BACKGROUND AND AIMS: Molecular evidence for natural primary hybrids composed of three different plant species is very rarely reported. An investigation was therefore carried out into the origin and a possible scenario for the rise of a sterile plant clone showing a combination of diagnostic morphological features of three separate, well-defined Potamogeton species. METHODS: The combination of sequences from maternally inherited cytoplasmic (rpl20-rps12) and biparentally inherited nuclear ribosomal DNA (ITS) was used to identify the exact identity of the putative triple hybrid. KEY RESULTS: Direct sequencing showed ITS variants of three parental taxa, P. gramineus, P. lucens and P. perfoliatus, whereas chloroplast DNA identified P. perfoliatus as the female parent. A scenario for the rise of the triple hybrid through a fertile binary hybrid P. gramineus x P. lucens crossed with P. perfoliatus is described. CONCLUSIONS: Even though the triple hybrid is sterile, it possesses an efficient strategy for its existence and became locally successful even in the parental environment, perhaps as a result of heterosis. The population investigated is the only one known of this hybrid, P. x torssanderi, worldwide. Isozyme analysis indicated the colony to be genetically uniform. The plants studied represented a single clone that seems to have persisted at this site for a long time.

Institute of Botany Academy of Sciences of the Czech Republic CZ 252 43 Průhonice Czech Republic

Zobrazit více v PubMed

Álvarez I, Wendel JF. Ribosomal ITS sequences and plant phylogenetic inference. Molecular Phylogenetics and Evolution. 2003;29:417–434. PubMed

Arnold ML. Iris nelsonii (Iridaceae): origin and genetic composition of a homoploid hybrid species. American Journal of Botany. 1993;80:577–583. PubMed

Arnold ML. Natural hybridization and evolution. Oxford: Oxford University Press; 1997.

Arnold ML, Bulger MR, Burke JM, Hempel AL, Williams JH. Natural hybridization: how low can you go and still be important? Ecology. 1999;80:371–381.

Baldwin BG, Sanderson MJ, Porter JM, Wojciechowski MF, Campbell CS, Donoghue MJ. The ITS region of nuclear ribosomal DNA: a valuable source of evidence on angiosperm phylogeny. Annals of the Missouri Botanical Garden. 1995;82:247–277.

Barton N. The role of hybridization in evolution. Molecular Ecology. 2001;10:551–568. PubMed

Bothmer R, Bengtsson M, Flink J, Linde-Laursen I. Complex interspecific hybridization in barley (Hordeum vulgare L.) and the possible occurrence of apomixis. Theoretical and Applied Genetics. 1988;76:681–690. PubMed

Bothmer R, Claesson L, Flink J, Linde-Laursen I. Triple hybridization with cultivated barley (Hordeum vulgare L.) Theoretical and Applied Genetics. 1989;78:818–824. PubMed

Brux H, Todeskino D, Wiegleb G. Growth and reproduction of Potamogeton alpinus Balbis growing in disturbed habitats. Archiv fur Hydrobiologie, Beihefte. 1987;27:115–127.

Brux H, Herr W, Todeskino D, Wiegleb G. A study on floristic structure and dynamics of communities with Potamogeton alpinus Balbis in water bodies in the northern part of the Federal Republic of Germany. Aquatic Botany. 1988;32:23–44.

Bureš P. Cirsium Mill. In: Slavík B, Štěpánková J, Štěpánek J, editors. Květena České republiky [Flora of the Czech Republic] Vol. 7. Praha: Academia; 2004. pp. 385–419.

Campbell CS, Wojciechowski MF, Baldwin BG, Alice LA, Donoghue MJ. Persistent nuclear ribosomal DNA sequence polymorphism in the Amelanchier agamic complex. Molecular Biology and Evolution. 1997;14:81–90. PubMed

Clark WA. Pondweeds from North Uist (V.-C. 110), with a special consideration of Potamogeton rutilus Wulfg. and a new hybrid. Proceedings of the University of Durham Philosophical Society. 1942;10:368–373.

Dandy JE. Potamogeton L. In: Stace CA, editor. Hybridization and the flora of the British Isles. London/New York/San Francisco: Academic Press; 1975. pp. 444–459.

dePamphilis CW, Wyatt R. Electrophoretic confirmation of interspecific hybridization in Aesculus (Hippocastanaceae) and the genetic structure of a broad hybrid zone. Evolution. 1990;44:1295–1317. PubMed

Densmore LD, Wright JW, Brown WM. Mitochondrial-DNA analyses and the origin and relative age of parthenogenetic lizards (genus Cnemidophorus). II. C. neomexicanus and the C. tesselatus complex. Evolution. 1989;43:943–957. PubMed

Dionne LA. Studies on the use of Solanum acaule as a bridge between Solanum tuberosum and species in the series Bulbocastana, Cardiophylla and Pinnatisecta. Euphytica. 1963;12:263–269.

