Skip to main content
PMC home page
Genetics logoLink to Genetics
. 1991 Jul;128(3):595–606. doi: 10.1093/genetics/128.3.595

Sequence Identity in an Early Chorion Multigene Family Is the Result of Localized Gene Conversion

B L Hibner 1, W D Burke 1, T H Eickbush 1
PMCID: PMC1204533  PMID: 1874417

Abstract

The multigene families that encode the chorion (eggshell) of the silk moth, Bombyx mori, are closely linked on one chromosome. We report here the isolation and characterization of two segments, totaling 102 kb of genomic DNA, containing the genes expressed during the early period of choriogenesis. Most of these early genes can be divided into two multigene families, ErA and ErB, organized into five divergently transcribed ErA/ErB gene pairs. Nucleotide sequence identity in the major coding regions of the ErA genes was 96%, while nucleotide sequence identity for the ErB major coding regions was only 63%. Selection pressure on the encoded proteins cannot explain this difference in the level of sequence conservation between the ErA and ErB gene families, since when only fourfold redundant codon positions are considered, the divergence within the ErA genes is 8%, while the divergence within the ErB genes (corrected for multiple substitutions at the same site) is 110%. The high sequence identity of the ErA major exons can be explained by sequence exchange events similar to gene conversion localized to the major exon of the ErA genes. These gene conversions are correlated with the presence of clustered copies of the nucleotide sequence GGXGGX, encoding paired glycine residues. This sequence has previously been correlated with gradients of gene conversion that extend throughout the coding and noncoding regions of the High-cysteine (Hc) chorion genes of B. mori. We suggest that the difference in the extent of the conversion tracts in these gene families reflects a tendency for these recombination events to become localized over time to the protein encoding regions of the major exons.

