Turn off MathJax
Article Contents
Ze-Xian Zhu, Kazumi Matsubara, Foyez Shams, Jason Dobry, Erik Wapstra, Tony Gamble, Stephen D. Sarre, Arthur Georges, Jennifer A. Marshall Graves, Qi Zhou, Tariq Ezaz. Diversity of reptile sex chromosome evolution revealed by cytogenetic and linked-read sequencing. Zoological Research, 2022, 43(5): 719-733. doi: 10.24272/j.issn.2095-8137.2022.127
Citation: Ze-Xian Zhu, Kazumi Matsubara, Foyez Shams, Jason Dobry, Erik Wapstra, Tony Gamble, Stephen D. Sarre, Arthur Georges, Jennifer A. Marshall Graves, Qi Zhou, Tariq Ezaz. Diversity of reptile sex chromosome evolution revealed by cytogenetic and linked-read sequencing. Zoological Research, 2022, 43(5): 719-733. doi: 10.24272/j.issn.2095-8137.2022.127

Diversity of reptile sex chromosome evolution revealed by cytogenetic and linked-read sequencing

doi: 10.24272/j.issn.2095-8137.2022.127
#Authors contributed equally to this work
Funds:  This work was supported by the National Natural Science Foundation of China (32170415, 32061130208), Natural Science Foundation of Zhejiang Province (LD19C190001) and European Research Council Starting Grant (677696) to Q.Z. T.E. was supported by an ARC FT (FT110100733). This project was also partially supported by ARC DP (DP110102262) led by T.E. and University of Canberra Strategic Research Fund awarded to T.E. K.M. was supported by an ARC DP (DP110102262) led by T.E. T.G. was supported by NSF (IOS1146820). F.S. and J.D. were supported by the University of Canberra postgraduate research scholarships Current affiliation: Department of Environmental Biology, College of Bioscience and Biotechnology, Chubu University, Kasugai, Aichi 487-8501, Japan
More Information
  • Reptile sex determination is attracting much attention because the great diversity of sex-determination and dosage compensation mechanisms permits us to approach fundamental questions about mechanisms of sex chromosome turnover. Recent studies have made significant progress in better understanding diversity and conservation of reptile sex chromosomes, with however no reptile master sex determination genes identified. Here we describe an integrated genomics and cytogenetics pipeline, combining probes generated from the microdissected sex chromosomes with transcriptome and genome sequencing to explore the sex chromosome diversity in non-model Australian reptiles. We tested our pipeline on a turtle, two species of geckos, and a monitor lizard. Genes identified on sex chromosomes were compared to the chicken genome to identify homologous regions among the four species. We identified candidate sex determining genes within these regions, including conserved vertebrate sex-determining genes pdgfa, pdgfra amh and wt1, and demonstrated their testis or ovary-specific expression. All four species showed gene-by-gene rather than chromosome-wide dosage compensation. Our results imply that reptile sex chromosomes originated by independent acquisition of sex-determining genes on different autosomes, as well as translocations between different ancestral macro- and microchromosomes. We discuss the evolutionary drivers of the slow differentiation and turnover of reptile sex chromosomes.
