Cytogenetic and Genome Research

Original Article

Sex-Biased Expression of Young Genes in Silurana (Xenopus) tropicalis

Chain F.J.J.

Author affiliations

Department of Biology, McGill University, Montreal, Que., Canada

Keywords: Clawed frogsDuplicated genesFaster-ZLineage-specific genesSex-biased expressionSex chromosomesSiluranaXenopus

Related Articles for ""
Cytogenet Genome Res 2015;145:265-277
https://doi.org/10.1159/000430942

Log in to MyKarger to check if you already have access to this content.




Forgot your password
Sign up to MyKarger

Buy

  • FullText & PDF
  • Unlimited re-access via MyKarger
  • Unrestricted printing, no saving restrictions for personal use
read more
CHF 38.00 *
EUR 35.00 *
USD 39.00 *

Select

KAB

Buy a Karger Article Bundle (KAB) and profit from a discount!


If you would like to redeem your KAB credit, please log in.

Save over 20% compared to the individual article price.

Learn more

Rent/Cloud

  • Rent for 48h to view
  • Buy Cloud Access for unlimited viewing via different devices
  • Synchronizing in the ReadCube Cloud
  • Printing and saving restrictions apply
Rental: USD 8.50
Cloud: USD 20.00

Select

Subscribe

  • Access to all articles of the subscribed year(s) guaranteed for 5 years
  • Unlimited re-access via Subscriber Login or MyKarger
  • Unrestricted printing, no saving restrictions for personal use
read more

Subcription rates

Select
* The final prices may differ from the prices shown due to specifics of VAT rules.

Article / Publication Details

First-Page Preview
Abstract of Original Article

Published online: June 06, 2015
Issue release date: August 2015

Number of Print Pages: 13
Number of Figures: 6
Number of Tables: 2

ISSN: 1424-8581 (Print)
eISSN: 1424-859X (Online)

For additional information: https://www.karger.com/CGR

Abstract

Sex-biased gene expression can evolve from sex-specific selection and is often associated with sex-linked genes. Gene duplication is a particularly effective mechanism for the generation of sex-biased genes, in which a new copy can help resolve intralocus sexual conflicts. This study assesses sex-biased gene expression in an amphibian with homomorphic ZW sex chromosomes, the Western clawed frog Silurana (Xenopus)tropicalis. Previous work has shown that the sex chromosomes in this species are mainly undifferentiated and pseudoautosomal. Consistent with ongoing recombination between the sex chromosomes, this study detected little evidence for the general sexualization of sex-linked regions. A subset of genes closely linked to the sex determining locus displays a tendency for male-biased expression and elevated rates of evolution relative to genes in other genomic locations. This may be a symptom of an early stage of sex chromosome differentiation driven by, for example, chromosomal degeneration or natural selection on genes in this portion of the Z chromosome. Alternatively, it could reflect variation between the sexes in allelic copy number coupled with a lack of dosage compensation. Irrespective of the genomic location, lineage-specific genes and recently duplicated genes had significantly high levels of sex-biased expression, offering insights into the early transcriptional differentiation of young genes.

© 2015 S. Karger AG, Basel



Related Articles:

References

  1. Alexa A, Rahnenführer J, Lengauer T: Improved scoring of functional groups from gene expression data by decorrelating GO graph structure. Bioinformatics 22:1600-1607 (2006).
    External Resources
  2. Arunkumar KP, Mita K, Nagaraju J: The silkworm Z chromosome is enriched in testis-specific genes. Genetics 182:493-501 (2009).
    External Resources
  3. Bachtrog D: A dynamic view of sex chromosome evolution. Curr Opin Genet Dev 16:578-585 (2006).
    External Resources
  4. Bachtrog D: Y-chromosome evolution: emerging insights into processes of Y-chromosome degeneration. Nat Rev Genet 14:113-124 (2013).
    External Resources
  5. Baker RH, Narechania A, Johns PM, Wilkinson GS: Gene duplication, tissue-specific gene expression and sexual conflict in stalk-eyed flies (Diopsidae). Philos Trans R Soc Lond B Biol Sci 367:2357-2375 (2012).
    External Resources
  6. Betrán E, Thornton K, Long M: Retroposed new genes out of the X in Drosophila. Genome Res 12:1854-1859 (2002).
    External Resources
  7. Bewick AJ, Anderson DW, Evans BJ: Evolution of the closely related, sex-related genes DM-W and DMRT1 in African clawed frogs (Xenopus). Evolution 65:698-712 (2011).
    External Resources
  8. Bewick AJ, Chain FJ, Zimmerman LB, Sesay A, Gilchrist MJ, et al: A large pseudoautosomal region on the sex chromosomes of the frog Silurana tropicalis. Genome Biol Evol 5:1087-1098 (2013).
    External Resources
  9. Bowes JB, Snyder KA, Segerdell E, Gibb R, Jarabek C, et al: Xenbase: a Xenopus biology and genomics resource. Nucleic Acids Res 36:D761-D767 (2008).
    External Resources
  10. Castresana J: Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540-552 (2000).
    External Resources
  11. Chain FJ, Ilieva D, Evans BJ: Single-species microarrays and comparative transcriptomics. PLoS One 3:e3279 (2008a).
    External Resources
  12. Chain FJ, Ilieva D, Evans BJ: Duplicate gene evolution and expression in the wake of vertebrate allopolyploidization. BMC Evol Biol 8:43 (2008b).
    External Resources
  13. Chain FJ, Feulner PG, Panchal M, Eizaguirre C, Samonte IE, et al: Extensive copy-number variation of young genes across stickleback populations. PLoS Genet 10:e1004830 (2014).
    External Resources
  14. Charlesworth B: Model for evolution of Y chromosomes and dosage compensation. Proc Natl Acad Sci USA 75:5618-5622 (1978).
    External Resources
  15. Charlesworth B: The evolution of sex chromosomes. Science 251:1030-1033 (1991).
    External Resources
  16. Charlesworth B, Charlesworth D: The degeneration of Y chromosomes. Philos Trans R Soc Lond B Biol Sci 355:1563-1572 (2000).
    External Resources
  17. Charlesworth B, Coyne JA, Barton NH: The relative rates of evolution of sex chromosomes and autosomes. Am Nat 130:113-146 (1987).
    External Resources
  18. Charlesworth D, Charlesworth B, Marais G: Steps in the evolution of heteromorphic sex chromosomes. Heredity 95:118-128 (2005).
    External Resources
  19. Chen S, Ni X, Krinsky BH, Zhang YE, Vibranovski MD, et al: Reshaping of global gene expression networks and sex-biased gene expression by integration of a young gene. EMBO J 31:2798-2809 (2012).
    External Resources
  20. Connallon T, Clark AG: Sex linkage, sex-specific selection, and the role of recombination in the evolution of sexually dimorphic gene expression. Evolution 64:3417-3442 (2010).
    External Resources
  21. Connallon T, Clark AG: The resolution of sexual antagonism by gene duplication. Genetics 187:919-937 (2011).
    External Resources
  22. Connallon T, Knowles LL: Intergenomic conflict revealed by patterns of sex-biased gene expression. Trends Genet 21:495-499 (2005).
    External Resources
  23. Cutter AD, Ward S: Sexual and temporal dynamics of molecular evolution in C. elegans development. Mol Biol Evol 22:178-188 (2005).
    External Resources
  24. Dean R, Mank JE: The role of sex chromosomes in sexual dimorphism: discordance between molecular and phenotypic data. J Evol Biol 27:1443-1453 (2014).
    External Resources
