Abstract
Concerted evolution of multicopy gene families in vertebrates is recognized as an important force in the generation of biological novelty but has not been documented for the multicopy genes of protozoa. A multicopy locus, Tpr, which consists of tandemly arrayed open reading frames (ORFs) containing several repeated elements has been described for Theileria parva. Herein we show that probes derived from the 5'/N-terminal ends of ORFs in the genomic DNAs of T. parva Uganda (1,108 codons) and Boleni (699 codons) hybridized with multicopy sequences in homologous DNA but did not detect similar sequences in the DNA of 14 heterologous T. parva stocks and clones. The probe sequences were, however, protein coding according to predictive algorithms and codon usage. The 3'/C-terminal ends of the Uganda and Boleni ORFs exhibited 75% similarity and identity, respectively, to the previously identified Tpr1 and Tpr2 repetitive elements of T. parva Muguga. Tpr1-homologous sequences were detected in two additional species of Theileria. Eight different Tpr1-homologous transcripts were present in piroplasm mRNA from a single T. parva Muguga-infected animal. The Tpr1 and Tpr2 amino acid sequences contained six predicted membrane-associated segments. The ratio of synonymous to nonsynonymous substitutions indicates that Tpr1 evolves like protein-encoding DNA. The previously determined nucleotide sequence of the gene encoding the p67 antigen is completely identical in T. parva Muguga, Boleni, and Uganda, including the third base in codons. The data suggest that concerted evolution can lead to the radical divergence of coding sequences and that this can be a mechanism for the generation of novel genes.
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- Allsopp B., Carrington M., Baylis H., Sohal S., Dolan T., Iams K. Improved characterization of Theileria parva isolates using the polymerase chain reaction and oligonucleotide probes. Mol Biochem Parasitol. 1989 Jun 15;35(2):137–147. doi: 10.1016/0166-6851(89)90116-3. [DOI] [PubMed] [Google Scholar]
- Arnheim N., Krystal M., Schmickel R., Wilson G., Ryder O., Zimmer E. Molecular evidence for genetic exchanges among ribosomal genes on nonhomologous chromosomes in man and apes. Proc Natl Acad Sci U S A. 1980 Dec;77(12):7323–7327. doi: 10.1073/pnas.77.12.7323. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Baruch D. I., Pasloske B. L., Singh H. B., Bi X., Ma X. C., Feldman M., Taraschi T. F., Howard R. J. Cloning the P. falciparum gene encoding PfEMP1, a malarial variant antigen and adherence receptor on the surface of parasitized human erythrocytes. Cell. 1995 Jul 14;82(1):77–87. doi: 10.1016/0092-8674(95)90054-3. [DOI] [PubMed] [Google Scholar]
- Baylis H. A., Sohal S. K., Carrington M., Bishop R. P., Allsopp B. A. An unusual repetitive gene family in Theileria parva which is stage-specifically transcribed. Mol Biochem Parasitol. 1991 Nov;49(1):133–142. doi: 10.1016/0166-6851(91)90136-t. [DOI] [PubMed] [Google Scholar]
- Bishop R. P., Sohanpal B. K., Allsopp B. A., Spooner P. R., Dolan T. T., Morzaria S. P. Detection of polymorphisms among Theileria parva stocks using repetitive, telomeric and ribosomal DNA probes and anti-schizont monoclonal antibodies. Parasitology. 1993 Jul;107(Pt 1):19–31. doi: 10.1017/s0031182000079361. [DOI] [PubMed] [Google Scholar]
- Blum M. L., Down J. A., Gurnett A. M., Carrington M., Turner M. J., Wiley D. C. A structural motif in the variant surface glycoproteins of Trypanosoma brucei. Nature. 1993 Apr 15;362(6421):603–609. doi: 10.1038/362603a0. [DOI] [PubMed] [Google Scholar]
- Boles E., Zimmermann F. K. Open reading frames in the antisense strands of genes coding for glycolytic enzymes in Saccharomyces cerevisiae. Mol Gen Genet. 1994 May 25;243(4):363–368. doi: 10.1007/BF00280465. [DOI] [PubMed] [Google Scholar]
- Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
- Conrad P. A., Iams K., Brown W. C., Sohanpal B., ole-MoiYoi O. K. DNA probes detect genomic diversity in Theileria parva stocks. Mol Biochem Parasitol. 1987 Oct;25(3):213–226. doi: 10.1016/0166-6851(87)90085-5. [DOI] [PubMed] [Google Scholar]
- Cross G. A. Cellular and genetic aspects of antigenic variation in trypanosomes. Annu Rev Immunol. 1990;8:83–110. doi: 10.1146/annurev.iy.08.040190.000503. [DOI] [PubMed] [Google Scholar]
- Dover G., Coen E. Springcleaning ribosomal DNA: a model for multigene evolution? Nature. 1981 Apr 30;290(5809):731–732. doi: 10.1038/290731a0. [DOI] [PubMed] [Google Scholar]
- Dover G. Molecular drive: a cohesive mode of species evolution. Nature. 1982 Sep 9;299(5879):111–117. doi: 10.1038/299111a0. [DOI] [PubMed] [Google Scholar]
- Eisenberg D., Schwarz E., Komaromy M., Wall R. Analysis of membrane and surface protein sequences with the hydrophobic moment plot. J Mol Biol. 1984 Oct 15;179(1):125–142. doi: 10.1016/0022-2836(84)90309-7. [DOI] [PubMed] [Google Scholar]
- Ellis J., Griffin H., Morrison D., Johnson A. M. Analysis of dinucleotide frequency and codon usage in the phylum Apicomplexa. Gene. 1993 Apr 30;126(2):163–170. doi: 10.1016/0378-1119(93)90363-8. [DOI] [PubMed] [Google Scholar]
- Fickett J. W. Recognition of protein coding regions in DNA sequences. Nucleic Acids Res. 1982 Sep 11;10(17):5303–5318. doi: 10.1093/nar/10.17.5303. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Han J. H., Stratowa C., Rutter W. J. Isolation of full-length putative rat lysophospholipase cDNA using improved methods for mRNA isolation and cDNA cloning. Biochemistry. 1987 Mar 24;26(6):1617–1625. doi: 10.1021/bi00380a020. [DOI] [PubMed] [Google Scholar]
- Higgins D. G., Sharp P. M. CLUSTAL: a package for performing multiple sequence alignment on a microcomputer. Gene. 1988 Dec 15;73(1):237–244. doi: 10.1016/0378-1119(88)90330-7. [DOI] [PubMed] [Google Scholar]
- Hopp T. P., Woods K. R. A computer program for predicting protein antigenic determinants. Mol Immunol. 1983 Apr;20(4):483–489. doi: 10.1016/0161-5890(83)90029-9. [DOI] [PubMed] [Google Scholar]
- Keese P. K., Gibbs A. Origins of genes: "big bang" or continuous creation? Proc Natl Acad Sci U S A. 1992 Oct 15;89(20):9489–9493. doi: 10.1073/pnas.89.20.9489. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Klein P., Kanehisa M., DeLisi C. The detection and classification of membrane-spanning proteins. Biochim Biophys Acta. 1985 May 28;815(3):468–476. doi: 10.1016/0005-2736(85)90375-x. [DOI] [PubMed] [Google Scholar]
- Kyte J., Doolittle R. F. A simple method for displaying the hydropathic character of a protein. J Mol Biol. 1982 May 5;157(1):105–132. doi: 10.1016/0022-2836(82)90515-0. [DOI] [PubMed] [Google Scholar]
- Lanzer M., Fischer K., Le Blancq S. M. Parasitism and chromosome dynamics in protozoan parasites: is there a connection? Mol Biochem Parasitol. 1995 Mar;70(1-2):1–8. doi: 10.1016/0166-6851(95)00021-r. [DOI] [PubMed] [Google Scholar]
- Marchuk D., Drumm M., Saulino A., Collins F. S. Construction of T-vectors, a rapid and general system for direct cloning of unmodified PCR products. Nucleic Acids Res. 1991 Mar 11;19(5):1154–1154. doi: 10.1093/nar/19.5.1154. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Matthews B. W., Rossmann M. G. Comparison of protein structures. Methods Enzymol. 1985;115:397–420. doi: 10.1016/0076-6879(85)15029-9. [DOI] [PubMed] [Google Scholar]
- McCutchan T. F., Dame J. B., Gwadz R. W., Vernick K. D. The genome of Plasmodium cynomolgi is partitioned into separable domains which appear to differ in sequence stability. Nucleic Acids Res. 1988 May 25;16(10):4499–4510. doi: 10.1093/nar/16.10.4499. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Minami T., Spooner P. R., Irvin A. D., Ocama J. G., Dobbelaere D. A., Fujinaga T. Characterisation of stocks of Theileria parva by monoclonal antibody profiles. Res Vet Sci. 1983 Nov;35(3):334–340. [PubMed] [Google Scholar]
- Miyata T., Yasunaga T., Nishida T. Nucleotide sequence divergence and functional constraint in mRNA evolution. Proc Natl Acad Sci U S A. 1980 Dec;77(12):7328–7332. doi: 10.1073/pnas.77.12.7328. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mohana Rao J. K., Argos P. A conformational preference parameter to predict helices in integral membrane proteins. Biochim Biophys Acta. 1986 Jan 30;869(2):197–214. doi: 10.1016/0167-4838(86)90295-5. [DOI] [PubMed] [Google Scholar]
- Morzaria S. P., Dolan T. T., Norval R. A., Bishop R. P., Spooner P. R. Generation and characterization of cloned Theileria parva parasites. Parasitology. 1995 Jul;111(Pt 1):39–49. doi: 10.1017/s0031182000064581. [DOI] [PubMed] [Google Scholar]
- Morzaria S. P., Spooner P. R., Bishop R. P., Musoke A. J., Young J. R. SfiI and NotI polymorphisms in Theileria stocks detected by pulsed field gel electrophoresis. Mol Biochem Parasitol. 1990 May;40(2):203–211. doi: 10.1016/0166-6851(90)90042-k. [DOI] [PubMed] [Google Scholar]
- Morzaria S. P., Young J. R. Restriction mapping of the genome of the protozoan parasite Theileria parva. Proc Natl Acad Sci U S A. 1992 Jun 15;89(12):5241–5245. doi: 10.1073/pnas.89.12.5241. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nagylaki T. Evolution of multigene families under interchromosomal gene conversion. Proc Natl Acad Sci U S A. 1984 Jun;81(12):3796–3800. doi: 10.1073/pnas.81.12.3796. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nei M., Gojobori T. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol. 1986 Sep;3(5):418–426. doi: 10.1093/oxfordjournals.molbev.a040410. [DOI] [PubMed] [Google Scholar]
- Nene V., Iams K. P., Gobright E., Musoke A. J. Characterisation of the gene encoding a candidate vaccine antigen of Theileria parva sporozoites. Mol Biochem Parasitol. 1992 Mar;51(1):17–27. doi: 10.1016/0166-6851(92)90196-q. [DOI] [PubMed] [Google Scholar]
- Nene V., Musoke A., Gobright E., Morzaria S. Conservation of the sporozoite p67 vaccine antigen in cattle-derived Theileria parva stocks with different cross-immunity profiles. Infect Immun. 1996 Jun;64(6):2056–2061. doi: 10.1128/iai.64.6.2056-2061.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pays E., Vanhamme L., Berberof M. Genetic controls for the expression of surface antigens in African trypanosomes. Annu Rev Microbiol. 1994;48:25–52. doi: 10.1146/annurev.mi.48.100194.000325. [DOI] [PubMed] [Google Scholar]
- Roditi I., Pearson T. W. The procyclin coat of African trypanosomes (or the not-so-naked trypanosome). Parasitol Today. 1990 Mar;6(3):79–82. doi: 10.1016/0169-4758(90)90216-q. [DOI] [PubMed] [Google Scholar]
- Senapathy P. Origin of eukaryotic introns: a hypothesis, based on codon distribution statistics in genes, and its implications. Proc Natl Acad Sci U S A. 1986 Apr;83(7):2133–2137. doi: 10.1073/pnas.83.7.2133. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shepherd J. C. Method to determine the reading frame of a protein from the purine/pyrimidine genome sequence and its possible evolutionary justification. Proc Natl Acad Sci U S A. 1981 Mar;78(3):1596–1600. doi: 10.1073/pnas.78.3.1596. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Smith G. P. Unequal crossover and the evolution of multigene families. Cold Spring Harb Symp Quant Biol. 1974;38:507–513. doi: 10.1101/sqb.1974.038.01.055. [DOI] [PubMed] [Google Scholar]
- Smith J. D., Chitnis C. E., Craig A. G., Roberts D. J., Hudson-Taylor D. E., Peterson D. S., Pinches R., Newbold C. I., Miller L. H. Switches in expression of Plasmodium falciparum var genes correlate with changes in antigenic and cytoadherent phenotypes of infected erythrocytes. Cell. 1995 Jul 14;82(1):101–110. doi: 10.1016/0092-8674(95)90056-x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Su X. Z., Heatwole V. M., Wertheimer S. P., Guinet F., Herrfeldt J. A., Peterson D. S., Ravetch J. A., Wellems T. E. The large diverse gene family var encodes proteins involved in cytoadherence and antigenic variation of Plasmodium falciparum-infected erythrocytes. Cell. 1995 Jul 14;82(1):89–100. doi: 10.1016/0092-8674(95)90055-1. [DOI] [PubMed] [Google Scholar]
- Südhof T. C., Goldstein J. L., Brown M. S., Russell D. W. The LDL receptor gene: a mosaic of exons shared with different proteins. Science. 1985 May 17;228(4701):815–822. doi: 10.1126/science.2988123. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wilson R. J., Ling I. Fractionation and characterization of Plasmodium falciparum antigens. Bull World Health Organ. 1979;57 (Suppl 1):123–133. [PMC free article] [PubMed] [Google Scholar]
- Wistow G. Lens crystallins: gene recruitment and evolutionary dynamism. Trends Biochem Sci. 1993 Aug;18(8):301–306. doi: 10.1016/0968-0004(93)90041-k. [DOI] [PubMed] [Google Scholar]
- Yomo T., Urabe I., Okada H. No stop codons in the antisense strands of the genes for nylon oligomer degradation. Proc Natl Acad Sci U S A. 1992 May 1;89(9):3780–3784. doi: 10.1073/pnas.89.9.3780. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Young R. A., Mehra V., Sweetser D., Buchanan T., Clark-Curtiss J., Davis R. W., Bloom B. R. Genes for the major protein antigens of the leprosy parasite Mycobacterium leprae. Nature. 1985 Aug 1;316(6027):450–452. doi: 10.1038/316450a0. [DOI] [PubMed] [Google Scholar]