Ancient Evolutionary Trade-Offs between Yeast Ploidy States
Publication Date
March 21, 2013
Journal
PLOS Genetics
Authors
Enikö Zörgö, Karolina Chwialkowska, Arne B. Gjuvsland, Elena Garré, et al
Volume
9
Issue
3
Pages
e1003388
DOI
https://dx.plos.org/10.1371/journal.pgen.1003388
Publisher URL
http://journals.plos.org/plosgenetics/article?id=10.1371%2Fjournal.pgen.1003388
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/23555297
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3605057
Europe PMC
http://europepmc.org/abstract/MED/23555297
Web of Science
000316866700060
Scopus
84875992955
Mendeley
http://www.mendeley.com/research/ancient-evolutionary-tradeoffs-between-yeast-ploidy-states
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Mendeley | Further Information

{"title"=>"Ancient Evolutionary Trade-Offs between Yeast Ploidy States", "type"=>"journal", "authors"=>[{"first_name"=>"Enikö", "last_name"=>"Zörgö", "scopus_author_id"=>"37087952600"}, {"first_name"=>"Karolina", "last_name"=>"Chwialkowska", "scopus_author_id"=>"57194481303"}, {"first_name"=>"Arne B.", "last_name"=>"Gjuvsland", "scopus_author_id"=>"15834440000"}, {"first_name"=>"Elena", "last_name"=>"Garré", "scopus_author_id"=>"25947392400"}, {"first_name"=>"Per", "last_name"=>"Sunnerhagen", "scopus_author_id"=>"6701416283"}, {"first_name"=>"Gianni", "last_name"=>"Liti", "scopus_author_id"=>"6508269095"}, {"first_name"=>"Anders", "last_name"=>"Blomberg", "scopus_author_id"=>"56348611800"}, {"first_name"=>"Stig W.", "last_name"=>"Omholt", "scopus_author_id"=>"6603707763"}, {"first_name"=>"Jonas", "last_name"=>"Warringer", "scopus_author_id"=>"6507234725"}], "year"=>2013, "source"=>"PLoS Genetics", "identifiers"=>{"doi"=>"10.1371/journal.pgen.1003388", "sgr"=>"84875992955", "issn"=>"15537390", "pui"=>"368694398", "isbn"=>"1553-7404", "pmid"=>"23555297", "scopus"=>"2-s2.0-84875992955"}, "id"=>"9dac324e-b93e-3ce8-abf3-026fde567b02", "abstract"=>"The number of chromosome sets contained within the nucleus of eukaryotic organisms is a fundamental yet evolutionarily poorly characterized genetic variable of life. Here, we mapped the impact of ploidy on the mitotic fitness of baker's yeast and its never domesticated relative Saccharomyces paradoxus across wide swaths of their natural genotypic and phenotypic space. Surprisingly, environment-specific influences of ploidy on reproduction were found to be the rule rather than the exception. These ploidy–environment interactions were well conserved across the 2 billion generations separating the two species, suggesting that they are the products of strong selection. Previous hypotheses of generalizable advantages of haploidy or diploidy in ecological contexts imposing nutrient restriction, toxin exposure, and elevated mutational loads were rejected in favor of more fine-grained models of the interplay between ecology and ploidy. On a molecular level, cell size and mating type locus composition had equal, but limited, explanatory power, each explaining 12.5%–17% of ploidy–environment interactions. The mechanism of the cell size–based superior reproductive efficiency of haploids during Li+ exposure was traced to the Li+ exporter ENA. Removal of the Ena transporters, forcing dependence on the Nha1 extrusion system, completely altered the effects of ploidy on Li+ tolerance and evoked a strong diploid superiority, demonstrating how genetic variation at a single locus can completely reverse the relative merits of haploidy and diploidy. Taken together, our findings unmasked a dynamic interplay between ploidy and ecology that was of unpredicted evolutionary importance and had multiple molecular roots.", "link"=>"http://www.mendeley.com/research/ancient-evolutionary-tradeoffs-between-yeast-ploidy-states", "reader_count"=>115, "reader_count_by_academic_status"=>{"Unspecified"=>4, "Professor > Associate Professor"=>7, "Student > Doctoral Student"=>3, "Researcher"=>30, "Student > Ph. D. Student"=>26, "Student > Postgraduate"=>6, "Student > Master"=>13, "Other"=>3, "Student > Bachelor"=>13, "Professor"=>10}, "reader_count_by_user_role"=>{"Unspecified"=>4, "Professor > Associate Professor"=>7, "Student > Doctoral Student"=>3, "Researcher"=>30, "Student > Ph. D. Student"=>26, "Student > Postgraduate"=>6, "Student > Master"=>13, "Other"=>3, "Student > Bachelor"=>13, "Professor"=>10}, "reader_count_by_subject_area"=>{"Unspecified"=>8, "Engineering"=>2, "Environmental Science"=>2, "Biochemistry, Genetics and Molecular Biology"=>18, "Mathematics"=>1, "Agricultural and Biological Sciences"=>77, "Medicine