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. 1998 Dec;150(4):1625–1637. doi: 10.1093/genetics/150.4.1625

Extraordinary ribosomal spacer length heterogeneity in a neotyphodium endophyte hybrid: implications for concerted evolution.

A R Ganley 1, B Scott 1
PMCID: PMC1460432  PMID: 9832538

Abstract

An extraordinary level of length heterogeneity was found in the ribosomal DNA (rDNA) of an asexual hybrid Neotyphodium grass endophyte, isolate Lp1. This hybrid Neotyphodium endophyte is an interspecific hybrid between two grass endophytes, Neotyphodium lolii, and a sexual form, Epichlöe typhina, and the length heterogeneity was not found in either of these progenitor species. The length heterogeneity in the hybrid is localized to the intergenic spacer (IGS) and is the result of copy-number variation of a tandemly repeated subrepeat class within the IGS, the 111-/119-bp subrepeats. Copy number variation of this subrepeat class appears to be a consequence of mitotic unequal crossing over that occurs between these subrepeats. This implies that unequal crossing over plays a role in the concerted evolution of the whole rDNA. Changes in the pattern of IGS length variants occurred in just two rounds of single-spore purification. Analysis of the IGS length heterogeneity revealed features that are unexpected in a simple model of unequal crossing over. Potential refinements of the molecular details of unequal crossing over are presented, and we also discuss evidence for a combination of homogenization mechanisms that drive the concerted evolution of the Lp1 rDNA.

