Chromosomal diversification and karyotype evolution of diploids in the cytologically diverse genus Prospero (Hyacinthaceae)

BMC Evolutionary Biology

Hanna Weiss-Schneeweiss³  Franz Speta¹  Andrew R Leitch⁴  Eva M Temsch³  John Parker²  Khatere Emadzade³  Tae-Soo Jang³ 

[1] Dornacher Strasse 1, Linz 4040, Austria;Cambridge University Botanic Garden, Cambridge CB2 1JF, UK;Department of Systematic and Evolutionary Botany, University of Vienna, Rennweg 14, A-1030, Vienna, Austria;Queen Mary College, University of London, London, UK

关键词: rDNA;    Prospero;    Phylogeny;    ITS;    Hyacinthaceae;    Genome size;    FISH;    Chromosomal evolution;   

Others  :  1086961
DOI  :  10.1186/1471-2148-13-136

 received in 2013-04-03, accepted in 2013-06-27,  发布年份 2013

【 摘 要 】

Background

Prospero (Hyacinthaceae) provides a unique system to assess the impact of genome rearrangements on plant diversification and evolution. The genus exhibits remarkable chromosomal variation but very little morphological differentiation. Basic numbers of x = 4, 5, 6 and 7, extensive polyploidy, and numerous polymorphic chromosome variants were described, but only three species are commonly recognized: P. obtusifolium, P. hanburyi, and P. autumnale s.l., the latter comprising four diploid cytotypes. The relationship between evolutionary patterns and chromosomal variation in diploids, the basic modules of the extensive cytological diversity, is presented.

Results

Evolutionary inferences were derived from fluorescence in situ hybridization (FISH) with 5S and 35S rDNA, genome size estimations, and phylogenetic analyses of internal transcribed spacer (ITS) of 35S rDNA of 49 diploids in the three species and all cytotypes of P. autumnale s.l. All species and cytotypes possess a single 35S rDNA locus, interstitial except in P. hanburyi where it is sub-terminal, and one or two 5S rDNA loci (occasionally a third in P. obtusifolium) at fixed locations. The localization of the two rDNA types is unique for each species and cytotype. Phylogenetic data in the P. autumnale complex enable tracing of the evolution of rDNA loci, genome size, and direction of chromosomal fusions: mixed descending dysploidy of x = 7 to x = 6 and independently to x = 5, rather than successive descending dysploidy, is proposed.

Conclusions

All diploid cytotypes are recovered as well-defined evolutionary lineages. The cytogenetic and phylogenetic approaches have provided excellent phylogenetic markers to infer the direction of chromosomal change in Prospero. Evolution in Prospero, especially in the P. autumnale complex, has been driven by differentiation of an ancestral karyotype largely unaccompanied by morphological change. These new results provide a framework for detailed analyses of various types of chromosomal rearrangements and karyotypic variation in polyploids.