Full Text

The Full Text of this article is available as a PDF (2.5 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adams D. S., Eickbush T. H., Herrera R. J., Lizardi P. M. A highly reiterated family of transcribed oligo(A)-terminated, interspersed DNA elements in the genome of Bombyx mori. J Mol Biol. 1986 Feb 20;187(4):465–478. doi: 10.1016/0022-2836(86)90327-x. [DOI] [PubMed] [Google Scholar]
  2. Atchison M., Adesnik M. Gene conversion in a cytochrome P-450 gene family. Proc Natl Acad Sci U S A. 1986 Apr;83(8):2300–2304. doi: 10.1073/pnas.83.8.2300. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Borts R. H., Haber J. E. Length and distribution of meiotic gene conversion tracts and crossovers in Saccharomyces cerevisiae. Genetics. 1989 Sep;123(1):69–80. doi: 10.1093/genetics/123.1.69. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Burke W. D., Eickbush T. H. The silkmoth late chorion locus. I. Variation within two paired multigene families. J Mol Biol. 1986 Aug 5;190(3):343–356. doi: 10.1016/0022-2836(86)90006-9. [DOI] [PubMed] [Google Scholar]
  5. Coen E., Strachan T., Dover G. Dynamics of concerted evolution of ribosomal DNA and histone gene families in the melanogaster species subgroup of Drosophila. J Mol Biol. 1982 Jun 15;158(1):17–35. doi: 10.1016/0022-2836(82)90448-x. [DOI] [PubMed] [Google Scholar]
  6. Crain W. R., Jr, Boshar M. F., Cooper A. D., Durica D. S., Nagy A., Steffen D. The sequence of a sea urchin muscle actin gene suggests a gene conversion with a cytoskeletal actin gene. J Mol Evol. 1987;25(1):37–45. doi: 10.1007/BF02100039. [DOI] [PubMed] [Google Scholar]
  7. Dover G. A. DNA fingerprinting. Mapping 'frozen accidents'. Nature. 1990 Apr 26;344(6269):812–813. doi: 10.1038/344812a0. [DOI] [PubMed] [Google Scholar]
  8. Eickbush T. H., Burke W. D. Silkmoth chorion gene families contain patchwork patterns of sequence homology. Proc Natl Acad Sci U S A. 1985 May;82(9):2814–2818. doi: 10.1073/pnas.82.9.2814. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Eickbush T. H., Burke W. D. The silkmoth late chorion locus. II. Gradients of gene conversion in two paired multigene families. J Mol Biol. 1986 Aug 5;190(3):357–366. doi: 10.1016/0022-2836(86)90007-0. [DOI] [PubMed] [Google Scholar]
  10. Eickbush T. H., Kafatos F. C. A walk in the chorion locus of Bombyx mori. Cell. 1982 Jun;29(2):633–643. doi: 10.1016/0092-8674(82)90179-9. [DOI] [PubMed] [Google Scholar]
  11. Eickbush T. H., Rodakis G. C., Lecanidou R., Kafatos F. C. A complex set of early chorion DNA sequences from Bombyx mori. Dev Biol. 1985 Dec;112(2):368–376. doi: 10.1016/0012-1606(85)90408-7. [DOI] [PubMed] [Google Scholar]
  12. Geliebter J., Nathenson S. G. Microrecombinations generate sequence diversity in the murine major histocompatibility complex: analysis of the Kbm3, Kbm4, Kbm10, and Kbm11 mutants. Mol Cell Biol. 1988 Oct;8(10):4342–4352. doi: 10.1128/mcb.8.10.4342. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Goldsmith M. R., Clermont-Rattner E. Organization of the Chorion Genes of BOMBYX MORI, a Multigene Family. II. Partial Localization of Three Gene Clusters. Genetics. 1979 Aug;92(4):1173–1185. doi: 10.1093/genetics/92.4.1173. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Goldsmith M. R., Clermont-Rattner E. Organization of the chorion genes of Bombyx mori, a multigene family. III. Detailed marker composition of three gene clusters. Genetics. 1980 Sep;96(1):201–212. doi: 10.1093/genetics/96.1.201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Goldsmith M. R., Kafatos F. C. Developmentally regulated genes in silkmoths. Annu Rev Genet. 1984;18:443–487. doi: 10.1146/annurev.ge.18.120184.002303. [DOI] [PubMed] [Google Scholar]
  16. Gumucio D. L., Wiebauer K., Caldwell R. M., Samuelson L. C., Meisler M. H. Concerted evolution of human amylase genes. Mol Cell Biol. 1988 Mar;8(3):1197–1205. doi: 10.1128/mcb.8.3.1197. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hibner B. L., Burke W. D., Lecanidou R., Rodakis G. C., Eickbush T. H. Organization and expression of three genes from the silkmoth early chorion locus. Dev Biol. 1988 Feb;125(2):423–431. doi: 10.1016/0012-1606(88)90223-0. [DOI] [PubMed] [Google Scholar]
  18. Iatrou K., Tsitilou S. G., Kafatos F. C. Developmental classes and homologous families of chorion genes in Bombyx mori. J Mol Biol. 1982 May 25;157(3):417–434. doi: 10.1016/0022-2836(82)90469-7. [DOI] [PubMed] [Google Scholar]
  19. Jackson J. A., Fink G. R. Gene conversion between duplicated genetic elements in yeast. Nature. 1981 Jul 23;292(5821):306–311. doi: 10.1038/292306a0. [DOI] [PubMed] [Google Scholar]
  20. Jeffreys A. J., Neumann R., Wilson V. Repeat unit sequence variation in minisatellites: a novel source of DNA polymorphism for studying variation and mutation by single molecule analysis. Cell. 1990 Feb 9;60(3):473–485. doi: 10.1016/0092-8674(90)90598-9. [DOI] [PubMed] [Google Scholar]
  21. Jeffreys A. J., Wilson V., Thein S. L. Hypervariable 'minisatellite' regions in human DNA. Nature. 1985 Mar 7;314(6006):67–73. doi: 10.1038/314067a0. [DOI] [PubMed] [Google Scholar]
  22. Judd S. R., Petes T. D. Physical lengths of meiotic and mitotic gene conversion tracts in Saccharomyces cerevisiae. Genetics. 1988 Mar;118(3):401–410. doi: 10.1093/genetics/118.3.401. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Kafatos F. C., Regier J. C., Mazur G. D., Nadel M. R., Blau H. M., Petri W. H., Wyman A. R., Gelinas R. E., Moore P. B., Paul M. The eggshell of insects: differentiation-specific proteins and the control of their synthesis and accumulation during development. Results Probl Cell Differ. 1977;8:45–145. doi: 10.1007/978-3-540-37332-2_2. [DOI] [PubMed] [Google Scholar]
