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Chromosome size-correlated and chromosome size-uncorrelated homogenization of centromeric repetitive sequences in New World quails

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Abstract

Many families of centromeric repetitive DNA sequences isolated from Struthioniformes, Galliformes, Falconiformes, and Passeriformes are localized primarily to microchromosomes. However, it is unclear whether chromosome size-correlated homogenization is a common characteristic of centromeric repetitive sequences in Aves. New World and Old World quails have the typical avian karyotype comprising chromosomes of two distinct sizes, and C-positive heterochromatin is distributed in centromeric regions of most autosomes and the whole W chromosome. We isolated six types of centromeric repetitive sequences from three New World quail species (Colinus virginianus, CVI; Callipepla californica, CCA; and Callipepla squamata, CSQ; Odontophoridae) and one Old World quail species (Alectoris chukar, ACH; Phasianidae), and characterized the sequences by nucleotide sequencing, chromosome in situ hybridization, and filter hybridization. The 385-bp CVI-MspI, 591-bp CCA-BamHI, 582-bp CSQ-BamHI, and 366-bp ACH-Sau3AI fragments exhibited tandem arrays of the monomer unit, and the 224-bp CVI-HaeIII and 135-bp CCA-HaeIII fragments were composed of minisatellite-like and microsatellite-like repeats, respectively. ACH-Sau3AI was a homolog of the chicken nuclear membrane repeat sequence, whose homologs are common in Phasianidae. CVI-MspI, CCA-BamHI, and CSQ-BamHI showed high homology and were specific to the Odontophoridae. CVI-MspI was localized to microchromosomes, whereas CVI-HaeIII, CCA-BamHI, and CSQ-BamHI were mapped to almost all chromosomes. CCA-HaeIII was localized to five pairs of macrochromosomes and most microchromosomes. ACH-Sau3AI was distributed in three pairs of macrochromosomes and all microchromosomes. Centromeric repetitive sequences may be homogenized in chromosome size-correlated and -uncorrelated manners in New World quails, although there may be a mechanism that causes homogenization of centromeric repetitive sequences primarily between microchromosomes, which is commonly observed in phasianid birds.

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Abbreviations

AAU:

Amazona autumnalis

ACH:

Alectoris chukar

ACY:

Anser cygnoides var. orientalis

APL:

Anas platyrhynchos var. domesticus

BBL:

Bubo blakistoni

BrdU:

5-Bromo-2′-deoxyuridine

CCA:

Callipepla californica

CCD:

Charge-coupled device

CCH:

Coturnix chinensis

CCY:

Cygnus cygnus

cDNA:

Complementary DNA

CJA:

Coturnix japonica

CNM:

Chicken nuclear membrane

CSQ:

Callipepla squamata

CVI :

Colinus virginianus

DDBJ:

DNA Data Bank of Japan

DIG:

Digoxigenin

DNO:

Dromaius novaehollandiae

dNTP:

Deoxynucleotide triphosphate

EEL:

Eudromia elegans

FISH:

Fluorescence in situ hybridization

FITC:

Fluorescein isothiocyanate

GGA:

Gallus gallus

GLE:

Grus leucogeranus

HRU:

Hirundo rustica

Kb:

Kilobase pairs

NME:

Numida meleagris

NNI:

Nisaetus nipalensis orientalis

PAT:

Probosciger aterrimus

PCR:

Polymerase chain reaction

PHA:

Pandion haliaetus

PI:

Propidium iodide

PMI:

Platalea minor

SCA:

Struthio camelus

SDS:

Sodium dodecyl sulfate

SSC:

Saline sodium citrate

TM:

Turkey microchromosome

UV:

Ultraviolet

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Acknowledgments

This research was partially supported by the National BioResource Project (NBRP) Chicken/Quail, and Grants-in-Aid for Scientific Research on Innovative Areas (no. 23113004) and a Grant-in-Aid for Scientific Research (B) (no. 22370081) from the Ministry of Education, Culture, Sports, Science and Technology, Japan.

Author information

Authors and Affiliations

  1. Laboratory of Animal Genetics, Department of Applied Molecular Biosciences, Graduate School of Bioagricultural Sciences, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, Aichi, 464-8601, Japan

    Satoshi Ishishita, Yuri Tsuruta, Yoshinobu Uno & Yoichi Matsuda

  2. Faculty of Agriculture, Shinshu University, Minamiminowa, Nagano, 399-4598, Japan

    Yuri Tsuruta & Tamao Ono

  3. Biosystems Science Course, Graduate School of Life Science, Hokkaido University, Kita 10, Nishi 8, Kita-ku, Sapporo, Hokkaido, 060-0810, Japan

    Atsushi Nakamura

  4. Department of Natural History Sciences, Faculty of Science, Hokkaido University, Kita 10, Nishi 8, Kita-ku, Sapporo, Hokkaido, 060-0810, Japan

    Chizuko Nishida

  5. School of Biosciences, University of Kent, Canterbury, UK

    Darren K. Griffin

  6. Laboratory of Animal Breeding and Genetics, Graduate School of Biosphere Science, Hiroshima University, Kagamiyama, Higashi-Hiroshima, Hiroshima, 739-8528, Japan

    Masaoki Tsudzuki

  7. Avian Bioscience Research Center, Graduate School of Bioagricultural Sciences, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, Aichi, 464-8601, Japan

    Yoichi Matsuda

Authors
  1. Satoshi Ishishita
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  2. Yuri Tsuruta
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  3. Yoshinobu Uno
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  4. Atsushi Nakamura
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  5. Chizuko Nishida
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  6. Darren K. Griffin
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  7. Masaoki Tsudzuki
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  8. Tamao Ono
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  9. Yoichi Matsuda
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Corresponding author

Correspondence to Yoichi Matsuda.

