Sex Chromosome-Specific Regulation in the Drosophila Male Germline But Little Evidence for Chromosomal Dosage Compensation or Meiotic Inactivation
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{"title"=>"Sex chromosome-specific regulation in the drosophila male germline but little evidence for chromosomal dosage compensation or meiotic inactivation", "type"=>"journal", "authors"=>[{"first_name"=>"Colin D.", "last_name"=>"Meiklejohn", "scopus_author_id"=>"6602672818"}, {"first_name"=>"Emily L.", "last_name"=>"Landeen", "scopus_author_id"=>"51161447500"}, {"first_name"=>"Jodi M.", "last_name"=>"Cook", "scopus_author_id"=>"51161090500"}, {"first_name"=>"Sarah B.", "last_name"=>"Kingan", "scopus_author_id"=>"8927855000"}, {"first_name"=>"Daven C.", "last_name"=>"Presgraves", "scopus_author_id"=>"6602188861"}], "year"=>2011, "source"=>"PLoS Biology", "identifiers"=>{"issn"=>"15449173", "scopus"=>"2-s2.0-80052324184", "pui"=>"362471731", "doi"=>"10.1371/journal.pbio.1001126", "isbn"=>"1545-7885 (Electronic)\\r1544-9173 (Linking)", "sgr"=>"80052324184", "pmid"=>"21857805"}, "id"=>"442772ff-5c3e-3f8e-9462-4c3ac0c8e42b", "abstract"=>"The evolution of heteromorphic sex chromosomes (e.g., XY in males or ZW in females) has repeatedly elicited the evolution of two kinds of chromosome-specific regulation: dosage compensation--the equalization of X chromosome gene expression in males and females--and meiotic sex chromosome inactivation (MSCI)--the transcriptional silencing and heterochromatinization of the X during meiosis in the male (or Z in the female) germline. How the X chromosome is regulated in the Drosophila melanogaster male germline is unclear. Here we report three new findings concerning gene expression from the X in Drosophila testes. First, X chromosome-wide dosage compensation appears to be absent from most of the Drosophila male germline. Second, microarray analysis provides no evidence for X chromosome-specific inactivation during meiosis. Third, we confirm the previous discovery that the expression of transgene reporters driven by autosomal spermatogenesis-specific promoters is strongly reduced when inserted on the X chromosome versus the autosomes; but we show that this chromosomal difference in expression is established in premeiotic cells and persists in meiotic cells. The magnitude of the X-autosome difference in transgene expression cannot be explained by the absence of dosage compensation, suggesting that a previously unrecognized mechanism limits expression from the X during spermatogenesis in Drosophila. These findings help to resolve several previously conflicting reports and have implications for patterns of genome evolution and speciation in Drosophila.", "link"=>"http://www.mendeley.com/research/sex-chromosomespecific-regulation-drosophila-male-germline-little-evidence-chromosomal-dosage-compen", "reader_count"=>70, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>8, "Researcher"=>14, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>28, "Student > Postgraduate"=>4, "Other"=>3, "Student > Master"=>6, "Student > Bachelor"=>3, "Professor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>8, "Researcher"=>14, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>28, "Student > Postgraduate"=>4, "Other"=>3, "Student > Master"=>6, "Student > Bachelor"=>3, "Professor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Biochemistry, Genetics and Molecular Biology"=>10, "Agricultural and Biological Sciences"=>56, "Chemistry"=>1, "Social Sciences"=>1, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Chemistry"=>{"Chemistry"=>1}, "Social Sciences"=>{"Social Sciences"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>56}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>10}, "Unspecified"=>{"Unspecified"=>1}}, "reader_count_by_country"=>{"Colombia"=>1, "Sweden"=>2, "Netherlands"=>1, "United States"=>4, "Japan"=>1, "Italy"=>1, "United Kingdom"=>1, "Germany"=>1}, "group_count"=>2}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/745375"], "description"=>"<p>Spermatogenic stage and chromosomal effects on the expression of <i>ocn</i> transgenes.</p>", "links"=>[], "tags"=>["chromosomal"], "article_id"=>415757, "categories"=>["Genetics", "Evolutionary Biology"], "users"=>["Colin D. Meiklejohn", "Emily L. Landeen", "Jodi M. Cook", "Sarah B. Kingan", "Daven C. Presgraves"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1001126.t005", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Spermatogenic_stage_and_chromosomal_effects_on_the_expression_of_ocn_transgenes_/415757", "title"=>"Spermatogenic stage and chromosomal effects on the expression of <i>ocn</i> transgenes.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-08-16 01:35:57"}