Dodd RS, Afzal-Rafii Z. Selection and dispersal in a multispecies oak hybrid zone. Evolution. 2004;58:261–269. PubMed

Dvořák J. Genome analysis in the Triticum-Aegilops alliance. In: Slinkard AE, editor. Proceedings of the 9th International Wheat Genetics Symposium. Vol. 1. Saskatoon, Saskatchewan, Canada. Saskatoon: University Extension Press; 1998. pp. 8–11.

Dvořák J, Zhang HB. Variation in repeated nucleotide sequences sheds light on the phylogeny of the wheat B and G genomes. Proceedings of the National Academy of Sciences of the USA. 1990;87:9640–9644. PubMed PMC

Dvořák J, McGuire PE, Cassidy B. Apparent sources of the A genomes of wheat inferred from polymorphism in abundance and restriction fragment length of repeated nucleotide sequences. Genome. 1988;30:680–689.

Dvořák J, di Terlizzi P, Zhang HB, Resta P. The evolution of polyploid wheats: identification of the A genome donor species. Genome. 1993;36:21–31. PubMed

Dvořák J, Luo M-C, Yang Z-L, Zhang H-B. The structure of the Aegilops tauschii gene pool and the evolution of hexaploid wheat. Theoretical and Applied Genetics. 1998;97:657–670.

Fant JB, Preston CD. Genetic structure and morphological variation of British populations of the hybrid Potamogeton × salicifolius. Botanical Journal of the Linnean Society. 2004;144:99–111.

Fant JB, Preston CD, Barrett JA. Isozyme evidence for the origin of Potamogeton × sudermanicus as a hybrid between P. acutifolius and P. berchtoldii. Aquatic Botany. 2001a;71:199–208.

Fant JB, Preston CD, Barrett JA. Isozyme evidence of the parental origin and possible fertility of the hybrid Potamogeton × fluitans Roth. Plant Systematics and Evolution. 2001b;229:45–57.

Fant JB, Kamau EA, Preston CD. Chloroplast evidence for the multiple origins of the hybrid Potamogeton × sudermanicus Hagstr. Aquatic Botany. 2003;75:351–356.

Fehrer J, Gemeinholzer B, Chrtek J, Jr, Bräutigam S. Incongruent plastid and nuclear DNA phylogenies reveal ancient intergeneric hybridization in Pilosella hawkweeds (Hieracium, Cichorieae, Asteraceae) Molecular Phylogenetics and Evolution. 2007;42:347–361. PubMed

Gadella TWJ. Notes on some triple and inter-sectional hybrids in Hieracium L. subgenus Pilosella (Hill) S. F. Gray. Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen. 1992;95:51–63.

Gill KS, Lubbers EL, Gill BS, Raupp WJ, Cox TS. A genetic linkage map of Triticum tauschii (DD) and its relationship to the D genome of bread wheat (AABBDD) Genome. 1991;34:362–374.

Gonzáles SS, Barrio E, Gafner J, Querol A. Natural hybrids from Saccharomyces cerevisiae, Saccharomyces bayanus and Saccharomyces kudriavzevii in wine fermentations. FEMS Yeast Research. 2006;6:1221–1234. PubMed

Graebner P. Potamogeton (Tourn.) L. In: Engler A, editor. Das Pflanzenreich, Regni vegetabilis conspectus. IV.11. Vol. 31. Berlin, Germany: 1907.

Guggisberg A, Bretagnolle F, Mansion G. Allopolyploid origin of the Mediterranean endemic, Centaurium bianoris (Gentianaceae), inferred by molecular markers. Systematic Botany. 2006;31:368–379.

Hagström JO. Critical researches on the Potamogetons. Kungliga Svenska Vetenskapsakademiens Handlingar. 1916;55:1–281.

Hall TA. BioEdit, a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series. 1999;41:95–98.

Hamilton MB. Four primer pairs for the amplification of chloroplast intergenic regions with intraspecific variation. Molecular Ecology. 1999;8:521–423. PubMed

Hermsen JGTh, Ramanna MS. Double-bridge hybrids of Solanum bulbocastanum and cultivars of Solanum tuberosum. Euphytica. 1973;22:457–466.