Additional information

Responsible Editors: Darren K. Griffin and Beth A. Sullivan.

Electronic supplementary material

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Supplementary Table 1

Summary of copy numbers and amounts of repetitive sequences in the genome (XLSX 11 kb)

Supplementary Fig. 1

Nucleotide sequences of CVI-MspI, CVI-NsiI, and CVI-BamHI fragments. Asterisks indicate that sequences are rearranged to compare with CVI-BamHI. Dots indicate identity with nucleotides in the consensus sequence at the top, and hyphens indicate gaps. Internal restriction sites of six endonucleases are represented as follows: EcoRI (), BamHI (GGATCC), HpaII/MspI (CCGG), NsiI (), and TaqI () (JPEG 1882 kb)

High resolution image (EPS 4503 kb)

Supplementary Fig. 2

Nucleotide sequences of CCA-BamHI fragments. Dots indicate identity with nucleotides in the consensus sequence at the top, and hyphens indicate gaps. Restriction sites of three endonucleases are represented as follows: BamHI (), HpaII/MspI (CCGG), and TaqI () (JPEG 1900 kb)

High resolution image (EPS 5633 kb)

Supplementary Fig. 3

Nucleotide sequences of CSQ-BamHI fragments. Dots in CSQ-BamHI-33 indicate identity with nucleotides of CSQ-BamHI-26, and hyphens indicate gaps. Restriction sites of four endonucleases are represented as follows: BamHI (), HpaII/MspI (CCGG), TaqI (), and HaeIII (GGCC) (JPEG 1862 kb)

High resolution image (EPS 3299 kb)

Supplementary Fig. 4

Comparison of the CCA-BamHI consensus sequence, CSQ-BamHI-26 fragment (CSQ-BamHI), and the consensus sequences of the CVI-MspI, CVI-NsiI, and CVI-BamHI fragments (CVI-MspI). a Conserved regions are located at positions 2–334 bp and 547–589 bp of CCA-BamHI, which are indicated by dotted arrows. b Neighbor-joining tree representing phylogenetic relationships among the CCA-BamHI, CSQ-BamHI, and CVI-MspI sequence families (JPEG 1896 kb)

High resolution image (EPS 6768 kb)

Supplementary Fig. 5

Southern blot hybridization patterns of three families of centromeric repetitive sequences, CVI-HaeIII, CCA-HaeIII, and ACH-Sau3AI. a Hybridization probed with the CVI-HaeIII-1 fragment to genomic DNA of C. virginianus female, which was digested with six endonucleases (HaeIII, BamHI, EcoRI, PstI, HpaII, and MspI). b Hybridization of the CCA-HaeIII-1 fragment to genomic DNA of C. californica female. c Hybridization of the ACH-Sau3AI-34 fragment to genomic DNA of A. chukar female. A mixture of λDNA–HindIII and φX174 DNA–HaeIII digests was used as a molecular weight marker (JPEG 1839 kb)

High resolution image (EPS 13583 kb)

Supplementary Fig. 6

Comparison of southern blot hybridization patterns of CVI-MspI between male and female genomic DNA. Hybridization probed with the CVI-MspI-2 fragment to genomic DNA of C. virginianus male and female, which were digested with six endonucleases (MspI, HpaII, BamHI, EcoRI, NsiI, and PstI). A mixture of λDNA–HindIII and φX174 DNA–HaeIII digests was used as a molecular weight marker (JPEG 1831 kb)

High resolution image (EPS 5814 kb)

Supplementary Fig. 7

Quantification of the CVI-HaeIII, CVI-MspI (CVI-NsiI, CVI-BamHI), CCA-BamHI, CCA-HaeIII, CSQ-BamHI, and ACH-Sau3AI family repetitive sequences in the genome by slot-blot hybridization. Eight different concentrations of genomic DNA of C. virginianus, C. californica, C. squamata, and A. chukar and plasmid DNA clones containing the DNA fragment of CVI-HaeIII-1, CVI-MspI-2, CCA-BamHI-1, CCA-HaeIII-1, CSQ-BamHI-26, and ACH-Sau3AI-34 were blotted on a membrane and probed by hybridization with the DNA fragment of CVI-HaeIII-1, CVI-MspI-2, CCA-BamHI-1, CCA-HaeIII-1, CSQ-BamHI-26, and ACH-Sau3AI-34 labeled with digoxigenin-11-dUTP (JPEG 2523 kb)

High resolution image (EPS 14938 kb)

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Ishishita, S., Tsuruta, Y., Uno, Y. et al. Chromosome size-correlated and chromosome size-uncorrelated homogenization of centromeric repetitive sequences in New World quails. Chromosome Res 22, 15–34 (2014). https://doi.org/10.1007/s10577-014-9402-3

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