  • #Authors contributed equally to this work
  • loading
  • [1]
    Alam SMI, Sarre SD, Gleeson D, Georges A, Ezaz T. 2018. Did lizards follow unique pathways in sex chromosome evolution?. Genes, 9(5): 239. doi: 10.3390/genes9050239
    [2]
    Alföldi J, Di Palma F, Grabherr M, Williams C, Kong LS, Mauceli E, et al. 2011. The genome of the green anole lizard and a comparative analysis with birds and mammals. Nature, 477(7366): 587−591. doi: 10.1038/nature10390
    [3]
    Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. Journal of Molecular Biology, 215(3): 403−410. doi: 10.1016/S0022-2836(05)80360-2
    [4]
    Alvarez-Cubero MJ, Santiago O, Martínez-Labarga C, Martínez-García B, Marrero-Díaz R, Rubio-Roldan A, et al. 2018. Methodology for Y Chromosome Capture: A complete genome sequence of Y chromosome using flow cytometry, laser microdissection and magnetic streptavidin-beads. Scientific Reports, 8(1): 9436. doi: 10.1038/s41598-018-27819-x
    [5]
    Assis R, Zhou Q, Bachtrog D. 2012. Sex-biased transcriptome evolution in Drosophila. Genome Biology and Evolution, 4(11): 1189−1200. doi: 10.1093/gbe/evs093
    [6]
    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 Biology and Evolution, 13(7): evab119. doi: 10.1093/gbe/evab119
    [7]
    Bachtrog D. 2013. Y-chromosome evolution: emerging insights into processes of Y-chromosome degeneration. Nature Reviews Genetics, 14(2): 113−124. doi: 10.1038/nrg3366
    [8]
    Badenhorst D, Stanyon R, Engstrom T, Valenzuela N. 2013. A ZZ/ZW microchromosome system in the spiny softshell turtle, Apalone spinifera, reveals an intriguing sex chromosome conservation in Trionychidae. Chromosome Research, 21(2): 137−147. doi: 10.1007/s10577-013-9343-2
    [9]
    Bellott DW, Page DC. 2021. Dosage-sensitive functions in embryonic development drove the survival of genes on sex-specific chromosomes in snakes, birds, and mammals. Genome Research, 31(2): 198−210. doi: 10.1101/gr.268516.120
    [10]
    Bellott DW, Skaletsky H, Cho TJ, Brown L, Locke D, Chen N, et al. 2017. Avian W and mammalian Y chromosomes convergently retained dosage-sensitive regulators. Nature Genetics, 49(3): 387−394. doi: 10.1038/ng.3778
    [11]
    Birney E, Clamp M, Durbin R. 2004. GeneWise and genomewise. Genome Research, 14(5): 988−995. doi: 10.1101/gr.1865504
    [12]
    Bista B, Valenzuela N. 2020. Turtle insights into the evolution of the reptilian karyotype and the genomic architecture of sex determination. Genes, 11(4): 416. doi: 10.3390/genes11040416
    [13]
    Bista B, Wu ZQ, Literman R, Valenzuela N. 2021. Thermosensitive sex chromosome dosage compensation in ZZ/ZW softshell turtles. Apalone spinifera. Philosophical Transactions of the Royal Society B:Biological Sciences, 376(1833): 20200101. doi: 10.1098/rstb.2020.0101
    [14]
    Brennan J, Tilmann C, Capel B. 2003. Pdgfr-α mediates testis cord organization and fetal Leydig cell development in the XY gonad. Genes & Development, 17(6): 800−810.
    [15]
    Brůna T, Hoff KJ, Lomsadze A, Stanke M, Borodovsky M. 2021. BRAKER2: automatic eukaryotic genome annotation with GeneMark-EP+ and AUGUSTUS supported by a protein database. NAR Genomics and Bioinformatics, 3(1): lqaa108. doi: 10.1093/nargab/lqaa108
    [16]
    Charlesworth B, Charlesworth D. 2000. The degeneration of Y chromosomes. Philosophical Transactions of the Royal Society B:Biological Sciences, 355(1403): 1563−1572. doi: 10.1098/rstb.2000.0717
    [17]
    Cocca E, Petraccioli A, Morescalchi MA, Odierna G, Capriglione T. 2015. Laser microdissection-based analysis of the Y sex chromosome of the Antarctic fish Chionodraco hamatus (Notothenioidei, Channichthyidae). Comparative Cytogenetics, 9(1): 1−15. doi: 10.3897/CompCytogen.v9i1.8731
    [18]
    Cornejo-Páramo P, Dissanayake DSB, Lira-Noriega A, Martínez-Pacheco ML, Acosta A, Ramírez-Suástegui C, et al. 2020. Viviparous reptile regarded to have temperature-dependent sex determination has old XY chromosomes. Genome Biology and Evolution, 12(6): 924−930. doi: 10.1093/gbe/evaa104
    [19]
    Cortez D, Marin R, Toledo-Flores D, Froidevaux L, Liechti A, Waters PD, et al. 2014. Origins and functional evolution of Y chromosomes across mammals. Nature, 508(7497): 488−493.
