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. 1998 Mar;148(3):1043–1054. doi: 10.1093/genetics/148.3.1043

Organization of chromosome ends in Ustilago maydis. RecQ-like helicase motifs at telomeric regions.

P Sánchez-Alonso 1, P Guzmán 1
PMCID: PMC1460024  PMID: 9539423

Abstract

In this study we have established the structure of chromosome ends in the basidiomycete fungus Ustilago maydis. We isolated and characterized several clones containing telomeric regions and found that as in other organisms, they consist of middle repeated DNA sequences. Two principal types of sequence were found: UTASa was highly conserved in nucleotide sequence and located almost exclusively at the chromosome ends, and UTASb was less conserved in nucleotide sequence than UTASa and found not just at the ends but highly interspersed throughout the genome. Sequence analysis revealed that UTASa encodes an open reading frame containing helicase motifs with the strongest homology to RecQ helicases; these are DNA helicases whose function involves the maintenance of genome stability in Saccharomyces cerevisiae and in humans, and the suppression of illegitimate recombination in Escherichia coli. Both UTASa and UTASb contain a common region of about 300 bp located immediately adjacent to the telomere repeats that are also found interspersed in the genome. The analysis of the chromosome ends of U. maydis provides information on the general structure of chromosome ends in eukaryotes, and the putative RecQ helicase at UTASa may reveal a novel mechanism for the maintenance of chromosome stability.

