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.
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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)
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)
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)
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)
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)
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)
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)
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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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DOI: https://doi.org/10.1007/s10577-014-9402-3