    [20]
    Cutting A, Chue J, Smith CA. 2013. Just how conserved is vertebrate sex determination?. Developmental Dynamics, 242(4): 380−387. doi: 10.1002/dvdy.23944
    [21]
    Deakin JE, Edwards MJ, Patel H, O'Meally D, Lian JM, Stenhouse R, et al. 2016. Anchoring genome sequence to chromosomes of the central bearded dragon (Pogona vitticeps) enables reconstruction of ancestral squamate macrochromosomes and identifies sequence content of the Z chromosome. BMC Genomics, 17: 447. doi: 10.1186/s12864-016-2774-3
    [22]
    Deakin JE, Ezaz T. 2014. Tracing the evolution of amniote chromosomes. Chromosoma, 123(3): 201−216. doi: 10.1007/s00412-014-0456-y
    [23]
    Deakin JE, Ezaz T. 2019. Understanding the evolution of reptile chromosomes through applications of combined cytogenetics and genomics approaches. Cytogenetic and Genome Research, 157(1–2): 7–20.
    [24]
    Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, et al. 2013. STAR: ultrafast universal RNA-seq aligner. Bioinformatics, 29(1): 15−21. doi: 10.1093/bioinformatics/bts635
    [25]
    Ezaz T, Azad B, O'Meally D, Young MJ, Matsubara K, Edwards MJ, et al. 2013. Sequence and gene content of a large fragment of a lizard sex chromosome and evaluation of candidate sex differentiating gene R-spondin 1. BMC Genomics, 14: 899. doi: 10.1186/1471-2164-14-899
    [26]
    Ezaz T, Quinn AE, Miura I, Sarre SD, Georges A, Marshall Graves JA. 2005. The dragon lizard Pogona vitticeps has ZZ/ZW micro-sex chromosomes. Chromosome Research, 13(8): 763−776. doi: 10.1007/s10577-005-1010-9
    [27]
    Ezaz T, Quinn AE, Sarre SD, O'Meally D, Georges A, Graves JAM. 2009a. Molecular marker suggests rapid changes of sex-determining mechanisms in Australian dragon lizards. Chromosome Research, 17(1): 91−98. doi: 10.1007/s10577-008-9019-5
    [28]
    Ezaz T, Sarre SD, O'Meally D, Graves JAM, Georges A. 2009b. Sex chromosome evolution in lizards: independent origins and rapid transitions. Cytogenetic and Genome Research, 127(2–4): 249–260.
    [29]
    Ezaz T, Srikulnath K, Graves JAM. 2017. Origin of Amniote sex chromosomes: an ancestral super-sex chromosome, or common requirements?. Journal of Heredity, 108(1): 94−105. doi: 10.1093/jhered/esw053
    [30]
    Fu LM, Niu BF, Zhu ZW, Wu ST, Li WZ. 2012. CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics, 28(23): 3150−3152. doi: 10.1093/bioinformatics/bts565
    [31]
    Gamble T, Castoe TA, Nielsen SV, Banks JL, Card DC, Schield DR, et al. 2017. The discovery of XY sex chromosomes in a boa and python. Current Biology, 27(14): 2148−2153.e4. doi: 10.1016/j.cub.2017.06.010
    [32]
    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. Molecular Biology and Evolution, 32(5): 1296−1309. doi: 10.1093/molbev/msv023
    [33]
    Giovannotti M, Trifonov VA, Paoletti A, Kichigin IG, O’Brien PCM, Kasai F, et al. 2017. New insights into sex chromosome evolution in anole lizards (Reptilia, Dactyloidae). Chromosoma, 126(2): 245−260. doi: 10.1007/s00412-016-0585-6
    [34]
    Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, et al. 2011. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnology, 29(7): 644−652. doi: 10.1038/nbt.1883
    [35]
    Gu LQ, Walters JR. 2017. Evolution of sex chromosome dosage compensation in animals: a beautiful theory, undermined by facts and bedeviled by details. Genome Biology and Evolution, 9(9): 2461−2476. doi: 10.1093/gbe/evx154
    [36]
    Harris RS. 2007. Improved Pairwise Alignmnet of Genomic DNA. Ph. D. dissertation, The Pennsylvania State University, University Park.
