Widespread Compensatory Evolution Conserves DNA-Encoded Nucleosome Organization in Yeast
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{"title"=>"Widespread compensatory evolution conserves DNA-encoded nucleosome organization in yeast", "type"=>"journal", "authors"=>[{"first_name"=>"Ephraim", "last_name"=>"Kenigsberg", "scopus_author_id"=>"36915372400"}, {"first_name"=>"Amir", "last_name"=>"Bar", "scopus_author_id"=>"15828764800"}, {"first_name"=>"Eran", "last_name"=>"Segal", "scopus_author_id"=>"35485628500"}, {"first_name"=>"Amos", "last_name"=>"Tanay", "scopus_author_id"=>"8090658900"}], "year"=>2010, "source"=>"PLoS Computational Biology", "identifiers"=>{"pui"=>"361077248", "sgr"=>"78651240895", "issn"=>"1553734X", "pmid"=>"21203484", "scopus"=>"2-s2.0-78651240895", "doi"=>"10.1371/journal.pcbi.1001039", "isbn"=>"1553-7358 (Electronic)\\r1553-734X (Linking)"}, "id"=>"b04cc8bb-71ca-39e6-8fa3-d8776af4daa7", "abstract"=>"Evolution maintains organismal fitness by preserving genomic information. This is widely assumed to involve conservation of specific genomic loci among species. Many genomic encodings are now recognized to integrate small contributions from multiple genomic positions into quantitative dispersed codes, but the evolutionary dynamics of such codes are still poorly understood. Here we show that in yeast, sequences that quantitatively affect nucleosome occupancy evolve under compensatory dynamics that maintain heterogeneous levels of A+T content through spatially coupled A/T-losing and A/T-gaining substitutions. Evolutionary modeling combined with data on yeast polymorphisms supports the idea that these substitution dynamics are a consequence of weak selection. This shows that compensatory evolution, so far believed to affect specific groups of epistatically linked loci like paired RNA bases, is a widespread phenomenon in the yeast genome, affecting the majority of intergenic sequences in it. The model thus derived suggests that compensation is inevitable when evolution conserves quantitative and dispersed genomic functions.", "link"=>"http://www.mendeley.com/research/widespread-compensatory-evolution-conserves-dnaencoded-nucleosome-organization-yeast", "reader_count"=>66, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>7, "Student > Doctoral Student"=>1, "Researcher"=>15, "Student > Ph. D. Student"=>28, "Student > Master"=>5, "Other"=>4, "Student > Bachelor"=>2, "Professor"=>3}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>7, "Student > Doctoral Student"=>1, "Researcher"=>15, "Student > Ph. D. Student"=>28, "Student > Master"=>5, "Other"=>4, "Student > Bachelor"=>2, "Professor"=>3}, "reader_count_by_subject_area"=>{"Biochemistry, Genetics and Molecular Biology"=>5, "Agricultural and Biological Sciences"=>55, "Medicine and Dentistry"=>1, "Physics and Astronomy"=>1, "Computer Science"=>2, "Linguistics"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>55}, "Computer Science"=>{"Computer Science"=>2}, "Linguistics"=>{"Linguistics"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>5}}, "reader_count_by_country"=>{"Greece"=>1, "Netherlands"=>1, "United States"=>6, "Japan"=>1, "United Kingdom"=>2, "Israel"=>3, "Spain"=>2, "Russia"=>1}, "group_count"=>0}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/809703"], "description"=>"<p>Shown is a comparison of the rate of A/T gaining substitutions near inferred sites of A/T-losing (black) and A/T-gaining (red) substitution (<a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1001039#s4\" target=\"_blank\">Methods</a>), plotted for different ranges of nucleosome occupancy (X-axis). The rate of A/T gain near conserved loci is shown for reference (green). We observe an elevated rate of A/T gain near A/T-losing sites. <b>B) A/T loss rates are faster next to A/T gain events.</b> Similar analysis of A/T losing substitution rates around inferred A/T gain and A/T loss events.</p>", "links"=>[], "tags"=>["substitutions", "spatially", "rates", "inferred"], "article_id"=>480066, "categories"=>["Medicine", "Genetics", "Infectious Diseases", "Evolutionary Biology"], "users"=>["Ephraim Kenigsberg", "Amir Bar", "Eran Segal", "Amos Tanay"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1001039.g003", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_A_T_gaining_and_A_T_losing_substitutions_are_spatially_coupled_A_A_T_gain_rates_are_faster_next_to_inferred_A_T_loss_events_/480066", "title"=>"A/T-gaining and A/T-losing substitutions are spatially coupled. A) A/T gain rates are faster next to inferred A/T loss events.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-12-23 00:01:06"}
