Repeated reunions and splits feature the highly dynamic evolution of 5S and 35S ribosomal RNA genes (rDNA) in the Asteraceae family
Tóm tắt
In flowering plants and animals the most common ribosomal RNA genes (rDNA) organisation is that in which 35S (encoding 18S-5.8S-26S rRNA) and 5S genes are physically separated occupying different chromosomal loci. However, recent observations established that both genes have been unified to a single 35S-5S unit in the genus Artemisia (Asteraceae), a genomic arrangement typical of primitive eukaryotes such as yeast, among others. Here we aim to reveal the origin, distribution and mechanisms leading to the linked organisation of rDNA in the Asteraceae by analysing unit structure (PCR, Southern blot, sequencing), gene copy number (quantitative PCR) and chromosomal position (FISH) of 5S and 35S rRNA genes in ~200 species representing the family diversity and other closely related groups. Dominant linked rDNA genotype was found within three large groups in subfamily Asteroideae: tribe Anthemideae (93% of the studied cases), tribe Gnaphalieae (100%) and in the "Heliantheae alliance" (23%). The remaining five tribes of the Asteroideae displayed canonical non linked arrangement of rDNA, as did the other groups in the Asteraceae. Nevertheless, low copy linked genes were identified among several species that amplified unlinked units. The conserved position of functional 5S insertions downstream from the 26S gene suggests a unique, perhaps retrotransposon-mediated integration event at the base of subfamily Asteroideae. Further evolution likely involved divergence of 26S-5S intergenic spacers, amplification and homogenisation of units across the chromosomes and concomitant elimination of unlinked arrays. However, the opposite trend, from linked towards unlinked arrangement was also surmised in few species indicating possible reversibility of these processes. Our results indicate that nearly 25% of Asteraceae species may have evolved unusual linked arrangement of rRNA genes. Thus, in plants, fundamental changes in intrinsic structure of rDNA units, their copy number and chromosomal organisation may occur within relatively short evolutionary time. We hypothesize that the 5S gene integration within the 35S unit might have repeatedly occurred during plant evolution, and probably once in Asteraceae.
Tài liệu tham khảo
Drouin G, de Sa MM: The concerted evolution of 5S ribosomal genes linked to the repeat units of other multigene families. Mol Biol Evol. 1995, 12 (3): 481-493.
Vahidi H, Purac A, LeBlanc JM, Honda BM: Characterization of potentially functional 5S rRNA-encoding genes within ribosomal DNA repeats of the nematode Meloidogyne arenaria. Gene. 1991, 108 (2): 281-284. 10.1016/0378-1119(91)90446-I.
Bergeron J, Drouin G: The evolution of 5S ribosomal RNA genes linked to the rDNA units of fungal species. Curr Genet. 2008, 54 (3): 123-131. 10.1007/s00294-008-0201-2.
Drouin G, Hofman JD, Doolittle WF: Unusual ribosomal RNA gene organization in copepods of the genus Calanus. J Mol Biol. 1987, 196 (4): 943-946. 10.1016/0022-2836(87)90417-7.
Maizels N: Dictyostelium 17S, 25S, and 5S rDNAs lie within a 38,000 base pair repeated unit. Cell. 1976, 9 (3): 431-438. 10.1016/0092-8674(76)90088-X.
Capesius I: Analysis of the ribosomal RNA gene repeat from the moss Funaria hygrometrica. Plant Mol Biol. 1997, 33 (3): 559-564. 10.1023/A:1005740031313.
Sone T, Fujisawa M, Takenaka M, Nakagawa S, Yamaoka S, Sakaida M, Nishiyama R, Yamato KT, Ohmido N, Fukui K, et al: Bryophyte 5S rDNA was inserted into 45S rDNA repeat units after the divergence from higher land plants. Plant Mol Biol. 1999, 41 (5): 679-685. 10.1023/A:1006398419556.
