Cytogenetic Analysis of the Fish Genus Carassius Indicates Divergence, Fission, and Segmental Duplication as Drivers of Tandem Repeat and Microchromosome Evolution

. 2024 Mar 02 ; 16 (3) : .

Jazyk angličtina Země Anglie, Velká Británie Médium print

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid38340334

Grantová podpora
# CZ.02.01.01/00/22_010/0002902 P JAC project
MSCA Fellowships CZ-UK
# 54123 Grant Agency of Charles University
# MZE-RO0523 Ministry of Agriculture of the Czech Republic

Fishes of the genus Carassius are useful experimental vertebrate models for the study of evolutionary biology and cytogenetics. Carassius demonstrates diverse biological characteristics, such as variation in ploidy levels and chromosome numbers, and presence of microchromosomes. Those Carassius polyploids with ≥150 chromosomes have microchromosomes, but the origin of microchromosomes, especially in European populations, is unknown. We used cytogenetics to study evolution of tandem repeats (U1 and U2 small nuclear DNAs and H3 histone) and microchromosomes in Carassius from the Czech Republic. We tested the hypotheses whether the number of tandem repeats was affected by polyploidization or divergence between species and what mechanism drives evolution of microchromosomes. Tandem repeats were found in tetraploid and hexaploid Carassius gibelio, and tetraploid Carassius auratus and Carassius carassius in conserved numbers, with the exception of U1 small nuclear DNA in C. auratus. This conservation indicates reduction and/or loss in the number of copies per locus in hexaploids and may have occurred by divergence rather than polyploidization. To study the evolution of microchromosomes, we used the whole microchromosome painting probe from hexaploid C. gibelio and hybridized it to tetraploid and hexaploid C. gibelio, and tetraploid C. auratus and C. carassius. Our results revealed variation in the number of microchromosomes in hexaploids and indicated that the evolution of the Carassius karyotype is governed by macrochromosome fissions followed by segmental duplication in pericentromeric areas. These are potential mechanisms responsible for the presence of microchromosomes in Carassius hexaploids. Differential efficacy of one or both of these mechanisms in different tetraploids could ensure variability in chromosome number in polyploids in general.

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Ağdamar  S, Baysal  Ö, Yıldız  A, Tarkan  AS. Genetic differentiation of non-native populations of Gibel Carp, Carassius gibelio in Western Turkey by ISSR and SRAP markers. Zool Middle East. 2020:66(4):302–310. 10.1080/09397140.2020.1835215. DOI

Bertollo  LAC, Cioffi  MdB. Direct chromosome preparation from freshwater teleost fishes. In: Ozouf-Costaz C, Pisano E, Foresti F, Foresti LdAT, editors. Fish cytogenet. Tech. Ray-Fin fishes chondrichthyans. Enfield: CRC Press; 2015. p. 21–26.

Bi  K, Bogart  JP. Identification of intergenomic recombinations in unisexual salamanders of the genus Ambystoma by genomic in situ hybridization (GISH). Cytogenet Genome Res. 2006:112(3–4):307–312. 10.1159/000089885. PubMed DOI

Bishani  A, et al. Evolution of tandemly arranged repetitive DNAs in three species of Cyprinoidei with different ploidy levels. Cytogenet Genome Res. 2021:161(1–2):32–42. 10.1159/000513274. PubMed DOI

Blanc  G, Barakat  A, Guyot  R, Cooke  R, Delseny  M. Extensive duplication and reshuffling in the Arabidopsis genome. Plant Cell. 2000:12(7):1093–1101. 10.1105/tpc.12.7.1093. PubMed DOI PMC

Braasch  I, Gehrke  AR, Smith  JJ, Kawasaki  K, Manousaki  T, Pasquier  J, Amores  A, Desvignes  T, Batzel  P, Catchen  J, et al. The spotted gar genome illuminates vertebrate evolution and facilitates human-teleost comparisons. Nat Genet. 2016:48(4):427–437. 10.1038/ng.3526. PubMed DOI PMC