Hillis DM, Moritz C, Porter CA, Baker RJ. Evidence for biased gene conversion in concerted evolution of ribosomal DNA. Science. 1991;251:308–310. PubMed

Hodálová I. A new hybrid Senecio × slovacus from the S. nemorensis group (Compositae) in the West Carpathians. Biologia (Bratislava) 2002;57:75–82.

Hollingsworth PM, Preston CD, Gornall RJ. Isozyme evidence for hybridization between Potamogeton natans and P. nodosus (Potamogetonaceae) in Britain. Botanical Journal of the Linnean Society. 1995;117:59–69.

Hollingsworth PM, Preston CD, Gornall RJ. Isozyme evidence for the parentage and multiple origins of Potamogeton × suecicus (P. pectinatus × P. filiformis, Potamogetonaceae) Plant Systematics and Evolution. 1996;202:219–232.

Hollingsworth PM, Preston CD, Gornall RJ. Euploid and aneuploid evolution in Potamogeton (Potamogetonaceae): a factual basis for interpretation. Aquatic Botany. 1998;60:337–358.

Holmgren PK, Holmgren NH. Regnum Vegetabile. Ed. 8. Vol. 120. The Herbaria of the World; 1990. Index Herbariorum. Part I; pp. 1–693.

Holub J. Crataegus L. In: Hejný S, Slavík B, Kirschner J, Křísa B, editors. Květena České republiky [Flora of the Czech Republic] Vol. 3. Praha: Academia; 1992. pp. 488–525.

Huang XQ, Borner A, Roder MS, Ganal MW. Assessing genetic diversity of wheat (Triticum aestivum L.) germplasm using microsatellite markers. Theoretical and Applied Genetics. 2002;105:699–707. PubMed

Hughes CE, Bailey CD, Harris SA. Divergent and reticulate species relationships in Leucaena (Fabaceae) inferred from multiple data sources: insights into polyploid origins and nrDNA polymorphism. American Journal of Botany. 2002;89:1057–1073. PubMed

Iida S, Kadono Y. Genetic diversity and origin of Potamogeton anguillanus (Potamogetonaceae) in Lake Biwa, Japan. Journal of Plant Research. 2002;115:11–16. PubMed

Kalasa Balicka M. The triple hybrid (Solanum tuberosum L. × S. vernei Bitt. et Wittm.) × S. bulbocastanum Dun. Genetica Polonica. 1976;17:165–169.

Kalasa Balicka M. Meiosis and microspore formation in the triple hybrid of (Solanum tuberosum L. × Solanum vernei Bitt. et Wittm.) × Solanum bulbocastanum Dun. Genetica Polonica. 1980;21:425–431.

Kaplan Z. Phenotypic plasticity in Potamogeton (Potamogetonaceae) Folia Geobotanica. 2002;37:141–170.

Kaplan Z. First record of Potamogeton × salicifolius for Italy, with isozyme evidence for plants collected in Italy and Sweden. Plant Biosystems. 2007;141 in press.

Kaplan Z, Fehrer J. Evidence for the hybrid origin of Potamogeton × cooperi (Potamogetonaceae): traditional morphology-based taxonomy and molecular techniques in concert. Folia Geobotanica. 2004;39:431–453.

Kaplan Z, Fehrer J. Comparison of natural and artificial hybridization in Potamogeton. Preslia. 2006;78:303–316.

Kaplan Z, Štěpánek J. Genetic variation within and between populations of Potamogeton pusillus agg. Plant Systematics and Evolution. 2003;239:95–112.

Kaplan Z, Wolff P. A morphological, anatomical and isozyme study of Potamogeton × schreberi: confirmation of its recent occurrence in Germany and first documented record in France. Preslia. 2004;76:141–161.

Kaplan Z, Plačková I, Štěpánek J. Potamogeton × fluitans (P. natans × P. lucens) in the Czech Republic. II. Isozyme analysis. Preslia. 2002;74:187–195.

Kautsky L. In situ experiments on interrelationships between six brackish macrophyte species. Aquatic Botany. 1991;39:159–172.