and Dentistry"=>5, "Pharmacology, Toxicology and Pharmaceutical Science"=>1, "Chemistry"=>1}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>2}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>5}, "Chemistry"=>{"Chemistry"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>77}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>18}, "Mathematics"=>{"Mathematics"=>1}, "Unspecified"=>{"Unspecified"=>8}, "Environmental Science"=>{"Environmental Science"=>2}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}}, "reader_count_by_country"=>{"Colombia"=>1, "United States"=>5, "United Kingdom"=>3, "Spain"=>1, "Canada"=>1, "Norway"=>1, "Taiwan"=>1, "Denmark"=>1, "Poland"=>1, "Italy"=>1, "Israel"=>1, "France"=>1, "Australia"=>1, "Chile"=>1}, "group_count"=>5}

CrossRef

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/993673"], "description"=>"<p>A) The mitotic fitness components lag (time to initiate proliferation), rate (population doubling time) and efficiency (total change in population density) of asexual reproduction were extracted from high density growth curves of 24 <i>S. cerevisiae</i> and 27 <i>S. paradoxus</i> strains cultivated as haploids (n = 4) and diploids (n = 2) in an array of environmental contexts. Performance was log(2) transformed and normalized to that of the universal reference strain S288c, providing relative performance measures. B) The performances of haploids and diploids were compared over all species, strains, mitotic fitness components and environments. Line indicates the 1∶1 correlation. C) The performance of haploids and diploids over all strains and environments. Note that performance is on a log(2) scale. No significant difference between the two ploidy states (FDR, α = 0.05) were found. Error bars represent SEM.</p>", "links"=>[], "tags"=>["interactions", "yeast", "haploidy", "diploidy"], "article_id"=>657052, "categories"=>["Genetics", "Microbiology", "Evolutionary Biology"], "users"=>["Enikö Zörgö", "Karolina Chwialkowska", "Arne B. Gjuvsland", "Elena Garré", "Per Sunnerhagen", "Gianni Liti", "Anders Blomberg", "Stig W. Omholt", "Jonas Warringer"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1003388.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Ploidy_8211_environment_interactions_are_the_rule_rather_than_the_exception_in_yeast_and_favor_haploidy_and_diploidy_equally_/657052", "title"=>"Ploidy–environment interactions are the rule rather than the exception in yeast and favor haploidy and diploidy equally.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-22 04:26:03"}
  • {"files"=>["https://ndownloader.figshare.com/files/993674"], "description"=>"<p>A) Fitness component measures with a significant (FDR, α = 0.05) difference in performance between haploids and diploids in <i>S. cerevisiae</i>, in <i>S. paradoxus</i> or in both species. To compare haploid and diploid asexual proliferative capacity, a mean of the log(2) relative performance of the two haploid mating types (each n = 2) was used to derive a single measure of haploid performance. This was compared to that of the diploid (n = 4), by calculating the mean difference between haploid and diploid phenotypes. Each species was treated separately. Error bars represent the SEM (n = 24 for <i>S. cerevisiae</i>, n = 27 for <i>S. paradoxus</i>). B) Left panels show pairwise Pearson correlation coefficients, based on ploidy effects over all mitotic traits, between strains belonging to the same (627 pairs) or different (648 pairs) species, the same (43 pairs) or different (233 pairs) <i>S. cerevisiae</i> population and the same (65 pairs) or different (211 pairs) <i>S. cerevisiae</i> source environment. Species, population and source environment, all have significant impact on ploidy effects (ANOVA F-test; p-values displayed, note the large sample size for the between/within species comparison, and the correspondingly low SEM), but explained only 2.5%, 9.3% and 1.8% of the overall variation in correlation coefficients (R2-adj). Right panels resolve <i>S. cerevisiae</i> populations into the Malaysian, European, African and North American populations and <i>S. cerevisiae</i> sources into Clinical, Fermentation, Lab and Wild strains. Top and bottom of boxes represent 25th and 75th quartiles, bands represent medians, whiskers show the lowest and highest data point still within 1.5 interquartile range of the lower and upper quartile respectively and filled circles represent data points outside this range.</p>", "links"=>[], "tags"=>["interactions", "conserved"], "article_id"=>657053, "categories"=>["Genetics", "Microbiology", "Evolutionary Biology"], "users"=>["Enikö Zörgö", "Karolina Chwialkowska", "Arne B. Gjuvsland", "Elena Garré", "Per Sunnerhagen", "Gianni Liti", "Anders Blomberg", "Stig W. Omholt", "Jonas Warringer"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1003388.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Ploidy_environments_interactions_are_conserved_since_before_the_S_cerevisae_and_S_paradoxus_radiation_/657053", "title"=>"Ploidy–environments interactions are conserved since before the <i>S. cerevisae</i> and <i>S. paradoxus</i> radiation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-22 04:26:17"}