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Selected References

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

  1. Arnheim N., Kuehn M. The genetic behaviour of a cloned mouse ribosomal DNA segment mimics mouse ribosomal gene evolution. J Mol Biol. 1979 Nov 15;134(4):743–763. doi: 10.1016/0022-2836(79)90483-2. [DOI] [PubMed] [Google Scholar]
  2. Barker R. F., Harberd N. P., Jarvis M. G., Flavell R. B. Structure and evolution of the intergenic region in a ribosomal DNA repeat unit of wheat. J Mol Biol. 1988 May 5;201(1):1–17. doi: 10.1016/0022-2836(88)90434-2. [DOI] [PubMed] [Google Scholar]
  3. Botchan P., Reeder R. H., Dawid I. B. Restriction analysis of the nontranscribed spacers of Xenopus laevis ribosomal DNA. Cell. 1977 Jul;11(3):599–607. doi: 10.1016/0092-8674(77)90077-0. [DOI] [PubMed] [Google Scholar]
  4. Brown D. D., Wensink P. C., Jordan E. A comparison of the ribosomal DNA's of Xenopus laevis and Xenopus mulleri: the evolution of tandem genes. J Mol Biol. 1972 Jan 14;63(1):57–73. doi: 10.1016/0022-2836(72)90521-9. [DOI] [PubMed] [Google Scholar]
  5. Coen E. S., Thoday J. M., Dover G. Rate of turnover of structural variants in the rDNA gene family of Drosophila melanogaster. Nature. 1982 Feb 18;295(5850):564–568. doi: 10.1038/295564a0. [DOI] [PubMed] [Google Scholar]
  6. Collett M. A., Bradshaw R. E., Scott D. B. A mutualistic fungal symbiont of perennial ryegrass contains two different pyr4 genes, both expressing orotidine-5'-monophosphate decarboxylase. Gene. 1995 May 26;158(1):31–39. doi: 10.1016/0378-1119(95)00143-t. [DOI] [PubMed] [Google Scholar]
  7. Crease T. J. Ribosomal DNA evolution at the population level: nucleotide variation in intergenic spacer arrays of Daphnia pulex. Genetics. 1995 Dec;141(4):1327–1337. doi: 10.1093/genetics/141.4.1327. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Dover G. A., Linares A. R., Bowen T., Hancock J. M. Detection and quantification of concerted evolution and molecular drive. Methods Enzymol. 1993;224:525–541. doi: 10.1016/0076-6879(93)24039-w. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. Dvorák J., Appels R. Investigation of Homologous Crossing over and Sister Chromatid Exchange in the Wheat Nor-B2 Locus Coding for Rrna and Gli-B2 Locus Coding for Gliadins. Genetics. 1986 Aug;113(4):1037–1056. doi: 10.1093/genetics/113.4.1037. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dvorák J., Jue D., Lassner M. Homogenization of tandemly repeated nucleotide sequences by distance-dependent nucleotide sequence conversion. Genetics. 1987 Jul;116(3):487–498. doi: 10.1093/genetics/116.3.487. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Eggleston A. K., West S. C. Exchanging partners: recombination in E. coli. Trends Genet. 1996 Jan;12(1):20–26. doi: 10.1016/0168-9525(96)81384-9. [DOI] [PubMed] [Google Scholar]
  13. Elder J. F., Jr, Turner B. J. Concerted evolution of repetitive DNA sequences in eukaryotes. Q Rev Biol. 1995 Sep;70(3):297–320. doi: 10.1086/419073. [DOI] [PubMed] [Google Scholar]
  14. Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
  15. Frischauf A. M., Lehrach H., Poustka A., Murray N. Lambda replacement vectors carrying polylinker sequences. J Mol Biol. 1983 Nov 15;170(4):827–842. doi: 10.1016/s0022-2836(83)80190-9. [DOI] [PubMed] [Google Scholar]
  16. Hibner B. L., Burke W. D., Eickbush T. H. Sequence identity in an early chorion multigene family is the result of localized gene conversion. Genetics. 1991 Jul;128(3):595–606. doi: 10.1093/genetics/128.3.595. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hillis D. M., Moritz C., Porter C. A., Baker R. J. Evidence for biased gene conversion in concerted evolution of ribosomal DNA. Science. 1991 Jan 18;251(4991):308–310. doi: 10.1126/science.1987647. [DOI] [PubMed] [Google Scholar]
  18. Israelewski N., Schmidt E. R. Spacer size heterogeneity in ribosomal DNA of Chironomus thummi is due to a 120 bp repeat homologous to a predominantly centromeric repeated sequence. Nucleic Acids Res. 1982 Dec 11;10(23):7689–7700. doi: 10.1093/nar/10.23.7689. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Jeffreys A. J., MacLeod A., Tamaki K., Neil D. L., Monckton D. G. Minisatellite repeat coding as a digital approach to DNA typing. Nature. 1991 Nov 21;354(6350):204–209. doi: 10.1038/354204a0. [DOI] [PubMed] [Google Scholar]
  20. Jinks-Robertson S., Michelitch M., Ramcharan S. Substrate length requirements for efficient mitotic recombination in Saccharomyces cerevisiae. Mol Cell Biol. 1993 Jul;13(7):3937–3950. doi: 10.1128/mcb.13.7.3937. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Jinks-Robertson S., Petes T. D. Experimental determination of rates of concerted evolution. Methods Enzymol. 1993;224:631–646. doi: 10.1016/0076-6879(93)24047-x. [DOI] [PubMed] [Google Scholar]
  22. Kellogg E. A., Appels R. Intraspecific and interspecific variation in 5S RNA genes are decoupled in diploid wheat relatives. Genetics. 1995 May;140(1):325–343. doi: 10.1093/genetics/140.1.325. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Kelly R. J., Johnson R. D., Siegel A. Heterogeneity and organization of the ribosomal RNA genes of Cucurbita maxima. Plant Mol Biol. 1990 Jun;14(6):927–933. doi: 10.1007/BF00019390. [DOI] [PubMed] [Google Scholar]
  24. Krystal M., Arnheim N. Length heterogeneity in a region of the human ribosomal gene spacer is not accompanied by extensive population polymorphism. J Mol Biol. 1978 Nov 25;126(1):91–104. doi: 10.1016/0022-2836(78)90281-4. [DOI] [PubMed] [Google Scholar]
  25. Loidl J., Nairz K. Karyotype variability in yeast caused by nonallelic recombination in haploid meiosis. Genetics. 1997 May;146(1):79–88. doi: 10.1093/genetics/146.1.79. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Long E. O., Dawid I. B. Repeated genes in eukaryotes. Annu Rev Biochem. 1980;49:727–764. doi: 10.1146/annurev.bi.49.070180.003455. [DOI] [PubMed] [Google Scholar]
