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Expression properties exhibit correlated patterns with the fate of duplicated genes, their divergence, and transcriptional plasticity in Saccharomycotina

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Expression properties exhibit correlated patterns with the fate of duplicated genes, their divergence, and transcriptional plasticity in Saccharomycotina

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dc.contributor.author Mattenberger, Florian es_ES
dc.contributor.author Sabater-Muñoz, Beatriz es_ES
dc.contributor.author Toft, Christina es_ES
dc.contributor.author Sablok, Gaurav es_ES
dc.contributor.author Fares Riaño, Mario Ali es_ES
dc.date.accessioned 2020-10-28T04:32:42Z
dc.date.available 2020-10-28T04:32:42Z
dc.date.issued 2017-12 es_ES
dc.identifier.issn 1340-2838 es_ES
dc.identifier.uri http://hdl.handle.net/10251/153360
dc.description.abstract [EN] Gene duplication is an important source of novelties and genome complexity. What genes are preserved as duplicated through long evolutionary times can shape the evolution of innovations. Identifying factors that influence gene duplicability is therefore an important aim in evolutionary biology. Here, we show that in the yeast Saccharomyces cerevisiae the levels of gene expression correlate with gene duplicability, its divergence, and transcriptional plasticity. Genes that were highly expressed before duplication are more likely to be preserved as duplicates for longer evolutionary times and wider phylogenetic ranges than genes that were lowly expressed. Duplicates with higher expression levels exhibit greater divergence between their gene copies. Duplicates that exhibit higher expression divergence are those enriched for TATA-containing promoters. These duplicates also show transcriptional plasticity, which seems to be involved in the origin of adaptations to environmental stresses in yeast. While the expression properties of genes strongly affect their duplicability, divergence and transcriptional plasticity are enhanced after gene duplication. We conclude that highly expressed genes are more likely to be preserved as duplicates due to their promoter architectures, their greater tolerance to expression noise, and their ability to reduce the noise-plasticity conflict. es_ES
dc.description.sponsorship We would like to thank members of Fares' Lab for a careful reading and discussion of the results in the manuscript. We are also grateful to colleagues at Trinity College for helpful discussions. This work was supported by a grant from the Spanish Ministerio de Economia y Competitividad (MINECO-FEDER; BFU2015-66073-P) to M.A.F. F.M. is supported by a PhD grant from the Spanish Ministerio de Economia y Competitividad (reference: BES-2016-076677). C.T. was supported by a grant Juan de la Cierva from the Spanish Ministerio de Economia y Competitividad (reference: JCA-2012-14056). es_ES
dc.language Inglés es_ES
dc.publisher Oxford University Press es_ES
dc.relation.ispartof DNA Research es_ES
dc.rights Reconocimiento - No comercial (by-nc) es_ES
dc.subject Gene expression es_ES
dc.subject Gene duplication es_ES
dc.subject Transcriptional plasticity es_ES
dc.subject Duplicability es_ES
dc.subject Saccharomyces cerevisiae es_ES
dc.title Expression properties exhibit correlated patterns with the fate of duplicated genes, their divergence, and transcriptional plasticity in Saccharomycotina es_ES
dc.type Artículo es_ES
dc.identifier.doi 10.1093/dnares/dsx025 es_ES
dc.relation.projectID info:eu-repo/grantAgreement/MINECO//BFU2015-66073-P/ES/CARACTERIZANDO LOS MECANISMOS DE INNOVACION POR DUPLICACION GENICA/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/MINECO//JCI-2012-14056/ES/JCI-2012-14056/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/AEI//BES-2016-076677/ es_ES
dc.rights.accessRights Abierto es_ES
dc.contributor.affiliation Universitat Politècnica de València. Instituto Universitario Mixto de Biología Molecular y Celular de Plantas - Institut Universitari Mixt de Biologia Molecular i Cel·lular de Plantes es_ES
dc.description.bibliographicCitation Mattenberger, F.; Sabater-Muñoz, B.; Toft, C.; Sablok, G.; Fares Riaño, MA. (2017). Expression properties exhibit correlated patterns with the fate of duplicated genes, their divergence, and transcriptional plasticity in Saccharomycotina. DNA Research. 24(6):559-570. https://doi.org/10.1093/dnares/dsx025 es_ES
dc.description.accrualMethod S es_ES
dc.relation.publisherversion https://doi.org/10.1093/dnares/dsx025 es_ES
dc.description.upvformatpinicio 559 es_ES
dc.description.upvformatpfin 570 es_ES
dc.type.version info:eu-repo/semantics/publishedVersion es_ES
dc.description.volume 24 es_ES
dc.description.issue 6 es_ES
dc.relation.pasarela S\352636 es_ES
dc.contributor.funder Ministerio de Economía y Competitividad es_ES
dc.contributor.funder Agencia Estatal de Investigación es_ES
dc.description.references Ohno, S. (1999). Gene duplication and the uniqueness of vertebrate genomes circa 1970–1999. Seminars in Cell & Developmental Biology, 10(5), 517-522. doi:10.1006/scdb.1999.0332 es_ES
dc.description.references Lynch, M. (2000). The Evolutionary Fate and Consequences of Duplicate Genes. Science, 290(5494), 1151-1155. doi:10.1126/science.290.5494.1151 es_ES
dc.description.references Otto, S. P., & Whitton, J. (2000). Polyploid Incidence and Evolution. Annual Review of Genetics, 34(1), 401-437. doi:10.1146/annurev.genet.34.1.401 es_ES
dc.description.references Carretero-Paulet, L., & Fares, M. A. (2012). Evolutionary Dynamics and Functional Specialization of Plant Paralogs Formed by Whole and Small-Scale Genome Duplications. Molecular Biology and Evolution, 29(11), 3541-3551. doi:10.1093/molbev/mss162 es_ES
dc.description.references Cui, L. (2006). Widespread genome duplications throughout the history of flowering plants. Genome Research, 16(6), 738-749. doi:10.1101/gr.4825606 es_ES
dc.description.references Holub, E. B. (2001). The arms race is ancient history in Arabidopsis, the wildflower. Nature Reviews Genetics, 2(7), 516-527. doi:10.1038/35080508 es_ES
dc.description.references Lespinet, O. (2002). The Role of Lineage-Specific Gene Family Expansion in the Evolution of Eukaryotes. Genome Research, 12(7), 1048-1059. doi:10.1101/gr.174302 es_ES
dc.description.references Wendel, J. F. (2000). Plant Molecular Biology, 42(1), 225-249. doi:10.1023/a:1006392424384 es_ES
dc.description.references Soltis, D. E., Albert, V. A., Leebens-Mack, J., Bell, C. D., Paterson, A. H., Zheng, C., … Soltis, P. S. (2009). Polyploidy and angiosperm diversification. American Journal of Botany, 96(1), 336-348. doi:10.3732/ajb.0800079 es_ES
dc.description.references De Peer, Y. V. (2004). Computational approaches to unveiling ancient genome duplications. Nature Reviews Genetics, 5(10), 752-763. doi:10.1038/nrg1449 es_ES
dc.description.references Hoegg, S., Brinkmann, H., Taylor, J. S., & Meyer, A. (2004). Phylogenetic Timing of the Fish-Specific Genome Duplication Correlates with the Diversification of Teleost Fish. Journal of Molecular Evolution, 59(2), 190-203. doi:10.1007/s00239-004-2613-z es_ES
dc.description.references Grant, S. G. N. (2016). The molecular evolution of the vertebrate behavioural repertoire. Philosophical Transactions of the Royal Society B: Biological Sciences, 371(1685), 20150051. doi:10.1098/rstb.2015.0051 es_ES
dc.description.references Green, S. A., & Bronner, M. E. (2013). Gene duplications and the early evolution of neural crest development. Seminars in Cell & Developmental Biology, 24(2), 95-100. doi:10.1016/j.semcdb.2012.12.006 es_ES
dc.description.references Conant, G. C., & Wolfe, K. H. (2007). Increased glycolytic flux as an outcome of whole‐genome duplication in yeast. Molecular Systems Biology, 3(1), 129. doi:10.1038/msb4100170 es_ES
dc.description.references Wolfe, K. H., & Shields, D. C. (1997). Molecular evidence for an ancient duplication of the entire yeast genome. Nature, 387(6634), 708-713. doi:10.1038/42711 es_ES
dc.description.references Fares, M. A., Keane, O. M., Toft, C., Carretero-Paulet, L., & Jones, G. W. (2013). The Roles of Whole-Genome and Small-Scale Duplications in the Functional Specialization of Saccharomyces cerevisiae Genes. PLoS Genetics, 9(1), e1003176. doi:10.1371/journal.pgen.1003176 es_ES
dc.description.references Blanc, G., & Wolfe, K. H. (2004). Widespread Paleopolyploidy in Model Plant Species Inferred from Age Distributions of Duplicate Genes. The Plant Cell, 16(7), 1667-1678. doi:10.1105/tpc.021345 es_ES
dc.description.references Blanc, G., & Wolfe, K. H. (2004). Functional Divergence of Duplicated Genes Formed by Polyploidy during Arabidopsis Evolution. The Plant Cell, 16(7), 1679-1691. doi:10.1105/tpc.021410 es_ES
dc.description.references Conant, G. C., & Wolfe, K. H. (2008). Turning a hobby into a job: How duplicated genes find new functions. Nature Reviews Genetics, 9(12), 938-950. doi:10.1038/nrg2482 es_ES
dc.description.references Fares, M. A., Byrne, K. P., & Wolfe, K. H. (2005). Rate Asymmetry After Genome Duplication Causes Substantial Long-Branch Attraction Artifacts in the Phylogeny of Saccharomyces Species. Molecular Biology and Evolution, 23(2), 245-253. doi:10.1093/molbev/msj027 es_ES
dc.description.references Freeling, M. (2009). Bias in Plant Gene Content Following Different Sorts of Duplication: Tandem, Whole-Genome, Segmental, or by Transposition. Annual Review of Plant Biology, 60(1), 433-453. doi:10.1146/annurev.arplant.043008.092122 es_ES
dc.description.references Conant, G. C., Birchler, J. A., & Pires, J. C. (2014). Dosage, duplication, and diploidization: clarifying the interplay of multiple models for duplicate gene evolution over time. Current Opinion in Plant Biology, 19, 91-98. doi:10.1016/j.pbi.2014.05.008 es_ES
dc.description.references Keane, O. M., Toft, C., Carretero-Paulet, L., Jones, G. W., & Fares, M. A. (2014). Preservation of genetic and regulatory robustness in ancient gene duplicates ofSaccharomyces cerevisiae. Genome Research, 24(11), 1830-1841. doi:10.1101/gr.176792.114 es_ES
dc.description.references Fares, M. A. (2015). The origins of mutational robustness. Trends in Genetics, 31(7), 373-381. doi:10.1016/j.tig.2015.04.008 es_ES
dc.description.references Gout, J.-F., & Lynch, M. (2015). Maintenance and Loss of Duplicated Genes by Dosage Subfunctionalization. Molecular Biology and Evolution, 32(8), 2141-2148. doi:10.1093/molbev/msv095 es_ES
dc.description.references Altschul, S. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research, 25(17), 3389-3402. doi:10.1093/nar/25.17.3389 es_ES
dc.description.references Byrne, K. P. (2005). The Yeast Gene Order Browser: Combining curated homology and syntenic context reveals gene fate in polyploid species. Genome Research, 15(10), 1456-1461. doi:10.1101/gr.3672305 es_ES
dc.description.references Lohse, M., Bolger, A. M., Nagel, A., Fernie, A. R., Lunn, J. E., Stitt, M., & Usadel, B. (2012). RobiNA: a user-friendly, integrated software solution for RNA-Seq-based transcriptomics. Nucleic Acids Research, 40(W1), W622-W627. doi:10.1093/nar/gks540 es_ES
dc.description.references Robinson, M. D., McCarthy, D. J., & Smyth, G. K. (2009). edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics, 26(1), 139-140. doi:10.1093/bioinformatics/btp616 es_ES
dc.description.references Anders, S., & Huber, W. (2010). Differential expression analysis for sequence count data. Genome Biology, 11(10). doi:10.1186/gb-2010-11-10-r106 es_ES
dc.description.references Brion, C., Pflieger, D., Souali-Crespo, S., Friedrich, A., & Schacherer, J. (2016). Differences in environmental stress response among yeasts is consistent with species-specific lifestyles. Molecular Biology of the Cell, 27(10), 1694-1705. doi:10.1091/mbc.e15-12-0816 es_ES
dc.description.references Linde, J., Duggan, S., Weber, M., Horn, F., Sieber, P., Hellwig, D., … Kurzai, O. (2015). Defining the transcriptomic landscape of Candida glabrata by RNA-Seq. Nucleic Acids Research, 43(3), 1392-1406. doi:10.1093/nar/gku1357 es_ES
dc.description.references Seoighe, C., & Wolfe, K. H. (1999). Yeast genome evolution in the post-genome era. Current Opinion in Microbiology, 2(5), 548-554. doi:10.1016/s1369-5274(99)00015-6 es_ES
dc.description.references Aury, J.-M., Jaillon, O., Duret, L., Noel, B., Jubin, C., Porcel, B. M., … Wincker, P. (2006). Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia. Nature, 444(7116), 171-178. doi:10.1038/nature05230 es_ES
dc.description.references Gout, J.-F., Kahn, D., & Duret, L. (2010). The Relationship among Gene Expression, the Evolution of Gene Dosage, and the Rate of Protein Evolution. PLoS Genetics, 6(5), e1000944. doi:10.1371/journal.pgen.1000944 es_ES