Kearney M. Hybridization, glaciation and geographical parthenogenesis. Trends in Ecology and Evolution. 2005;20 PubMed

Kihara H. Discovery of the DD-analyser, one of the ancestors of Triticum vulgare. Agricultural Horticulture. 1944;19:889–890. [In Japanese]

King RA, Gornall RJ, Preston CD, Croft JM. Molecular confirmation of Potamogeton × bottnicus (P. pectinatus × P. vaginatus, Potamogetonaceae) in Britain. Botanical Journal of the Linnean Society. 2001;135:67–70.

Kirschner J, Skalický V. Violaceae Batsch. In: Hejný S, Slavík B, Hrouda L, Skalický V, editors. Květena České republiky [Flora of the Czech Republic] Vol. 2. Praha: Academia; 1990. pp. 394–431.

Kitchener GD. A triple hybrid willowherb: Epilobium ciliatum × E. hirsutum × E. parviflorum. BSBI News. 1997;75:66–67.

Koch M, Dobeš C, Mitchell-Olds T. Multiple hybrid formation in natural populations: concerted evolution of the internal transcribed spacer of nuclear ribosomal DNA (ITS) in North American Arabis divaricarpa (Brassicaceae) Molecular Biology and Evolution. 2003;20:338–350. PubMed

Lancaster ML, Gemmell NJ, Negro S, Goldsworthy S, Sunnucks P. Ménage á trois on Macquarie Island: hybridization among three species of fur seal (Arctocephalus spp.) following historical population extinction. Molecular Ecology. 2006;15:3681–3692. PubMed

Les DH, Cleland MA, Waycott M. Phylogenetic studies in Alismatidae. II. Evolution of marine angiosperms (seagrasses) and hydrophily. Systematic Botany. 1997;22:443–463.

Lilienfield FA. H. Kihara: genome analysis in Triticum and Aegilops. Concluding review. Cytologia. 1951;16:101–123.

Linnaeus C. Species plantarum, exhibentes plantas rite cognitas, ad genera relatas, cum differentiis specificis, nominibus trivialibus, synonymis selectis, locis natalibus, secundum systema sexuale digestas. Holmiae: 1753.

Linton EF. Hybrids among British phanerogams. Journal of Botany. 1907;45:296–304.

McFadden ES, Sears ER. The origin of Triticum spelta and its free-threshing hexaploid relatives. Journal of Heredity. 1946;37 PubMed

Ma X-F, Gustafson JP. Genome evolution of allopolyploids: a process of cytological and genetic diploidization. Cytogenetic and Genome Research. 2005;109:236–249. PubMed

Maekawa M, Ha S, Kita F. Identification of reciprocal translocations observed in several Melilotus species (subgenus Eumelilotus) by interspecific triple crossings. Euphytica. 1991;54:255–261.

Mantovani B, Passamonti M, Scali V. The mitochondrial cytochrome oxidase II gene in Bacillus stick insects: ancestry of hybrids, androgenesis, and phylogenetic relationships. Molecular Phylogenetics and Evolution. 2001;19:157–163. PubMed

Mason-Gamer RJ. Reticulate evolution, introgression, and intertribal gene capture in an allohexaploid grass. Systematic Biology. 2004;53:25–37. PubMed

Mateos M, Vrijenhoek RC. Independent origins of allotriploidy in the fish genus Poeciliopsis. Journal of Heredity. 2005;96:32–39. PubMed

Molina MD, García MD, López CG, Ferrero VM. Meiotic pairing in the hybrid (Zea diploperennis × Zea perennis) × Zea mays and its reciprocal. Hereditas. 2004;141:135–141. PubMed

Mráz P, Paule J. Experimental hybridization in the genus Hieracium s. str.: crosses between diploid taxa. Preslia. 2006;78:1–26.

Nelson-Jones EB, Briggs D, Smith AG. The origin of intermediate species of the genus Sorbus. Theoretical and Applied Genetics. 2002;105:953–963. PubMed

Nieto Feliner G, Gutiérrez Larena B, Fuertes Aguilar J. Fine-scale geographical structure, intra-individual polymorphism and recombination in nuclear ribosomal internal transcribed spacers in Armeria (Plumbaginaceae) Annals of Botany. 2004;93:189–200. PubMed PMC

Nilsson NH. Über Hochkomplexe Bastardverbindungen in der Gattung Salix. Hereditas. 1954;40:517–522.

O'Kane SL, Jr, Schaal BA, Al-Shebaz IA. The origins of Arabidopsis suecica (Brassicaceae) as indicated by nuclear rDNA sequences. Systematic Botany. 1996;21:559–566.

