SPO24 Is a Transcriptionally Dynamic, Small ORF-Encoding Locus Required for Efficient Sporulation in Saccharomyces cerevisiae
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{"title"=>"SPO24 is a transcriptionally dynamic, small ORF-encoding locus required for efficient sporulation in Saccharomyces cerevisiae", "type"=>"journal", "authors"=>[{"first_name"=>"Sara", "last_name"=>"Hurtado", "scopus_author_id"=>"37026144100"}, {"first_name"=>"Karen S.", "last_name"=>"Kim Guisbert", "scopus_author_id"=>"56805151500"}, {"first_name"=>"Erik J.", "last_name"=>"Sontheimer", "scopus_author_id"=>"6701762981"}], "year"=>2014, "source"=>"PLoS ONE", "identifiers"=>{"doi"=>"10.1371/journal.pone.0105058", "scopus"=>"2-s2.0-84940255078", "pui"=>"373772120", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "pmid"=>"25127041", "issn"=>"19326203", "sgr"=>"84940255078"}, "id"=>"84aae47e-6b4c-3ec0-881d-797983a3e679", "abstract"=>"In Saccharomyces cerevisiae, meiosis and sporulation are highly regulated responses that are driven in part by changes in RNA expression. Alternative mRNA forms with extended 5' UTRs are atypical in S. cerevisiae, and 5' extensions with upstream open reading frames (uORFs) are even more unusual. Here we characterize the gene YPR036W-A, now renamed SPO24, which encodes a very small (67-amino-acid) protein. This gene gives rise to two mRNA forms: a shorter form throughout meiosis and a longer, 5'-extended form in mid-late meiosis. The latter form includes a uORF for a 14-amino-acid peptide (Spo24u14). Deletion of the downstream ORF (dORF) leads to sporulation defects and the appearance of pseudohyphae-like projections. Experiments with luciferase reporters indicate that the uORF does not downregulate dORF translation. The protein encoded by the dORF (Spo24d67) localizes to the prospore membrane and is differentially phosphorylated during meiosis. Transcription of the 5'-extended mRNA in mid-meiosis depends upon the presence of two middle sporulation elements (MSEs). Removal of the MSEs severely inhibits the mid-meiotic appearance of the 5'-extended mRNA and limits the ability of plasmid-borne SPO24 to rescue the sporulation defect of a spo24Δ mutant, suggesting that the 5'-extended mRNA is functionally important. These results reveal Spo24d67 as a sporulation-related factor that is encoded by a transcriptionally dynamic, uORF-containing locus.", "link"=>"http://www.mendeley.com/research/spo24-transcriptionally-dynamic-small-orfencoding-locus-required-efficient-sporulation-saccharomyces", "reader_count"=>12, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Researcher"=>3, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>3, "Other"=>1, "Professor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Researcher"=>3, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>3, "Other"=>1, "Professor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Biochemistry, Genetics and Molecular Biology"=>3, "Materials Science"=>1, "Agricultural and Biological Sciences"=>6, "Pharmacology, Toxicology and Pharmaceutical Science"=>1}, "reader_count_by_subdiscipline"=>{"Materials Science"=>{"Materials Science"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>6}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>3}, "Unspecified"=>{"Unspecified"=>1}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}}, "reader_count_by_country"=>{"United States"=>1, "Germany"=>1}, "group_count"=>0}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1638085", "https://ndownloader.figshare.com/files/1638086", "https://ndownloader.figshare.com/files/1638087", "https://ndownloader.figshare.com/files/1638088", "https://ndownloader.figshare.com/files/1638089", "https://ndownloader.figshare.com/files/1638090", "https://ndownloader.figshare.com/files/1638091", "https://ndownloader.figshare.com/files/1638092", "https://ndownloader.figshare.com/files/1638093", "https://ndownloader.figshare.com/files/1638094", "https://ndownloader.figshare.com/files/1638095"], "description"=>"<div><p>In <i>Saccharomyces cerevisiae</i>, meiosis and sporulation are highly regulated responses that are driven in part by changes in RNA expression. Alternative mRNA forms with extended 5′ UTRs are atypical in <i>S. cerevisiae</i>, and 5′ extensions with upstream open reading frames (uORFs) are even more unusual. Here we characterize the gene <i>YPR036W-A</i>, now renamed <i>SPO24</i>, which encodes a very small (67-amino-acid) protein. This gene gives rise to two mRNA forms: a shorter form throughout meiosis and a longer, 5′-extended form in mid-late meiosis. The latter form includes a uORF for a 