Garcia S, Lim KY, Chester M, Garnatje T, Pellicer J, Valles J, Leitch AR, Kovarik A: Linkage of 35S and 5S rRNA genes in Artemisia (family Asteraceae): first evidence from angiosperms. Chromosoma. 2009, 118 (1): 85-97. 10.1007/s00412-008-0179-z.
Funk VA, Bayer RJ, Keeley S, Chan R, Watson L, Gemeinholzer B, Schilling E, Panrelo JL, Baldwin BG, Garcia-Jacas N, et al: Everywhere but Antartica: using a supertree to understand the diversity and distribution of the Compositae. Biol Skr. Edited by: Friis I, Balslev H. 2005, 55: 343-373.
Kim KJ, Choi KS, Jansen RK: Two chloroplast DNA inversions originated simultaneously during the early evolution of the sunflower family (Asteraceae). Mol Biol Evol. 2005, 22 (9): 1783-1792. 10.1093/molbev/msi174.
Funk VA, Robinson H: Sampera, a new genus of Liabeae (Compositae or Asteraceae) from the northern Andes. P Biol Soc Wash. 2009, 122 (2): 155-161. 10.2988/08-31.1.
Fransz PF, Alonso-Blanco C, Liharska TB, Peeters AJ, Zabel P, de Jong JH: High-resolution physical mapping in Arabidopsis thaliana and tomato by fluorescence in situ hybridization to extended DNA fibres. Plant J. 1996, 9 (3): 421-430. 10.1046/j.1365-313X.1996.09030421.x.
Pires JC, Lim KY, Kovarík A, Matyasek R, Boyd A, Leitch AR, Leitch IJ, Bennett MD, Soltis PS, Soltis DE: Molecular cytogenetic analysis of recently evolved Tragopogon (Asteraceae) allopolyploids reveal a karyotype that is additive of the diploid progenitors. Am J Bot. 2004, 91 (7): 1022-1035. 10.3732/ajb.91.7.1022.
Dydak M, Kolano B, Nowak T, Siwinska D, Maluszynska J: Cytogenetic studies of three European species of Centaurea L. (Asteraceae). Hereditas. 2009, 146 (4): 152-161. 10.1111/j.1601-5223.2009.02113.x.
Cuellar T, Belhassen E, FernandezCalvin B, Orellana J, Bella JL: Chromosomal differentiation in Helianthus annuus var macrocarpus: Heterochromatin characterization and rDNA location. Heredity. 1996, 76: 586-591. 10.1038/hdy.1996.84.
Ruas CD, Vanzela ALL, Santos MO, Fregonezi JN, Ruas PM, Matzenbacher NI, de Aguiar-Perecin MLR: Chromosomal organization and phylogenetic relationships in Hypochaeris species (Asteraceae) from Brazil. Genet Mol Biol. 2005, 28 (1): 129-139. 10.1590/S1415-47572005000100023.
Weiss-Schneeweiss H, Stuessy TF, Siljak-Yakovlev S, Baeza CM, Parker J: Karyotype evolution in South American species of Hypochaeris (Asteraceae, Lactuceae). Plant Syst Evol. 2003, 241 (3-4): 171-184. 10.1007/s00606-003-0026-x.
Torrell M, Cerbah M, Siljak-Yakovlev S, Valles J: Molecular cytogenetics of the genus Artemisia (Asteraceae, Anthemideae): fluorochrome banding and fluorescence in situ hybridization. I. Subgenus Seriphidium and related taxa. Plant Syst Evol. 2003, 239 (1-2): 141-153. 10.1007/s00606-002-0259-0.
Garcia S, Garnatje T, Hidalgo O, McArthur ED, Siljak-Yakovlev S, Valles J: 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. 2007, 267 (1-4): 79-92. 10.1007/s00606-007-0558-6.
Yoshikazu H, Matoba H, Kondo K: Physical mapping of ribosomal RNA genes in the genus Artemisia L. (Asteraceae). Caryologia. 2006, 59 (4): 312-318.