Bueno  D, Palacios-Gimenez  OM, Cabral-de-Mello  DC. Chromosomal mapping of repetitive DNAs in the grasshopper Abracris flavolineata reveal possible ancestry of the B chromosome and H3 histone spreading. PLoS One. 2013:8(6):e66532. 10.1371/journal.pone.0066532. PubMed DOI PMC

Cabral-De-Mello  DC, Valente  GT, Nakajima  RT, Martins  C. Genomic organization and comparative chromosome mapping of the U1 snRNA gene in cichlid fish, with an emphasis in Oreochromis niloticus. Chromosome Res. 2012:20(2):279–292. 10.1007/s10577-011-9271-y. PubMed DOI

Cannon  SB, Mitra  A, Baumgarten  A, Young  ND, May  G. The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol. 2004:4(1):10. 10.1186/1471-2229-4-10. PubMed DOI PMC

Carvalho  PC, et al. First chromosomal analysis in Hepsetidae (Actinopterygii, Characiformes): insights into relationship between African and Neotropical fish groups. Front Genet. 2017:8(203):1–12. 10.3389/fgene.2017.00203. PubMed DOI PMC

Cherfas  NB. Natural triploidy in females of the unisexual form of silver crucian carp (Carassius auratus gibelio Bloch). Genetika. 1966:5:16–24.

Chobot  K, Němec  M. Červený seznam ohrožených druhů České republiky. Obratlovci: red list of threatened species of the Czech Republic. Příroda. 2017:34:1–182.

Colgan  DJ, et al. Histone H3 and U2 snRNA DNA sequences and arthropod molecular evolution. Aust J Zool. 1998:46(5):419. 10.1071/ZO98048. DOI

de Souza  MS, et al. Highly conserved microchromosomal organization in passeriformes birds revealed via BAC-FISH analysis. Birds. 2023:4(2):236–244. 10.3390/birds4020020. DOI

Ding  M, et al. Genomic anatomy of male-specific microchromosomes in a gynogenetic fish. PLoS Genet. 2021:17(9):1–25. 10.1371/journal.pgen.1009760. PubMed DOI PMC

Edgar  RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004:32(5):1792–1797. 10.1093/nar/gkh340. PubMed DOI PMC

Fedorčák  J, Križek  P, Koščo  J. Which factors influence spatio-temporal changes in the distribution of invasive and native species of genus Carassius?  Aquat Invasions. 2023:18(2):219–230. 10.3391/ai.2023.18.2.105240. DOI

Fornaini  NR, et al. Consequences of polyploidy and divergence as revealed by cytogenetic mapping of tandem repeats in African clawed frogs (Xenopus, Pipidae). Eur J Wildl Res. 2023:69(4):81. 10.1007/s10344-023-01709-8. PubMed DOI PMC

Fuad  MMH, Vetenk  L, Šimková  A. Is gynogenetic reproduction in gibel carp (Carassius gibelio) a major trait responsible for invasiveness?  J Vertebr Biol. 2021:70(4):21049. 10.25225/jvb.21049. DOI

Gvoždík  V, Knytl  M, Zassi-Boulou  AG, Fornaini  NR, Bergelová  B. Tetraploidy in the Boettger’s dwarf clawed frog (Pipidae: Hymenochirus boettgeri) from the Congo indicates non-conspecificity with the captive population. Zool J Linn Soc. 2023:1–14. 10.1093/zoolinnean/zlad119 DOI

Hakoyama  H, Nishimura  T, Matsubara  N, Iguchi  K. Difference in parasite load and nonspecific immune reaction between sexual and gynogenetic forms of Carassius auratus. Biol J Linn Soc. 2001:72(3):401–407. 10.1006/bijl.2000.0507. DOI

Hasegawa  M, Kishino  H, Yano  T. Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol. 1985:22(2):160–174. 10.1007/BF02101694. PubMed DOI