14-amino-acid peptide (Spo24<sup>u14</sup>). Deletion of the downstream ORF (dORF) leads to sporulation defects and the appearance of pseudohyphae-like projections. Experiments with luciferase reporters indicate that the uORF does not downregulate dORF translation. The protein encoded by the dORF (Spo24<sup>d67</sup>) localizes to the prospore membrane and is differentially phosphorylated during meiosis. Transcription of the 5′-extended mRNA in mid-meiosis depends upon the presence of two middle sporulation elements (MSEs). Removal of the MSEs severely inhibits the mid-meiotic appearance of the 5′-extended mRNA and limits the ability of plasmid-borne <i>SPO24</i> to rescue the sporulation defect of a <i>spo24</i>Δ mutant, suggesting that the 5′-extended mRNA is functionally important. These results reveal Spo24<sup>d67</sup> as a sporulation-related factor that is encoded by a transcriptionally dynamic, uORF-containing locus.</p></div>", "links"=>[], "tags"=>["Spo 24d localizes", "spo", "middle sporulation elements", "Saccharomyces cerevisiae", "appearance", "meiosi", "Alternative mRNA forms", "uorf", "Spo 24u Deletion", "downregulate dORF translation", "defect", "protein", "mse", "gene YPR 036W", "utr"], "article_id"=>1140937, "categories"=>["Biological Sciences"], "users"=>["Sara Hurtado", "Karen S. Kim Guisbert", "Erik J. Sontheimer"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0105058.s001", "https://dx.doi.org/10.1371/journal.pone.0105058.s002", "https://dx.doi.org/10.1371/journal.pone.0105058.s003", "https://dx.doi.org/10.1371/journal.pone.0105058.s004", "https://dx.doi.org/10.1371/journal.pone.0105058.s005", "https://dx.doi.org/10.1371/journal.pone.0105058.s006", "https://dx.doi.org/10.1371/journal.pone.0105058.s007", "https://dx.doi.org/10.1371/journal.pone.0105058.s008", "https://dx.doi.org/10.1371/journal.pone.0105058.s009", "https://dx.doi.org/10.1371/journal.pone.0105058.s010", "https://dx.doi.org/10.1371/journal.pone.0105058.s011"], "stats"=>{"downloads"=>28, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_SPO24_Is_a_Transcriptionally_Dynamic_Small_ORF_Encoding_Locus_Required_for_Efficient_Sporulation_in_Saccharomyces_cerevisiae_/1140937", "title"=>"<i>SPO24</i> Is a Transcriptionally Dynamic, Small ORF-Encoding Locus Required for Efficient Sporulation in <i>Saccharomyces cerevisiae</i>", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2014-08-15 03:47:58"}
  • {"files"=>["https://ndownloader.figshare.com/files/1638083"], "description"=>"<p>(<b>A</b>) Protein samples from a sportulation time course were subjected to Western analysis with antibodies against a 9-Myc tag fused to the C-terminus of Spo24<sup>d67</sup>. The blots reveal a protein of the expected molecular weight (21.5 kDa), indicating that the Spo24<sup>d67</sup> protein is expressed throughout meiosis. Nap1 was also analyzed as a loading control. The protein appears as a doublet at multiple time points, suggesting the existence of a posttranslationally modified form. (<b>B</b>) The upper band of the Spo24<sup>d67</sup> doublet is susceptible to λ phosphatase treatment. Both Spo24 bands persist after mock digestion, whereas the upper band is abolished by λ phosphatase, indicating that the upper band is a phosphorylated isoform.</p>", "links"=>[], "tags"=>["Spo 24d localizes", "spo", "middle sporulation elements", "Saccharomyces cerevisiae", "appearance", "meiosi", "Alternative mRNA forms", "uorf", "Spo 24u Deletion", "downregulate dORF translation", "defect", "protein", "mse", "gene YPR 036W", "utr"], "article_id"=>1140935, "categories"=>["Biological Sciences"], "users"=>["Sara Hurtado", "Karen S. Kim Guisbert", "Erik J. Sontheimer"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0105058.g005", "stats"=>{"downloads"=>0, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Western_analysis_of_epitope_tagged_Spo24_d67_protein_/1140935", "title"=>"Western analysis of epitope-tagged Spo24<sup>d67</sup> protein.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-08-15 03:47:58"}
