Chromosoma

, 118:85 | Cite as

Linkage of 35S and 5S rRNA genes in Artemisia (family Asteraceae): first evidence from angiosperms

  • Sònia Garcia
  • K. Yoong Lim
  • Michael Chester
  • Teresa Garnatje
  • Jaume Pellicer
  • Joan Vallès
  • Andrew R. Leitch
  • Aleš Kovařík
Research Article

Abstract

Typically in plants, the 5S and 35S ribosomal DNA (rDNA) encoding two major ribosomal RNA species occur at separate loci. However, in some algae, bryophytes and ferns, they are at the same locus (linked arranged). Southern blot hybridisation, polymerase chain reactions (PCR), fluorescent in situ hybridisation, cloning and sequencing were used to reveal 5S and 35S rDNA genomic organisation in Artemisia. We observed thousands of rDNA units at two–three loci containing 5S rDNA in an inverted orientation within the inter-genic spacer (IGS) of 35S rDNA. The sequenced clones of 26–18S IGS from Artemisia absinthium appeared to contain a conserved 5S gene insertion proximal to the 26S gene terminus (5S rDNA-1) and a second less conserved 5S insertion (5S rDNA-2) further downstream. Whilst the 5S rDNA-1 showed all the structural features of a functional gene, the 5S-rDNA-2 had a deletion in the internal promoter and probably represents a pseudogene. The linked arrangement probably evolved before the divergence of Artemisia from the rest of Asteraceae (>10 Myrs). This arrangement may have involved retrotransposons and once formed spread via mechanisms of concerted evolution. Heterogeneity in unit structure may reflect ongoing homogenisation of variant unit types without fixation for any particular variant.

Supplementary material

412_2008_179_MOESM1_ESM.doc (50 kb)
Table S1Origin and collection data of the specimens studied (DOC 50.0 KB).
412_2008_179_MOESM2_ESM.doc (106 kb)
Fig. S1Sequencing of the IGS clones (Fig. 1) from A. absinthium and A. tridentata. Alignment of the IGS1 (between the 26S and 5S genes) clones was carried out using Clustal X program. The characteristic sequence features are indicated in colours. Blue—26S and 18S rDNA genes; red—5S rDNA genes; dark green—102-bp sub-repeats; light green—248-bp sub-repeats; grey shading—imperfect 5′ inverted repeat from a putative Cassandra element; yellow shading—imperfect (−) strand priming site (DOC 106 KB).
412_2008_179_MOESM3_ESM.doc (638 kb)
Fig. S2Southern blot hybridisation of A. tridentata ssp. wyomingensis genomic DNA digested with different restriction enzymes and hybridised with the 26S and 5S rDNA probes. Note that both probes co-hybridised to the most of the fragments (arrows). The hybridisation of the upper ∼6 kb EcoRV was stronger with the 5S probe than to the 26S probe which can be explained by the presence of 5S tandem repeat (double 5S) in the gene family corresponding to upper band (DOC 638 KB).
412_2008_179_MOESM4_ESM.doc (412 kb)
Fig. S3Dot matrix self comparison of the IGS from A. absinthium clone 8 (window = 21; stringency = 14). TIS, transcription initiation site (DOC 411 KB).