    [37]
    Herpin A, Schartl M. 2015. Plasticity of gene-regulatory networks controlling sex determination: of masters, slaves, usual suspects, newcomers, and usurpators. EMBO Reports, 16(10): 1260−1274. doi: 10.15252/embr.201540667
    [38]
    Hill PL, Burridge CP, Ezaz T, Wapstra E. 2018. Conservation of sex-linked markers among conspecific populations of a viviparous skink, Niveoscincus ocellatus, exhibiting genetic and temperature-dependent sex determination. Genome Biology and Evolution, 10(4): 1079−1087. doi: 10.1093/gbe/evy042
    [39]
    Hiort O. 2013. The differential role of androgens in early human sex development. BMC Medicine, 11: 152. doi: 10.1186/1741-7015-11-152
    [40]
    Hobza R, Vyskot B. 2007. Laser microdissection‐based analysis of plant sex chromosomes. Methods in Cell Biology, 82: 433−453.
    [41]
    Holleley CE, O'Meally D, Sarre SD, Marshall Graves JA, Ezaz T, Matsubara K, et al. 2015. Sex reversal triggers the rapid transition from genetic to temperature-dependent sex. Nature, 523(7558): 79−82. doi: 10.1038/nature14574
    [42]
    Hossain A, Saunders GF. 2001. The human sex-determining gene SRY is a direct target of WT1. Journal of Biological Chemistry, 276(20): 16817–16823.
    [43]
    Iannucci A, Altmanová M, Ciofi C, Ferguson-Smith M, Milan M, Pereira JC, et al. 2019. Conserved sex chromosomes and karyotype evolution in monitor lizards (Varanidae). Heredity, 123(2): 215−227. doi: 10.1038/s41437-018-0179-6
    [44]
    International Chicken Genome Sequencing Consortium. 2004. Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature, 432(7018): 695−716. doi: 10.1038/nature03154
    [45]
    Itoh Y, Melamed E, Yang X, Kampf K, Wang S, Yehya N, et al. 2007. Dosage compensation is less effective in birds than in mammals. Journal of Biology, 6(1): 2. doi: 10.1186/jbiol53
    [46]
    Kawagoshi T, Uno Y, Matsubara K, Matsuda Y, Nishida C. 2009. The ZW micro-sex chromosomes of the Chinese soft-shelled turtle (Pelodiscus sinensis, Trionychidae, Testudines) have the same origin as chicken chromosome 15. Cytogenet. Cytogenetic and Genome Research, 125(2): 125−131. doi: 10.1159/000227837
    [47]
    Kawagoshi T, Uno Y, Nishida C, Matsuda Y. 2014. The Staurotypus turtles and aves share the same origin of sex chromosomes but evolved different types of heterogametic sex determination. PLoS One, 9(8): e105315. doi: 10.1371/journal.pone.0105315
    [48]
    Kichigin IG, Giovannotti M, Makunin AI, Ng BL, Kabilov MR, Tupikin AE, et al. 2016. Evolutionary dynamics of Anolis sex chromosomes revealed by sequencing of flow sorting-derived microchromosome-specific DNA. Molecular Genetics and Genomics, 291(5): 1955−1966. doi: 10.1007/s00438-016-1230-z
    [49]
    Kostmann A, Kratochvíl L, Rovatsos M. 2021. Poorly differentiated XX/XY sex chromosomes are widely shared across skink radiation. Philosophical Transactions of the Royal Society B:Biological Sciences, 288(1943): 20202139. doi: 10.1098/rspb.2020.2139
    [50]
    Koubová M, Pokorná MJ, Rovatsos M, Farkačová K, Altmanová M, Kratochvíl L. 2014. Sex determination in Madagascar geckos of the genus Paroedura (Squamata: Gekkonidae): are differentiated sex chromosomes indeed so evolutionary stable?. Chromosome Research, 22(4): 441−452. doi: 10.1007/s10577-014-9430-z
    [51]
    Kratochvíl L, Gamble T, Rovatsos M. 2021a. Sex chromosome evolution among amniotes: is the origin of sex chromosomes non-random?. Philosophical Transactions of the Royal Society B:Biological Sciences, 376(1833): 20200108. doi: 10.1098/rstb.2020.0108
    [52]
    Kratochvíl L, Stöck M, Rovatsos M, Bullejos M, Herpin A, Jeffries DL, et al. 2021b. Expanding the classical paradigm: what we have learnt from vertebrates about sex chromosome evolution. Philosophical Transactions of the Royal Society B:Biological Sciences, 376(1833): 20200097. doi: 10.1098/rstb.2020.0097
    [53]
    Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with Bowtie 2. Nature Methods, 9(4): 357−359. doi: 10.1038/nmeth.1923
    [54]
    Lee L, Montiel EE, Navarro-Domínguez BM, Valenzuela N. 2019a. Chromosomal rearrangements during turtle evolution altered the synteny of genes involved in vertebrate sex determination. Cytogenetic and Genome Research, 157(1–2): 77–88.