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Selected References

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  1. Banuett F., Herskowitz I. Different a alleles of Ustilago maydis are necessary for maintenance of filamentous growth but not for meiosis. Proc Natl Acad Sci U S A. 1989 Aug;86(15):5878–5882. doi: 10.1073/pnas.86.15.5878. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Blackburn E. H. Telomerases. Annu Rev Biochem. 1992;61:113–129. doi: 10.1146/annurev.bi.61.070192.000553. [DOI] [PubMed] [Google Scholar]
  3. Blasco M. A., Funk W., Villeponteau B., Greider C. W. Functional characterization and developmental regulation of mouse telomerase RNA. Science. 1995 Sep 1;269(5228):1267–1270. doi: 10.1126/science.7544492. [DOI] [PubMed] [Google Scholar]
  4. Borst P., Rudenko G. Antigenic variation in African trypanosomes. Science. 1994 Jun 24;264(5167):1872–1873. doi: 10.1126/science.7516579. [DOI] [PubMed] [Google Scholar]
  5. Brown W. R., MacKinnon P. J., Villasanté A., Spurr N., Buckle V. J., Dobson M. J. Structure and polymorphism of human telomere-associated DNA. Cell. 1990 Oct 5;63(1):119–132. doi: 10.1016/0092-8674(90)90293-n. [DOI] [PubMed] [Google Scholar]
  6. Bölker M., Böhnert H. U., Braun K. H., Görl J., Kahmann R. Tagging pathogenicity genes in Ustilago maydis by restriction enzyme-mediated integration (REMI). Mol Gen Genet. 1995 Sep 20;248(5):547–552. doi: 10.1007/BF02423450. [DOI] [PubMed] [Google Scholar]
  7. Chan C. S., Tye B. K. A family of Saccharomyces cerevisiae repetitive autonomously replicating sequences that have very similar genomic environments. J Mol Biol. 1983 Aug 15;168(3):505–523. doi: 10.1016/s0022-2836(83)80299-x. [DOI] [PubMed] [Google Scholar]
  8. Chan C. S., Tye B. K. Organization of DNA sequences and replication origins at yeast telomeres. Cell. 1983 Jun;33(2):563–573. doi: 10.1016/0092-8674(83)90437-3. [DOI] [PubMed] [Google Scholar]
  9. Collins K., Kobayashi R., Greider C. W. Purification of Tetrahymena telomerase and cloning of genes encoding the two protein components of the enzyme. Cell. 1995 Jun 2;81(5):677–686. doi: 10.1016/0092-8674(95)90529-4. [DOI] [PubMed] [Google Scholar]
  10. Cooper J. P., Nimmo E. R., Allshire R. C., Cech T. R. Regulation of telomere length and function by a Myb-domain protein in fission yeast. Nature. 1997 Feb 20;385(6618):744–747. doi: 10.1038/385744a0. [DOI] [PubMed] [Google Scholar]
  11. Corcoran L. M., Thompson J. K., Walliker D., Kemp D. J. Homologous recombination within subtelomeric repeat sequences generates chromosome size polymorphisms in P. falciparum. Cell. 1988 Jun 3;53(5):807–813. doi: 10.1016/0092-8674(88)90097-9. [DOI] [PubMed] [Google Scholar]
  12. Counter C. M., Meyerson M., Eaton E. N., Weinberg R. A. The catalytic subunit of yeast telomerase. Proc Natl Acad Sci U S A. 1997 Aug 19;94(17):9202–9207. doi: 10.1073/pnas.94.17.9202. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Dore E., Pace T., Ponzi M., Picci L., Frontali C. Organization of subtelomeric repeats in Plasmodium berghei. Mol Cell Biol. 1990 May;10(5):2423–2427. doi: 10.1128/mcb.10.5.2423. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Ellis N. A., Groden J., Ye T. Z., Straughen J., Lennon D. J., Ciocci S., Proytcheva M., German J. The Bloom's syndrome gene product is homologous to RecQ helicases. Cell. 1995 Nov 17;83(4):655–666. doi: 10.1016/0092-8674(95)90105-1. [DOI] [PubMed] [Google Scholar]
  15. Flint J., Bates G. P., Clark K., Dorman A., Willingham D., Roe B. A., Micklem G., Higgs D. R., Louis E. J. Sequence comparison of human and yeast telomeres identifies structurally distinct subtelomeric domains. Hum Mol Genet. 1997 Aug;6(8):1305–1313. doi: 10.1093/hmg/6.8.1305. [DOI] [PubMed] [Google Scholar]
  16. Fotheringham S., Holloman W. K. Cloning and disruption of Ustilago maydis genes. Mol Cell Biol. 1989 Sep;9(9):4052–4055. doi: 10.1128/mcb.9.9.4052. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Gangloff S., McDonald J. P., Bendixen C., Arthur L., Rothstein R. The yeast type I topoisomerase Top3 interacts with Sgs1, a DNA helicase homolog: a potential eukaryotic reverse gyrase. Mol Cell Biol. 1994 Dec;14(12):8391–8398. doi: 10.1128/mcb.14.12.8391. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Gorbalenya A. E., Koonin E. V., Donchenko A. P., Blinov V. M. Two related superfamilies of putative helicases involved in replication, recombination, repair and expression of DNA and RNA genomes. Nucleic Acids Res. 1989 Jun 26;17(12):4713–4730. doi: 10.1093/nar/17.12.4713. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Gottschling D. E., Aparicio O. M., Billington B. L., Zakian V. A. Position effect at S. cerevisiae telomeres: reversible repression of Pol II transcription. Cell. 1990 Nov 16;63(4):751–762. doi: 10.1016/0092-8674(90)90141-z. [DOI] [PubMed] [Google Scholar]
