Abstract
Dosage compensation system with X chromosome upregulation and inactivation have evolved to overcome the genetic imbalance between sex chromosomes in both male and female of mammals. Although recent development of chromosome-wide technologies has allowed us to test X upregulation, discrete data processing and analysis methods draw disparate conclusions. A series of expression studies revealed status of dosage compensation in some species belonging to monotremes, marsupials, rodents and primates. However, X upregulation in the Artiodactyla order including cattle have not been studied yet. In this study, we surveyed the genome-wide transcriptional upregulation in X chromosome in cattle RNA-seq data using different gene filtration methods. Overall examination of RNA-seq data revealed that X chromosome in the pituitary gland expressed more genes than in other peripheral tissues, which was consistent with the previous results observed in human and mouse. When analyzed with globally expressed genes, a median X:A expression ratio was 0.94. The ratio of 1-to-1 ortholog genes between chicken and mammals, however, showed considerable reduction to 0.68. These results indicate that status of dosage compensation for cattle is not deviated from those found in rodents and primate, and this is consistent with the evolutionary history of cattle.
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References
Anders S (2010) HTSeq: Analysing high-throughput sequencing data with Python. http://www-huber.embl.de/users/anders/HTSeq/doc/overview.html
Bachtrog D (2013) Y-chromosome evolution: emerging insights into processes of Y-chromosome degeneration. Nat Rev Genet 14:113–124. doi:10.1038/nrg3366
Bellott DW et al (2014) Mammalian Y chromosomes retain widely expressed dosage-sensitive regulators. Nature 508:494
Berletch JB, Yang F, Xu J, Carrel L, Disteche CM (2011) Genes that escape from X inactivation. Hum Genet 130:237–245. doi:10.1007/s00439-011-1011-z
Birchler JA, Veitia RA (2007) The gene balance hypothesis: from classical genetics to modern genomics. Plant Cell 19:395–402
Birchler JA, Veitia RA (2012) Gene balance hypothesis: connecting issues of dosage sensitivity across biological disciplines. Proc Natl Acad Sci USA 109:14746–14753. doi:10.1073/pnas.1207726109
Birchler JA, Riddle NC, Auger DL, Veitia RA (2005) Dosage balance in gene regulation: biological implications. Trends Genet 21:219–226
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30(15):2114–2120. doi:10.1093/bioinformatics/btu170
Bovine Genome S, Consortium A et al (2009) The genome sequence of taurine cattle: a window to ruminant biology and evolution. Science 324:522–528. doi:10.1126/science.1169588
Calabrese JM et al (2012) Site-specific silencing of regulatory elements as a mechanism of X inactivation. Cell 151:951–963
Carrel L, Willard HF (2005) X-inactivation profile reveals extensive variability in X-linked gene expression in females. Nature 434:400–404
Chen Y, Lun ATL, Smyth GK (2014) Differential expression analysis of complex RNA-seq experiments using edgeR. In: Datta S, Nettleton DS (eds) Statistical analysis of next generation sequencing data. Springer, New York, pp 51–74
Das PJ, Chowdhary BP, Raudsepp T (2009) Characterization of the bovine pseudoautosomal region and comparison with sheep, goat, and other mammalian pseudoautosomal regions. Cytogenet Genome Res 126:139–147. doi:10.1159/000245913
Deng X et al (2011) Evidence for compensatory upregulation of expressed X-linked genes in mammals, Caenorhabditis elegans and Drosophila melanogaster. Nat Genet 43:1179–1185. doi:10.1038/ng.948
Deng X, Berletch JB, Nguyen DK, Disteche CM (2014) X chromosome regulation: diverse patterns in development, tissues and disease. Nat Rev Genet 15:367–378. doi:10.1038/nrg3687
Ercan S (2015) Mechanisms of X chromosome dosage compensation. J Genom 3:1–19. doi:10.7150/jgen.10404
Gelbart ME, Kuroda MI (2009) Drosophila dosage compensation: a complex voyage to the X chromosome. Development 136:1399–1410. doi:10.1242/dev.029645
Gupta V (2006) Global analysis of X-chromosome dosage compensation. J Biol 5:3
Hedges SB, Kumar S (2009) The timetree of life. Oxford University Press, Oxford
Hedges SB, Marin J, Suleski M, Paymer M, Kumar S (2015) Tree of life reveals clock-like speciation and diversification. Mol Biol Evol 32(4):835–845. doi:10.1093/molbev/msv037
Helena Mangs A, Morris BJ (2007) The human pseudoautosomal region (PAR): origin, function and future. Curr Genom 8:129–136
Johnston CM, Lovell FL, Leongamornlert DA, Stranger BE, Dermitzakis ET, Ross MT (2008) Large-scale population study of human cell lines indicates that dosage compensation is virtually complete. PLoS Genet 4:e9. doi:10.1371/journal.pgen.0040009
Jue NK et al (2013) Determination of dosage compensation of the mammalian X chromosome by RNA-seq is dependent on analytical approach. BMC Genom 14:150. doi:10.1186/1471-2164-14-150
Julien P et al (2012) Mechanisms and evolutionary patterns of mammalian and avian dosage compensation. PLoS Biol 10:e1001328. doi:10.1371/journal.pbio.1001328
Kharchenko PV, Xi R, Park PJ (2011) Evidence for dosage compensation between the X chromosome and autosomes in mammals. Nat Genet 43:1167–1169. doi:10.1038/ng.991
Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL (2013) TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 14:R36
Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359