    [55]
    Lee L, Montiel EE, Valenzuela N. 2019b. Discovery of putative XX/XY Male heterogamety in Emydura subglobosa turtles exposes a novel trajectory of sex chromosome evolution in Emydura. Cytogenetic and Genome Research, 158(3): 160–169.
    [56]
    Lewin HA, Robinson GE, Kress WJ, Baker WJ, Coddington J, Crandall KA, et al. 2018. Earth BioGenome Project: sequencing life for the future of life. Proceedings of the National Academy of Sciences of the United States of America, 115(17): 4325−4333. doi: 10.1073/pnas.1720115115
    [57]
    Li B, Dewey CN. 2011. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics, 12: 323. doi: 10.1186/1471-2105-12-323
    [58]
    Li H. 2011. A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics, 27(21): 2987−2993. doi: 10.1093/bioinformatics/btr509
    [59]
    Lind AL, Lai YYY, Mostovoy Y, Holloway AK, Iannucci A, Mak ACY, et al. 2019. Genome of the Komodo dragon reveals adaptations in the cardiovascular and chemosensory systems of monitor lizards. Nature Ecology & Evolution, 3(8): 1241−1252.
    [60]
    Liu J, Wang ZJ, Li J, Xu LH, Liu JQ, Feng SH, et al. 2021. A new emu genome illuminates the evolution of genome configuration and nuclear architecture of avian chromosomes. Genome Research, 31(3): 497−511.
    [61]
    Luo RB, Liu BH, Xie YL, Li ZY, Huang WH, Yuan JY, et al. 2012. SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. GigaScience, 1(1): 18. doi: 10.1186/2047-217X-1-18
    [62]
    Mank JE, Avise JC. 2009. Evolutionary diversity and turn-over of sex determination in teleost fishes. Sexual Development, 3(2–3): 60–67.
    [63]
    Marin R, Cortez D, Lamanna F, Pradeepa MM, Leushkin E, Julien P, et al. 2017. Convergent origination of a Drosophila-like dosage compensation mechanism in a reptile lineage. Genome Research, 27(12): 1974−1987. doi: 10.1101/gr.223727.117
    [64]
    Martinez PA, Ezaz T, Valenzuela N, Georges A, Marshall Graves JA. 2008. An XX/XY heteromorphic sex chromosome system in the Australian chelid turtle Emydura macquarii: a new piece in the puzzle of sex chromosome evolution in turtles. Chromosome Research, 16(6): 815−825. doi: 10.1007/s10577-008-1228-4
    [65]
    Matsubara K, Gamble T, Matsuda Y, Zarkower D, Sarre SD, Georges A, et al. 2014a. Non-homologous sex chromosomes in two geckos (Gekkonidae: Gekkota) with female heterogamety. Cytogenetic and Genome Research, 143(4): 251−258. doi: 10.1159/000366172
    [66]
    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). Molecular Cytogenetics, 6(1): 60. doi: 10.1186/1755-8166-6-60
    [67]
    Matsubara K, Sarre SD, Georges A, Matsuda Y, Graves JAM, Ezaz T. 2014b. Highly differentiated ZW sex microchromosomes in the Australian Varanus species evolved through rapid amplification of repetitive sequences. PLoS One, 9(4): e95226. doi: 10.1371/journal.pone.0095226
    [68]
    Mezzasalma M, Guarino FM, Odierna G. 2021. Lizards as model organisms of sex chromosome evolution: what we really know from a systematic distribution of available data?. Genes, 12(9): 1341. doi: 10.3390/genes12091341
    [69]
    Miura I. 2017. Sex determination and sex chromosomes in amphibia. Sexual Development, 11(5–6): 298–306.