References

  1. Ali HB, Fransz P, Schubert I (2000) Localization of 5S RNA genes on tobacco chromosomes. Chromosom Res 8:85–87Google Scholar
  2. Bedard JE, Schurko AM, de Cock AW, Klassen GR (2006) Diversity and evolution of 5S rRNA gene family organization in Pythium. Mycol Res 110:86–95PubMedCrossRefGoogle Scholar
  3. Belkhiri A, Buchko J, Klassen GR (1992) The 5S ribosomal-RNA gene in Pythium species—2 different genomic locations. Mol Biol Evol 9:1089–1102PubMedGoogle Scholar
  4. Benson G (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 27:573–580PubMedCrossRefGoogle Scholar
  5. Capesius I (1997) Analysis of the ribosomal RNA gene repeat from the moss Funaria hygrometrica. Plant Mol Biol 33:559–564PubMedCrossRefGoogle Scholar
  6. Castilho A, Heslop-Harrison JS (1995) Physical mapping of 5S and 18S–25S rDNA and repetitive DNA-sequences in Aegilops umbellulata. Genome 38:91–96PubMedGoogle Scholar
  7. Cloix C, Yukawa Y, Tutois S, Sugiura M, Tourmente S (2003) In vitro analysis of the sequences required for transcription of the Arabidopsis thaliana 5S rRNA genes. Plant J 35:251–261PubMedCrossRefGoogle Scholar
  8. Cohen S, Houben A, Segal D (2008) Extrachromosomal circular DNA derived from tandemly repeated genomic sequences in plants. Plant J 53:1027–1034PubMedCrossRefGoogle Scholar
  9. Cronn RC, Zhao X, Paterson AH, Wendel JF (1996) Polymorphism and concerted evolution in a tandemly repeated gene family: 5S ribosomal DNA in diploid and allopolyploid cottons. J Mol Evol 42:685–705PubMedCrossRefGoogle Scholar
  10. Douet J, Tourmente S (2007) Transcription of the 5S rRNA heterochromatic genes is epigenetically controlled in Arabidopsis thaliana and Xenopus laevis. Heredity 99:5–13PubMedCrossRefGoogle Scholar
  11. Drouin G, Moniz de Sá M (1995) The concerted evolution of 5S ribosomal genes linked to the repeat units of other multigene families. Mol Biol Evol 12:481–493PubMedGoogle Scholar
  12. Dubcovsky J, Dvorak J (1995) Ribosomal-RNA multigene loci—nomads of the Triticeae genomes. Genetics 140:1367–1377PubMedGoogle Scholar
  13. Fulnecek J, Matyasek R, Kovarik A, Bezdek M (1998) Mapping of 5-methylcytosine residues in Nicotiana tabacum 5S rRNA genes by genomic sequencing. Mol Gen Genet 259:133–141PubMedCrossRefGoogle Scholar
  14. Fulnecek J, Lim KY, Leitch AR, Kovarik A, Matyasek R (2002) Evolution and structure of 5S rDNA loci in allotetraploid Nicotiana tabacum and its putative parental species. Heredity 88:19–25PubMedCrossRefGoogle Scholar
  15. Fulnecek J, Matyasek R, Kovarik A (2006) Plant 5S rDNA has multiple alternative nucleosome positions. Genome 49:840–850PubMedCrossRefGoogle Scholar
  16. Funk VA, Bayer RJ, Keeley S, Chan R, Watson L, Gemeinholzer B, Schilling E, Panrelo JL, Baldwin BG, Garcia-Jacas N, Susanna A, Jansen RK (2005) Everywhere but Antarctica: using a supertree to understand the diversity and distribution of the Compositae. In: Friis I, Balslev H (eds) Proceedings of a symposium on plant diversity and complexity patterns–local, regional and global dimensions, Biological Skrifter, vol 55. Royal Danish Academy of Sciences and Letters, Copenhagen, Denmark, pp 343–373Google Scholar
  17. Garcia S, Sanz M, Garnatje T, Kreitschitz A, McArthur ED, Valles J (2004) Variation of DNA amount in 47 populations of the subtribe Artemisiinae and related taxa (Asteraceae, Anthemideae): karyological, ecological, and systematic implications. Genome 47:1004–1014PubMedCrossRefGoogle Scholar
  18. Garcia S, Garnatje T, Hidalgo O, McArthur ED, Siljak-Yakovlev S, Valles J (2007) Extensive ribosomal DNA (18S-5.8S-26S and 5S) colocalization in the North American endemic sagebrushes (subgenus Tridentatae, Artemisia, Asteraceae) revealed by FISH. Plant Syst Evol 267:79–92CrossRefGoogle Scholar