  • {"files"=>["https://ndownloader.figshare.com/files/993675"], "description"=>"<p>Performance of haploid (n = 4) and diploid (n = 2) versions of individual <i>S. cerevisiae</i> (blue) and <i>S. paradoxus</i> (red) strains in DNA damage inducing environments and nitrogen restricted environments. Note that data is shown on a log(2) scale. Broken lines indicate the 1∶1 correlation (null hypothesis expectation).</p>", "links"=>[], "tags"=>["interactions", "refute", "generalizing", "hypotheses", "mutational", "toxin"], "article_id"=>657054, "categories"=>["Genetics", "Microbiology", "Evolutionary Biology"], "users"=>["Enikö Zörgö", "Karolina Chwialkowska", "Arne B. Gjuvsland", "Elena Garré", "Per Sunnerhagen", "Gianni Liti", "Anders Blomberg", "Stig W. Omholt", "Jonas Warringer"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1003388.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Patterns_of_ploidy_8211_environment_interactions_refute_generalizing_hypotheses_on_the_effects_of_mutational_load_toxin_exposure_and_nutrient_restriction_/657054", "title"=>"Patterns of ploidy–environment interactions refute generalizing hypotheses on the effects of mutational load, toxin exposure, and nutrient restriction.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-22 04:26:44"}
  • {"files"=>["https://ndownloader.figshare.com/files/993676"], "description"=>"<p>A–B) Fitness components measures with a significant (FDR, α = 0.05) difference, both between large (n = 10) and small (n = 10) S288c haploids and between large (n = 29) and small (n = 20) S288c diploids. Large and small cells were constructed through individual deletion of different cell size defining genes. Note that data is shown on a log(2) scale. rror bars represent SEM. A) Performance of large and small diploid cells. B) Performance of large and small haploid cells. C) The tandem genes encoding the Li<sup>+</sup> exporters <i>ENA1</i>,<i>2</i> and <i>5</i>, were deleted in the haploid S288c derivative BY4741 and the haploid deletion strain was autodiploidized through mating type switching. The total change in density (the efficiency) of mitotically reproducing populations exposed to 30 mM LiCl was obtained for <i>ena1</i>Δ<i>2</i>Δ<i>5</i>Δ haploids (n = 8) and diploids (n = 56) and compared to that of WT haploids (n = 16) and diploids (n = 16) in presence of 225 mM LiCl. Note that data is shown on a log(2) scale. Error bars represent SEM, p-values = Student's t-test. D) Growth efficiency of haploid and diploid versions of individual <i>S. cerevisiae</i> and <i>S. paradoxus</i> strains. Broken lines represent 1∶1 correlation (null hypothesis expectation).</p>", "links"=>[], "tags"=>["explains"], "article_id"=>657055, "categories"=>["Genetics", "Microbiology", "Evolutionary Biology"], "users"=>["Enikö Zörgö", "Karolina Chwialkowska", "Arne B. Gjuvsland", "Elena Garré", "Per Sunnerhagen", "Gianni Liti", "Anders Blomberg", "Stig W. Omholt", "Jonas Warringer"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1003388.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Cell_size_partially_explains_ploidy_8211_environment_interactions_/657055", "title"=>"Cell size partially explains ploidy–environment interactions.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-22 04:26:53"}