  • {"files"=>["https://ndownloader.figshare.com/files/809864"], "description"=>"<p>We simulated the evolution of a fixed size population of small (20 bp) “genomes” in simple fitness landscapes that depend only on the G+C content of the sequence (<a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1001039#s4\" target=\"_blank\">Methods</a>). We used a mutational input that favors A/T over G/C, resulting in a neutral stationary G+C content of 30%. <b>A</b>) <b>G+C goal fitness landscape.</b> Shown are fitness landscapes (fitness value as a function of the G+C content) preferring low G+C content (the “low occupancy” regime). We generated regimes with different selection intensities (denoted by η) by changing the slope of the depicted parabola (shown are the landscapes for two different intensities). <b>B</b>) <b>Substitution rates.</b> Shown are substitution rates of A/T loss (red) and A/T gain (blue) measured in populations evolving under different levels of selection intensities (X axis) in the low G+C content fitness landscape. We note the increase in A/T gain rate to values higher than neutral at intermediate selection intensities. <b>C</b>) <b>Stationary G+C content.</b> Shown are the population average G+C contents for population evolving in different selection intensities (X-axis), showing that at intermediate levels of selection where A/T gain rate were elevated (dashed line), the average G/C content is only slightly higher than the optimum. <b>D</b>) <b>Substitution rates for intermediate selection intensity.</b> We summarize the simulation by showing substitution rates for a specific level of selection intensity (marked in dashed lines in B and C). Data is shown for the low G+C fitness landscape and for a high G+C fitness landscape that was defined symmetrically with a preferred G+C content of 40% (<b><a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1001039#pcbi.1001039.s008\" target=\"_blank\">Fig S8</a></b>). The data are generally compatible with our empirical observations on yeast divergence rates (<a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1001039#pcbi-1001039-g002\" target=\"_blank\"><b>Fig 2C</b></a><b>, </b><a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1001039#pcbi-1001039-g004\" target=\"_blank\"><b>4C</b></a>). <b>E–H</b>) <b>Evolutionary dynamics for a threshold fitness landscape.</b> An analysis similar to the above, but with a threshold-function fitness landscape (E) reveals that an increase in A/T gaining substitution rates can be observed over a wide range of fitness intensities. <b>I</b>) <b>Compensatory evolution explains the increase in A/T gaining substitution rates.</b> According to our model, the evolution of low occupancy sequences is attempting to maintain low G+C content in spite of a flux of slightly deleterious mutations that pushes toward a higher stationary G+C content. Selection may not be sufficiently powerful to purge every deviation from the optimum and mutations that decrease A/T content may persist (even partially) in the population. These mutations trigger adaptive evolution of corrective mutations, which is efficient since it can occur at multiple positions. The schematic shown here assumes evolution in the threshold fitness landscape (E–H), in which A/T gaining substitutions are never deleterious and therefore robustly increased in rate even if selection is intensive. A variation of the same argument shows why A/T gain rate increases in the fitness landscape of A–D.</p>", "links"=>[], "tags"=>["compensatory", "evolutionary", "yeast", "occupancy"], "article_id"=>480228, "categories"=>["Medicine", "Genetics", "Infectious Diseases", "Evolutionary Biology"], "users"=>["Ephraim Kenigsberg", "Amir Bar", "Eran Segal", "Amos Tanay"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1001039.g005", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_A_model_of_weak_compensatory_selection_predicts_the_evolutionary_dynamics_at_yeast_low_occupancy_sequences_/480228", "title"=>"A model of weak compensatory selection predicts the evolutionary dynamics at yeast low occupancy sequences.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-12-23 00:03:48"}