  24. Kobori J. A., Strauss E., Minard K., Hood L. Molecular analysis of the hotspot of recombination in the murine major histocompatibility complex. Science. 1986 Oct 10;234(4773):173–179. doi: 10.1126/science.3018929. [DOI] [PubMed] [Google Scholar]
  25. Konsolaki M., Komitopoulou K., Tolias P. P., King D. L., Swimmer C., Kafatos F. C. The chorion genes of the medfly, Ceratitis capitata, I: Structural and regulatory conservation of the s36 gene relative to two Drosophila species. Nucleic Acids Res. 1990 Apr 11;18(7):1731–1737. doi: 10.1093/nar/18.7.1731. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Le Blancq S. M., Swinkels B. W., Gibson W. C., Borst P. Evidence for gene conversion between the phosphoglycerate kinase genes of Trypanosoma brucei. J Mol Biol. 1988 Apr 5;200(3):439–447. doi: 10.1016/0022-2836(88)90534-7. [DOI] [PubMed] [Google Scholar]
  27. Lecanidou R., Eickbush T. H., Rodakis G. C., Kafatos F. C. Novel B family sequence from an early chorion cDNA library of Bombyx mori. Proc Natl Acad Sci U S A. 1983 Apr;80(7):1955–1959. doi: 10.1073/pnas.80.7.1955. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Loenen W. A., Blattner F. R. Lambda Charon vectors (Ch32, 33, 34 and 35) adapted for DNA cloning in recombination-deficient hosts. Gene. 1983 Dec;26(2-3):171–179. doi: 10.1016/0378-1119(83)90187-7. [DOI] [PubMed] [Google Scholar]
  29. Lyons K. M., Stein J. H., Smithies O. Length polymorphisms in human proline-rich protein genes generated by intragenic unequal crossing over. Genetics. 1988 Sep;120(1):267–278. doi: 10.1093/genetics/120.1.267. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Mitsialis S. A., Kafatos F. C. Regulatory elements controlling chorion gene expression are conserved between flies and moths. Nature. 1985 Oct 3;317(6036):453–456. doi: 10.1038/317453a0. [DOI] [PubMed] [Google Scholar]
  31. Mitsialis S. A., Spoerel N., Leviten M., Kafatos F. C. A short 5'-flanking DNA region is sufficient for developmentally correct expression of moth chorion genes in Drosophila. Proc Natl Acad Sci U S A. 1987 Nov;84(22):7987–7991. doi: 10.1073/pnas.84.22.7987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Nagylaki T., Petes T. D. Intrachromosomal gene conversion and the maintenance of sequence homogeneity among repeated genes. Genetics. 1982 Feb;100(2):315–337. doi: 10.1093/genetics/100.2.315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Parham P., Lomen C. E., Lawlor D. A., Ways J. P., Holmes N., Coppin H. L., Salter R. D., Wan A. M., Ennis P. D. Nature of polymorphism in HLA-A, -B, and -C molecules. Proc Natl Acad Sci U S A. 1988 Jun;85(11):4005–4009. doi: 10.1073/pnas.85.11.4005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Park Y. S., Kramer J. M. Tandemly duplicated Caenorhabditis elegans collagen genes differ in their modes of splicing. J Mol Biol. 1990 Jan 20;211(2):395–406. doi: 10.1016/0022-2836(90)90360-X. [DOI] [PubMed] [Google Scholar]
  35. Powers P. A., Smithies O. Short gene conversions in the human fetal globin gene region: a by-product of chromosome pairing during meiosis? Genetics. 1986 Feb;112(2):343–358. doi: 10.1093/genetics/112.2.343. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Reynaud C. A., Anquez V., Grimal H., Weill J. C. A hyperconversion mechanism generates the chicken light chain preimmune repertoire. Cell. 1987 Feb 13;48(3):379–388. doi: 10.1016/0092-8674(87)90189-9. [DOI] [PubMed] [Google Scholar]
  37. Ruppert S., Scherer G., Schütz G. Recent gene conversion involving bovine vasopressin and oxytocin precursor genes suggested by nucleotide sequence. Nature. 1984 Apr 5;308(5959):554–557. doi: 10.1038/308554a0. [DOI] [PubMed] [Google Scholar]
  38. Seperack P., Slatkin M., Arnheim N. Linkage disequilibrium in human ribosomal genes: implications for multigene family evolution. Genetics. 1988 Aug;119(4):943–949. doi: 10.1093/genetics/119.4.943. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Smith G. P. Evolution of repeated DNA sequences by unequal crossover. Science. 1976 Feb 13;191(4227):528–535. doi: 10.1126/science.1251186. [DOI] [PubMed] [Google Scholar]
  40. Smith G. R., Kunes S. M., Schultz D. W., Taylor A., Triman K. L. Structure of chi hotspots of generalized recombination. Cell. 1981 May;24(2):429–436. doi: 10.1016/0092-8674(81)90333-0. [DOI] [PubMed] [Google Scholar]
  41. Szostak J. W., Wu R. Unequal crossing over in the ribosomal DNA of Saccharomyces cerevisiae. Nature. 1980 Apr 3;284(5755):426–430. doi: 10.1038/284426a0. [DOI] [PubMed] [Google Scholar]
  42. Vollrath D., Nathans J., Davis R. W. Tandem array of human visual pigment genes at Xq28. Science. 1988 Jun 17;240(4859):1669–1672. doi: 10.1126/science.2837827. [DOI] [PubMed] [Google Scholar]
  43. Wheeler C. J., Maloney D., Fogel S., Goodenow R. S. Microconversion between murine H-2 genes integrated into yeast. Nature. 1990 Sep 13;347(6289):192–194. doi: 10.1038/347192a0. [DOI] [PubMed] [Google Scholar]
  44. Yanisch-Perron C., Vieira J., Messing J. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene. 1985;33(1):103–119. doi: 10.1016/0378-1119(85)90120-9. [DOI] [PubMed] [Google Scholar]
  45. Yue X. N., Sakaguchi B., Eickbush T. H. Gene conversions can generate sequence variants in the late chorion multigene families of Bombyx mori. Genetics. 1988 Sep;120(1):221–231. doi: 10.1093/genetics/120.1.221. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES