Skip to main content
Log in

Initial characterization of a protochordate histocompatibility locus

  • Original Paper
  • Published:
Immunogenetics Aims and scope Submit manuscript

Abstract

The colonial protochordate, Botryllus schlosseri, undergoes a natural transplantation reaction which is controlled by a single, highly polymorphic locus called the Fu/HC. We are using map-based cloning to identify Fu/HC gene(s), and have currently delineated their location to an approximately 1-cM region of the B. schlosseri genome. The Fu/HC physical map currently consists of 85 sequence-tagged sites mapped on a minimum tiling path of 800 kb which consists of five contigs, with four gaps remaining to be crossed, and is estimated to be 75% completed. Approximately half this region has been sequenced throughout the locus, allowing the first analysis of a metazoan histocompatibility locus outside of vertebrates. This has resulted in the identification of 18 predicted genes, a number of which have been found to be expressed. Several of these genes are well conserved among the chordates; however, none of the predicted or expressed genes are linked within the genome of any organism in the databases. In addition, the Fu/HC is one of the most polymorphic loci ever described, and physical mapping has revealed that the locus is quite dynamic, and includes features such as hotspots of recombination.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search Programs. Nucleic Acids Res 25:3389–3402

    PubMed  Google Scholar 

  • Azumi K, De Santis R, De Tomaso AW, Rigoutsos I, Yoshizaki F, Pinto MR, Marino R, Shida K, Ikeda M, Ikeda M, Arai M, Inoue Y, Shimizu Y, Satoh N, Rokhsar DS, DuPasquier L, Kasahara M, Satake M, Nonaka M (2003) Genomic analysis of immunity in a basal chordate and the emergence of the vertebrate immune system: waiting for Godot. Immunogenetics (in press)

    Google Scholar 

  • Boyd HC, Brown SK, Harp JA, Weissman IL (1986) Growth and sexual maturation of laboratory-cultured Monterey Botryllus schlosseri. Biol Bull 170:91–109

    Google Scholar 

  • Burge CB, Karlin S (1998) Finding the genes in genomic DNA. Curr Opin Struct Biol 8:346–354

    Google Scholar 

  • Burnet FM (1971) Self-recognition in colonial marine forms and flowering plants in relation to the evolution of immunity. Nature 232:123–126

    Google Scholar 

  • Cannon JP, Haire RN, Litman GW (2002) Identification of diversified genes that contain immunoglobulin-like variable regions in a protochordate. Nature Immunology 3:1200–1207

    Google Scholar 

  • De Tomaso AW, Weissman IL (2003) Construction and characterization of large insert libraries (BAC and Fosmid) from the colonial protochordate Botryllus schlosseri. Marine Biotechnol 5:103–115

    Google Scholar 

  • De Tomaso AW, Saito Y, Ishizuka KJ, Palmeri KJ, Weissman IL (1998) Mapping the genome of a model protochordate. I. A low resolution genetic map encompassing the fusion/histocompatibility (Fu/HC) locus of Botryllus schlosseri. Genetics 149:277–287

    CAS  PubMed  Google Scholar 

  • Dehal P et al (2002) The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. Science 298:2157–2167

    Article  CAS  PubMed  Google Scholar 

  • DuPasquier L, Flajnik M (1999) Origin and evolution of the vertebrate immune system. In: Paul WE (ed) Fundamental immunology. Lippincott-Raven, Philadelphia

  • Flajnik MF, Kasahara M (2001) Comparative genomics of the MHC: glimpses into the evolution of the adaptive immune system. Immunity 15:351–62

    PubMed  Google Scholar 

  • Flajnik MF, Ohta Y, Namikawa-Yamada C, Nonaka M (1999) Insight into the primordial MHC from studies in ecothermal vertebrates. Immunol Rev 167:59–68

    PubMed  Google Scholar 

  • Frohman MA, Dush MK, Martin GR (1987) Rapid production of full-length cDNAs from rare transcripts; amplification using a single gene-specific oligonucleotide primer. Proc Natl Acad Sci USA 85:8998–9002