  • {"files"=>["https://ndownloader.figshare.com/files/809617"], "description"=>"<p>Shown are the inferred C to T substitution rates for the <i>S. cerevisiae</i> lineage (X-axis), and other <i>sensu stricto</i> lineages (color coded, Y-axis). Each point represents the C to T substitution rate in one of 4x4 different flanking nucleotide contexts which are defined using the 5′ and 3′ nucleotides depicted on top. The data reveal a four-fold variation in substitution rates at different contexts, which is consistent among the different lineages (as shown by the fit between the independently inferred substitution rates of <i>S. cerevisiae</i> and of the other lineages). Controlling for this variation is important when comparing substitution dynamics in A+T rich vs. A+T poor genomic regions, such as low and high occupancy sequences. <b>B) Different evolutionary dynamics in low and high occupancy loci.</b> Shown are log-ratios of substitution rates in low vs. high occupancy sequences (Y-axis) plotted against the substitution rates at high occupancy sequences (X-axis). Each point represents the rate of one of four types of substitutions (color coded) in loci flanked by the 5′ and 3′ nucleotide depicted inside the data point. Substitutions in reverse complementary contexts are averaged and shown only once. A/T-losing substitutions (red, pink) are ∼45% slower in low occupancy loci, an effect that is observed independently for transitions and transversions across the different flanking sequence contexts. A/T-gaining substitutions (blue, cyan) are highly dependent on the context, with the main group having rates which are independent of the nucleosome occupancy and with A/T gains in G/C flanking contexts highly conserved in low occupancy sequences. <b>C) Averaged substitution trends.</b> Shown are overall rates of A/T-gaining and A/T-losing substitutions in high and low nucleosome occupancy (occ.) averaged over all contexts. The simplified divergence pattern is difficult to explain using standard models of selection, since different types of substitution are differentially affected. <b>D) The S. cerevisiae lineage maintained the G+C content of low and high occupancy sequences.</b> Shown are the average G+C content in the extant <i>S. cerevisiae</i> genome and in the inferred common ancestor of <i>S. cerevisiae</i> and <i>S. paradoxus</i>, depicted for 10 levels of <i>S. cerevisiae</i> nucleosome occupancy (<a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1001039#s4\" target=\"_blank\">Methods</a>). The analysis suggests that the highly variable substitution rates shown in B are not driving divergence in net G+C content but take part in a conservative process.</p>", "links"=>[], "tags"=>["occupancy", "sequences", "nucleotides", "context-dependent", "yeast", "substitution", "rates", "robustly", "correlated", "flanking"], "article_id"=>479973, "categories"=>["Medicine", "Genetics", "Infectious Diseases", "Evolutionary Biology"], "users"=>["Ephraim Kenigsberg", "Amir Bar", "Eran Segal", "Amos Tanay"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1001039.g002", "stats"=>{"downloads"=>2, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Low_occupancy_sequences_lose_A_T_nucleotides_slowly_and_gain_them_in_a_context_dependent_fashion_A_Yeast_substitution_rates_are_robustly_correlated_with_the_flanking_nucleotides_/479973", "title"=>"Low occupancy sequences lose A/T nucleotides slowly and gain them in a context-dependent fashion. A) Yeast substitution rates are robustly correlated with the flanking nucleotides.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-12-23 02:46:13"}
  • {"files"=>["https://ndownloader.figshare.com/files/809988"], "description"=>"<p>A/T gain and loss delta parameters.</p>", "links"=>[], "tags"=>["delta"], "article_id"=>480361, "categories"=>["Medicine", "Genetics", "Infectious Diseases", "Evolutionary Biology"], "users"=>["Ephraim Kenigsberg", "Amir Bar", "Eran Segal", "Amos Tanay"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1001039.t001", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_A_T_gain_and_loss_delta_parameters_/480361", "title"=>"A/T gain and loss delta parameters.