Huang  S, Spector  DL. U1 and U2 small nuclear RNAs are present in nuclear speckles. Proc Natl Acad Sci USA. 1992:89(1):305–308. 10.1073/pnas.89.1.305. PubMed DOI PMC

International Chicken Genome Sequencing Consortium . Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature. 2004:432(7018):695–716. 10.1038/nature03154. PubMed DOI

Jan  G, et al. Karyotypic analysis of crucian carp, Carassius Carassius (Linnaeus, 1758) from cold waters of Kashmir Himalayas. Caryologia. 2023:76(2):23–30. 10.36253/caryologia-2112. DOI

Kalous  L, Bohlen  J, Rylková  K, Petrtýl  M. Hidden diversity within the Prussian carp and designation of a neotype for Carassius gibelio (Teleostei: Cyprinidae). Ichthyol Explor Freshwaters. 2012:23(1):11–18.

Kalous  L, Knytl  M. Karyotype diversity of the offspring resulting from reproduction experiment between diploid male and triploid female of silver Prussian carp, Carassius gibelio (Cyprinidae, Actinopterygii). Folia Zool. 2011:60(2):115–121. 10.25225/fozo.v60.i2.a5.2011. DOI

Kalous  L, Knytl  M, Krajáková  L. Usage of non-destructive method of chromosome preparation applied on silver Prussian carp (Carassius gibelio). In: Kubík Š, Barták M, editors. Work. Anim. biodiversity. Jevany: Czech University of Life Sciences in Prague; 2010. p. 57–60.

Kalous  L, Šlechtová  V, Bohlen  J, Petrtýl  M, Švátora  M. First European record of Carassius langsdorfii from the Elbe basin. J Fish Biol. 2007:70(sa):132–138. 10.1111/j.1095-8649.2006.01290.x. DOI

Kalyaanamoorthy  S, Minh  BQ, Wong  TKF, von Haeseler  A, Jermiin  LS. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods. 2017:14(6):587–589. 10.1038/nmeth.4285. PubMed DOI PMC

Khosravi  M, Abdoli  A, Tajbakhsh  F, Ahmadzadeh  F, Nemati  H. et al.  An effort toward species delimitation in the genus Carassius (Cyprinidae) using morphology and the related challenges: a case study from Inland waters of Iran. J Ichthyol. 2022:62(2):185–194. 10.1134/S0032945222020096. DOI

Knytl  M, Fornaini  N. Measurement of chromosomal arms and fish reveal complex genome architecture and standardized karyotype of model fish, genus Carassius. Cells. 2021:10(9):2343. 10.3390/cells10092343. PubMed DOI PMC

Knytl  M, et al. Divergent subgenome evolution in the allotetraploid frog Xenopus calcaratus. Gene. 2023:851:146974. 10.1016/j.gene.2022.146974. PubMed DOI

Knytl  M, Forsythe  A, Kalous  L. A fish of multiple faces, which show us enigmatic and incredible phenomena in nature: biology and cytogenetics of the genus Carassius. Int J Mol Sci. 2022:23(15):8095. 10.3390/ijms23158095. PubMed DOI PMC

Knytl  M, Kalous  L, Rab  P. Karyotype and chromosome banding of endangered Crucian carp, Carassius Carassius (Linnaeus, 1758) (Teleostei, Cyprinidae). Comp Cytogenet. 2013a:7(3):205–213. 10.3897/compcytogen.v7i3.5411. PubMed DOI PMC

Knytl  M, et al. Morphologically indistinguishable hybrid Carassius female with 156 chromosomes: a threat for the threatened Crucian carp, C. carassius, L. PLoS One. 2018:13(1):e0190924. 10.1371/journal.pone.0190924. PubMed DOI PMC

Knytl  M, Kalous  L, Symonová  R, Rylková  K, Ráb  P. Chromosome studies of European cyprinid fishes: cross-species painting reveals natural allotetraploid origin of a Carassius female with 206 chromosomes. Cytogenet Genome Res. 2013b:139(4):276–283. 10.1159/000350689. PubMed DOI