  20. Greider C. W. Telomere length regulation. Annu Rev Biochem. 1996;65:337–365. doi: 10.1146/annurev.bi.65.070196.002005. [DOI] [PubMed] [Google Scholar]
  21. Guzmán P. A., Sánchez J. G. Characterization of telomeric regions from Ustilago maydis. Microbiology. 1994 Mar;140(Pt 3):551–557. doi: 10.1099/00221287-140-3-551. [DOI] [PubMed] [Google Scholar]
  22. Hanada K., Ukita T., Kohno Y., Saito K., Kato J., Ikeda H. RecQ DNA helicase is a suppressor of illegitimate recombination in Escherichia coli. Proc Natl Acad Sci U S A. 1997 Apr 15;94(8):3860–3865. doi: 10.1073/pnas.94.8.3860. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Harrington L., McPhail T., Mar V., Zhou W., Oulton R., Bass M. B., Arruda I., Robinson M. O. A mammalian telomerase-associated protein. Science. 1997 Feb 14;275(5302):973–977. doi: 10.1126/science.275.5302.973. [DOI] [PubMed] [Google Scholar]
  24. Hernandez-Rivas R., Mattei D., Sterkers Y., Peterson D. S., Wellems T. E., Scherf A. Expressed var genes are found in Plasmodium falciparum subtelomeric regions. Mol Cell Biol. 1997 Feb;17(2):604–611. doi: 10.1128/mcb.17.2.604. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Horn D., Cross G. A. A developmentally regulated position effect at a telomeric locus in Trypanosoma brucei. Cell. 1995 Nov 17;83(4):555–561. doi: 10.1016/0092-8674(95)90095-0. [DOI] [PubMed] [Google Scholar]
  26. Irino N., Nakayama K., Nakayama H. The recQ gene of Escherichia coli K12: primary structure and evidence for SOS regulation. Mol Gen Genet. 1986 Nov;205(2):298–304. doi: 10.1007/BF00430442. [DOI] [PubMed] [Google Scholar]
  27. Kinscherf T. G., Leong S. A. Molecular analysis of the karyotype of Ustilago maydis. Chromosoma. 1988;96(6):427–433. doi: 10.1007/BF00303036. [DOI] [PubMed] [Google Scholar]
  28. Kirk K. E., Harmon B. P., Reichardt I. K., Sedat J. W., Blackburn E. H. Block in anaphase chromosome separation caused by a telomerase template mutation. Science. 1997 Mar 7;275(5305):1478–1481. doi: 10.1126/science.275.5305.1478. [DOI] [PubMed] [Google Scholar]
  29. Kronstad J. W., Wang J., Covert S. F., Holden D. W., McKnight G. L., Leong S. A. Isolation of metabolic genes and demonstration of gene disruption in the phytopathogenic fungus Ustilago maydis. Gene. 1989 Jun 30;79(1):97–106. doi: 10.1016/0378-1119(89)90095-4. [DOI] [PubMed] [Google Scholar]
  30. Levis R. W., Ganesan R., Houtchens K., Tolar L. A., Sheen F. M. Transposons in place of telomeric repeats at a Drosophila telomere. Cell. 1993 Dec 17;75(6):1083–1093. doi: 10.1016/0092-8674(93)90318-k. [DOI] [PubMed] [Google Scholar]
  31. Levis R., Hazelrigg T., Rubin G. M. Effects of genomic position on the expression of transduced copies of the white gene of Drosophila. Science. 1985 Aug 9;229(4713):558–561. doi: 10.1126/science.2992080. [DOI] [PubMed] [Google Scholar]
  32. Lingner J., Hughes T. R., Shevchenko A., Mann M., Lundblad V., Cech T. R. Reverse transcriptase motifs in the catalytic subunit of telomerase. Science. 1997 Apr 25;276(5312):561–567. doi: 10.1126/science.276.5312.561. [DOI] [PubMed] [Google Scholar]
  33. Louis E. J., Haber J. E. The structure and evolution of subtelomeric Y' repeats in Saccharomyces cerevisiae. Genetics. 1992 Jul;131(3):559–574. doi: 10.1093/genetics/131.3.559. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Louis E. J., Naumova E. S., Lee A., Naumov G., Haber J. E. The chromosome end in yeast: its mosaic nature and influence on recombinational dynamics. Genetics. 1994 Mar;136(3):789–802. doi: 10.1093/genetics/136.3.789. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Lundblad V., Blackburn E. H. An alternative pathway for yeast telomere maintenance rescues est1- senescence. Cell. 1993 Apr 23;73(2):347–360. doi: 10.1016/0092-8674(93)90234-h. [DOI] [PubMed] [Google Scholar]
  36. Marcand S., Gilson E., Shore D. A protein-counting mechanism for telomere length regulation in yeast. Science. 1997 Feb 14;275(5302):986–990. doi: 10.1126/science.275.5302.986. [DOI] [PubMed] [Google Scholar]
  37. McEachern M. J., Blackburn E. H. Runaway telomere elongation caused by telomerase RNA gene mutations. Nature. 1995 Aug 3;376(6539):403–409. doi: 10.1038/376403a0. [DOI] [PubMed] [Google Scholar]