【 授权许可】

   
2013 Jang et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Lysak MA, Berr A, Pecinka A, Schmidt R, McBreen K, Schubert I: Mechanisms of chromosome number reduction in Arabidopsis thaliana and related Brassicaceae species. Proc Natl Acad Sci USA 2006, 103:5224-5229.
• [2]Schubert I: Chromosome evolution. Curr Opin Plant Biol 2007, 10:109-115.
• [3]Clarkson JJ, Lim KY, Kovarik A, Chase MW, Knapp S, Leitch AR: Long-term genome diploidization in allopolyploid Nicotiana section Repandae (Solanaceae). New Phytol 2005, 168:241-252.
• [4]Weiss-Schneeweiss H, Tremetsberger K, Schneeweiss GM, Parker JS, Stuessy TF: Karyotype diversification and evolution in diploid and polyploidy South American Hypochaeris (Asteraceae) inferred from rDNA localization and genetic fingerprint data. Ann Bot 2008, 101:909-918.
• [5]Weiss-Schneeweiss H, Schneeweiss GM: Karyotype diversity and evolutionary trends in angiosperms. In Plant Genome Diversity. Volume 2. Physical Structure, Behavior and Evolution of Plant Genomes. Edited by Leitch IJ, Greilhuber J, Doležel J, Wendel JF. Springer-Verlag: Wien; 2013:209-230.
• [6]Kulikova O, Gualtieri G, Geurts R, Kim DJ, Cook D, Huquet T, De Jong JH, Fransz PF, Bisseling T: Integration of the FISH pachytene and genetic maps of Medicago truncatula. Plant J 2001, 27:49-58.
• [7]Cuadrado A, Jouve N: Evolutionary trends of different repetitive DNA sequences during speciation in the genus Secale. J Hered 2002, 93:339-345.
• [8]Mishima M, Ohmido N, Fukui K, Yahara T: Trends in site-number change of rDNA loci during polyploidy evolution in Sanguisorba (Rosaceae). Chromosoma 2002, 110:550-558.
• [9]Pedrosa A, Sandal N, Stougaard J, Schweizer D, Bachmair A: Chromosomal map of the model legume Lotus japonicus. Genetics 2002, 161:1661-1672.
• [10]Schwarzacher T, Heslop-Harrison P: Practical in situ Hybridization. 2nd edition. Oxford, UK: BIOS; 2000.
• [11]Lim KY, Matyasek R, Lichtenstein CP, Leitch AR: Molecular cytogenetic analyses and phylogenetic studies in the Nicotiana section Tomentosae. Chromosoma 2000, 109:245-258.
• [12]Schmidt T, Heslop-Harrison JS: High-resolution mapping of repetitive DNA by in situ hybridization: molecular and chromosomal features of prominent dispersed and discretely localized DNA families from the wild beet species Beta procumbens. Plant Mol Biol 1996, 30:1099-1113.
• [13]Mandakova T, Mummenhoff K, Al-Shehbaz IA, Mucina L, Mühlhausen A, Lysak MA: Whole-genome triplication and species radiation in the southern African tribe Heliophileae (Brassicaceae). Taxon 2012, 61:989-1000.
• [14]Weiss-Schneeweiss H, Schneeweiss GM, Stuessy TF, Mbuchi T, Park JM, Jang CG, Sun BY: Chromosomal stasis in diploids contrasts with genome restructuring in auto- and allopolyploid taxa of Hepatica (Ranunculaceae). New Phytol 2007, 174:669-682.
• [15]Mlinarec J, Šatović Z, Malenica N, Ivančić-Baće I I, Besendorfer V: Evolution of the tetraploid Anemone multifida (2n = 32) and hexaploid A. baldensis (2n = 48) (Ranunculaceae) was accompanied by rDNA loci loss and intergenomic translocation: evidence for their common genome origin. Ann Bot 2012, 110:703-712.
• [16]Weiss-Schneeweiss H, Blöch C, Turner B, Villaseñor JL, Stuessy TF, Schneeweiss GM: The promiscuous and the chaste: frequent allopolyploid speciation and its genomic consequences in American daisies (Melampodium sect. Melampodium, Asteraceae). Evolution 2012, 66:211-228.
• [17]Garcia S, Panero JL, Siroky J, Kovarik A: Repeated reunions and splits feature the highly dynamic evolution of 5S and 35S ribosomal RNA genes (rDNA) in the Asteraceae family. BMC Plant Biol 2010, 10:176. BioMed Central Full Text
• [18]Lapitan NLV, Ganal MW, Tanksley SD: Organization of the 5S ribosomal RNA genes in the genome of tomato. Genome 1991, 34:509-514.
• [19]Sastri DC, Hilu K, Appels R, Lagudah ES, Playford J, Baum BR: An overview of evolution in plant 5S DNA. Plant Syst Evol 1992, 183:169-181.