Knytl  M, et al. Chromosome divergence during evolution of the tetraploid clawed frogs, Xenopus mellotropicalis and Xenopus epitropicalis as revealed by Zoo-FISH. PLoS One. 2017:12(5):e0177087. 10.1371/journal.pone.0177087. PubMed DOI PMC

Kretschmer  R, et al. Novel insights into chromosome evolution of charadriiformes: extensive genomic reshuffling in the wattled jacana (Jacana jacana, Charadriiformes, Jacanidae). Genet Mol Biol. 2020:43(1):1–8. 10.1590/1678-4685-GMB-2019-0236. PubMed DOI PMC

Krylov  V, et al. Preparation of Xenopus tropicalis whole chromosome painting probes using laser microdissection and reconstruction of X. laevis tetraploid karyotype by Zoo-FISH. Chromosome Res. 2010:18(4):431–439. 10.1007/s10577-010-9127-x. PubMed DOI

Kubickova  S, Cernohorska  H, Musilova  P, Rubes  J. The use of laser microdissection for the preparation of chromosome-specific painting probes in farm animals. Chromosome Res. 2002:10(7):571–577. 10.1023/A:1020914702767. PubMed DOI

Kuhl  H, et al. Equilibrated evolution of the mixed auto-/allopolyploid haplotype-resolved genome of the invasive hexaploid Prussian carp. Nat Commun. 2022:13(1):1–11. 10.1038/s41467-022-31515-w. PubMed DOI PMC

Lamatsch  D, Stöck  M. Sperm-dependent parthenogenesis and hybridogenesis in teleost fishes. In: Schöne I, Martens K, van Dijk P, editors. Lost sex evol. biol. parthenogenes. Dordrecht: Springer; 2009. p. 399–432.

Leister  D. Tandem and segmental gene duplication and recombination in the evolution of plant disease resistance genes. Trends Genet. 2004:20(3):116–122. 10.1016/j.tig.2004.01.007. PubMed DOI

Li  XY, et al. Origin and transition of sex determination mechanisms in a gynogenetic hexaploid fish. Heredity (Edinb). 2018:121(1):64–74. 10.1038/s41437-017-0049-7. PubMed DOI PMC

Li  JT, et al. Parallel subgenome structure and divergent expression evolution of allo-tetraploid common carp and goldfish. Nat Genet. 2021:53(10):1493–1503. 10.1038/s41588-021-00933-9. PubMed DOI PMC

Li  XY, et al. Extra microchromosomes play male determination role in polyploid gibel carp. Genetics. 2016:203(3):1415–1424. 10.1534/genetics.115.185843. PubMed DOI PMC

Lu  M, Zhou  L, Gui  J. Evolutionary mechanisms and practical significance of reproductive success and clonal diversity in unisexual vertebrate polyploids. Sci China Life Sci. 2023. 10.1007/s11427-023-2486-2. PubMed DOI

Lusk  S, Lusková  V, Hanel  L. Alien fish species in the Czech Republic and their impact on the native fish fauna. Folia Zool. 2010:59(1):57–72. 10.25225/fozo.v59.i1.a9.2010. DOI

Malimpensa  GDC, et al.  Chromosomal diversification in two species of Pimelodus (Siluriformes: Pimelodidae): comparative cytogenetic mapping of multigene families. Zebrafish. 2020:17(4):278–286. 10.1089/zeb.2020.1892. PubMed DOI

Minh  BQ, et al. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol. 2020:37(5):1530–1534. 10.1093/molbev/msaa015. PubMed DOI PMC

Nanda  I, Schmid  M. Localization of the telomeric (TTAGGG)n sequence in chicken (Gallus domesticus) chromosomes. Cytogenet Cell Genet. 1994:65(3):190–193. 10.1159/000133630. PubMed DOI