    [70]
    Montiel EE, Badenhorst D, Tamplin J, Burke RL, Valenzuela N. 2017. Discovery of the youngest sex chromosomes reveals first case of convergent co-option of ancestral autosomes in turtles. Chromosoma, 126(1): 105−113. doi: 10.1007/s00412-016-0576-7
    [71]
    O'Meally D, Ezaz T, Georges A, Sarre SD, Graves JAM. 2012. Are some chromosomes particularly good at sex? Insights from amniotes. Chromosome Research, 20(1): 7−19. doi: 10.1007/s10577-011-9266-8
    [72]
    Pennell MW, Kirkpatrick M, Otto SP, Vamosi JC, Peichel CL, Valenzuela N, et al. 2015. Y fuse? Sex chromosome fusions in fishes and reptiles. PLoS Genetics, 11(5): e1005237. doi: 10.1371/journal.pgen.1005237
    [73]
    Pensabene E, Kratochvíl L, Rovatsos M. 2020. Independent evolution of sex chromosomes in eublepharid geckos, a lineage with environmental and genotypic sex determination. Life, 10(12): 342. doi: 10.3390/life10120342
    [74]
    Pokorná M, Rábová M, Ráb P, Ferguson-Smith MA, Rens W, Kratochvíl L. 2010. Differentiation of sex chromosomes and karyotypic evolution in the eye-lid geckos (Squamata: Gekkota: Eublepharidae), a group with different modes of sex determination. Chromosome Research, 18(7): 809−820. doi: 10.1007/s10577-010-9154-7
    [75]
    Pyron RA, Burbrink FT, Wiens JJ. 2013. A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evolutionary Biology, 13: 93.
    [76]
    Rhen T, Jangula A, Schroeder A, Woodward-Bosh R. 2009. The platelet-derived growth factor signaling system in snapping turtle embryos, Chelydra serpentina: Potential role in temperature-dependent sex determination and testis development. General and Comparative Endocrinology, 161(3): 335−343.
    [77]
    Rhie A, McCarthy SA, Fedrigo O, Damas J, Formenti G, Koren S, et al. 2021. Towards complete and error-free genome assemblies of all vertebrate species. Nature, 592(7856): 737−746. doi: 10.1038/s41586-021-03451-0
    [78]
    Rovatsos M, Gamble T, Nielsen SV, Georges A, Ezaz T, Kratochvíl L. 2021. Do male and female heterogamety really differ in expression regulation? Lack of global dosage balance in pygopodid geckos. Philosophical Transactions of the Royal Society B:Biological Sciences, 376(1833): 20200102. doi: 10.1098/rstb.2020.0102
    [79]
    Rovatsos M, Rehák I, Velenský P, Kratochvíl L. 2019. Shared ancient sex chromosomes in varanids, beaded lizards, and alligator lizards. Molecular Biology and Evolution, 36(6): 1113−1120. doi: 10.1093/molbev/msz024
    [80]
    Rupp SM, Webster TH, Olney KC, Hutchins ED, Kusumi K, Sayres MAW. 2017. Evolution of dosage compensation in Anolis carolinensis, a reptile with XX/XY chromosomal sex determination. Genome Biology and Evolution, 9(1): 231−240.
    [81]
    Sankovic N, Delbridge ML, Grützner F, Ferguson-Smith MA, O'Brien PCM, Graves JAM. 2006. Construction of a highly enriched marsupial Y chromosome-specific BAC sub-library using isolated Y chromosomes. Chromosome Research, 14(6): 657−664. doi: 10.1007/s10577-006-1076-z
    [82]
    Schield DR, Card DC, Hales NR, Perry BW, Pasquesi GM, Blackmon H, et al. 2019. The origins and evolution of chromosomes, dosage compensation, and mechanisms underlying venom regulation in snakes. Genome Research, 29(4): 590−601. doi: 10.1101/gr.240952.118
    [83]
    Skaletsky H, Kuroda-Kawaguchi T, Minx PJ, Cordum HS, Hillier L, Brown LG, et al. 2003. The male-specific region of the human Y chromosome is a mosaic of discrete sequence classes. Nature, 423(6942): 825−837. doi: 10.1038/nature01722
    [84]
    Stöck M, Kratochvíl L, Kuhl H, Rovatsos M, Evans BJ, Suh A, et al. 2021. A brief review of vertebrate sex evolution with a pledge for integrative research: towards ‘sexomics’. Philosophical Transactions of the Royal Society B: Biological Sciences, 376(1832): 20200426.
