondrial functions similar to the S. cerevisiae yeasts. The evolutionary analysis indicated that genes involved in the transcription and translation process exhibited faster evolution in the Dekkera yeasts. We detected 90 positively selected genes, suggesting that the Dekkera yeasts evolved an efficient translation system to facilitate adaptive evolution. Moreover, we identified that 12 vacuolar H+-ATPase (V-ATPase) function genes that were under positive selection, which assists in developing tolerance to high alcohol and high sugar stress. We also revealed that the enzyme PGK1 is responsible for the increased rate of glycolysis in the Dekkera yeasts. These results provide important insights to understand the independent adaptive evolution of the Dekkera yeasts and provide tools for genetic modification promoting industrial usage.</description><subject>Adaptive systems</subject><subject>Adenosine triphosphatase</subject><subject>Alcohols</subject><subject>Amino Acid Sequence</subject><subject>Analysis</subject><subject>Biological Evolution</subject><subject>Biology and Life Sciences</subject><subject>Dekkera</subject><subject>Dekkera anomala</subject><subject>Ethanol</subject><subject>Evolution</subject><subject>Evolutionary genetics</subject><subject>Fermentation</subject><subject>Fungal Proteins - chemistry</subject><subject>Gene expression</subject><subject>Genes</subject><subject>Genetic aspects</subject><subject>Genetic modification</subject><subject>Genetically modified organisms</subject><subject>Genetics</subject><subject>Genome, Fungal</subject><subject>Genomes</subject><subject>Glucose tolerance</subject><subject>Glycolysis</subject><subject>H+-transporting ATPase</subject><subject>Industrial applications</subject><subject>Kinases</subject><subject>Laboratories</subject><subject>Mitochondria</subject><subject>Molecular biology</subject><subject>Ontology</subject><subject>Physical Sciences</subject><subject>Positive selection</subject><subject>Proteins</subject><subject>Regulatory sequences</subject><subject>Reproduction (copying)</subject><subject>Research and Analysis Methods</subject><subject>Respiration</subject><subject>Saccharomyces</subject><subject>Saccharomyces cerevisiae</subject><subject>Selection, Genetic</subject><subject>Sequence Homology, Amino Acid</subject><subject>Sugar</subject><subject>Transcription</subject><subject>Transcription (Genetics)</subject><subject>Translation systems</subject><subject>Yeast</subject><subject>Yeasts</subject><subject>Yeasts - 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The two lineages of yeasts independently evolved traits that include high glucose and ethanol tolerance, aerobic fermentation, and a rapid ethanol fermentation rate. The Saccharomyces yeasts attained these traits mainly through whole genome duplication approximately 100 million years ago (Mya). However, the Dekkera yeasts, which were separated from S. cerevisiae approximately 200 Mya, did not undergo whole genome duplication (WGD) but still occupy a niche similar to S. cerevisiae. Upon analysis of two Dekkera yeasts and five closely related non-WGD yeasts, we found that a massive loss of cis-regulatory elements occurred in an ancestor of the Dekkera yeasts, which led to improved mitochondrial functions similar to the S. cerevisiae yeasts. The evolutionary analysis indicated that genes involved in the transcription and translation process exhibited faster evolution in the Dekkera yeasts. We detected 90 positively selected genes, suggesting that the Dekkera yeasts evolved an efficient translation system to facilitate adaptive evolution. Moreover, we identified that 12 vacuolar H+-ATPase (V-ATPase) function genes that were under positive selection, which assists in developing tolerance to high alcohol and high sugar stress. We also revealed that the enzyme PGK1 is responsible for the increased rate of glycolysis in the Dekkera yeasts. These results provide important insights to understand the independent adaptive evolution of the Dekkera yeasts and provide tools for genetic modification promoting industrial usage.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>27152421</pmid><doi>10.1371/journal.pone.0155140</doi><oa>free_for_read</oa></addata></record> |
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| source | MEDLINE; DOAJ Directory of Open Access Journals; EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry; Public Library of Science (PLoS) Journals Open Acc |
| subjects | Adaptive systems Adenosine triphosphatase Alcohols Amino Acid Sequence Analysis Biological Evolution Biology and Life Sciences Dekkera Dekkera anomala Ethanol Evolution Evolutionary genetics Fermentation Fungal Proteins - chemistry Gene expression Genes Genetic aspects Genetic modification Genetically modified organisms Genetics Genome, Fungal Genomes Glucose tolerance Glycolysis H+-transporting ATPase Industrial applications Kinases Laboratories Mitochondria Molecular biology Ontology Physical Sciences Positive selection Proteins Regulatory sequences Reproduction (copying) Research and Analysis Methods Respiration Saccharomyces Saccharomyces cerevisiae Selection, Genetic Sequence Homology, Amino Acid Sugar Transcription Transcription (Genetics) Translation systems Yeast Yeasts Yeasts - genetics Zoology |
| title | Independent Evolution of Winner Traits without Whole Genome Duplication in Dekkera Yeasts |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-01T15%3A34%3A11IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Independent%20Evolution%20of%20Winner%20Traits%20without%20Whole%20Genome%20Duplication%20in%20Dekkera%20Yeasts&rft.jtitle=PloS%20one&rft.au=Guo,%20Yi-Cheng&rft.date=2016-05-06&rft.volume=11&rft.issue=5&rft.spage=e0155140&rft.epage=e0155140&rft.pages=e0155140-e0155140&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0155140&rft_dat=%3Cgale_plos_%3EA453370578%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1787256556&rft_id=info:pmid/27152421&rft_galeid=A453370578&rft_doaj_id=oai_doaj_org_article_a6d671d9b3d442c18d8d95b8bc90be9c&rfr_iscdi=true |