Ohno  S, Muramoto  J, Christian  L, Atkin  NB. Diploid–tetraploid relationship among old-world members of the fish family Cyprinidae. Chromosoma. 1967:23(1):1–9. 10.1007/BF00293307. DOI

Pang  M, et al. Quantitative trait loci mapping for feed conversion efficiency in crucian carp (Carassius auratus). Sci Rep. 2017:7(1):1–11. 10.1038/s41598-017-17269-2. PubMed DOI PMC

Papoušek  I, et al. Identification of natural hybrids of gibel carp Carassius auratus gibelio (Bloch) and crucian carp Carassius carassius (L.) from lower Dyje river floodplain (Czech Republic). J Fish Biol. 2008:72(5):1230–1235. 10.1111/j.1095-8649.2007.01783.x. DOI

Pavlov  DA. Features of inner ear morphology of gibel carp Carassius gibelio (Cyprinidae). J Ichthyol. 2022a:62(2):195–204. 10.1134/S0032945222020138. DOI

Pavlov  DA. Life history of two Carassius (Cyprinidae) species in the conditions of sympatry. J Ichthyol. 2022b:62(6):1100–1115. 10.1134/S0032945222060212. DOI

Przybył  A, et al. Sex, size and ploidy ratios of Carassius gibelio from Poland. Aquat Invasions. 2020:15(1):1–20. 10.3391/ai.2020.15.2.08. DOI

Rylková  K, Kalous  L, Bohlen  J, Lamatsch  DK, Petrtl  M. Phylogeny and biogeographic history of the cyprinid fish genus Carassius (Teleostei: Cyprinidae) with focus on natural and anthropogenic arrivals in Europe. Aquaculture. 2013:380–383:13–20. 10.1016/j.aquaculture.2012.11.027. DOI

Sacerdot  C, Louis  A, Bon  C, Berthelot  C, Roest Crollius  H. Chromosome evolution at the origin of the ancestral vertebrate genome. Genome Biol. 2018:19(1):166. 10.1186/s13059-018-1559-1. PubMed DOI PMC

Sember  A, et al. Taxonomic diversity not associated with gross karyotype differentiation: the case of bighead carps, genus hypophthalmichthys (Teleostei, Cypriniformes, Xenocyprididae). Genes (Basel). 2020:11(5):479. 10.3390/genes11050479. PubMed DOI PMC

Seroussi  E, et al. Avian expression patterns and genomic mapping implicate leptin in digestion and TNF immunity, suggesting that their interacting adipokine role has been acquired only in mammals. Int J Mol Sci. 2019:20(18):4489. 10.3390/ijms20184489. PubMed DOI PMC

Silva  DM, Utsunomia  R, Pansonato-Alves  JC, Oliveira  C, Foresti  F. Chromosomal mapping of repetitive DNA sequences in five species of astyanax (Characiformes, Characidae) reveals independent location of U1 and U2 snRNA sites and association of U1 snRNA and 5S rDNA. Cytogenet Genome Res. 2015:146(2):144–152. 10.1159/000438813. PubMed DOI

Spoz  A, et al. Molecular cytogenetic analysis of the crucian carp, Carassius carassius (Linnaeus, 1758) (Teleostei, Cyprinidae), using chromosome staining and fluorescence in situ hybridisation with rDNA probes. Comp Cytogenet. 2014:8(3):233–248. 10.3897/compcytogen.v8i3.7718. PubMed DOI PMC

Srikulnath  K, Ahmad  SF, Singchat  W, Panthum  T. Why do some vertebrates have microchromosomes?  Cells. 2021:10(9):1–33. 10.3390/cells10092182. PubMed DOI PMC

Symonová  R, Howell  WM. Vertebrate genome evolution in the light of fish cytogenomics and rDNAomics. Genes (Basel). 2018:9(2):1–27. 10.3390/genes9020096. PubMed DOI PMC

Symonová  R, et al. Genome compositional organization in gars shows more similarities to mammals than to other ray-finned fish. J Exp Zool Part B Mol Dev Evol. 2017:328(7):607–619. 10.1002/jez.b.22719. PubMed DOI

