Do male and female heterogamety really differ in expression regulation? Lack of global dosage balance in pygopodid geckos
Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
34304587
PubMed Central
PMC8310713
DOI
10.1098/rstb.2020.0102
Knihovny.cz E-zdroje
- Klíčová slova
- Gekkota, RNA-seq, dosage compensation, reptiles, sex chromosomes, sex determination,
- MeSH
- ještěři genetika MeSH
- kompenzace dávky (genetika) * MeSH
- pohlavní chromozomy genetika MeSH
- regulace genové exprese * MeSH
- zvířata MeSH
- Check Tag
- mužské pohlaví MeSH
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
Differentiation of sex chromosomes is thought to have evolved with cessation of recombination and subsequent loss of genes from the degenerated partner (Y and W) of sex chromosomes, which in turn leads to imbalance of gene dosage between sexes. Based on work with traditional model species, theory suggests that unequal gene copy numbers lead to the evolution of mechanisms to counter this imbalance. Dosage compensation, or at least achieving dosage balance in expression of sex-linked genes between sexes, has largely been documented in lineages with male heterogamety (XX/XY sex determination), while ZZ/ZW systems are assumed to be usually associated with the lack of chromosome-wide gene dose regulatory mechanisms. Here, we document that although the pygopodid geckos evolved male heterogamety with a degenerated Y chromosome 32-72 Ma, one species in particular, Burton's legless lizard (Lialis burtonis), does not possess dosage balance in the expression of genes in its X-specific region. We summarize studies on gene dose regulatory mechanisms in animals and conclude that there is in them no significant dichotomy between male and female heterogamety. We speculate that gene dose regulatory mechanisms are likely to be related to the general mechanisms of sex determination instead of type of heterogamety. This article is part of the theme issue 'Challenging the paradigm in sex chromosome evolution: empirical and theoretical insights with a focus on vertebrates (Part II)'.
Bell Museum of Natural History University of Minnesota Saint Paul MN 55108 USA
Department of Biological Sciences Marquette University Milwaukee WI 53201 USA
Department of Ecology Charles University Prague CZ 12844 Czech Republic
Florida Museum of Natural History University of Florida Gainesville FL 32611 USA
Milwaukee Public Museum 800 W Wells Street Milwaukee WI 53233 USA
Zobrazit více v PubMed
Beukeboom LW, Perrin N. 2014. The evolution of sex determination. Oxford, UK: Oxford University Press & British Academy.
Birchler JA, Riddle NC, Auger DL, Veitia RA. 2005. Dosage balance in gene regulation: biological implications. Trends Genet. 21, 219-226. (10.1016/j.tig.2005.02.010) PubMed DOI
Birchler JA. 2014. Facts and artifacts in studies of gene expression in aneuploids and sex chromosomes. Chromosoma 123, 459-469. (10.1007/s00412-014-0478-5) PubMed DOI
Zhang Y, Oliver B. 2007. Dosage compensation goes global. Curr. Opin Genet. Dev. 17, 113-120. (10.1016/j.gde.2007.02.002) PubMed DOI
Dürrbaum M, Storchová Z. 2016. Effects of aneuploidy on gene expression: implications for cancer. FEBS J. 283, 791-802. (10.1111/febs.13591) PubMed DOI
Gu L, Walters JR. 2017. Evolution of sex chromosome dosage compensation in animals: a beautiful theory, undermined by facts and bedeviled by details. Genome Biol. Evol. 9, 2461-2476. (10.1093/gbe/evx154) PubMed DOI PMC
Muller HJ. 1918. Genetic variability, twin hybrids and constant hybrids, in a case of balanced lethal factors. Genetics 3, 422-499. (10.1093/genetics/3.5.422) PubMed DOI PMC
Ohno S. 1967. Sex chromosomes and sex-linked genes. Berlin, Germany: Springer.