• [20]Maluszynska J, Hasterok R, Weiss H: rRNA genes – Their distribution and activity in plants. In Plant cytogenetics. Edited by Maluszynska J. Katowice: Silesian University Press; 1998.
• [21]Heslop-Harrison JS: Comparative genome organization in plants: from sequence and markers to chromatin and chromosomes. Plant Cell 2000, 12:617-636.
• [22]Krishnan P, Sapra VT, Soliman KM, Zipf A: FISH mapping of the 5S and 18S-28S rDNA loci in different species of glycine. J Hered 2001, 92:282-287.
• [23]Zimmer EA, Wen J: Using nuclear gene data for plant phylogenetics: progress and prospects. Mol Phylogenet Evol 2012, 65:774-785.
• [24]Ainsworth CC, Parker JS, Horton DM: Chromosome variation and evolution in Scilla autumnalis. In Kew Chromosome Conference II. Edited by Brandham PE, Bennett MD. London: George Allen & Unwin; 1983:261-268.
• [25]Parker JS, Lozano R, Taylor S, Ruiz Rejòn M: Chromosomal structure of populations of Scilla autumnalis in the Iberian Peninsula. Heredity 1991, 67:287-297.
• [26]Vaughan HE, Taylor S, Parker JS: The ten cytological races of the Scilla autumnalis species complex. Heredity 1997, 79:371-379.
• [27]Speta F: Die Gattungen Scilla L. s. str. und Prospero Salisb. im pannonischen Raum. Veröffentl Intern Clusius-Forschungsges Güssing 1982, 5:1-19.
• [28]Speta F: Systematische Analyse der Gattung Scilla L. s.l. (Hyacinthaceae). Phyton 1998, 38:1-141.
• [29]Speta F: Beitrag zur Kenntnis der Gattung Prospero Salisb (Hyacinthaceae) auf der griechischen Insel Kreta. Linz Biol Beitr 2000, 32:1323-1326.
• [30]Tzanoudakis D, Kypriotakis Z: A new polyploid Scilla (Liliaceae) from the Cretan area (Greece). Folia Geobot 1998, 33:103-108.
• [31]Jeanmonod D, Gamisans J: Flora Corsica. Edisud: Aix-en-Provence La Compagnie des éditions de la Lesse; 2007.
• [32]Brullo C, Brullo S, Gtusso Del Galdo G, Pavone P, Salmeri C: Prospero hierae (Hyacinthaceae), a new species from Marettimo Island (Sicily). Phyton 2009, 49:93-104.
• [33]Govaerts R, Zonneveld BJM, Zona SA: World Checklist of Asparagaceae. UK; [Facilitated by the Royal Botanic Gardens Kew] http://apps.kew.org/wcsp/ webcite Retrieved 2013-03-18
• [34]Taylor S: Chromosomal evolution of Scilla autumnalis . London, UK: University of London; 1997. [PhD thesis]
• [35]White J, Jenkins G, Parker JS: Elimination of multivalents during meiotic prophase in Scilla autumnalis. I. Diploid and triploid. Genome 1988, 30:930-939.
• [36]Jenkins G, White J, Parker JS: Elimination of multivalent during meiotic prophase in Scilla autumnalis II. Tetraploid. Genome 1988, 30:940-946.
• [37]Ebert I, Greilhuber J, Speta F: Chromosome banding and genome size differentiation in Prospero (Hyacinthaceae): diploids. Plant Syst Evol 1996, 203:143-177.
• [38]Pfosser M, Speta F: Phylogenetics of Hyacinthaceae based on plastid DNA sequences. Ann Mo Bot Gard 1999, 86:852-875.
• [39]Pfosser M, Wetschnig W, Ungar S, Prenner G: Phylogenetic relationships among genera of Massonieae (Hyacinthaceae) inferred from plastid DNA and seed morphology. J Plant Res 2003, 116:115-132.
• [40]Ali SS, Yu Y, Pfosser M, Wetschnig W: Inferences of biogeographical histories within subfamily Hyacinthoideae using S-DIVA and Bayesian binary MCMC analysis implemented in RASP (Reconstruct Ancestral State in Phylogenies). Ann Bot 2012, 109:95-107.
• [41]Hong DY: Cytotype variation and polyploidy in Scilla autumnalis L. (Liliaceae). Hereditas 1982, 97:227-235.
• [42]Vaughan HE, Jamilena M, Ruiz Rejón C, Parker JS, Garrido-Ramos MA: Loss of nucleolar-organizer regions during polyploidy evolution in Scilla autumnalis. Heredity 1993, 71:574-580.
• [43]Hasterok R, Wolny E, Hosiawa M, Kowalczyk M, Kulak-Ksiazczyk S, Ksiazczyk T, Heneen WK, Maluszynska J: Comparative analysis of rDNA distribution in chromosomes of various species of Brassicaceae. Ann Bot 2006, 97:205-216.
