Cytogenetic characterization and description of an X1X1X2X2/X1X2Y sex chromosome system in Collichthys lucidus (Richardson, 1844)

ZHANG Shoukang; ZHENG Jiao; ZHANG Jing; WANG Zhiyong; WANG Yilei; CAI Mingyi

doi:10.1007/s13131-018-1152-1

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Article Navigation > Acta Oceanologica Sinica > 2018 > 37(4): 34-39

ZHANG Shoukang, ZHENG Jiao, ZHANG Jing, WANG Zhiyong, WANG Yilei, CAI Mingyi. Cytogenetic characterization and description of an X1X1X2X2/X1X2Y sex chromosome system in Collichthys lucidus (Richardson, 1844)[J]. Acta Oceanologica Sinica, 2018, 37(4): 34-39. doi: 10.1007/s13131-018-1152-1

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ZHANG Shoukang, ZHENG Jiao, ZHANG Jing, WANG Zhiyong, WANG Yilei, CAI Mingyi. Cytogenetic characterization and description of an X₁X₁X₂X₂/X₁X₂Y sex chromosome system in Collichthys lucidus (Richardson, 1844)[J]. Acta Oceanologica Sinica, 2018, 37(4): 34-39. doi: 10.1007/s13131-018-1152-1

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Cytogenetic characterization and description of an X₁X₁X₂X₂/X₁X₂Y sex chromosome system in Collichthys lucidus (Richardson, 1844)

doi: 10.1007/s13131-018-1152-1

The Key Laboratory of Healthy Mariculture for the East China Sea, Ministry of Agriculture, Xiamen 361021, China;Fisheries College, Jimei University, Xiamen 361021, China

Received Date: 2017-03-02

Abstract

Abstract

The chromosomes of spinyhead croaker Collichthys lucidus (Richardson, 1844) were characterized for the first time by fluorescence staining, self genomic in situ hybridization (self-GISH), and multicolor fluorescence in situ hybridization (FISH) with 18S rDNA, 5S rDNA and telomeric sequence probes. The female karyotype has exclusively 24 pairs of acrocentric chromosomes (2n=48a, NF=48), while the male one consists of 22 pairs of acrocentric chromosomes, 2 monosomic acrocentric chromosomes and a metacentric chromosome (2n=1m+46a, NF=48). The difference between female and male karyotypes indicates the presence of a sex chromosome of X₁X₁X₂X₂/X₁X₂Y type, where Y is the unique metacentric chromosome in the male karyotype. As revealed by FISH, 5S rDNA and 18S rDNA sites were mapped at syntenic position of the largest acrocentric chromosome (X₁), and the short arms of the Y chromosome as well. An X₁-chromosome specific interstitial telomeric signal (ITS) was detected overlapping the 5S rDNA sites. In addition, self-GISH revealed that the repetitive DNAs accumulated on all the putative sex chromosome. Chromosome fusion accompanied by a partial deletion in the ancestral karyotype (2n=48a) is hypothesized for the origin of such multiple sex chromosome system. The present study, as the first description of differentiated sex chromosome in family Sciaenidae, will give clues to the studies on the sex chromosome of other Sciaenids.
- Collichthys lucidus,
- karyotype,
- sex chromosome,
- rDNA,
- fluorescence in situ hybridization

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Accioly I V, Molina W F. 2008. Cytogenetic studies in Brazilian marine Sciaenidae and Sparidae fishes (Perciformes). Genet Mol Res, 7(2): 358-370

Arai R. 2011. Fish Karyotypes: A Check List. Tokyo: Springer, 163–209

Artoni R F, Bertollo L A C. 2002. Evolutionary aspects of the ZZ/ZW sex chromosome system in the Characidae fish, genus Triportheus. A monophyletic state and NOR location on the W chromosome. Heredity, 89(1): 15-19

Bitencourt J A, Sampaio I, Ramos R T C, et al. 2017. First report of sex chromosomes in Achiridae (Teleostei: Pleuronectiformes) with inferences about the origin of the multiple X₁X₁X₂X₂/X₁X₂Y system and dispersal of ribosomal genes in Achirus achirus. Zebrafish, 14(1): 90-95