  19. Garnatje T, Vallès J, Vilatersana R, Garcia-Jacas N, Susanna A, Siljak-Yakovlev S (2004) Molecular cytogenetics of Xeranthemum L. and related genera (Asteraceae, Cardueae). Pl Biol 6:140–146CrossRefGoogle Scholar
  20. Gerlach WL, Bedbrook JR (1979) Cloning and characterization of ribosomal RNA genes in wheat. Nucleic Acids Res 7:1869–1885PubMedCrossRefGoogle Scholar
  21. Goyon C, Rossignol JL, Faugeron G (1996) Native DNA repeats and methylation in Ascobolus. Nucleic Acids Res 24:3348–3356PubMedCrossRefGoogle Scholar
  22. Gruendler P, Unfried I, Pascher K, Schweizer D (1991) rDNA intergenic region from Arabidopsis thaliana. Structural analysis, intraspecific variation and functional implications. J Mol Biol 221:1209–1222PubMedCrossRefGoogle Scholar
  23. Grummt I, Pikaard CS (2003) Epigenetic silencing of RNA polymerase I transcription. Nat Rev Mol Cell Biol 4:641–649PubMedCrossRefGoogle Scholar
  24. Hemleben V, Grierson D (1978) Evidence that in higher plants the 25S and 18S rRNA genes are not interspersed with genes for 5S rRNA. Chromosoma 65:353–358CrossRefGoogle Scholar
  25. Hemleben V, Werts D (1988) Sequence organization and putative regulatory elements in the 5S rRNA genes of two higher plants (Vigna radiata and Matthiola incana). Gene 62:165–169PubMedCrossRefGoogle Scholar
  26. Hemleben V, Zentgraf U (1994) Structural organisation and regulation of transcription by RNA polymerase I of plant nuclear ribosomal genes. In: Nover L (ed) Results and problems in cell differentiation 20: plant promoters and transcription factors. Springer, Berlin, Germany, pp 3–24Google Scholar
  27. Hemleben V, Ganal M, Gerstner J, Schiebel K, Torres RA (1988) Organization and length heterogeneity of plant ribosomal RNA genes. In: Kahl G (ed) Architecture of eukarytoic genes. VHC, Weinheim, Germany, pp 371–383Google Scholar
  28. Kalendar R, Tanskanen J, Chang W, Antonius K, Sela H, Peleg O, Schulman AH (2008) Cassandra retrotransposons carry independently transcribed 5S RNA. Proc Natl Acad Sci USA 15:5833–5838CrossRefGoogle Scholar
  29. Kapitonov VV, Jurka J (2003) A novel class of SINE elements derived from 5S rRNA. Mol Biol Evol 20:694–702PubMedCrossRefGoogle Scholar
  30. Kawai H, Nakayama T, Inouye I, Kato A (1997) Linkage of 5S ribosomal DNA to other rDNAs in the chromophytic algae and related taxa. J Phycol 33:505–511CrossRefGoogle Scholar
  31. Kitamura S, Inoue M, Shikazano N, Tanaka A (2001) Relationships among Nicotiana species revealed by the 5S rDNA spacer sequence and fluorescence in situ hybridization. Theor Appl Genet 103:678–686CrossRefGoogle Scholar
  32. Komarova NY, Grabe T, Huigen DJ, Hemleben V, Volkov RA (2004) Organization, differential expression and methylation of rDNA in artificial Solanum allopolyploids. Plant Mol Biol 56:439–463PubMedCrossRefGoogle Scholar
  33. Kovarik A, Koukalova B, Lim KY, Matyasek R, Lichtenstein CP, Leitch AR, Bezdek M (2000) Comparative analysis of DNA methylation in tobacco heterochromatic sequences. Chromosome Res 8:527–541PubMedCrossRefGoogle Scholar
  34. Kovarik A, Pires JC, Leitch AR, Lim KY, Sherwood AM, Matyasek R, Rocca J, Soltis DE, Soltis PS (2005) Rapid concerted evolution of nuclear ribosomal DNA in two Tragopogon allopolyploids of recent and recurrent origin. Genetics 169:931–944PubMedCrossRefGoogle Scholar
  35. Lapitan NLV (1992) Organization and evolution of higher plant nuclear genomes. Genome 35:171–181Google Scholar