  • {"files"=>["https://ndownloader.figshare.com/files/745283"], "description"=>"<p>(A) Expression of <i>ocn:lacZ</i> transgenes is low or absent in females, and is significantly lower for <i>X</i>-linked inserts than autosomal inserts in males. Bars indicate the mean expression measured from 8 <i>X</i>-linked and 8 autosomal <i>WOL</i> inserts and 6 <i>X</i>-linked and 5 autosomal <i>YLZ</i> inserts. RNA was extracted from whole adult flies and expression from autosomal inserts was measured in both heterozygous and homozygous male and homozygous female genotypes. (B) The difference between <i>X-</i>linked and autosomal inserts persists from premeiotic to meiotic cells in the male germline. A subset of genotypes (two <i>X-</i>linked and one autosomal <i>WOL</i> and two <i>X-</i>linked and one autosomal <i>YLZ</i>) shown in panel A were used for dissections (see <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1001126#s4\" target=\"_blank\">Materials and Methods</a> for details). In both panels, gene expression is measured relative to a <i>Rpl32</i> control probe and error bars indicate 95% confidence intervals.</p>", "links"=>[], "tags"=>["spermatogenic"], "article_id"=>415660, "categories"=>["Genetics", "Evolutionary Biology"], "users"=>["Colin D. Meiklejohn", "Emily L. Landeen", "Jodi M. Cook", "Sarah B. Kingan", "Daven C. Presgraves"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1001126.g005", "stats"=>{"downloads"=>2, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Sex_chromosome_and_spermatogenic_stage_effects_on_the_expression_of_WOL_and_YLZ_transgenes_/415660", "title"=>"Sex, chromosome, and spermatogenic stage effects on the expression of <i>WOL</i> and <i>YLZ</i> transgenes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-08-16 01:34:20"}
  • {"files"=>["https://ndownloader.figshare.com/files/745469"], "description"=>"a<p>Autosomal totals exclude genes on the 4th chromosome.</p>", "links"=>[], "tags"=>["log2", "changes", "stages"], "article_id"=>415846, "categories"=>["Genetics", "Evolutionary Biology"], "users"=>["Colin D. Meiklejohn", "Emily L. Landeen", "Jodi M. Cook", "Sarah B. Kingan", "Daven C. Presgraves"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1001126.t002", "stats"=>{"downloads"=>3, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Median_log2_magnitude_of_changes_in_expression_between_stages_of_spermatogenesis_/415846", "title"=>"Median log2 magnitude of changes in expression between stages of spermatogenesis.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-08-16 01:37:26"}
  • {"files"=>["https://ndownloader.figshare.com/files/375824", "https://ndownloader.figshare.com/files/375933", "https://ndownloader.figshare.com/files/376000", "https://ndownloader.figshare.com/files/376372", "https://ndownloader.figshare.com/files/376403", "https://ndownloader.figshare.com/files/376439", "https://ndownloader.figshare.com/files/376476", "https://ndownloader.figshare.com/files/376519", "https://ndownloader.figshare.com/files/376570", "https://ndownloader.figshare.com/files/376610"], "description"=>"<div><p>The evolution of heteromorphic sex chromosomes (e.g., <em>XY</em> in males or <em>ZW</em> in females) has repeatedly elicited the evolution of two kinds of chromosome-specific regulation: dosage compensation—the equalization of <em>X</em> chromosome gene expression in males and females— and meiotic sex chromosome inactivation (MSCI)—the transcriptional silencing and heterochromatinization of the <em>X</em> during meiosis in the male (or <em>Z</em> in the female) germline. How the <em>X</em> chromosome is regulated in the <em>Drosophila melanogaster</em> male germline is unclear. Here we report three new findings concerning gene expression from the <em>X</em> in <em>Drosophila</em> testes. First, <em>X</em> chromosome-wide dosage compensation appears to be absent from most of the <em>Drosophila</em> male germline. Second, microarray analysis provides no evidence for <em>X</em> chromosome-specific inactivation during meiosis. Third, we confirm the previous discovery that the expression of transgene reporters driven by autosomal spermatogenesis-specific promoters is strongly reduced when inserted on the <em>X</em> chromosome versus the autosomes; but we show that this chromosomal difference in expression is established in premeiotic cells and persists in meiotic cells. The magnitude of the <em>X</em>-autosome difference in transgene expression cannot be explained by the absence of dosage compensation, suggesting that a previously unrecognized mechanism limits expression from the <em>X</em> during spermatogenesis in <em>Drosophila</em>. These findings help to resolve several previously conflicting reports and have implications for patterns of genome evolution and speciation in <em>Drosophila</em>.