    Google Scholar 

  • Karre K (1997) How to recognize a foreign submarine. Immunol Rev 155:5–9

    CAS  PubMed  Google Scholar 

  • Kasahara M (1998) What do the paralogous regions in the genome tell us about the origin of the adaptive immune system? Immunol Rev 166:159–175

    Google Scholar 

  • Kaufman J, Milne S, Gobel TW, Walker BA, Jacob JP, Auffray C, Zoorob R, Beck S (1999) The chicken B locus is a minimal essential major histocompatibility complex. Nature 1999 401:923–925

    Article  CAS  Google Scholar 

  • Michelmore RW, Paran I, Kesseli RV (1991) Identification of markers lined to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. Proc Natl Acad Sci USA 88:9828–9832

    PubMed  Google Scholar 

  • Oka H, Watanabe H (1960) Problems of colony specificity in compound ascidians. Bull Biol Stn Asamushi 10:153–155

    Google Scholar 

  • Olson M, Hood L, Cantor C, Botstein D (1989) A common language for physical mapping of the human genome. Science 245:1434–1435

    CAS  PubMed  Google Scholar 

  • Orita M, Iwahana H, Kanazawa H, Hayashi K, Sikeya T (1989) Detection of polymorphisms of human DNA by gel electrophoresis as single strand conformation polymorphisms. Proc Natl Acad Sci USA 86:2766–2770

    PubMed  Google Scholar 

  • Rosati F, De Santis R (1978) Studies on fertilization in the ascidians 1. Self-sterility and specific recognition between gametes of Ciona intestinalis. Exp Cell Res 121:111–119

    Google Scholar 

  • Ross MT, LaBrie S, McPherson J, Stanton VP Jr (1999) Screening large-insert libraries by hybridization. In In: Boyl A (ed) Current protocols in human genetics. Wiley, New York, pp 5.6.1–5.6.52

    Google Scholar 

  • Sabbadin A (1962) Le basi genetiche dell capacita di fusione fra colonie in Botryllus schlosseri (Ascidiacea). Atti Accad Na Lincei Rend 32:1031–1035

    Google Scholar 

  • Scofield VL, Schlumpberger JM, West LA, Weissman IL (1982) Protochordate allorecognition is controlled by an MHC-like gene system. Nature 295:499–502

    CAS  PubMed  Google Scholar 

  • Sorrentino R, Iannicola C, Costanzi S, Chersi A, Tosi R (1991) Detection of complex alleles by direct analysis of DNA heteroduplexes. Immunogenetics 33:118–123

    CAS  PubMed  Google Scholar 

  • Stone SL, Anderson EM, Mullen RT, Goring DR (2003) ARC1 is an E3 Ubiquitin ligase and promotes the ubiquitination of proteins during the rejection of self-incompatible Brassica pollen. Plant Cell 15:885–898

    Article  PubMed  Google Scholar 

  • Vos P, Rogers R, Bleeker M, Reijans M, van de Lee T, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M, Zabeau M (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23:4407–4414

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We are indebted to Ron Davis, Audrey Southwick and Molly Miranda at the Stanford Genome and Technology Center for their generosity in the sequencing of large-insert clones. Fosmid sequencing is also being done at the University of Oklahoma Genome Center, under the auspices of the NIH-funded Genome Sequencing Network. We also thank David Ransom for tips and protocols on AFLP cloning. Kathi Ishizuka, Karla Palmeri and Vicki Tacaks have been responsible for B. schlosseri mariculture and breeding, and K. Palmeri has assisted in library screening. This work was supported by the NIH (RO1AI41588) to I.L.W. A.W.D. was an NIH postdoctoral scholar. Accession numbers for genomic sequence are: AC135107, AC139528, AC138022, AC140855, AC140856, AC139257, AC138953, AC139529 AC142501, AC136512, AC140854.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Anthony W. De Tomaso.

Rights and permissions

Reprints and permissions

About this article

Cite this article

De Tomaso, A.W., Weissman, I.L. Initial characterization of a protochordate histocompatibility locus. Immunogenetics 55, 480–490 (2003). https://doi.org/10.1007/s00251-003-0612-7

Download citation

  • Received:

  • Revised:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00251-003-0612-7

Keywords

Navigation