    [85]
    Tarailo-Graovac M, Chen NS. 2009. Using RepeatMasker to identify repetitive elements in genomic sequences. Current Protocols in Bioinformatics, Chapter 4: Unit 4.10.
    [86]
    Thépot D. 2021. Sex chromosomes and master sex-determining genes in turtles and other reptiles. Genes, 12(11): 1822. doi: 10.3390/genes12111822
    [87]
    Tomaszkiewicz M, Rangavittal S, Cechova M, Sanchez RC, Fescemyer HW, Harris R, et al. 2016. A time-and cost-effective strategy to sequence mammalian Y Chromosomes: an application to the de novo assembly of gorilla Y. Genome Research, 26(4): 530−540. doi: 10.1101/gr.199448.115
    [88]
    Vicoso B, Bachtrog D. 2015. Numerous transitions of sex chromosomes in Diptera. PLoS Biology, 13(4): e1002078.
    [89]
    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 Biology, 11(8): e1001643. doi: 10.1371/journal.pbio.1001643
    [90]
    Wang O, Chin R, Cheng XF, Wu MKY, Mao Q, Tang JB, et al. 2019. Efficient and unique cobarcoding of second-generation sequencing reads from long DNA molecules enabling cost-effective and accurate sequencing, haplotyping, and de novo assembly. Genome Research, 29(5): 798−808. doi: 10.1101/gr.245126.118
    [91]
    Wang Z, Pascual-Anaya J, Zadissa A, Li WQ, Niimura Y, Huang ZY, et al. 2013. The draft genomes of soft-shell turtle and green sea turtle yield insights into the development and evolution of the turtle-specific body plan. Nature Genetics, 45(6): 701−706. doi: 10.1038/ng.2615
    [92]
    Waters PD, Patel HR, Ruiz-Herrera A, Álvarez-González L, Lister NC, Simakov O, et al. 2021a. Microchromosomes are building blocks of bird, reptile, and mammal chromosomes. Proceedings of the National Academy of Sciences of the United States of America, 118(45): e2112494118. doi: 10.1073/pnas.2112494118
    [93]
    Waters PD, Patel HR, Ruiz-Herrera A, Álvarez-González L, Lister NC, Simakov O, et al. 2021b. Microchromosomes are building blocks of bird, reptile and mammal chromosomes. bioRxiv,doi: 10.1101/2021.07.06.451394.
    [94]
    Weisenfeld NI, Kumar V, Shah P, Church DM, Jaffe DB. 2017. Direct determination of diploid genome sequences. Genome Research, 27(5): 757−767.
    [95]
    Wilson JD, Griffin JE, George FW. 1980. Sexual differentiation: early hormone synthesis and action. Biology of Reproduction, 22(1): 9−17. doi: 10.1095/biolreprod22.1.9
    [96]
    Yano A, Guyomard R, Nicol B, Jouanno E, Quillet E, Klopp C, et al. 2012. An immune-related gene evolved into the master sex-determining gene in rainbow trout. Oncorhynchus mykiss. Current Biology, 22(15): 1423−1428. doi: 10.1016/j.cub.2012.05.045
    [97]
    Zhou Q, Zhang JL, Bachtrog D, An N, Huang QF, Jarvis ED, et al. 2014. Complex evolutionary trajectories of sex chromosomes across bird taxa. Science, 346(6215): 1246338. doi: 10.1126/science.1246338
    [98]
    Zhou Y, Shearwin-Whyatt L, Li J, Song ZZ, Hayakawa T, Stevens D, et al. 2021. Platypus and echidna genomes reveal mammalian biology and evolution. Nature, 592(7856): 756−762. doi: 10.1038/s41586-020-03039-0
    [99]
    Zhou YJ, Sun W, Cai H, Bao HS, Zhang Y, Qian GY, et al. 2019. The role of anti-müllerian hormone in testis differentiation reveals the significance of the TGF-β pathway in reptilian sex determination. Genetics, 213(4): 1317−1327. doi: 10.1534/genetics.119.302527
  • ZR-2022-127-Supplementary Materials.pdf
  • 加载中

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Figures(6)

    Article Metrics

    Article views (423) PDF downloads(71) Cited by()
    Proportional views
    Related

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return