  38. Meyerson M., Counter C. M., Eaton E. N., Ellisen L. W., Steiner P., Caddle S. D., Ziaugra L., Beijersbergen R. L., Davidoff M. J., Liu Q. hEST2, the putative human telomerase catalytic subunit gene, is up-regulated in tumor cells and during immortalization. Cell. 1997 Aug 22;90(4):785–795. doi: 10.1016/s0092-8674(00)80538-3. [DOI] [PubMed] [Google Scholar]
  39. Nakamura T. M., Morin G. B., Chapman K. B., Weinrich S. L., Andrews W. H., Lingner J., Harley C. B., Cech T. R. Telomerase catalytic subunit homologs from fission yeast and human. Science. 1997 Aug 15;277(5328):955–959. doi: 10.1126/science.277.5328.955. [DOI] [PubMed] [Google Scholar]
  40. Nakayama J., Saito M., Nakamura H., Matsuura A., Ishikawa F. TLP1: a gene encoding a protein component of mammalian telomerase is a novel member of WD repeats family. Cell. 1997 Mar 21;88(6):875–884. doi: 10.1016/s0092-8674(00)81933-9. [DOI] [PubMed] [Google Scholar]
  41. Nimmo E. R., Cranston G., Allshire R. C. Telomere-associated chromosome breakage in fission yeast results in variegated expression of adjacent genes. EMBO J. 1994 Aug 15;13(16):3801–3811. doi: 10.1002/j.1460-2075.1994.tb06691.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Pryde F. E., Huckle T. C., Louis E. J. Sequence analysis of the right end of chromosome XV in Saccharomyces cerevisiae: an insight into the structural and functional significance of sub-telomeric repeat sequences. Yeast. 1995 Apr 15;11(4):371–382. doi: 10.1002/yea.320110410. [DOI] [PubMed] [Google Scholar]
  43. Shore D. Telomeres. Different means to common ends. Nature. 1997 Feb 20;385(6618):676–677. doi: 10.1038/385676a0. [DOI] [PubMed] [Google Scholar]
  44. Sinclair D. A., Mills K., Guarente L. Accelerated aging and nucleolar fragmentation in yeast sgs1 mutants. Science. 1997 Aug 29;277(5330):1313–1316. doi: 10.1126/science.277.5330.1313. [DOI] [PubMed] [Google Scholar]
  45. Singer M. S., Gottschling D. E. TLC1: template RNA component of Saccharomyces cerevisiae telomerase. Science. 1994 Oct 21;266(5184):404–409. doi: 10.1126/science.7545955. [DOI] [PubMed] [Google Scholar]
  46. Sánchez-Alonso P., Valverde M. E., Paredes-López O., Guzmán P. Detection of genetic variation in Ustilago maydis strains by probes derived from telomeric sequences. Microbiology. 1996 Oct;142(Pt 10):2931–2936. doi: 10.1099/13500872-142-10-2931. [DOI] [PubMed] [Google Scholar]
  47. Wang J., Holden D. W., Leong S. A. Gene transfer system for the phytopathogenic fungus Ustilago maydis. Proc Natl Acad Sci U S A. 1988 Feb;85(3):865–869. doi: 10.1073/pnas.85.3.865. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Watt P. M., Hickson I. D., Borts R. H., Louis E. J. SGS1, a homologue of the Bloom's and Werner's syndrome genes, is required for maintenance of genome stability in Saccharomyces cerevisiae. Genetics. 1996 Nov;144(3):935–945. doi: 10.1093/genetics/144.3.935. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Watt P. M., Louis E. J., Borts R. H., Hickson I. D. Sgs1: a eukaryotic homolog of E. coli RecQ that interacts with topoisomerase II in vivo and is required for faithful chromosome segregation. Cell. 1995 Apr 21;81(2):253–260. doi: 10.1016/0092-8674(95)90335-6. [DOI] [PubMed] [Google Scholar]
  50. Yu C. E., Oshima J., Fu Y. H., Wijsman E. M., Hisama F., Alisch R., Matthews S., Nakura J., Miki T., Ouais S. Positional cloning of the Werner's syndrome gene. Science. 1996 Apr 12;272(5259):258–262. doi: 10.1126/science.272.5259.258. [DOI] [PubMed] [Google Scholar]
  51. Zakian V. A., Blanton H. M. Distribution of telomere-associated sequences on natural chromosomes in Saccharomyces cerevisiae. Mol Cell Biol. 1988 May;8(5):2257–2260. doi: 10.1128/mcb.8.5.2257. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Zakian V. A. Structure, function, and replication of Saccharomyces cerevisiae telomeres. Annu Rev Genet. 1996;30:141–172. doi: 10.1146/annurev.genet.30.1.141. [DOI] [PubMed] [Google Scholar]
  53. de Bruin D., Lanzer M., Ravetch J. V. The polymorphic subtelomeric regions of Plasmodium falciparum chromosomes contain arrays of repetitive sequence elements. Proc Natl Acad Sci U S A. 1994 Jan 18;91(2):619–623. doi: 10.1073/pnas.91.2.619. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. van Steensel B., de Lange T. Control of telomere length by the human telomeric protein TRF1. Nature. 1997 Feb 20;385(6618):740–743. doi: 10.1038/385740a0. [DOI] [PubMed] [Google Scholar]

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