  25. Donoghue MT, Keshavaiah C, Swamidatta SH, Spillane C: Evolutionary origins of Brassicaceae specific genes in Arabidopsis thaliana. BMC Evol Biol 11:47 (2011).
    External Resources
  26. Duncan RP, Nathanson L, Wilson AC: Novel male-biased expression in paralogs of the aphid slimfast nutrient amino acid transporter expansion. BMC Evol Biol 11:253 (2011).
    External Resources
  27. Ellegren H: Sex-chromosome evolution: recent progress and the influence of male and female heterogamety. Nat Rev Genet 12:157-166 (2011).
    External Resources
  28. Ellegren H, Parsch J: The evolution of sex-biased genes and sex-biased gene expression. Nat Rev Genet 8:689-698 (2007).
    External Resources
  29. Flicek P, Amode MR, Barrell D, Beal K, Brent S, et al: Ensembl 2012. Nucleic Acids Res 40:D84-D90 (2012).
    External Resources
  30. Gallach M, Betrán E: Intralocus sexual conflict resolved through gene duplication. Trends Ecol Evol 26:222-228 (2011).
    External Resources
  31. Gallach M, Domingues S, Betrán E: Gene duplication and the genome distribution of sex-biased genes. Int J Evol Biol 2011:989438 (2011).
    External Resources
  32. Gibson JR, Chippindale AK, Rice WR: The X chromosome is a hot spot for sexually antagonistic fitness variation. Proc Biol Sci 269:499-505 (2002).
    External Resources
  33. Gnad F, Parsch J: Sebida: a database for the functional and evolutionary analysis of genes with sex-biased expression. Bioinformatics 22:2577-2579 (2006).
    External Resources
  34. Griffin RM, Dean R, Grace JL, Rydén P, Friberg U: The shared genome is a pervasive constraint on the evolution of sex-biased gene expression. Mol Biol Evol 30:2168-2176 (2013).
    External Resources
  35. Haerty W, Jagadeeshan S, Kulathinal RJ, Wong A, Ravi Ram K, et al: Evolution in the fast lane: rapidly evolving sex-related genes in Drosophila. Genetics 177:1321-1335 (2007).
    External Resources
  36. Hellsten U, Khokha MK, Grammer TC, Harland RM, Richardson P, Rokhsar DS: Accelerated gene evolution and subfunctionalization in the pseudotetraploid frog Xenopus laevis. BMC Biol 5:31 (2007).
    External Resources
  37. Huang X, Hong CS, O'Donnell M, Saint-Jeannet JP: The doublesex-related gene, XDmrt4, is required for neurogenesis in the olfactory system. Proc Natl Acad Sci USA 102:11349-11354 (2005).
    External Resources
  38. James-Zorn C, Ponferrada VG, Jarabek CJ, Burns KA, Segerdell EJ, et al: Xenbase: expansion and updates of the Xenopus model organism database. Nucleic Acids Res 41:D865-D870 (2013).
    External Resources
  39. Kaiser VB, Ellegren H: Nonrandom distribution of genes with sex-biased expression in the chicken genome. Evolution 60:1945-1951 (2006).
    External Resources
  40. Karpinka JB, Fortriede JD, Burns KA, James-Zorn C, Ponferrada VG, et al: Xenbase, the Xenopus model organism database; new virtualized system, data types and genomes. Nucleic Acids Res 43:D756-D763 (2014).
    External Resources
  41. Kent WJ: BLAT - the BLAST-like alignment tool. Genome Res 12:656-664 (2002).
    External Resources
  42. Kirkpatrick M, Hall DW: Sexual selection and sex linkage. Evolution 58:683-691 (2004).
    External Resources
  43. Levine MT, Jones CD, Kern AD, Lindfors HA, Begun DJ: Novel genes derived from noncoding DNA in Drosophila melanogaster are frequently X-linked and exhibit testis-biased expression. Proc Natl Acad Sci USA 103:9935-9939 (2006).
    External Resources
  44. Long M, Vibranovski MD, Zhang YE: Evolutionary interactions between sex chromosomes and autosomes, in Singh RS, Jiianping X, Kulathinal RJ (eds): Rapidly Evolving Genes and Genetic Systems, pp 101-114 (Oxford University Press, Oxford 2012).
    External Resources
  45. Malone JH, Hawkins DL Jr, Michalak P: Sex-biased gene expression in a ZW sex determination system. J Mol Evol 63:427-436 (2006).
    External Resources
  46. Mank JE: Sex chromosomes and the evolution of sexual dimorphism: lessons from the genome. Am Nat 173:141-150 (2009a).
    External Resources
  47. Mank JE: The W, X, Y and Z of sex-chromosome dosage compensation. Trends Genet 25:226-233 (2009b).