  • {"files"=>["https://ndownloader.figshare.com/files/993677"], "description"=>"<p>Fitness component measures of S288c haploids, diploids heterozygotic, <b>a</b>/α, at the mating type locus and diploids hemizygotic, <b>a</b> or α, at the mating type locus, in various environments (n = 4). A) Mitotic growth rate in hydroxyurea, a sample environment where mating type locus composition fails to explain fitness differences between haploids and diploids. Note that data is shown on a log(2) scale. B–D) Environments in which fitness differences between ploidy states are partially or completely explained by mating type locus compositions (FDR, α = 0.05). Note that data is shown on a log(2) scale. B) Mitotic growth rate during rapamycin exposure C) Growth rate in nutrient excess and absence of stress D) Mitotic growth efficiency during doxorubicin exposure.</p>", "links"=>[], "tags"=>["locus", "explains"], "article_id"=>657056, "categories"=>["Genetics", "Microbiology", "Evolutionary Biology"], "users"=>["Enikö Zörgö", "Karolina Chwialkowska", "Arne B. Gjuvsland", "Elena Garré", "Per Sunnerhagen", "Gianni Liti", "Anders Blomberg", "Stig W. Omholt", "Jonas Warringer"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1003388.g005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Mating_type_locus_composition_partially_explains_ploidy_8211_environment_interactions_/657056", "title"=>"Mating type locus composition partially explains ploidy–environment interactions.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-22 04:27:00"}
  • {"files"=>["https://ndownloader.figshare.com/files/993678", "https://ndownloader.figshare.com/files/993679", "https://ndownloader.figshare.com/files/993680", "https://ndownloader.figshare.com/files/993681", "https://ndownloader.figshare.com/files/993682", "https://ndownloader.figshare.com/files/993683", "https://ndownloader.figshare.com/files/993684", "https://ndownloader.figshare.com/files/993685", "https://ndownloader.figshare.com/files/993686", "https://ndownloader.figshare.com/files/993687"], "description"=>"<div><p>The number of chromosome sets contained within the nucleus of eukaryotic organisms is a fundamental yet evolutionarily poorly characterized genetic variable of life. Here, we mapped the impact of ploidy on the mitotic fitness of baker's yeast and its never domesticated relative <i>Saccharomyces paradoxus</i> across wide swaths of their natural genotypic and phenotypic space. Surprisingly, environment-specific influences of ploidy on reproduction were found to be the rule rather than the exception. These ploidy–environment interactions were well conserved across the 2 billion generations separating the two species, suggesting that they are the products of strong selection. Previous hypotheses of generalizable advantages of haploidy or diploidy in ecological contexts imposing nutrient restriction, toxin exposure, and elevated mutational loads were rejected in favor of more fine-grained models of the interplay between ecology and ploidy. On a molecular level, cell size and mating type locus composition had equal, but limited, explanatory power, each explaining 12.5%–17% of ploidy–environment interactions. The mechanism of the cell size–based superior reproductive efficiency of haploids during Li<sup>+</sup> exposure was traced to the Li<sup>+</sup> exporter <i>ENA</i>. Removal of the Ena transporters, forcing dependence on the Nha1 extrusion system, completely altered the effects of ploidy on Li<sup>+</sup> tolerance and evoked a strong diploid superiority, demonstrating how genetic variation at a single locus can completely reverse the relative merits of haploidy and diploidy. Taken together, our findings unmasked a dynamic interplay between ploidy and ecology that was of unpredicted evolutionary importance and had multiple molecular roots.</p> </div>", "links"=>[], "tags"=>["evolutionary", "trade-offs", "yeast", "ploidy", "states"], "article_id"=>657057, "categories"=>["Genetics", "Microbiology", "Evolutionary Biology"], "users"=>["Enikö Zörgö", "Karolina Chwialkowska", "Arne B. Gjuvsland", "Elena Garré", "Per Sunnerhagen", "Gianni Liti", "Anders Blomberg", "Stig W. Omholt", "Jonas Warringer"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1003388.s001", "https://dx.doi.org/10.1371/journal.pgen.1003388.s002", "https://dx.doi.org/10.1371/journal.pgen.1003388.s003", "https://dx.doi.org/10.1371/journal.pgen.1003388.s004", "https://dx.doi.org/10.1371/journal.pgen.1003388.s005", "https://dx.doi.org/10.1371/journal.pgen.1003388.s006", "https://dx.doi.org/10.1371/journal.pgen.1003388.s007", "https://dx.doi.org/10.1371/journal.pgen.1003388.s008", "https://dx.doi.org/10.1371/journal.pgen.1003388.s009", "https://dx.doi.org/10.1371/journal.pgen.1003388.s010"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Ancient_Evolutionary_Trade_Offs_between_Yeast_Ploidy_States__/657057", "title"=>"Ancient Evolutionary Trade-Offs between Yeast Ploidy States", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2013-03-22 04:27:16"}

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Relative Metric

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