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A cytogenetic and comparative map of camelid chromosome 36 and the minute in alpacas

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Abstract

Recent advances in camelid genomics have provided draft sequence assemblies and the first comparative and gene maps for the dromedary (CDR) and the alpaca (LPA). However, no map information is currently available for the smallest camelid autosome—chr36. The chromosome is also of clinical interest because of its involvement in the minute chromosome syndrome (MCS) in infertile alpacas. Here, we developed molecular markers for camelid chr36 by direct sequencing CDR36 and LPA minute and by bioinformatics analysis of alpaca unplaced sequence scaffolds. We constructed a cytogenetic map for chr36 in the alpaca, llama, and dromedary and showed its homology to human chromosome 7 (HSA7) at 49.8–55.5 Mb. The chr36 map comprised seven markers, including two genes—ZPBP and WVC2. Comparative status of HSA7 was further refined by cytogenetic mapping of 16 HSA7 orthologs in camelid chromosomes 7 and 18 and by the analysis of HSA7-conserved synteny blocks across 11 vertebrate species. Finally, mapping chr36 markers in infertile alpacas confirmed that the minute chromosome was a derivative of chr36, but the small size was not a result of a large deletion or a translocation. Instead, cytogenetic mapping of 5.8S, 18S, and 28S rRNA genes (nucleolus organizer region (NOR)) revealed that the size difference between chr36 homologs in infertile alpacas was due to a heterozygous presence of NOR, whereas chr36 in fertile alpacas had no NOR. We theorized that the heterozygous NOR might affect chr36 pairing, recombination, and segregation in meiosis and, thus fertility.

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Abbreviations

CBA:

Bactrian camel (Camelus bactrianus)

CDR:

Dromedary (Camelus dromedarius,)

EBR:

Evolutionary breakpoint region

FISH:

Fluorescence in situ hybridization

HSA:

Human (Homo sapiens)

LGL:

Llama (Lama glama)

LPA:

Alpaca (Lama pacos)

MCS:

Minute chromosome syndrome

NGS:

Next-generation sequencing

NOR:

Nucleolus organizer region; location of 18S, 28S, and 5.8S rRNA genes

RH:

Radiation hybrid

rRNA:

Ribosomal RNA

SMRT:

Single molecule real time

References

  • Avila F, Das PJ, Kutzler M et al (2014) Development and application of camelid molecular cytogenetic tools. J Hered 105:858–869

    Article  PubMed  Google Scholar 

  • Balmus G, Trifonov VA, Biltueva LS et al (2007) Cross-species chromosome painting among camel, cattle, pig and human: further insights into the putative Cetartiodactyla ancestral karyotype. Chromosom Res 15:499–515

    Article  CAS  Google Scholar 

  • Bernardi G, Olofsson B, Filipski J et al (1985) The mosaic genome of warm-blooded vertebrates. Science 228:953–958

    Article  CAS  PubMed  Google Scholar 

  • Bianchi NO, Larramendy ML, Bianchi MS, Cortes L (1986) Karyological conservation in South American camelids. Experientia 42:622–624

    Article  Google Scholar 

  • Chowdhary BP, Raudsepp T (2005) Mapping genomes at the chromosomal level. In: Ruvinsky A, Marshall Graves J (eds) Mammalian genomics. Oxfordshire, UK, pp 23–65

    Chapter  Google Scholar 

  • Constantini M, Clay O, Auletta F, Bernardi G (2006) An isochore map of human chromosomes. Genome Res 16:536–541

    Article  Google Scholar 

  • Das PJ, Lyle SK, Beehan D, Chowdhary BP, Raudsepp T (2012) Cytogenetic and molecular characterization of Y isochromosome in a 63XO/64Xi(Yq) mosaic karyotype of an intersex horse. Sex Dev 6:117–127

    Article  CAS  PubMed  Google Scholar 

  • Di Berardino D, Nicodemo D, Coppola G et al (2006) Cytogenetic characterization of alpaca (Lama pacos, fam. Camelidae) prometaphase chromosomes. Cytogenet Genome Res 115:138–144

    Article  PubMed  Google Scholar 

  • Drew ML, Meyers-Wallen VN, Acland GM, Guyer CL, Steinheimer DN (1999) Presumptive Sry-negative XX sex reversal in a llama with multiple congenital anomalies. J Am Vet Med Assoc 215:1134–1139

    CAS  PubMed  Google Scholar 

  • Fedoriw AM, Starmer J, Yee D, Magnuson T (2012) Nucleolar association and transcriptional inhibition through 5S rDNA in mammals. PLoS Genet 8:e1002468

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Fellows E, Kutzler M, Avila F, Das PJ, Raudsepp T (2014) Ovarian dysgenesis in an alpaca with a minute chromosome 36. J Hered 105:870–874

    Article  PubMed  Google Scholar 

  • Graphodatsky AS, Trifonov VA, Stanyon R (2011) The genome diversity and karyotype evolution of mammals. Mol Cytogenet 4:22

    Article  PubMed Central  PubMed  Google Scholar 

  • Gustafson AL, Tallmadge RL, Ramlachan N et al (2003) An ordered BAC contig map of the equine major histocompatibility complex. Cytogenet Genome Res 102:189–195

    Article  CAS  PubMed  Google Scholar 

  • Huddleston J, Ranade S, Malig M et al (2014) Reconstructing complex regions of genomes using long-read sequencing technology. Genome Res 24:688–696

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kemkemer C, Kohn M, Cooper DN et al (2009) Gene synteny comparisons between different vertebrates provide new insights into breakage and fusion events during mammalian karyotype evolution. BMC Evol Biol 9:84