</p> </div>", "links"=>[], "tags"=>["chromosome-specific", "germline", "chromosomal", "dosage", "meiotic", "inactivation"], "article_id"=>134237, "categories"=>["Genetics", "Evolutionary Biology"], "users"=>["Colin D. Meiklejohn", "Emily L. Landeen", "Jodi M. Cook", "Sarah B. Kingan", "Daven C. Presgraves"], "doi"=>["https://dx.doi.org/10.1371/journal.pbio.1001126.s001", "https://dx.doi.org/10.1371/journal.pbio.1001126.s002", "https://dx.doi.org/10.1371/journal.pbio.1001126.s003", "https://dx.doi.org/10.1371/journal.pbio.1001126.s004", "https://dx.doi.org/10.1371/journal.pbio.1001126.s005", "https://dx.doi.org/10.1371/journal.pbio.1001126.s006", "https://dx.doi.org/10.1371/journal.pbio.1001126.s007", "https://dx.doi.org/10.1371/journal.pbio.1001126.s008", "https://dx.doi.org/10.1371/journal.pbio.1001126.s009", "https://dx.doi.org/10.1371/journal.pbio.1001126.s010"], "stats"=>{"downloads"=>10, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Sex_Chromosome_Specific_Regulation_in_the_Drosophila_Male_Germline_But_Little_Evidence_for_Chromosomal_Dosage_Compensation_or_Meiotic_Inactivation/134237", "title"=>"Sex Chromosome-Specific Regulation in the <em>Drosophila</em> Male Germline But Little Evidence for Chromosomal Dosage Compensation or Meiotic Inactivation", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2011-08-16 01:10:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/744836"], "description"=>"<p>(A) Autosome and <i>X</i> chromosome expression in cells in the male thorax and female thorax. (B) Autosome and <i>X</i> chromosome gene expression from control cells and from <i>SL2</i> cells in which dosage compensation has been knocked down by RNAi against <i>msl2 </i><a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1001126#pbio.1001126-Hamada1\" target=\"_blank\">[43]</a>. (C–E) Autosome and <i>X</i> chromosome gene expression in the male germline. Premeiotic cells were dissected from the apical tip of the testes; meiotic cells were dissected from the proximal region of the testes. Data in (C) are from Agilent <i>Drosophila</i> gene expression microarrays; (D) shows previously published data <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1001126#pbio.1001126-Vibranovski1\" target=\"_blank\">[41]</a> using Affymetrix GeneChips. (E) Previously published <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1001126#pbio.1001126-Gan1\" target=\"_blank\">[48]</a> RNA-seq data from wild-type testes. *** <i>p</i><0.001 (Mann-Whitney test).</p>", "links"=>[], "tags"=>["chromosome", "autosomal", "dosage"], "article_id"=>415210, "categories"=>["Genetics", "Evolutionary Biology"], "users"=>["Colin D. Meiklejohn", "Emily L. Landeen", "Jodi M. Cook", "Sarah B. Kingan", "Daven C. Presgraves"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1001126.g001", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_X_chromosome_and_autosomal_gene_expression_are_consistent_with_no_dosage_compensation_in_Drosophila_primary_spermatocytes_/415210", "title"=>"<i>X</i> chromosome and autosomal gene expression are consistent with no dosage compensation in <i>Drosophila</i> primary spermatocytes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-08-16 01:26:50"}
  • {"files"=>["https://ndownloader.figshare.com/files/745501"], "description"=>"a<p>Autosomal totals exclude genes on the 4th chromosome.</p>", "links"=>[], "tags"=>["genes", "differences", "stages"], "article_id"=>415877, "categories"=>["Genetics", "Evolutionary Biology"], "users"=>["Colin D. Meiklejohn", "Emily L. Landeen", "Jodi M. Cook", "Sarah B. Kingan", "Daven C. Presgraves"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1001126.t001", "stats"=>{"downloads"=>2, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Number_of_genes_with_significant_differences_in_expression_between_stages_of_spermatogenesis_/415877", "title"=>"Number of genes with significant differences in expression between stages of spermatogenesis.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-08-16 01:37:57"}
  • {"files"=>["https://ndownloader.figshare.com/files/744937"], "description"=>"<p>(A) The distributions of expression differences between <i>msl2</i>-RNAi and control cells for <i>X</i> chromosome and autosomal probes <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1001126#pbio.1001126-Hamada1\" target=\"_blank\">[43]</a>. (B) The distributions of expression differences between male germline cells and male thorax tissue for <i>X</i> and autosomal probes. Black lines indicate the median values of each distribution; the difference between the median log2 expression of autosomal and <i>X-</i>linked probes is 0.398 in (A) and 0.568 in (B).</p>", "links"=>[], "tags"=>["autosomal", "male-like", "cells", "dosage", "differences", "somatic", "germline"], "article_id"=>415301, "categories"=>["Genetics", "Evolutionary Biology"], "users"=>["Colin D. Meiklejohn", "Emily L. Landeen", "Jodi M. Cook", "Sarah B. Kingan", "Daven C. Presgraves"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1001126.g002", "stats"=>{"downloads"=>3, "page_views"=>38, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Differences_in_X_linked_and_autosomal_gene_expression_between_male_like_SL2_cells_with_and_without_dosage_compensation_are_similar_to_the_differences_between_somatic_and_germline_cells_in_males_/415301", "title"=>"Differences in <i>X</i>-linked and autosomal gene expression between male-like <i>SL2</i> cells with and without dosage compensation are similar to the differences between somatic and germline cells in males.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-08-16 01:28:21"}