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2010-12-23 00:06:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/404258", "https://ndownloader.figshare.com/files/404278", "https://ndownloader.figshare.com/files/404304", "https://ndownloader.figshare.com/files/404334", "https://ndownloader.figshare.com/files/404381", "https://ndownloader.figshare.com/files/404412", "https://ndownloader.figshare.com/files/404438", "https://ndownloader.figshare.com/files/404467", "https://ndownloader.figshare.com/files/404501", "https://ndownloader.figshare.com/files/404525", "https://ndownloader.figshare.com/files/404553", "https://ndownloader.figshare.com/files/404584", "https://ndownloader.figshare.com/files/404613"], "description"=>"<div><p>Evolution maintains organismal fitness by preserving genomic information. This is widely assumed to involve conservation of specific genomic loci among species. Many genomic encodings are now recognized to integrate small contributions from multiple genomic positions into quantitative dispersed codes, but the evolutionary dynamics of such codes are still poorly understood. Here we show that in yeast, sequences that quantitatively affect nucleosome occupancy evolve under compensatory dynamics that maintain heterogeneous levels of A+T content through spatially coupled A/T-losing and A/T-gaining substitutions. Evolutionary modeling combined with data on yeast polymorphisms supports the idea that these substitution dynamics are a consequence of weak selection. This shows that compensatory evolution, so far believed to affect specific groups of epistatically linked loci like paired RNA bases, is a widespread phenomenon in the yeast genome, affecting the majority of intergenic sequences in it. The model thus derived suggests that compensation is inevitable when evolution conserves quantitative and dispersed genomic functions.</p></div>", "links"=>[], "tags"=>["compensatory", "conserves", "dna-encoded", "nucleosome", "yeast"], "article_id"=>139884, "categories"=>["Medicine", "Genetics", "Cancer", "Evolutionary Biology"], "users"=>["Ephraim Kenigsberg", "Amir Bar", "Eran Segal", "Amos Tanay"], "doi"=>["https://dx.doi.org/10.1371/journal.pcbi.1001039.s001", "https://dx.doi.org/10.1371/journal.pcbi.1001039.s002", "https://dx.doi.org/10.1371/journal.pcbi.1001039.s003", "https://dx.doi.org/10.1371/journal.pcbi.1001039.s004", "https://dx.doi.org/10.1371/journal.pcbi.1001039.s005", "https://dx.doi.org/10.1371/journal.pcbi.1001039.s006", "https://dx.doi.org/10.1371/journal.pcbi.1001039.s007", "https://dx.doi.org/10.1371/journal.pcbi.1001039.s008", "https://dx.doi.org/10.1371/journal.pcbi.1001039.s009", "https://dx.doi.org/10.1371/journal.pcbi.1001039.s010", "https://dx.doi.org/10.1371/journal.pcbi.1001039.s011", "https://dx.doi.org/10.1371/journal.pcbi.1001039.s012", "https://dx.doi.org/10.1371/journal.pcbi.1001039.s013"], "stats"=>{"downloads"=>23, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Widespread_Compensatory_Evolution_Conserves_DNA_Encoded_Nucleosome_Organization_in_Yeast/139884", "title"=>"Widespread Compensatory Evolution Conserves DNA-Encoded Nucleosome Organization in Yeast", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2010-12-23 02:44:44"}
  • {"files"=>["https://ndownloader.figshare.com/files/809935"], "description"=>"<p>Data <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1001039#pcbi.1001039-Liti1\" target=\"_blank\">[39]</a> on allele frequencies in a sample of <i>S. cerevisiae</i> strains was used to test the hypotheses that low and high occupancy sequences maintain their local G+C content due to weak selection. Theory predicts that allele frequencies of deleterious mutations would tend to be smaller than frequencies of neutral mutations and that SNPs representing beneficial mutations would be frequently observed at higher allele frequencies. <b>A</b>) <b>Classifying SNPs.</b> Major and minor alleles at SNPs representing postulated A/T gain and A/T loss at low and high occupancy loci were determined as illustrated. Loci with G/C flanking context were analyzed separately. <b>B–E</b>) <b>Allele frequencies.</b> The groups of SNPs were compared by computing the fraction of SNPs with minor allele frequency smaller than 20%. Shown is the fraction of rare alleles in cases of A/T gain, A/T loss and A/T neutral polymorphisms in non G/C contexts in low occupancy sequences (B), non G/C contexts in high occupancy sequences (C), G/C contexts in low occupancy sequences (D), G/C contexts in high occupancy sequences (E). The data show A/T losing SNPs tend to be rarer than neutral SNPs and A/T gaining SNPs in low occupancy sequences. The opposite behavior is observed at high occupancy sequences or at G/C contexts, confirming the predictions of our evolutionary model.</p>", "links"=>[], "tags"=>["compensatory"], "article_id"=>480302, "categories"=>["Medicine", "Genetics", "Infectious Diseases", "Evolutionary Biology"], "users"=>["Ephraim Kenigsberg", "Amir Bar", "Eran Segal", "Amos Tanay"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1001039.g006", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_SNP_data_support_the_compensatory_evolution_hypothesis_/480302", "title"=>"SNP data support the compensatory evolution hypothesis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-12-23 00:05:02"}
  • {"files"=>["https://ndownloader.figshare.com/files/809529"], "description"=>"<p>Shown is the distribution of G+C content in small (20 bp) bins across intergenic sequences in the <i>S. cerevisae</i> genome (see <b><a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1001039#pcbi.1001039.s001\" target=\"_blank\">Fig S1</a></b> for further analysis). <b>B) Partitioning the genome into high and low occupancy sequences.</b> Shown is the distribution of <i>in-vivo</i> nucleosome occupancy scores across all yeast intergenic loci (data from Kaplan et al., 2009). <b>C) A/T trinucleotides are enriched at low occupancy loci.</b> The frequencies of all trinucleotides in loci with high (top) and low (bottom) nucleosome occupancy are depicted. As shown before, A/T trinucleotides are in excess at low occupancy loci. Also observed is the correlation between the number of G/C nucleotides within the trinucleotide and the relative abundance of the trinucleotide in high vs low occupancy loci.</p>", "links"=>[], "tags"=>["heterogeneity", "correlated", "nucleosome", "heterogeneous"], "article_id"=>479895, "categories"=>["Medicine", "Genetics", "Infectious Diseases", "Evolutionary Biology"], "users"=>["Ephraim Kenigsberg", "Amir Bar", "Eran Segal", "Amos Tanay"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1001039.g001", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Yeast_sequence_heterogeneity_is_correlated_with_nucleosome_occupancy_A_Heterogeneous_local_G_C_content_in_yeast_/479895", "title"=>"Yeast sequence heterogeneity is correlated with nucleosome occupancy. A) Heterogeneous local G+C content in yeast.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-12-23 02:44:55"}
  • {"files"=>["https://ndownloader.figshare.com/files/809759"], "description"=>"<p><b>A</b>) <b>The TSS-distal trinucleotide spectrum is modified.</b> Shown are trinucleotide frequencies at TSS-distal high and low occupancy sequences. Compared to the distribution at TSS-proximal sequences, the low occupancy sequences contain more A/T trinucleotides and less G/C trinucleotides. <b>B</b>) <b>TSS-distal low occupancy sequences lose A/T slowly and gain them rapidly.</b> Shown are ratios of substitution rates in low vs. high occupancy sequences (Y-axis) plotted against the substitution rates at high occupancy sequences (X-axis). Each point represents the rate of one of four types of substitution (color coded) in loci flanked by the 5′ and 3′ nucleotide depicted inside the data point. A/T losing substitutions (red, pink) are consistently slower in TSS-distal low occupancy loci, with very similar dynamics to those observed in TSS-proximal sequences (compare <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1001039#pcbi-1001039-g002\" target=\"_blank\"><b>Fig 2</b></a>). A/T gaining substitutions (blue, cyan) generally occur more rapidly in low occupancy loci than in high occupancy loci. A/T gains in G/C flanking contexts are somewhat conserved, though not to the extent observed in TSS-proximal low occupancy loci. <b>C</b>) <b>Averaged substitution rates.</b> Shown are the rates of A/T-gaining and A/T-losing substitutions at TSS distal (bars) and TSS proximal (gray ticks) high and low occupancy sequences, averaged over all flanking contexts. <b>D</b>) <b>Evolution of G+C content at different occupancy levels.</b> Shown are average G+C contents in the extant <i>S. cerevisiae</i> genome and in the inferred common ancestor of <i>S. cerevisiae</i> and <i>S. paradoxus</i>, depicted for 10 levels of nucleosome occupancy (<a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1001039#s4\" target=\"_blank\">Methods</a>). An overall conservation of G+C content is observed. Conservation is disrupted for low occupancy sequences, suggesting that some of the low occupancy TSS-distal sequences in <i>S. cerevisae</i> have decreased their G+C content recently.</p>", "links"=>[], "tags"=>["tss-distal"], "article_id"=>480127, "categories"=>["Medicine", "Genetics", "Infectious Diseases", "Evolutionary Biology"], "users"=>["Ephraim Kenigsberg", "Amir Bar", "Eran Segal", "Amos Tanay"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1001039.g004", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Compensatory_evolution_at_TSS_distal_sequences_/480127", "title"=>"Compensatory evolution at TSS-distal sequences.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-12-23 00:02:07"}

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