Panero JL, Funk VA: The value of sampling anomalous taxa in phylogenetic studies: Major clades of the Asteraceae revealed. Mol Phylogenet Evol. 2008, 47 (2): 757-782. 10.1016/j.ympev.2008.02.011.
Funk VA, Susanna A, Stuessy TF, Robinson H: Classification of Compositae. Systematics, evolution, and biogeography of Compositae. Edited by: Funk VA, Susanna A, Stuessy TF, Bayer RJ. 2009, Michigan, USA.: Sheridan Books Inc, 171-192.
Lim KY, Kovarik A, Matyasek R, Bezdek M, Lichtenstein CP, Leitch AR: Gene conversion of ribosomal DNA in Nicotiana tabacum is associated with undermethylated, decondensed and probably active gene units. Chromosoma. 2000, 109 (3): 161-172. 10.1007/s004120050424.
Fulnecek J, Matyasek R, Kovarik A, Bezdek M: Mapping of 5-methylcytosine residues in Nicotiana tabacum 5S rRNA genes by genomic sequencing. Mol Gen Genet. 1998, 259 (2): 133-141. 10.1007/s004380050798.
Tate JA, Ni Z, Scheen A-C, Koh J, Gilbert CA, Lefkowitz D, Chen ZJ, Soltis PA, Soltis DE: Evolution and expression of homeologous loci in Tragopogon miscellus (Asteraceae), a recent and reciprocally formed allopolyploid. Genetics. 2006, 3: 1599-1611. 10.1534/genetics.106.057646.
Bancheva S, Greilhuber J: Genome size in Bulgarian Centaurea s.l. (Asteraceae). Plant Syst Evol. 2006, 257 (1-2): 95-117. 10.1007/s00606-005-0384-7.
Torrell M, Valles J: Genome size in 21 Artemisia L. species (Asteraceae, Anthemideae): Systematic, evolutionary, and ecological implications. Genome. 2001, 44 (2): 231-238. 10.1139/gen-44-2-231.
Garcia S, Inceer H, Garnatje T, Valles J: Genome size variation in some representatives of the genus Tripleurospermum. Biol Plantarum. 2005, 49 (3): 381-387. 10.1007/s10535-005-0011-z.
Zonneveld BJM, Leitch IJ, Bennett MD: First nuclear DNA amounts in more than 300 angiosperms. Ann Bot-London. 2005, 96 (2): 229-244. 10.1093/aob/mci170.
Komarova NY, Grabe T, Huigen DJ, Hemleben V, Volkov RA: Organization, differential expression and methylation of rDNA in artificial Solanum allopolyploids. Plant Mol Biol. 2004, 56 (3): 439-463. 10.1007/s11103-004-4678-x.
Hall TA: BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser. 1999, 41: 95-98.
Galtier N, Gouy M, Gautier C: SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Comput Appl Biosci. 1996, 12 (6): 543-548.
Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R: DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics. 2003, 19 (18): 2496-2497. 10.1093/bioinformatics/btg359.
Panero JL, Funk VA: The value of sampling anomalous taxa in phylogenetic studies: major clades of the Asteraceae revealed. Mol Phylogenet Evol. 2008, 47 (2): 757-782. 10.1016/j.ympev.2008.02.011.
Kapitonov VV, Jurka J: A novel class of SINE elements derived from 5S rRNA. Mol Biol Evol. 2003, 20 (5): 694-702. 10.1093/molbev/msg075.
Kalendar R, Tanskanen J, Chang W, Antonius K, Sela H, Peleg O, Schulman AH: Cassandra retrotransposons carry independently transcribed 5S RNA. Proc Natl Acad Sci USA. 2008, 105 (15): 5833-5838. 10.1073/pnas.0709698105.