  • {"files"=>["https://ndownloader.figshare.com/files/1638084"], "description"=>"<p>(<b>A</b>) <i>spo24</i>Δ cells carrying a plasmid (pSH112) expressing Spo24-GFP were sporulated on SPM plates for 24 hours. GFP fluorescence microscopy (right panel) revealed ring-like structures that appear to correspond with spore locations in the DIC image left panel). (<b>B</b>) As in (A), except that the cells carrying a plasmid (pRS426_RFP_ Spo20<sup>51–91</sup> Spo24_GFP) expressing both RFP-Spo20<sup>51–91</sup> (a prospore marker) and Spo24-GFP. The GFP ring-like structures co-localize with the prospore marker protein (in red, merge represented by yellow), suggesting that Spo24 is associated with the prospore cortex.</p>", "links"=>[], "tags"=>["Spo 24d localizes", "spo", "middle sporulation elements", "Saccharomyces cerevisiae", "appearance", "meiosi", "Alternative mRNA forms", "uorf", "Spo 24u Deletion", "downregulate dORF translation", "defect", "protein", "mse", "gene YPR 036W", "utr"], "article_id"=>1140936, "categories"=>["Biological Sciences"], "users"=>["Sara Hurtado", "Karen S. Kim Guisbert", "Erik J. Sontheimer"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0105058.g006", "stats"=>{"downloads"=>0, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Spo24_d67_localizes_to_the_prospore_cortex_/1140936", "title"=>"Spo24<sup>d67</sup> localizes to the prospore cortex.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-08-15 03:47:58"}
  • {"files"=>["https://ndownloader.figshare.com/files/1638082"], "description"=>"<p>The data show wildtype and <i>spo24</i>Δ sporulation efficiencies in comparison with those of the deletion strain carrying a <i>SPO24</i> wildtype rescue plasmid (pSH101) and a derivative with its two MSEs deleted (pSH110). The wildtype plasmid fully rescues the <i>spo24</i>Δ sporulation defect, whereas the ΔMSE derivative does not.</p>", "links"=>[], "tags"=>["Spo 24d localizes", "spo", "middle sporulation elements", "Saccharomyces cerevisiae", "appearance", "meiosi", "Alternative mRNA forms", "uorf", "Spo 24u Deletion", "downregulate dORF translation", "defect", "protein", "mse", "gene YPR 036W", "utr"], "article_id"=>1140934, "categories"=>["Biological Sciences"], "users"=>["Sara Hurtado", "Karen S. Kim Guisbert", "Erik J. Sontheimer"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0105058.g004", "stats"=>{"downloads"=>0, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Deletion_of_the_Ndt80_binding_sites_from_the_SPO24_promoter_decreases_sporulation_efficiency_/1140934", "title"=>"Deletion of the Ndt80 binding sites from the <i>SPO24</i> promoter decreases sporulation efficiency.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-08-15 03:47:58"}
  • {"files"=>["https://ndownloader.figshare.com/files/1638079"], "description"=>"<p>(<b>A</b>) Map of the <i>YPR036W</i>-<i>A</i> locus in <i>S. cerevisiae</i>. The region upstream of the 204-nt <i>YPR036W-A</i> dORF includes a 45-nt uORF that is present in a longer form of expressed mRNA that is induced in mid-meiosis. Further upstream are two consensus Ndt80 transcription factor binding sites (middle sporulation elements, or MSEs). The line denotes the boundaries of the genomic fragment included in the rescue plasmid pSH101. Black arrows mark the approximate transcription start sites, as mapped through the tiling array signal and confirmed by 5′ RACE. (<b>B</b>) Heat map of tiling array data showing <i>YPR036W-A</i> expression during meiosis. Genomic coordinates along the <i>YPR036W-A</i> locus correspond to the horizontal axis. The array signals (from three separate cultures for each time point) are stacked vertically with the beginning of meiosis at the top, and with sporulation times indicated to the right of the heat map. The bottom six layers are from log-phase haploid and diploid cells. The positions of the uORF and dORF are given by the upper arrows. After ∼6 hours of sporulation a meiosis-specific RNA is induced. Small arrows underneath represent primer-binding sites for reverse (R), forward (F), and upstream forward (uF) primers. (<b>C</b>) qRT-PCR analyses using the primers depicted in (B) show expression patterns consistent with the array data, confirming the presence of a longer RNA. Moreover the analysis indicates that the extended signal detected on the arrays is a longer RNA that is contiguous into the dORF, and does not simply reflect expression of a distinct, neighboring transcript that abuts a shorter <i>YPR036W-A</i> mRNA. Error bars represent the standard error of the mean (SEM) from three biological replicates.</p>", "links"=>[], "tags"=>["Spo 24d localizes", "spo", "middle sporulation elements", "Saccharomyces cerevisiae", "appearance", "meiosi", "Alternative mRNA forms", "uorf", "Spo 24u Deletion", "downregulate dORF translation", "defect", "protein", "mse", "gene YPR 036W", "utr"], "article_id"=>1140931, "categories"=>["Biological Sciences"], "users"=>["Sara Hurtado", "Karen S. Kim Guisbert", "Erik J. Sontheimer"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0105058.g001", "stats"=>{"downloads"=>0, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_YPR036W_A_expresses_two_mRNA_forms_/1140931", "title"=>"<i>YPR036W-A</i> expresses two mRNA forms.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-08-15 03:47:58"}