Blanco D R, Vicari M R, Lui R L, et al. 2014. Origin of the X₁X₁X₂X₂/X₁X₂Y sex chromosome system of Harttia punctata (Siluriformes, Loricariidae) inferred from chromosome painting and FISH with ribosomal DNA markers. Genetica, 142(2): 119-126

Born G G, Bertollo L A C. 2000. An XX/XY sex chromosome system in a fish species, Hoplias malabaricus, with a polymorphic NOR-bearing X chromosome. Chromosome Res, 8(2): 111-118

Chalopin D, Volff J N, Galiana D, et al. 2015. Transposable elements and early evolution of sex chromosomes in fish. Chromosome Res, 23(3): 545-560

Charlesworth D, Charlesworth B, Marais G. 2005. Steps in the evolution of heteromorphic sex chromosomes. Heredity, 95(2): 118-128

Chen Songlin, Zhang Guojie, Shao Changwei, et al. 2014. Whole-genome sequence of a flatfish provides insights into ZW sex chromosome evolution and adaptation to a benthic lifestyle. Nat Genet, 46(3): 253-260

Cheng Jiao, Ma Guoqiang, Miao Zhenqing, et al. 2012. Complete mitochondrial genome sequence of the spinyhead croaker Collichthys lucidus (Perciformes, Sciaenidae) with phylogenetic considerations. Mol Biol Rep, 39(4): 4249-4259

Devlin R H, Nagahama Y. 2002. Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture, 208(3-4): 191-364

Diniz D, Moreira-Filho O, Bertollo L A C. 2008. Molecular cytogenetics and characterization of a ZZ/ZW sex chromosome system in Triportheus nematurus (Characiformes, Characidae). Genetica, 133(1): 85-91

Ferreira M, Garcia C, Matoso D A, et al. 2016. A new multiple sex chromosome system X₁X₁X₂X₂/X₁Y₁X₂Y₂ in Siluriformes: cytogenetic characterization of Bunocephalus coracoideus (Aspredinidae). Genetica, 144(5): 591-599

Gold J R, Li Y C, Shipley N S, et al. 1990. Improved methods for working with fish chromosomes with a review of metaphase chromosome banding. J Fish Biol, 37(4): 563-575

Gornung E. 2013. Twenty years of physical mapping of major ribosomal RNA genes across the teleosts: a review of research. Cytogenet Genome Res, 141(2-3): 90-102

Graves J A M. 2006. Sex chromosome specialization and degeneration in mammals. Cell, 124(5): 901-914

Howell W M, Black D A. 1979. Location of the nucleolus organizer regions on the sex chromosomes of the banded killifish, Fundulus diaphanus. Copeia, 1979(3): 544-546

Ijdo J W, Wells R A, Baldini A, et al. 1991. Improved telomere detection using a telomere repeat probe (TTAGGG)n generated by PCR. Nucleic Acids Res, 19(17): 4780

Kitano J, Peichel C L. 2012. Turnover of sex chromosomes and speciation in fishes. Environ Biol Fishes, 94(3): 549-558

Kitano J, Ross J A, Mori S, et al. 2009. A role for a neo-sex chromosome in stickleback speciation. Nature, 461(7267): 1079-1083

Levan A, Fredga K, Sandberg A A. 1964. Nomenclature for centromeric position on chromosomes. Hereditas, 52(2): 201-220

Liao Mengxian, Zheng Jiao, Wang Zhiyong, et al. 2017. Molecular cytogenetic of the Amoy croaker, Argyrosomus amoyensis (Teleostei, Sciaenidae). Chin J Oceanol Limnol, doi: 10.1007/s00343-018-6272-0

Liu Zhiyong, Moore P H, Ma Hao, et al. 2004. A primitive Y chromosome in papaya marks incipient sex chromosome evolution. Nature, 427(6972): 348-352

Nelson J S, Grande T C, Wilson M V H. 2016. Fishes of the World. 5th ed. New York: John Wiley and Sons Inc, 498–499

Palacios-Gimenez O M, Castillo E R, Martí D A, et al. 2013. Tracking the evolution of sex chromosome systems in Melanoplinae grasshoppers through chromosomal mapping of repetitive DNA sequences. BMC Evol Biol, 13: 167