  • {"files"=>["https://ndownloader.figshare.com/files/745167"], "description"=>"<p>RNA-seq data <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1001126#pbio.1001126-Gan1\" target=\"_blank\">[48]</a> from wild-type ovaries, <i>bam</i> mutant ovaries, and <i>bam</i> mutant testes. * <i>p</i><0.05, *** <i>p</i><0.001 (Mann-Whitney test).</p>", "links"=>[], "tags"=>["chromosome", "autosome", "ovaries", "germline"], "article_id"=>415539, "categories"=>["Genetics", "Evolutionary Biology"], "users"=>["Colin D. Meiklejohn", "Emily L. Landeen", "Jodi M. Cook", "Sarah B. Kingan", "Daven C. Presgraves"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1001126.g003", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_X_chromosome_and_autosome_expression_is_similar_in_ovaries_and_germline_stem_cells_/415539", "title"=>"<i>X</i> chromosome and autosome expression is similar in ovaries and germline stem cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-08-16 01:32:19"}
  • {"files"=>["https://ndownloader.figshare.com/files/745404"], "description"=>"<p>Sex, transgene, and chromosomal effects on the expression of <i>ocn</i> transgenes.</p>", "links"=>[], "tags"=>["chromosomal"], "article_id"=>415782, "categories"=>["Genetics", "Evolutionary Biology"], "users"=>["Colin D. Meiklejohn", "Emily L. Landeen", "Jodi M. Cook", "Sarah B. Kingan", "Daven C. Presgraves"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1001126.t004", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Sex_transgene_and_chromosomal_effects_on_the_expression_of_ocn_transgenes_/415782", "title"=>"Sex, transgene, and chromosomal effects on the expression of <i>ocn</i> transgenes.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-08-16 01:36:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/745228"], "description"=>"<p>(A & B) qRT-PCR results for 12 genes from premeiotic and meiotic dissections show good correspondence with previously published microarray results <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1001126#pbio.1001126-Vibranovski1\" target=\"_blank\">[41]</a>. (C) Apical dissections (premeiotic cells) including the testis sheath show slight but detectable increases in the expression of <i>X</i>-linked genes relative to apical dissections from which the sheath has been removed. *** <i>p</i><0.001.</p>", "links"=>[], "tags"=>["indicates", "contaminating", "testis", "sheath", "detectable"], "article_id"=>415602, "categories"=>["Genetics", "Evolutionary Biology"], "users"=>["Colin D. Meiklejohn", "Emily L. Landeen", "Jodi M. Cook", "Sarah B. Kingan", "Daven C. Presgraves"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1001126.g004", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_qRT_PCR_analysis_indicates_the_contaminating_effect_of_testis_sheath_has_a_detectable_effect_on_gene_expression_/415602", "title"=>"qRT-PCR analysis indicates the contaminating effect of testis sheath has a detectable effect on gene expression.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-08-16 01:33:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/745443"], "description"=>"<p>Gene expression differences are log2 fold-change between the various dissections. qRT-PCR values were normalized by three control genes (see <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1001126#s4\" target=\"_blank\">Materials and Methods</a>).</p>a<p>Premeiotic dissections with testis sheath included − meiotic dissections.</p>b<p>Premeiotic dissections with testis sheath included − premeiotic dissections with testis sheath removed.</p>c<p>Sheath effect is calculated as the ratio of (Ps−Pn)/(Ps−M) from qRT-PCR.</p>d<p><i>p-</i>value calculated from paired <i>t</i> tests between Ps and Pn.</p>", "links"=>[], "tags"=>["somatic", "testis", "sheath", "detectable", "changes", "stages"], "article_id"=>415807, "categories"=>["Genetics", "Evolutionary Biology"], "users"=>["Colin D. Meiklejohn", "Emily L. Landeen", "Jodi M. Cook", "Sarah B. Kingan", "Daven C. Presgraves"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1001126.t003", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Contamination_by_somatic_testis_sheath_has_detectable_effects_on_changes_in_gene_expression_between_stages_of_spermatogenesis_/415807", "title"=>"Contamination by somatic testis sheath has detectable effects on changes in gene expression between stages of spermatogenesis.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-08-16 01:36:47"}

PMC Usage Stats | Further Information

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