  36. Leitch AR, Lim KY, Webb DR, McFadden GI (2001) In situ hybridisation. In: Hawes C, Satiat-Jeunemaitre B (eds) Plant cell biology, a practical approach. Oxford University Press, Oxford, UK, pp 267–293Google Scholar
  37. Lim KY, Kovarik A, Matyasek R, Bezdek M, Lichtenstein CP, Leitch AR (2000) Gene conversion of ribosomal DNA in Nicotiana tabacum is associated with undermethylated, decondensed and probably active gene units. Chromosoma 109:161–172PubMedCrossRefGoogle Scholar
  38. Lim KY, Skalicka K, Koukalova B, Volkov RA, Matyasek R, Hemleben V, Leitch AR, Kovarik A (2004) Dynamic changes in the distribution of a satellite homologous to intergenic 26–18S rDNA spacer in the evolution of Nicotiana. Genetics 166:1935–1946PubMedCrossRefGoogle Scholar
  39. Macas J, Navratilova A, Meszaros T (2003) Sequence subfamilies of satellite repeats related to rDNA intergenic spacer are differentially amplified on Vicia sativa chromosomes. Chromosoma 112:152–158PubMedCrossRefGoogle Scholar
  40. Matoba H, Soejima A, Hoshi Y, Kondon K (2005) Molecular cytogenetic organization of 5S and 18S rDNA loci in Aster ageratoides var. ageratoides, A. iinumae (=Kalimeris pinnatifida) and A. microcephalus var. ovatus in Japan. Cytologia 70:323–330CrossRefGoogle Scholar
  41. Muravenko OV, Amosova AV, Samatadze TE, Semenova OY, Nosova IV, Popov KV, Shostak NG, Zoschuk SA, Zelenin AV (2004) Chromosome localization of 5S and 45S ribosomal DNA in the genomes of Linum L. species of the section Linum (Syn. Protolinum and Adenolinum). Russ J Genet 40:193–196CrossRefGoogle Scholar
  42. Murray BG, Friesen N, Heslop-Harrison JS (2002) Molecular cytogenetic analysis of Podocarpus and comparison with other gymnosperm species. Annals Bot (London) 89:483–489CrossRefGoogle Scholar
  43. Nakao Y, Taira T, Horiuchi S, Kenji K, Mukai Y (2005) Chromosomal difference between male and female trees of Ginkgo biloba examined by karyotype analysis and mapping of rDNA on the chromosomes by fluorescence in situ hybridisation. J Jpn Soc Hortic Sci 74:275–280CrossRefGoogle Scholar
  44. Oberprieler C (2005) Temporal and spatial diversification of Circum-Mediterranean Compositae-Anthemideae. Taxon 54:951–966Google Scholar
  45. Ochsmann J (2000) Morphologische und molekularsystematische Untersuchungen an der Centaurea stoebe L.-Gruppe (Asteraceae-Cardueae) in Europa. Dissertation on Botany 324:1–242Google Scholar
  46. Pellicer J, Garcia S, Garnatje T, Hidalgo O, Siljak-Yakovlev S, Vallès J (2008) Molecular cytogenetic characterization of some representatives of the subgenera Artemisia and Absinthium (genus Artemisia, Asteraceae). Collect Bot 27:13–21CrossRefGoogle Scholar
  47. Pires JC, Lim KY, Kovarík A, Matyasek R, Boyd A, Leitch AR, Leitch IJ, Bennett MD, Soltis PS, Soltis DE (2004) Molecular cytogenetic analysis of recently evolved Tragopogon (Asteracea) allopolyploids reveal a karyotype that is additive of the diploid progenitors. Am J Bot 91:1022–1035CrossRefGoogle Scholar
  48. Riddle NC, Richards EJ (2005) Genetic variation in epigenetic inheritance of ribosomal RNA gene methylation in Arabidopsis. Plant J 41:524–532PubMedCrossRefGoogle Scholar
  49. Röser M, Winterfeld G, Grebenstein B, Hemleben V (2001) Molecular diversity and physical mapping of 5S rDNA in wild and cultivated oat grasses (Poaceae: Aveneae). Mol Phylogenet Evol 21:198–217PubMedCrossRefGoogle Scholar
  50. Schlotterer C, Tautz D (1994) Chromosomal homogeneity of Drosophila ribosomal DNA arrays suggests intrachromosomal exchanges drive concerted evolution. Curr Biol 4:777–783PubMedCrossRefGoogle Scholar
  51. Schmidt T, Heslop-Harrison JS (1998) Genomes, genes and junk: the large-scale organisation of plant chromosomes. Trends Plant Sci 3:1995–1999CrossRefGoogle Scholar