    Article  PubMed Central  PubMed  Google Scholar 

  • Kulemzina AI, Trifonov VA, Perelman PL et al (2009) Cross-species chromosome painting in Cetartiodactyla: reconstructing the karyotype evolution in key phylogenetic lineages. Chromosome Res 17:419–436

    Article  CAS  PubMed  Google Scholar 

  • Kulemzina AI, Yang F, Trifonov VA et al (2011) Chromosome painting in Tragulidae facilitates the reconstruction of Ruminantia ancestral karyotype. Chromosome Res 19:531–539

    Article  CAS  PubMed  Google Scholar 

  • Larkin DM, Pape G, Donthu R et al (2009) Breakpoint regions and homologous synteny blocks in chromosomes have different evolutionary histories. Genome Res 19:770–777

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Maden BE, Dent CL, Farrell TE et al (1987) Clones of human ribosomal DNA containing the complete 18S-rRNA and 28 S-rRNA genes. Characterization, a detailed map of the human ribosomal transcription unit and diversity among clones. Biochem J 246:519–527

    PubMed Central  CAS  PubMed  Google Scholar 

  • Murphy WJ, Larkin DM, Everts-van der Wind A et al (2005) Dynamics of mammalian chromosome evolution inferred from multispecies comparative maps. Science 309:613–617

    Article  CAS  PubMed  Google Scholar 

  • Perelman P (2011) Second generation of alpaca radiation hybrid map: use of high-throughput genotyping. In Conference on Camelid Genetics & Reproduction Houston, TX, USA

    Google Scholar 

  • Raudsepp T (2014) Cytogenetics and infertility. In Llama and Alpaca Care: Medicine, Surgery Reproduction, Nutrition and Herd Health C. Cebra, ed. St. Louis, Missouri, USA: Elsevier Inc., pp 243–249

  • Raudsepp T, Chowdhary BP (2008) FISH for mapping single copy genes. Methods Mol Biol 422:31–49

    Article  CAS  PubMed  Google Scholar 

  • Raudsepp T, Chowdhary BP (2011) Cytogenetics and physical chromosome maps. In The Genetics of the Pig, A. Ruvinsky, M. Rothschild, eds.: CAB International, pp 134–178

  • Raudsepp T, Chowdhary BP (2013) Physical and comparative map. In: Chowdhary BP (ed) Equine genomics. Oxford, UK, Wiley-Blackwell, pp 49–72

    Chapter  Google Scholar 

  • Rens W, Fu B, O’Brien PC, Ferguson-Smith M (2006) Cross-species chromosome painting. Nat Protoc 1:783–790

    Article  CAS  PubMed  Google Scholar 

  • Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365–386

    CAS  PubMed  Google Scholar 

  • Rubes J, Pinton A, Bonnet-Garnier A et al (2009) Fluorescence in situ hybridization applied to domestic animal cytogenetics. Cytogenet Genome Res 126:34–48

    Article  CAS  PubMed  Google Scholar 

  • Scherthan H, Cremer T, Arnason U et al (1994) Comparative chromosome painting discloses homologous segments in distantly related mammals. Nat Genet 6:342–347

    Article  CAS  PubMed  Google Scholar 

  • Stanyon R, Rocchi M, Bigoni F, Archidiacono N (2012) Evolutionary molecular cytogenetics of catarrhine primates: past, present and future. Cytogenet Genome Res 137:273–284

    Article  CAS  PubMed  Google Scholar 

  • Telenius H, Carter NP, Bebb CE et al (1992) Degenerate oligonucleotide-primed PCR: general amplification of target DNA by a single degenerate primer. Genomics 13:718–725

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank Dr. Ahmed Tibary and Dr. Lisa Pearson for providing blood samples of normal and infertile alpacas and Dr. Natalia Serdukova for the human 5.8S, 18S, and 28S rDNA probe. The work was supported by Morris Animal Foundation grants D09LA-004 and D14LA-005 and a grant (2009–2011) by Alpaca Research Foundation.

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Authors and Affiliations

  1. Department of Veterinary Integrative Biosciences, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, TX, 77843-4458, USA

    Felipe Avila, Malorie P. Baily, Renuka Chowdhary, Jan Janečka & Terje Raudsepp

  2. Binghamton University (SUNY), Binghamton, NY, USA

    David A. Merriwether

  3. Institute of Molecular and Cellular Biology, SВ RAS, Novosibirsk, Russia

    Vladimir A. Trifonov

  4. Novosibirsk State University, Novosibirsk, Russia

    Vladimir A. Trifonov

  5. Veterinary Research Institute, Brno, Czech Republic

    Jiři Rubes

  6. Department of Animal and Rangeland Sciences, Oregon State University, Corvallis, OR, 97331, USA

    Michelle A. Kutzler

  7. Biological Sciences, Duquesne University, 236 Mellon Hall, 600 Forbes Ave, Pittsburgh, PA, 15282, USA

    Jan Janečka

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  1. Felipe Avila
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  2. Malorie P. Baily
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  3. David A. Merriwether
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  4. Vladimir A. Trifonov
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  5. Jiři Rubes
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  6. Michelle A. Kutzler
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  7. Renuka Chowdhary
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  8. Jan Janečka
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  9. Terje Raudsepp
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Correspondence to Terje Raudsepp.

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Avila, F., Baily, M.P., Merriwether, D.A. et al. A cytogenetic and comparative map of camelid chromosome 36 and the minute in alpacas. Chromosome Res 23, 237–251 (2015). https://doi.org/10.1007/s10577-014-9463-3

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  • DOI: https://doi.org/10.1007/s10577-014-9463-3

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