Brockdorff T, Turner BM. 2015. Dosage compensation in mammals. Cold Spring Harb. Perspect. Biol. 7, a019406. (10.1101/cshperspect.a019406) PubMed DOI PMC
Uebbing S, Konzer A, Xu L, Backström N, Brunström B, Bergquist J, Ellegren H. 2015. Quantitative mass spectrometry reveals partial translational regulation for dosage compensation in chicken. Mol. Biol. Evol. 32, 2716-2725. (10.1093/molbev/msv147) PubMed DOI PMC
Picard MAL, Cosseau C, Ferré S, Quack T, Grevelding CG, Couté Y, Vicoso B. 2018. Evolution of gene dosage on the Z-chromosome of schistosome parasites. eLife 7, e35684. (10.7554/eLife.35684) PubMed DOI PMC
Acosta A, Suárez-Varón G, Rodríguez-Miranda LA, Lira-Noriega A, Aguilar-Gómez D, Gutiérrez-Mariscal M, Hernández-Gallegos O, Méndez-de-la-Cruz F, Cortez D. 2019. Corytophanids replaced the pleurodont XY system with a new pair of XY chromosomes. Genome Biol. Evol. 11, 2666-2677. (10.1093/gbe/evz196) PubMed DOI PMC
Nielsen SV, Guzmán-Méndez IA, Gamble T, Blumer M, Pinto BJ, Kratochvíl L, Rovatsos M. 2019. Escaping the evolutionary trap? Sex chromosome turnover in basilisks and related lizards (Corytophanidae: Squamata). Biol. Lett. 15, 20190498. (10.1098/rsbl.2019.0498) PubMed DOI PMC
Mank JE. 2009. The W, X, Y and Z of sex-chromosome dosage compensation. Trends Genet. 25, 226-233. (10.1016/j.tig.2009.03.005) PubMed DOI PMC
Vicoso B, Emerson JJ, Zektser Y, Mahajan S, Bachtrog D. 2013. Comparative sex chromosome genomics in snakes: differentiation, evolutionary strata, and lack of global dosage compensation. PLoS Biol. 11, e1001643. (10.1371/journal.pbio.1001643) PubMed DOI PMC
Rovatsos M, Rehák I, Velenský P, Kratochvíl L. 2019. Shared ancient sex chromosomes in varanids, beaded lizards and alligator lizards. Mol. Biol. Evol. 36, 1113-1120. (10.1093/molbev/msz024) PubMed DOI
Gu L, Reilly PF, Lewis JJ, Reed RD, Andolfatto P, Walters JR. 2019. Dichotomy of dosage compensation along the neo Z chromosome of the monarch butterfly. Curr. Biol. 29, 4071-4077. (10.1016/j.cub.2019.09.056) PubMed DOI PMC
Huylmans AK, Toups MA, Macon A, Gammerdinger WJ, Vicoso B. 2019. Sex-biased gene expression and dosage compensation on the Artemia franciscana Z-chromosome. Genome Biol. Evol. 11, 1033-1044. (10.1093/gbe/evz053) PubMed DOI PMC
Rovatsos M, Kratochvíl L. 2021. Evolution of dosage compensation does not depend on genomic background. Mol. Ecol. 30, 1836-1845. (10.1111/mec.15853) PubMed DOI
Vicoso B, Bachtrog D. 2009. Progress and prospects toward our understanding of the evolution of dosage compensation. Chromosome Res. 17, 585-602. (10.1007/s10577-009-9053-y) PubMed DOI PMC
Wilson SMA, Makova KD. 2011. Genome analyses substantiate male mutation bias in many species. BioEssays 33, 938-945. (10.1002/bies.201100091) PubMed DOI PMC