  52. Schubert I, Wobus (1985) In situ hybridization confirms jumping nucleolus organizing regions in Allium. Chromosoma 92:143–148CrossRefGoogle Scholar
  53. Shcherban AB, Badaeva ED, Amosova AV, Adonina IG, Salina EA (2008) Genetic and epigenetic changes of rDNA in a synthetic allotetraploid, Aegilops sharonenesis x Ae. umbellulata. Genome 51:261–271PubMedCrossRefGoogle Scholar
  54. Siroky J, Lysak MA, Dolezel J, Kejnovsky E, Vyskot B (2001) Heterogeneity of rDNA distribution and genome size in Silene spp. Chromosome Res 9:387–393PubMedCrossRefGoogle Scholar
  55. Skalická K, Lim KY, Matyášek R, Koukalová B, Leitch A, Kovarik A (2003) Rapid evolution of parental rDNA in a synthetic tobacco allotetraploid line. Am J Bot 90:988–996CrossRefGoogle Scholar
  56. Sone T, Fujisawa M, Takenaka M, Nakagawa S, Yamaoka S, Sakaida M, Nishiyama R, Yamato KT, Ohmido N, Fukui K, Fukuzawa H, Ohyama K (1999) Bryophyte 5S rDNA was inserted into 45S rDNA repeat units after the divergence from higher land plants. Plant Mol Biol 41:679–685PubMedCrossRefGoogle Scholar
  57. Stupar RM, Song JQ, Tek AL, Cheng ZK, Dong FG, Jiang JM (2002) Highly condensed potato pericentromeric heterochromatin contains rDNA-related tandem repeats. Genetics 162:1435–1444PubMedGoogle Scholar
  58. Torrell M, Cerbah M, Siljak-Yakovlev S, Vallès J (2003) Molecular cytogenetics of the genus Artemisia (Asteraceae, Anthemideae): fluorochrome banding and fluorescence in situ hybridization. I. Subgenus Seriphidium and related taxa. Plant Syst Evol 239:141–153CrossRefGoogle Scholar
  59. Vahidi H, Curran J, Nelson DW, Webster JM, McClure MA, Honda BM (1988) Unusual Sequences, Homologous to 5S RNA, in Ribosomal DNA repeats of the nematode Meloidogyne arenaria. J Mol Evol 27:222–227PubMedCrossRefGoogle Scholar
  60. Venkateswarlu K, Lee SW, Nazar RN (1991) Conserved upstream sequence elements in plant 5S ribosomal RNA-encoding genes. Gene 105:249–254PubMedCrossRefGoogle Scholar
  61. Vitturi R, Colomba MS, Pirrone AM, Mandrioll M (2002) rDNA (18S-28S and 5S) colocalization and linkage between ribosomal genes and (TTAGGG)(n) telomeric sequence in the earthworm Octodrilus complanatus (Annelida, Oligochaeta, Lumbricidae), revealed by single- and double-color FISH. J Hered 93:279–282PubMedCrossRefGoogle Scholar
  62. Volkov RA, Borisjuk NV, Panchuk II, Schweizer D, Hemleben V (1999) Elimination and rearrangement of parental rDNA in the allotetraploid Nicotiana tabacum. Mol Biol Evol 16:311–320PubMedGoogle Scholar
  63. Volkov RA, Zanke C, Panchuk II, Hemleben V (2001) Molecular evolution of 5S rDNA of Solanum species (sect. Petota): application for molecular phylogeny and breeding. Theor Appl Genet 103:1273–1282CrossRefGoogle Scholar
  64. Yoshikazu H, Matoba H, Kondo K (2006) Physical mapping of ribosomal RNA genes in the genus Artemisia L. (Asteraceae). Caryologia 59:312–318Google Scholar
  65. Zentgraf U, Gana M, Hemleben V (1990) Length heterogeneity of the rRNA precursor in cucumber (Cucumis sativus). Plant Mol Biol 15:465–474PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Sònia Garcia
    • 1
    • 2
  • K. Yoong Lim
    • 3
  • Michael Chester
    • 3
  • Teresa Garnatje
    • 2
  • Jaume Pellicer
    • 1
  • Joan Vallès
    • 1
  • Andrew R. Leitch
    • 3
  • Aleš Kovařík
    • 4
  1. 1.Laboratori de Botànica, Facultat de FarmàciaUniversitat de BarcelonaCataloniaSpain
  2. 2.Institut Botànic de Barcelona(CSIC-ICUB)CataloniaSpain
  3. 3.School of Biological and Chemical Sciences, Queen MaryUniversity of LondonLondonUK
  4. 4.Institute of BiophysicsAcademy of Sciences of the Czech RepublicBrnoCzech Republic

Personalised recommendations