  27. McKee B. D., Habera L., Vrana J. A. Evidence that intergenic spacer repeats of Drosophila melanogaster rRNA genes function as X-Y pairing sites in male meiosis, and a general model for achiasmatic pairing. Genetics. 1992 Oct;132(2):529–544. doi: 10.1093/genetics/132.2.529. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Meselson M. S., Radding C. M. A general model for genetic recombination. Proc Natl Acad Sci U S A. 1975 Jan;72(1):358–361. doi: 10.1073/pnas.72.1.358. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. 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]
  30. Ohta T. Simple model for treating evolution of multigene families. Nature. 1976 Sep 2;263(5572):74–76. doi: 10.1038/263074a0. [DOI] [PubMed] [Google Scholar]
  31. Orr-Weaver T. L., Szostak J. W. Fungal recombination. Microbiol Rev. 1985 Mar;49(1):33–58. doi: 10.1128/mr.49.1.33-58.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Petes T. D., Botstein D. Simple Mendelian inheritance of the reiterated ribosomal DNA of yeast. Proc Natl Acad Sci U S A. 1977 Nov;74(11):5091–5095. doi: 10.1073/pnas.74.11.5091. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Petes T. D. Unequal meiotic recombination within tandem arrays of yeast ribosomal DNA genes. Cell. 1980 Mar;19(3):765–774. doi: 10.1016/s0092-8674(80)80052-3. [DOI] [PubMed] [Google Scholar]
  34. Reeder R. H., Brown D. D., Wellauer P. K., Dawid I. B. Patterns of ribosomal DNA spacer lengths are inherited. J Mol Biol. 1976 Aug 25;105(4):507–516. doi: 10.1016/0022-2836(76)90231-x. [DOI] [PubMed] [Google Scholar]
  35. Reeder R. H., Roan J. G. The mechanism of nucleolar dominance in Xenopus hybrids. Cell. 1984 Aug;38(1):38–44. doi: 10.1016/0092-8674(84)90524-5. [DOI] [PubMed] [Google Scholar]
  36. Schardl C. L., Leuchtmann A., Tsai H. F., Collett M. A., Watt D. M., Scott D. B. Origin of a fungal symbiont of perennial ryegrass by interspecific hybridization of a mutualist with the ryegrass choke pathogen, Epichloë typhina. Genetics. 1994 Apr;136(4):1307–1317. doi: 10.1093/genetics/136.4.1307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Schlötterer C., Tautz D. Chromosomal homogeneity of Drosophila ribosomal DNA arrays suggests intrachromosomal exchanges drive concerted evolution. Curr Biol. 1994 Sep 1;4(9):777–783. doi: 10.1016/s0960-9822(00)00175-5. [DOI] [PubMed] [Google Scholar]
  38. Schäfer M., Wyman A. R., White R. Length variation in the non-transcribed spacer of Calliphora erythrocephala ribosomal DNA is due to a 350 base-pair repeat. J Mol Biol. 1981 Feb 25;146(2):179–199. doi: 10.1016/0022-2836(81)90431-9. [DOI] [PubMed] [Google Scholar]
  39. Sekiguchi J., Seeman N. C., Shuman S. Resolution of Holliday junctions by eukaryotic DNA topoisomerase I. Proc Natl Acad Sci U S A. 1996 Jan 23;93(2):785–789. doi: 10.1073/pnas.93.2.785. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Stephan W., Cho S. Possible role of natural selection in the formation of tandem-repetitive noncoding DNA. Genetics. 1994 Jan;136(1):333–341. doi: 10.1093/genetics/136.1.333. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Szostak J. W., Orr-Weaver T. L., Rothstein R. J., Stahl F. W. The double-strand-break repair model for recombination. Cell. 1983 May;33(1):25–35. doi: 10.1016/0092-8674(83)90331-8. [DOI] [PubMed] [Google Scholar]
  42. 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]
  43. Tautz D., Tautz C., Webb D., Dover G. A. Evolutionary divergence of promoters and spacers in the rDNA family of four Drosophila species. Implications for molecular coevolution in multigene families. J Mol Biol. 1987 Jun 5;195(3):525–542. doi: 10.1016/0022-2836(87)90181-1. [DOI] [PubMed] [Google Scholar]
  44. Tsai H. F., Liu J. S., Staben C., Christensen M. J., Latch G. C., Siegel M. R., Schardl C. L. Evolutionary diversification of fungal endophytes of tall fescue grass by hybridization with Epichloë species. Proc Natl Acad Sci U S A. 1994 Mar 29;91(7):2542–2546. doi: 10.1073/pnas.91.7.2542. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Vieira J., Messing J. Production of single-stranded plasmid DNA. Methods Enzymol. 1987;153:3–11. doi: 10.1016/0076-6879(87)53044-0. [DOI] [PubMed] [Google Scholar]
  46. Wellauer P. K., Dawid I. B., Brown D. D., Reeder R. H. The molecular basis for length heterogeneity in ribosomal DNA from Xenopus laevis. J Mol Biol. 1976 Aug 25;105(4):461–486. doi: 10.1016/0022-2836(76)90229-1. [DOI] [PubMed] [Google Scholar]
  47. Wellauer P. K., Dawid I. B. Ribosomal DNA in Drosophila melanogaster. II. Heteroduplex mapping of cloned and uncloned rDNA. J Mol Biol. 1978 Dec 25;126(4):769–782. doi: 10.1016/0022-2836(78)90019-0. [DOI] [PubMed] [Google Scholar]
  48. Wendel J. F., Schnabel A., Seelanan T. Bidirectional interlocus concerted evolution following allopolyploid speciation in cotton (Gossypium). Proc Natl Acad Sci U S A. 1995 Jan 3;92(1):280–284. doi: 10.1073/pnas.92.1.280. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Williams S. M., Furnier G. R., Fuog E., Strobeck C. Evolution of the ribosomal DNA spacers of Drosophila melanogaster: different patterns of variation on X and Y chromosomes. Genetics. 1987 Jun;116(2):225–232. doi: 10.1093/genetics/116.2.225. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Williams S. M., Kennison J. A., Robbins L. G., Strobeck C. Reciprocal recombination and the evolution of the ribosomal gene family of Drosophila melanogaster. Genetics. 1989 Jul;122(3):617–624. doi: 10.1093/genetics/122.3.617. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Yuan L. W., Keil R. L. Distance-independence of mitotic intrachromosomal recombination in Saccharomyces cerevisiae. Genetics. 1990 Feb;124(2):263–273. doi: 10.1093/genetics/124.2.263. [DOI] [PMC free article] [PubMed] [Google Scholar]

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