dc.description.references McGrath, C. L., Gout, J.-F., Doak, T. G., Yanagi, A., & Lynch, M. (2014). Insights into Three Whole-Genome Duplications Gleaned from theParamecium caudatumGenome Sequence. Genetics, 197(4), 1417-1428. doi:10.1534/genetics.114.163287 es_ES
dc.description.references McGrath, C. L., Gout, J.-F., Johri, P., Doak, T. G., & Lynch, M. (2014). Differential retention and divergent resolution of duplicate genes following whole-genome duplication. Genome Research, 24(10), 1665-1675. doi:10.1101/gr.173740.114 es_ES
dc.description.references Albert, F. W., Muzzey, D., Weissman, J. S., & Kruglyak, L. (2014). Genetic Influences on Translation in Yeast. PLoS Genetics, 10(10), e1004692. doi:10.1371/journal.pgen.1004692 es_ES
dc.description.references Gout, J.-F., Duret, L., & Kahn, D. (2009). Differential Retention of Metabolic Genes Following Whole-Genome Duplication. Molecular Biology and Evolution, 26(5), 1067-1072. doi:10.1093/molbev/msp026 es_ES
dc.description.references Papp, B., Pál, C., & Hurst, L. D. (2003). Dosage sensitivity and the evolution of gene families in yeast. Nature, 424(6945), 194-197. doi:10.1038/nature01771 es_ES
dc.description.references Qian, W., Liao, B.-Y., Chang, A. Y.-F., & Zhang, J. (2010). Maintenance of duplicate genes and their functional redundancy by reduced expression. Trends in Genetics, 26(10), 425-430. doi:10.1016/j.tig.2010.07.002 es_ES
dc.description.references Birchler, J. A., & Veitia, R. A. (2012). Gene balance hypothesis: Connecting issues of dosage sensitivity across biological disciplines. Proceedings of the National Academy of Sciences, 109(37), 14746-14753. doi:10.1073/pnas.1207726109 es_ES
dc.description.references Pu, S., Wong, J., Turner, B., Cho, E., & Wodak, S. J. (2008). Up-to-date catalogues of yeast protein complexes. Nucleic Acids Research, 37(3), 825-831. doi:10.1093/nar/gkn1005 es_ES
dc.description.references Scannell, D. R., Byrne, K. P., Gordon, J. L., Wong, S., & Wolfe, K. H. (2006). Multiple rounds of speciation associated with reciprocal gene loss in polyploid yeasts. Nature, 440(7082), 341-345. doi:10.1038/nature04562 es_ES
dc.description.references Landry, C. R., Lemos, B., Rifkin, S. A., Dickinson, W. J., & Hartl, D. L. (2007). Genetic Properties Influencing the Evolvability of Gene Expression. Science, 317(5834), 118-121. doi:10.1126/science.1140247 es_ES
dc.description.references Lehner, B. (2010). Conflict between Noise and Plasticity in Yeast. PLoS Genetics, 6(11), e1001185. doi:10.1371/journal.pgen.1001185 es_ES
dc.description.references Mattenberger, F., Sabater-Muñoz, B., Hallsworth, J. E., & Fares, M. A. (2017). Glycerol stress inSaccharomyces cerevisiae: Cellular responses and evolved adaptations. Environmental Microbiology, 19(3), 990-1007. doi:10.1111/1462-2920.13603 es_ES
dc.description.references Mattenberger, F., Sabater-Muñoz, B., Toft, C., & Fares, M. A. (2016). The Phenotypic Plasticity of Duplicated Genes in Saccharomyces cerevisiae and the Origin of Adaptations. G3: Genes|Genomes|Genetics, 7(1), 63-75. doi:10.1534/g3.116.035329 es_ES
dc.description.references Blake, W. J., Balázsi, G., Kohanski, M. A., Isaacs, F. J., Murphy, K. F., Kuang, Y., … Collins, J. J. (2006). Phenotypic Consequences of Promoter-Mediated Transcriptional Noise. Molecular Cell, 24(6), 853-865. doi:10.1016/j.molcel.2006.11.003 es_ES
dc.description.references Raser, J. M. (2005). Noise in Gene Expression: Origins, Consequences, and Control. Science, 309(5743), 2010-2013. doi:10.1126/science.1105891 es_ES
dc.description.references Newman, J. R. S., Ghaemmaghami, S., Ihmels, J., Breslow, D. K., Noble, M., DeRisi, J. L., & Weissman, J. S. (2006). Single-cell proteomic analysis of S. cerevisiae reveals the architecture of biological noise. Nature, 441(7095), 840-846. doi:10.1038/nature04785 es_ES
dc.description.references Tirosh, I., Weinberger, A., Carmi, M., & Barkai, N. (2006). A genetic signature of interspecies variations in gene expression. Nature Genetics, 38(7), 830-834. doi:10.1038/ng1819 es_ES


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