Li H et al (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079
Lin H, Gupta V, Vermilyea MD, Falciani F, Lee JT, O’Neill LP, Turner BM (2007) Dosage compensation in the mouse balances up-regulation and silencing of X-linked genes. PLoS Biol 5:e326. doi:10.1371/journal.pbio.0050326
Lin H, Halsall JA, Antczak P, O’Neill LP, Falciani F, Turner BM (2011) Relative overexpression of X-linked genes in mouse embryonic stem cells is consistent with Ohno’s hypothesis. Nat Genet 43:1169–1170. doi:10.1038/ng.992
Lin F, Xing K, Zhang J, He X (2012) Expression reduction in mammalian X chromosome evolution refutes Ohno’s hypothesis of dosage compensation. Proc Natl Acad Sci USA 109:11752–11757. doi:10.1073/pnas.1201816109
Makino T, McLysaght A (2010) Ohnologs in the human genome are dosage balanced and frequently associated with disease. Proc Natl Acad Sci 107:9270–9274
Mank JE (2009) The W, X, Y and Z of sex-chromosome dosage compensation. Trends Genet 25:226–233
Mank JE (2013) Sex chromosome dosage compensation: definitely not for everyone. Trends Genet 29:677–683. doi:10.1016/j.tig.2013.07.005
Mueller JL et al (2013) Independent specialization of the human and mouse X chromosomes for the male germ line. Nat Genet 45:1083–1087
Nguyen DK, Disteche CM (2006) Dosage compensation of the active X chromosome in mammals. Nat Genet 38:47–53
Ohno S (1967) Sex chromosomes and sex linked genes. Springer Verlag, Berlin
Pessia E, Makino T, Bailly-Bechet M, McLysaght A, Marais GA (2012) Mammalian X chromosome inactivation evolved as a dosage-compensation mechanism for dosage-sensitive genes on the X chromosome. Proc Natl Acad Sci USA 109:5346–5351. doi:10.1073/pnas.1116763109
Pessia E, Engelstadter J, Marais GA (2014) The evolution of X chromosome inactivation in mammals: the demise of Ohno’s hypothesis? Cell Mol Life Sci CMLS 71:1383–1394. doi:10.1007/s00018-013-1499-6
Prasad TK et al (2009) Human protein reference database—2009 update. Nucleic Acids Res 37:D767–D772
Prince EG, Kirkland D, Demuth JP (2010) Hyperexpression of the X chromosome in both sexes results in extensive female bias of X-linked genes in the flour beetle. Genome Biol Evolut 2:336–346. doi:10.1093/gbe/evq024
Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140. doi:10.1093/bioinformatics/btp616
Rodriguez-Delgado CL, Waters SA, Waters PD (2014) Paternal X inactivation does not correlate with X chromosome evolutionary strata in marsupials. BMC Evol Biol 14:267. doi:10.1186/s12862-014-0267-z
Seo M et al (2016) Comprehensive identification of sexually dimorphic genes in diverse cattle tissues using RNA-seq. BMC Genom. doi:10.1186/s12864-016-2400-4
Strome S, Kelly WG, Ercan S, Lieb JD (2014) Regulation of the X chromosomes in Caenorhabditis elegans. Cold Spring Harb Perspect Biol. doi:10.1101/cshperspect.a018366
Talebizadeh Z, Simon SD, Butler MG (2006) X chromosome gene expression in human tissues: male and female comparisons. Genomics 88:675–681. doi:10.1016/j.ygeno.2006.07.016
Van Laere A-S, Coppieters W, Georges M (2008) Characterization of the bovine pseudoautosomal boundary: documenting the evolutionary history of mammalian sex chromosomes. Genome Res 18:1884–1895
Wang X, Douglas KC, Vandeberg JL, Clark AG, Samollow PB (2014) Chromosome-wide profiling of X-chromosome inactivation and epigenetic states in fetal brain and placenta of the opossum, Monodelphis domestica. Genome Res 24:70–83. doi:10.1101/gr.161919.113
Wu H et al (2014) Cellular resolution maps of X chromosome inactivation: implications for neural development, function, and disease. Neuron 81:103–119
Xiong Y et al (2010) RNA sequencing shows no dosage compensation of the active X-chromosome. Nat Genet 42:1043–1047. doi:10.1038/ng.711
Yang F, Babak T, Shendure J, Disteche CM (2010) Global survey of escape from X inactivation by RNA-sequencing in mouse. Genome Res 20:614–622
Yang X, Schadt EE, Wang S, Wang H, Arnold AP, Ingram-Drake L, Drake TA, Lusis AJ (2006) Tissuespecific expression and regulation of sexually dimorphic genes in mice. Genome Res 16:995–1004. doi:10.1101/gr.5217506
Yildirim E, Sadreyev RI, Pinter SF, Lee JT (2012) X-chromosome hyperactivation in mammals via nonlinear relationships between chromatin states and transcription. Nat Struct Mol Biol 19:56–61. doi:10.1038/nsmb.2195
Acknowledgments
This work was carried out with the support of “Cooperative Research Program for Agriculture Science and Technology Development (Project No. PJ01040604)” Rural Development Administration, and “Research Program for Agriculture Science and Technology Development (Project No. PJ01203102)” National Livestock Research Institute, Republic of Korea. We would like to thank Hyeongmin Kim, and Woncheol Park for providing valuable feedback during data analysis, and Hyunsuk Kim, Dongahn Yoo, and Kelsey Caetano-Anolles for English editing. The Silhouette image of opossum and mouse was created using Freepik from www.flaticon.com. Images of animals were obtained elsewhere: platypus and cow, http://silhouettes-clipart.com; human, http://www.freevectors.net.
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Sojeong Ka and Hyeonju Ahn have contributed equally.
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Ka, S., Ahn, H., Seo, M. et al. Status of dosage compensation of X chromosome in bovine genome. Genetica 144, 435–444 (2016). https://doi.org/10.1007/s10709-016-9912-3
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DOI: https://doi.org/10.1007/s10709-016-9912-3