Mank JE, Vicoso B, Berlin S, Charlesworth B. 2010. Effective population size and the faster-X effect: empirical results and their interpretation. Evolution 64, 663-674. (10.1111/j.1558-5646.2009.00853.x) PubMed DOI
Naurin S, Hansson B, Bensch S, Hasselquist D. 2012. Why does dosage compensation differ between XY and ZW taxa? Trends Genet. 26, 15-20. (10.1016/j.tig.2009.11.006) PubMed DOI
Mank JE. 2013. Sex chromosome dosage compensation: definitely not for everyone. Trends Genet. 29, 677-683. (10.1016/j.tig.2013.07.005) PubMed DOI
Mullon C, Wright AE, Reuter M, Pomiankowski A, Mank JE. 2015. Evolution of dosage compensation under sexual selection differs between X and Z chromosomes. Nat. Commun. 6, 7720. (10.1038/ncomms8720) PubMed DOI PMC
Gamble T, Coryell J, Ezaz T, Lynch J, Scantlebury DP, Zarkower D. 2015. Restriction site-associated DNA sequencing (RAD-seq) reveals an extraordinary number of transitions among gecko sex-determining systems. Mol. Biol. Evol. 32, 1296-1309. (10.1093/molbev/msv023) PubMed DOI
Johnson PM, Kratochvíl L. 2016. What was the ancestral sex-determining mechanism in amniote vertebrates? Biol Rev. 91, 1-12. (10.1111/brv.12156) PubMed DOI
Rovatsos M, Farkačová K, Altmanová M, Johnson Pokorná M, Kratochvíl L. 2019. The rise and fall of differentiated sex chromosomes in geckos. Mol. Ecol. 28, 3042-3052. (10.1111/mec.15126) PubMed DOI
Jiang X, Biedler JK, Qi Y, Hall AB, Tu Z. 2015. Complete dosage compensation in Anopheles stephensi and the evolution of sex-biased genes in mosquitoes. Genome Biol. Evol. 7, 1914-1924. (10.1093/gbe/evv115) PubMed DOI PMC
Linger RJ, Belikoff EJ, Scott MJ. 2015. Dosage compensation of X-linked Muller element F genes but not X-linked transgenes in the Australian sheep blowfly. PLoS ONE 10, e0141544. (10.1371/journal.pone.0141544) PubMed DOI PMC
Vicoso B, Bachtrog D. 2015. Numerous transitions of sex chromosomes in Diptera. PLoS Biol. 13, e1002078. (10.1371/journal.pbio.1002078) PubMed DOI PMC
Pal A, Vicoso B. 2015. The X chromosome of hemipteran insects: conservation, dosage compensation and sex-biased expression. Genome Biol. Evol. 7, 3259-3268. (10.1093/gbe/evv215) PubMed DOI PMC
Duan J, et al. 2019. Dosage compensation and gene expression of the X chromosome in sheep. G3 9, 305-314. (10.1534/g3.118.200815) PubMed DOI PMC
Darolti I, et al. 2019. Extreme heterogeneity in sex chromosome differentiation and dosage compensation in livebearers. Proc. Natl Acad. Sci. USA 116, 19 031-19 036. (10.1073/pnas.1905298116) PubMed DOI PMC
Uetz P, Freed P, Hošek J. 2020. The Reptile Database. See http://www.reptile-database.org (accessed 8 March 2020).
Vitt LJ, Caldwell JP. 2013. Herpetology: An introductory biology of amphibians and reptiles, 4th edn. New York, NY: Academic Press.