    External Resources
  48. Mank JE, Nam K, Ellegren H: Faster-Z evolution is predominantly due to genetic drift. Mol Biol Evol 27:661-670 (2010).
    External Resources
  49. Meisel RP, Connallon T: The faster-X effect: integrating theory and data. Trends Genet 29:537-544 (2013).
    External Resources
  50. Meisel RP, Malone JH, Clark AG: Faster-X evolution of gene expression in Drosophila. PLoS Genet 8:e1003013 (2012).
    External Resources
  51. Moyers BA, Zhang J: Phylostratigraphic bias creates spurious patterns of genome evolution. Mol Biol Evol 32:258-267 (2015).
    External Resources
  52. Nakagawa T, Sakurai T, Nishioka T, Touhara K: Insect sex-pheromone signals mediated by specific combinations of olfactory receptors. Science 307:1638-1642 (2005).
    External Resources
  53. Necsulea A, Soumillon M, Warnefors M, Liechti A, Daish T, et al: The evolution of lncRNA repertoires and expression patterns in tetrapods. Nature 505:635-640 (2014).
    External Resources
  54. Ohno S: Sex Chromosomes and Sex-Linked Genes (Springer, New York 1967).
    External Resources
  55. Ohno S: Evolution by Gene Duplication (Springer, New York 1970).
    External Resources
  56. Olmstead AW, Lindberg-Livingston A, Degitz SJ: Genotyping sex in the amphibian, Xenopus (Silurana) tropicalis, for endocrine disruptor bioassays. Aquat Toxicol 98:60-66 (2010).
    External Resources
  57. Parisi M, Nuttall R, Edwards P, Minor J, Naiman D, et al: A survey of ovary-, testis-, and soma-biased gene expression in Drosophila melanogaster adults. Genome Biol 5:R40 (2004).
    External Resources
  58. Parlier D, Moers V, Van Campenhout C, Preillon J, Leclère L, et al: The Xenopus doublesex-related gene Dmrt5 is required for olfactory placode neurogenesis. Dev Biol 373:39-52 (2013).
    External Resources
  59. Parsch J, Ellegren H: The evolutionary causes and consequences of sex-biased gene expression. Nat Rev Genet 14:83-87 (2013).
    External Resources
  60. Perry JC, Harrison PW, Mank JE: The ontogeny and evolution of sex-biased gene expression in Drosophila melanogaster. Mol Biol Evol 31:1206-1219 (2014).
    External Resources
  61. Pich I Rosello O, Kondrashov FA: Long-term asymmetrical acceleration of protein evolution after gene duplication. Genome Biol Evol 6:1949-1955 (2014).
    External Resources
  62. Pontius JU, Wagner L, Schuler GD: UniGene: A Unified View of the Transcriptome. The NCBI Handbook (National Library of Medicine, Bethesda 2003).
  63. Ranwez V, Harispe S, Delsuc F, Douzery EJ: MACSE: Multiple Alignment of Coding SEquences accounting for frameshifts and stop codons. PLoS One 6:e22594 (2011).
    External Resources
  64. Rice WR: Sex chromosomes and the evolution of sexual dimorphism. Evolution 38:735-742 (1984).
    External Resources
  65. Rice WR: Genetic hitchhiking and the evolution of reduced genetic activity of the Y sex chromosome. Genetics 116:161-167 (1987).
    External Resources
  66. Rice WR, Chippindale AK: Intersexual ontogenetic conflict. J Evol Biol 14:685-693 (2001).
    External Resources
  67. Robinson MD, Oshlack A: A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol 11:R25 (2010).
    External Resources
  68. Robinson MD, McCarthy DJ, Smyth GK: edgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139-140 (2010).
    External Resources
  69. Schmid M, Steinlein C, Bogart JP, Feichtinger W, León P, et al: The chromosomes of terraranan frogs. Insights into vertebrate cytogenetics. Cytogenet Genome Res 130-131:1-568 (2010).
    External Resources
  70. Seifertova E, Zimmerman LB, Gilchrist MJ, Macha J, Kubickova S, et al: Efficient high-throughput sequencing of a laser microdissected chromosome arm. BMC Genomics 14:357 (2013).
    External Resources
  71. Sémon M, Wolfe KH: Preferential subfunctionalization of slow-evolving genes after allopolyploidization in Xenopus laevis. Proc Natl Acad Sci USA 105:8333-8338 (2008).
    External Resources
  72. Swanson WJ, Vacquier VD: The rapid evolution of reproductive proteins. Nat Rev Genet 3:137-144 (2002).
    External Resources