Tamura  K, Stecher  G, Kumar  S. MEGA11: molecular evolutionary genetics analysis version 11. Mol Biol Evol. 2021:38(7):3022–3027. 10.1093/molbev/msab120. PubMed DOI PMC

Tapkir  S, et al. Invasive gibel carp (Carassius gibelio) outperforms threatened native crucian carp (Carassius carassius) in growth rate and effectiveness of resource use: field and experimental evidence. Aquat Conserv Mar Freshw Ecosyst. 2022:32(12):1901–1912. 10.1002/aqc.3894. DOI

Tapkir  S, et al. Invasive gibel carp use vacant space and occupy lower trophic niche compared to endangered native crucian carp. Biol Invasions. 2023:25(9):2917–2928. 10.1007/s10530-023-03081-9. DOI

Völker  M, Kullmann  H. Sequential chromosome banding from single acetic acid fixed embryos of Chromaphyosemion killifishes (Cyprinodontiformes, Nothobranchiidae). Cybium. 2006:30(2):171–176.

Völker  M, Sonnenberg  R, Ráb  P, Kullmann  H. Karyotype differentiation in Chromaphyosemion killifishes (Cyprinodontiformes, Nothobranchiidae) II: cytogenetic and mitochondrial DNA analyses demonstrate karyotype differentiation and its evolutionary direction in C. riggenbachi. Cytogenet Genome Res. 2006:115(1):70–83. 10.1159/000094803. PubMed DOI

Wang J, et al.  A novel allotriploid hybrid derived from female goldfish × male Bleeker’s yellow tail. Front Genet. 2022a:13(880591):1–12. 10.3389/fgene.2022.880591. PubMed DOI PMC

Wang  Y, et al. Comparative genome anatomy reveals evolutionary insights into a unique amphitriploid fish. Nat Ecol Evol. 2022b:6(9):1354–1366. 10.1038/s41559-022-01813-z. PubMed DOI PMC

Waters  PD, et al. Microchromosomes are building blocks of bird, reptile, and mammal chromosomes. Proc Natl Acad Sci USA. 2021:118(45):1–11. 10.1073/pnas.2112494118. PubMed DOI PMC

Wen  M, et al. Sex chromosome and sex locus characterization in goldfish, Carassius auratus (Linnaeus, 1758). BMC Genomics. 2020:21(1):1–12. 10.1186/s12864-020-06959-3. PubMed DOI PMC

Winfield  IJ, Nelson  JS. 2012. Cyprinid fishes: systematics, biology and exploitation. Dordrecht: Springer Science & Business Media. 10.1007/978-94-011-3092-9. DOI

Xiao  J, et al. Coexistence of diploid, triploid and tetraploid crucian carp (Carassius auratus) in natural waters. BMC Genet. 2011:12(1):20. 10.1186/1471-2156-12-20. PubMed DOI PMC

Yang  L, et al. Molecular phylogeny of the fishes traditionally referred to Cyprinini sensu stricto (Teleostei: Cypriniformes). Zool Scr. 2010:39(6):527–550. 10.1111/j.1463-6409.2010.00443.x. DOI

Yi  MS, et al. Molecular cytogenetic detection of paternal chromosome fragments in allogynogenetic gibel carp, Carassius auratus gibelio Bloch. Chromosome Res. 2003:11(7):665–71. 10.1023/a:1025985625706. PubMed DOI

Zhao  X, et al. Genotypic males play an important role in the creation of genetic diversity in gynogenetic gibel carp. Front Genet. 2021:12(691923):1–9. 10.3389/fgene.2021.691923. PubMed DOI PMC

Zhou  L, Gui  JF. Karyotypic diversity in polyploid gibel carp, Carassius auratus gibelio Bloch. Genetica. 2002:115(2):223–232. 10.1023/A:1020102409270. PubMed DOI

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