Matsubara K, Knopp T, Sarre SD, Georges A, Ezaz T. 2013. Karyotypic analysis and FISH mapping of microsatellite motifs reveal highly differentiated XX/XY sex chromosomes in the pink-tailed worm-lizard (Aprasia parapulchella, Pygopodidae, Squamata). Mol Cytogenet. 6, 60. (10.1186/1755-8166-6-60) PubMed DOI PMC
King M. 1987. Chromosomal evolution in the Diplodactylinae (Gekkonidae: Reptilia). I. Evolutionary relationships and patterns of change. Aust. J. Zool. 35, 507-531. (10.1071/ZO9870507) DOI
Gorman GC, Gress F. 1970. Sex chromosomes of a pygopodid lizard, Lialis burtonis. Experientia 26, 206-207. (10.1007/bf01895586) PubMed DOI
Rovatsos M, Johnson Pokorná M, Altmanová M, Kratochvíl L. 2016. Mixed-up sex chromosomes: identification of sex chromosomes in the X1X1X2X2/X1X2Y system of the legless lizards of the genus Lialis (Squamata: Gekkota: Pygopodidae). Cytogenet Genome Res. 149, 282-289. (10.1159/000450734) PubMed DOI
Bolger AM, Lohse M, Usadel B. 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114-2120. (10.1093/bioinformatics/btu170) PubMed DOI PMC
Andrews S. 2010. FastQC: a quality control tool for high throughput sequence data. See https://www.bioinformatics.babraham.ac.uk/projects/fastqc/.
Ewels P, Magnusson M, Lundin S, Käller M. 2016. MultiQC: summarize analysis results for multiple tools and samples in a single report. Bioinformatics 32, 3047-3048. (10.1093/bioinformatics/btw354) PubMed DOI PMC
Grabherr MG, et al. . 2011. Full-length transcriptome assembly from RNA-seq data without a reference genome. Nat. Biotechnol. 29, 644-652. (10.1038/nbt.1883) PubMed DOI PMC
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J. Mol. Biol. 215, 403-410. (10.1016/S0022-2836(05)80360-2) PubMed DOI
Alföldi J, et al. . 2011. The genome of the green anole lizard and a comparative analysis with birds and mammals. Nature 477, 587-591. (10.1038/nature10390) PubMed DOI PMC
Pokorná M, Giovannotti M, Kratochvíl L, Caputo V, Olmo E, Ferguson-Smith MA, Rens W. 2012. Conservation of chromosomes syntenic with avian autosomes in squamate reptiles revealed by comparative chromosome painting. Chromosoma 121, 409-418. (10.1007/s00412-012-0371-z) PubMed DOI
Nguyen P, Sýkorová M, Šíchová J, Kůta V, Dalíková M, Čapková Frydrychová R, Neven LG, Sahara K, Marec F. 2013. Neo-sex chromosomes and adaptive potential in tortricid pests. Proc. Natl Acad. Sci. USA 110, 6931-6936. (10.1073/pnas.1220372110) PubMed DOI PMC
Rovatsos M, Vukić J, Altmanová M, Johnson Pokorná M, Moravec J, Kratochvíl L. 2016. Conservation of sex chromosomes in lacertid lizards. Mol. Ecol. 25, 3120-3126. (10.1111/mec.13635) PubMed DOI
Ye J, Coulouris G, Zaretskaya I, Cutcutache I, Rozen S, Madden TL. 2012. Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinf. 13, 134. (10.1186/1471-2105-13-134) PubMed DOI PMC
Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG. 2012. Primer3--new capabilities and interfaces. Nucleic Acid Res. 40, e115. (10.1093/nar/gks596) PubMed DOI PMC
Rovatsos M, Altmanová M, Pokorná M, Kratochvíl L. 2014. Conserved sex chromosomes across adaptively radiated Anolis lizards. Evolution 68, 2079-2085. (10.1111/evo.12357) PubMed DOI
Griffin DK, Robertson LB, Tempest HG, Skinner BM. 2007. The evolution of the avian genome as revealed by comparative molecular cytogenetics. Cytogenet Genome Res. 117, 64-77. (10.1159/000103166) PubMed DOI