  73. Toll-Riera M, Bosch N, Bellora N, Castelo R, Armengol L, et al: Origin of primate orphan genes: a comparative genomics approach. Mol Biol Evol 26:603-612 (2008).
    External Resources
  74. Torgerson DG, Singh RS: Rapid evolution through gene duplication and subfunctionalization of the testes-specific alpha4 proteasome subunits in Drosophila. Genetics 168:1421-1432 (2004).
    External Resources
  75. Trapnell C, Pachter L, Salzberg SL: TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25:1105-1111 (2009).
    External Resources
  76. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, et al: Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28:516-520 (2010).
    External Resources
  77. Vicoso B, Charlesworth B: Effective population size and the faster-X effect: an extended model. Evolution 63:2413-2426 (2009).
    External Resources
  78. Vicoso B, Emerson JJ, Zektser Y, Mahajan S, Bachtrog D: Comparative sex chromosome genomics in snakes: differentiation, evolutionary strata, and lack of global dosage compensation. PLoS Biol 11:e1001643 (2013a).
    External Resources
  79. Vicoso B, Kaiser VB, Bachtrog D: Sex-biased gene expression at homomorphic sex chromosomes in emus and its implication for sex chromosome evolution. Proc Natl Acad Sci USA 110:6453-6458 (2013b).
    External Resources
  80. Vilella AJ, Severin J, Ureta-Vidal A, Heng L, Durbin R, Birney E: EnsemblCompara GeneTrees: complete, duplication-aware phylogenetic trees in vertebrates. Genome Res 19:327-335 (2008).
    External Resources
  81. Wolf YI, Novichkov PS, Karev GP, Koonin EV, Lipman DJ: The universal distribution of evolutionary rates of genes and distinct characteristics of eukaryotic genes of different apparent ages. Proc Natl Acad Sci USA 106:7273-7280 (2009).
    External Resources
  82. Wright AE, Mank JE: The scope and strength of sex-specific selection in genome evolution. J Evol Biol 26:1841-1853 (2013).
    External Resources
  83. Wright AE, Moghadam HK, Mank JE: Trade-off between selection for dosage compensation and masculinization on the avian Z chromosome. Genetics 192:1433-1445 (2012).
    External Resources
  84. Wyckoff GJ, Wang W, Wu CI: Rapid evolution of male reproductive genes in the descent of man. Nature 403:304-309 (2000).
    External Resources
  85. Wyman MJ, Cutter AD, Rowe L: Gene duplication in the evolution of sexual dimorphism. Evolution 66:1556-1566 (2012).
    External Resources
  86. Yanai I, Benjamin H, Shmoish M, Chalifa-Caspi V, Shklar M, et al: Genome-wide midrange transcription profiles reveal expression level relationships in human tissue specification. Bioinformatics 21:650-659 (2005).
    External Resources
  87. Yoshimoto S, Okada E, Umemoto H, Tamura K, Uno Y, et al: A W-linked DM-domain gene, DM-W, participates in primary ovary development in Xenopus laevis. Proc Natl Acad Sci USA 105:2469-2474 (2008).
    External Resources
  88. Zhang YE, Vibranovski MD, Krinsky BH, Long M: Age-dependent chromosomal distribution of male-biased genes in Drosophila. Genome Res 20:1526-1533 (2010a).
    External Resources
  89. Zhang YE, Vibranovski MD, Landback P, Marais GA, Long M: Chromosomal redistribution of male-biased genes in mammalian evolution with two bursts of gene gain on the X chromosome. PLoS Biol 8:e1000494 (2010b).
    External Resources
  90. Zhang Z, Li J, Zhao XQ, Wang J, Wong GK, Yu J: KaKs_Calculator: calculating Ka and Ks through model selection and model averaging. Genomics Proteomics Bioinformatics 4:259-263 (2006).
    External Resources

Article / Publication Details

First-Page Preview
Abstract of Original Article

Published online: June 06, 2015
Issue release date: August 2015

Number of Print Pages: 13
Number of Figures: 6
Number of Tables: 2

ISSN: 1424-8581 (Print)
eISSN: 1424-859X (Online)

For additional information: https://www.karger.com/CGR

Copyright / Drug Dosage / Disclaimer

Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.

Article Tools
Article Details

2015, Vol.145, No. 3-4

August 2015

Free Supplementary Material

Article

Recommend This
TOP