  • {"files"=>["https://ndownloader.figshare.com/files/1638081"], "description"=>"<p>(<b>A</b>) Diagram of the luciferase reporter constructs. The YCp22FL1 reporter carrying the wild-type <i>SPO24</i> uORF is shown at the top. A mutant in which the uORF AUG translation initiation codon was changed to a CUG codon was also generated (below, marked with an asterisk). Reporter expression is driven by the P<i><sub>TEF1</sub></i> promoter. (<b>B</b>) Plasmids in (A), as well as the control FL' plasmid, were introduced into (strain) and maintained in the absence of Trp, and lysates from these cells were subjected to luciferase assays. The graph shows luciferase expression in the presence of the wild-type uORF (WT) and the mutated uORF, normalized to expression from the control FL' plasmid. (<b>C</b>) qRT-PCR data of luciferase mRNA levels, normalized to those of <i>ACT1</i>. (<b>D</b>) Translational efficiency calculated from protein levels [luciferase expression, (B)] and mRNA levels [RT-qPCR data, (C)] shows a small increase in translational efficiency relative to wild type when the uORF is present. In B–D, error bars represent SEM calculated from three biological replicates.</p>", "links"=>[], "tags"=>["Spo 24d localizes", "spo", "middle sporulation elements", "Saccharomyces cerevisiae", "appearance", "meiosi", "Alternative mRNA forms", "uorf", "Spo 24u Deletion", "downregulate dORF translation", "defect", "protein", "mse", "gene YPR 036W", "utr"], "article_id"=>1140933, "categories"=>["Biological Sciences"], "users"=>["Sara Hurtado", "Karen S. Kim Guisbert", "Erik J. Sontheimer"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0105058.g003", "stats"=>{"downloads"=>0, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Modest_stimulation_of_luciferase_expression_by_the_SPO24_uORF_/1140933", "title"=>"Modest stimulation of luciferase expression by the <i>SPO24</i> uORF.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-08-15 03:47:58"}
  • {"files"=>["https://ndownloader.figshare.com/files/1638080"], "description"=>"<p>(<b>A–C</b>) Differential interference contrast (DIC) images of sporulated wildtype (DKB98) yeast cells (A), the <i>spo24</i>Δ/+ heterozygous deletion derivative (B), and the <i>spo24</i>Δ homozygous deletion derivative (C), respectively. The <i>spo24</i>Δ/+ heterozygote exhibits decreased sporulation efficiency and a more elongated morphology (B). Both the sporulation defect and the pseudohyphae-like morphology are exacerbated in the <i>spo24</i>Δ homozygote (C), suggesting a gene dosage effect on the phenotypes. (<b>D–F</b>) As in A–C, respectively, but with cells that harbor the <i>SPO24</i>-containing, <i>CEN</i> rescue plasmid pSH101 (see <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0105058#pone-0105058-g001\" target=\"_blank\">Figure 1A</a>). The rescue plasmid abolishes the sporulation efficiency defect as well as the elongated cellular morphology. (<b>G</b>) Quantification of sporulation efficiency, as measured by the number of spores per ascus (n = 200 for each of three biological replicates) after 40 hours on solid sporulation medium. Complementation of the <i>spo24</i> deletion with the pSH101 plasmid results in partial rescue the sporulation defect.</p>", "links"=>[], "tags"=>["Spo 24d localizes", "spo", "middle sporulation elements", "Saccharomyces cerevisiae", "appearance", "meiosi", "Alternative mRNA forms", "uorf", "Spo 24u Deletion", "downregulate dORF translation", "defect", "protein", "mse", "gene YPR 036W", "utr"], "article_id"=>1140932, "categories"=>["Biological Sciences"], "users"=>["Sara Hurtado", "Karen S. Kim Guisbert", "Erik J. Sontheimer"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0105058.g002", "stats"=>{"downloads"=>0, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_YPR036W_A_SPO24_is_required_for_efficient_sporulation_/1140932", "title"=>"<i>YPR036W-A</i> (<i>SPO24</i>) is required for efficient sporulation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-08-15 03:47:58"}

PMC Usage Stats | Further Information

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Relative Metric

{"start_date"=>"2014-01-01T00:00:00Z", "end_date"=>"2014-12-31T00:00:00Z", "subject_areas"=>[{"subject_area"=>"/Biology and life sciences/Biochemistry", "average_usage"=>[282]}, {"subject_area"=>"/Biology and life sciences/Cell biology", "average_usage"=>[286]}, {"subject_area"=>"/Biology and life sciences/Mycology", "average_usage"=>[348, 543]}]}
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