Skipwith PL, Bi K, Oliver PM. 2019. Relicts and radiations: Phylogenomics of an Australasian lizard clade with east Gondwanan origins (Gekkota: Diplodactyloidea). Mol. Phylogenet. Evol. 140, 106589. (10.1016/j.ympev.2019.106589) PubMed DOI
Augstenová B, Pensabene E, Veselý M, Kratochvíl L, Rovatsos M. 2021. Are geckos special in sex determination? Independently evolved differentiated ZZ/ZW sex chromosomes in carphodactylid geckos. Genome Biol. Evol. evab119. (10.1093/gbe/evab119) PubMed DOI PMC
Gamble T, Greenbaum E, Jackman TR, Bauer AM. 2015. Into the light: diurnality has evolved multiple times in geckos. Biol. J. Linn. Soc. Lond. 115, 896-910. (10.1111/bij.12536) DOI
Zheng Y, Wiens JJ. 2016. Combining phylogenomic and supermatrix approaches, and a time-calibrated phylogeny for squamate reptiles (lizards and snakes) based on 52 genes and 4162 species. Mol. Phylogenet. Evol. 94, 537-547. (10.1016/j.ympev.2015.10.009) PubMed DOI
Nielsen SV, Daza JD, Pinto BJ, Gamble T. 2019. ZZ/ZW sex chromosomes in the endemic Puerto Rican leaf-toed gecko (Phyllodactylus wirshingi). Cytogenet Genome Res. 157, 89-97. (10.1159/000496379) PubMed DOI
Kawai A, Ishijima J, Nishida C, Kosaka A, Ota H, Kohno S, Matsuda Y. 2009. The ZW sex chromosomes of Gekko hokouensis (Gekkonidae, Squamata) represent highly conserved homology with those of avian species. Chromosoma 118, 43-51. (10.1007/s00412-008-0176-2) PubMed DOI
Wheeler BS, Anderson E, Frøkjær-Jensen C, Bian Q, Jorgensen E, Meyer BJ. 2016. Chromosome-wide mechanisms to decouple gene expression from gene dose during sex-chromosome evolution. eLife 5, e17365. (10.7554/eLife.17365) PubMed DOI PMC
Albritton SE, Kranz A-L, Rao P, Kramer M, Dieterich C, Ercan S. 2014. Sex-biased gene expression and evolution of the X chromosome in nematodes. Genetics 197, 865-883. (10.1534/genetics.114.163311) PubMed DOI PMC
Julien P, Brawand D, Soumillon M, Necsulea A, Liechti A, Schütz F, Daish T, Grützner F, Kaessmann H. 2012. Mechanisms and evolutionary patterns of mammalian and avian dosage compensation. PLoS Biol. 10, e1001328. (10.1371/journal.pbio.1001328) PubMed DOI PMC
Clinton M. 1998. Sex determination and gonadal development: a bird's eye view. J. Exp. Zool. 281, 457-465. (10.1002/(SICI)1097-010X(19980801)281:5<457::AID-JEZ10>3.0.CO;2-6) PubMed DOI
Smith CA, Roeszler KN, Ohnesorg T, Cummins DM, Farlie PG, Doran TJ, Sinclair AH. 2009. The avian Z-linked gene DMRT1 is required for male sex determination in the chicken. Nature 461, 267-271. (10.1038/nature08298) PubMed DOI
Rovatsos M, Augstenová B, Altmanová M, Sloboda M, Kodym P, Kratochvíl L. 2018. Triploid colubrid snake provides insight into the mechanism of sex determination in advanced snakes. Sex Dev. 12, 251-255. (10.1159/000490124) PubMed DOI
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. (10.1038/ng.948) PubMed DOI PMC
Baker BS, Belote JM, 1983. Sex determination and dosage compensation in Drosophila melanogaster. Annu. Rev. Genet. 17, 345-393. (10.1146/annurev.ge.17.120183.002021) PubMed DOI
Zanetti S, Puoti A, 2013. Sex determination in the Caenorhabditis elegans germline. In Germ cell development in C. elegans. Advances in experimental medicine and biology (ed. Schedl T), vol. 757, pp. 41-69. New York, NY: Springer. PubMed
Sex chromosome evolution among amniotes: is the origin of sex chromosomes non-random?
figshare
10.6084/m9.figshare.c.5450571