• [44]Fukushima K, Imamura K, Nagano K, Hoshi Y: Contrasting patterns of the 5S and 45S rDNA evolutions in the Byblis liniflora complex (Byblidaceae). J Plant Res 2011, 124:231-244.
• [45]Adams SP, Leitch IJ, Bennett MD, Chase MW, Leitch AR: Ribosomal DNA evolution and phylogeny in Aloe (Asphodelaceae). Am J Bot 2000, 87:1578-1583.
• [46]Schubert I, Wobus U: In situ hybridization confirms jumping nucleolus organizing regions in Allium. Chromosoma 1985, 92:143-148.
• [47]Ali HB, Fransz P, Schubert I: Localization of 5S RNA genes on tobacco chromosomes. Chromosome Res 2000, 8:85-87.
• [48]Siroky J, Lysak MA, Doležel J, Kejnovsky E, Vyskot B: Heterogeneity of rDNA distribution and genome size in Silene spp. Chromosome Res 2001, 9:387-393.
• [49]Pires JC, Lim KY, Kovarik 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, 91:1022-1035.
• [50]Roa F, Guerra M: Trends on the distribution of the 45S rDNA ribosomal DNA in plants. In Abstract book of Annual Main Meeting of the Society for Experimental Biology: 30 June-3 July. Prague. London: Society for Experimental Biology; 2010:262.
• [51]Hanson RE, Islam-Faridi MN, Percival EA, Crane CF, Ji Y, McKnight TD, Stelly DM, Price HJ: Distribution of 5S and 18–28S rDNA loci in a tetraploid cotton (Gossypium hirsutum L.) and its putative diploid ancestors. Chromosoma 1996, 105:55-61.
• [52]Pedrosa-Harand A, De Almeida CC S, Mosiolek M, Blair MW, Schweizer D, Guerra M: Extensive ribosomal DNA amplification during Andean common bean (Phaseolus vulgaris L.) evolution. Theor Appl Genet 2006, 112:924-933.
• [53]Leitch IJ, Heslop–Harrison JS: Physical mapping of the 18S–5.8S–26S rRNA genes in barley by in situ hybridization. Genome 1992, 35:1013-1018.
• [54]Hamouche Y, Amirouche N, Misset MT, Amirouche R: Cytotaxonomy of autumnal flowering species of Hyacinthaceae from Algeria. Plant Syst Evol 2010, 285:177-187.
• [55]Weiss-Schneeweiss H, Villaseñor JL, Stuessy TF: Chromosome numbers, karyotypes, and evolution in Melampodium (Asteraceae). Int J Plant Sci 2009, 170:1168-1182.
• [56]Weiss-Schneeweiss H, Riha K, Jang CG, Puizina J, Scherthan H, Schweizer D: Chromosome termini of the monocot plant Othocallis siberica are maintained by telomerase, which specifically synthesises vertebrate-type telomere sequences. Plant J 2004, 37:484-493.
• [57]Doyle JJ, Doyle JL: A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 1987, 19:11-15.
• [58]Tel-Zur N, Abbo S, Myslabodski D, Mizrahi Y: Modified CTAB procedure for DNA isolation from epiphytic cacti of the genera Hylocereus and Selenicereus (Cactaceae). Plant Mol Biol Rep 1999, 17:249-254.
• [59]Gruenstaeudl M, Urtubey E, Jansen RK, Samuel R, Barfuss MH, Stuessy TF: Phylogeny of Barnadesioideae (Asteraceae) inferred from DNA sequence data and morphology. Mol Phylogenet Evol 2009, 51:572-587.
• [60]Hall TA: BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98NT. Nucleic Acids Symp Ser 1999, 41:95-98.
• [61]Simmons MP, Ochoterena H: Gaps as characters in sequence-based phylogenetic analyses. Syst Biol 2000, 49:369-381.
• [62]Müller K: SeqState—primer design and sequence statistics for phylogenetic DNA data sets. Appl Bioinformatics 2005, 4:65-69.
• [63]Swofford DL: PAUP*: phylogenetic analysis using parsimony (*and other methods). version 4.0.b10 . Sunderland, MA: Sinauer Associates; 2002.
• [64]Felsenstein J: Confidence limits on phylogenies: An approach using the bootstrap. Evolution (N Y) 1985, 39:783-791.
• [65]Huson DH, Bryant D: Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 2010, 23:254-267.
• [66]Temsch EM, Greilhuber J, Krisai R: Genome size in liverworts. Preslia 2010, 82:63-80.
• [67]Galbraith DW, Harkins KR, Maddox JM, Ayres NM, Sharma DP, Firoozabady E: Rapid flow cytometric analysis of the cell cycle in intact plant tissues. Science 1983, 220:1049-1051.
• [68]Otto F, Oldiges H, Gohde W, Jain VK: Flow cytometric measurement of nuclear DNA content variations as a potential in vivo mutagenicity test. Cytometry 1981, 2:189-191.