Sanz M, Vilatersana R, Hidalgo O, Garcia-Jacas N, Susanna A, Schneeweiss GM, Valles J: Molecular phylogeny and evolution of floral characters of Artemisia and allies (Anthemideae, Asteraceae): evidence from nrDNA ETS and ITS sequences. Taxon. 2008, 57 (1): 66-78.
Mazzella C, Rodriguez M, Vaio M, Gaiero P, Lopez-Carro B, Santinaque FF, Folle GA, Guerra M: Karyological Features of Achyrocline (Asteraceae, Gnaphalieae): Stable Karyotypes, Low DNA Content Variation and Linkage of rRNA Genes. Cytogenet Genome Res. 2010, 128 (1-3): 169-176. 10.1159/000290689.
Magallon S, Crane PR, Herendeen PS: Phylogenetic pattern, diversity, and diversification of eudicots. Ann Mo Bot Gard. 1999, 86 (2): 297-372. 10.2307/2666180.
Oberprieler C: Temporal and spatial diversification of Circum-Mediterranean Compositae-Anthemideae. Taxon. 2005, 54 (4): 951-966. 10.2307/25065480.
Jo SH, Koo DH, Kim JF, Hur CG, Lee S, Yang TJ, Kwon SY, Choi D: Evolution of ribosomal DNA-derived satellite repeat in tomato genome. BMC Plant Biol. 2009, 9: 42-10.1186/1471-2229-9-42.
Lim KY, Skalicka K, Koukalova B, Volkov RA, Matyasek R, Hemleben V, Leitch AR, Kovarik A: Dynamic changes in the distribution of a satellite homologous to intergenic 26-18S rDNA spacer in the evolution of Nicotiana. Genetics. 2004, 166 (4): 1935-1946. 10.1534/genetics.166.4.1935.
Eickbush TH, Eickbush DG: Finely orchestrated movements: evolution of the ribosomal RNA genes. Genetics. 2007, 175 (2): 477-485. 10.1534/genetics.107.071399.
Chester M, Sykorova E, Fajkus J, Leitch AR: Single integration and spread of a copia-like sequence nested in rDNA Intergenic Spacers of Allium cernuum (Alliaceae). Cytogenet Genome Res. 2010, 129 (1-3): 35-46. 10.1159/000312959.
Smith GP: Unequal crossover and the evolution of multigene families. Cold Spring Harb Symp Quant Biol. 1974, 38: 507-513.
Navratilova A, Koblizkova A, Macas J: Survey of extrachromosomal circular DNA derived from plant satellite repeats. Bmc Plant Biol. 2008, 8: 90-10.1186/1471-2229-8-90.
Cohen S, Agmon N, Sobol O, Segal D: Extrachromosomal circles of satellite repeats and 5S ribosomal DNA in human cells. Mob DNA. 2010, 1 (1): 11-10.1186/1759-8753-1-11.
Koukalova B, Moraes AP, Renny-Byfield S, Matyasek R, Leitch AR, Kovarik A: Fall and rise of satellite repeats in allopolyploids of Nicotiana over c. 5 million years. New Phytol. 2010, 186 (1): 148-160. 10.1111/j.1469-8137.2009.03101.x.
Ganley AR, Kobayashi T: Highly efficient concerted evolution in the ribosomal DNA repeats: total rDNA repeat variation revealed by whole-genome shotgun sequence data. Genome Res. 2007, 17 (2): 184-191. 10.1101/gr.5457707.
Tkach NV, Hoffmann MH, Roser M, Korobkov AA, von Hagen KB: Parallel evolutionary patterns in multiple lineages of arctic Artemisia L. (Asteraceae). Evolution. 2008, 62 (1): 184-198.
Cloix C, Yukawa Y, Tutois S, Sugiura M, Tourmente S: In vitro analysis of the sequences required for transcription of the Arabidopsis thaliana 5S rRNA genes. Plant J. 2003, 35 (2): 251-261. 10.1046/j.1365-313X.2003.01793.x.