Poltronieri J, Marquioni V, Bertollo L A C, et al. 2013. Comparative chromosomal mapping of microsatellites in Leporinus species (Characiformes, Anostomidae): unequal accumulation on the W chromosomes. Cytogenet Genome Res, 142(1): 40-45

Reed K M, Phillips R B. 1995. Molecular cytogenetic analysis of the double-CMA3 chromosome of lake trout, Salvelinus namaycush. Cytogenet Cell Genet, 70(1-2): 104-107

Reed K M, Phillips R B. 1997. Polymorphism of the nucleolus organizer region (NOR) on the putative sex chromosomes of Arctic char (Salvelinus alpinus) is not sex related. Chromosome Res, 5(4): 221-227

Ren X J, Eisenhour L, Hong C S, et al. 1997. Roles of rDNA spacer and transcription unit-sequences in X-Y meiotic chromosome pairing in Drosophila melanogaster males. Chromosoma, 106(1): 29-36

Ross J A, Peichel C L. 2008. Molecular cytogenetic evidence of rearrangements on the Y chromosome of the threespine stickleback fish. Genetics, 179(4): 2173-2182

Ross J A, Urton J R, Boland J, et al. 2009. Turnover of sex chromosomes in the stickleback fishes (Gasterosteidae). PLoS Genet, 5(2): e1000391

She Chaowen, Liu Jingyu, Diao Ying, et al. 2007. The distribution of repetitive DNAs along chromosomes in plants revealed by self-genomic in situ hybridization. J Genet Genomics, 34(5): 437-448

Stitou S, Burgos M, Zurita F, et al. 1997. Recent evolution of NOR-bearing and sex chromosomes of the North African rodent Lemniscomys barbarus. Chromosome Res, 5(7): 481-485

Uyeno T, Miller R R. 1971. Multiple sex chromosomes in a Mexican cyprinodontid fish. Nature, 231(5303): 452-453

Yano C F, Poltronieri J, Bertollo L A C, et al. 2014. Chromosomal mapping of repetitive DNAs in Triportheus trifurcatus (Characidae, Characiformes): insights into the differentiation of the Z and W chromosomes. PLoS One, 9(3): e90946

Zheng Jiao, Cao Kuan, Yang Anran, et al. 2016. Chromosome mapping using genomic DNA and repetitive DNA sequences as probes for somatic chromosome identification in Nibea albiflora. J Fish China (in Chinese), 40(8): 1156-1162

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6.	Alexandr Sember, Petr Nguyen, Manolo F. Perez, et al. Multiple sex chromosomes in teleost fishes from a cytogenetic perspective: state of the art and future challenges. Philosophical Transactions of the Royal Society B: Biological Sciences, 2021, 376(1833): 20200098. doi:10.1098/rstb.2020.0098
7.	Junzhu Xiao, Yu Zou, Shijun Xiao, et al. Development of a PCR-based genetic sex identification method in spinyhead croaker (Collichthys lucidus). Aquaculture, 2020, 522: 735130. doi:10.1016/j.aquaculture.2020.735130
8.	Yongshuang Xiao, Zhizhong Xiao, Daoyuan Ma, et al. Chromosome-Level Genome Reveals the Origin of Neo-Y Chromosome in the Male Barred Knifejaw Oplegnathus fasciatus. iScience, 2020, 23(4): 101039. doi:10.1016/j.isci.2020.101039
9.	小强高. Karyotype of the Maccullochella peelii. Open Journal of Fisheries Research, 2020, 07(03): 134. doi:10.12677/OJFR.2020.73019
10.	Dongdong Xu, Alexandr Sember, Qihui Zhu, et al. Deciphering the Origin and Evolution of the X1X2Y System in Two Closely-Related Oplegnathus Species (Oplegnathidae and Centrarchiformes). International Journal of Molecular Sciences, 2019, 20(14): 3571. doi:10.3390/ijms20143571
11.	Mingyi Cai, Yu Zou, Shijun Xiao, et al. Chromosome assembly of Collichthys lucidus, a fish of Sciaenidae with a multiple sex chromosome system. Scientific Data, 2019, 6(1) doi:10.1038/s41597-019-0139-x
12.	Wagner Franco Molina, Clóvis Coutinho da Motta-Neto, Gideão Wagner Werneck Félix da Costa. Conservation Genetics in the Neotropics. doi:10.1007/978-3-031-34854-9_8