Parker ED, Jr, Selander RK. The organization of genetic diversity in the parthenogenetic lizard Cnemidophorus tesselatus. Genetics. 1976;84:791–805. PubMed PMC

Preston CD. Pondweeds of Great Britain and Ireland. London: Botanical Society of the British Isles; 1995.

Preston CD, Hollingsworth PM, Gornall RJ. Potamogeton pectinatus L. × P. vaginatus Turcz. (P. × bottnicus Hagstr.), a newly identified hybrid in the British Isles. Watsonia. 1998;22:69–82.

Rauscher JT, Doyle JJ, Brown AHD. Internal transcribed spacer repeat-specific primers and the analysis of hybridization in the Glycine tomentella (Leguminosae) polyploid complex. Molecular Ecology. 2002;11:2691–2702. PubMed

Rees DJ, Dioli M, Kirkendall LR. Molecules and morphology: evidence for cryptic hybridization in African Hyalomma (Acari: Ixodidae) Molecular Phylogenetics and Evolution. 2003;27:131–142. PubMed

Rieseberg LH. Hybrid origins of plant species. Annual Review of Ecology and Systematics. 1997;28:359–389.

Rieseberg L, Carney S. Plant hybridization. New Phytologist. 1998;140:599–624. PubMed

Rieseberg LH, Ellstrand NC. What can molecular and morphological markers tell us about plant hybridization. Critical Reviews in Plant Sciences. 1993;12:213–241.

Rieseberg LH, Soltis DE. Phylogenetic consequences of cytoplasmic gene flow in plants. Evolutionary Trends in Plants. 1991;5:65–84.

Ritz CM, Schmuths S, Wissemann V. Evolution by reticulation: European dogroses originated by multiple hybridization across the genus. Rosa. Journal of Heredity. 2005;96:4–14. PubMed

Sang T, Crawford DJ, Stuessy TF. Documentation of reticulate evolution in peonies (Paeonia) using internal transcribed spacer sequences of nuclear ribosomal DNA: implications for biogeography and concerted evolution. Proceedings of the National Academy of Sciences of the USA. 1995;92:6813–6817. PubMed PMC

Scali V, Tinti F, Mantovani B, Marescalchi O. Mate recognition and gamete cytology features allow hybrid species poduction and evolution in Bacillus stick insect. Bollettino di Zoologia. 1995;62:59–70.

Simmonds NW. Evolution of crop plants. London: Longman; 1976.

Soltis PS, Soltis DE. Multiple origins of the allotetraploid Tragopogon mirus (Compositae): rDNA evidence. Systematic Botany. 1991;16:407–413.

Stace CA. Hybridization and the flora of the British Isles. London/New York/San Francisco: Academic Press; 1975.

Štěpánek J. Knautia L. In: Slavík B, Chrtek J, Tomšovic P, editors. Květena České republiky [Flora of the Czech Republic] Vol. 5. Praha: Academia; 1997. pp. 543–554.

Štorchová H, Hrdličková R, Chrtek J, Jr, Tetera M, Fitze D, Fehrer J. An improved method of DNA isolation from plants collected in the field and conserved in saturated NaCl/CTAB solution. Taxon. 2000;49:79–84.

Taberlet P, Gielly L, Pautou G, Bouvet J. Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Molecular Biology. 1991;17:1105–1109. PubMed

van Wijk RJ. Ecological studies on Potamogeton pectinatus L. III. Reproductive strategies and germination ecology. Aquatic Botany. 1989;33:271–299.

Wagner A, Blackstone N, Cartwright P, Dick M, Misof B, Snow P, et al. Surveys of gene families using polymerase chain reaction: PCR selection and PCR drift. Systematic Biology. 1994;43:250–261.

Wang GZ, Miyashita NT, Tsunewaki K. Plasmon analyses of Triticum (wheat) and Aegilops: PCR-single-stranded conformational polymorphism (PCR-SSCP) analyses of organellar DNAs. Proceedings of the National Academy of Sciences of the USA. 1997;94:14570–14577. PubMed PMC

Wendel JF, Schnabel A, Seelanan T. An unusual ribosomal DNA sequence from Gossypium gossypioides reveals ancient, cryptic, intergenomic introgression. Molecular Phylogenetics and Evolution. 1995;4:298–313. PubMed

Whittall J, Liston A, Gisler S, Meinke RJ. Detecting nucleotide additivity from direct sequences is a SNAP: an example from Sidalcea (Malvaceae) Plant Biology. 2000;2:211–217.

Whittall JB, Hellquist CB, Schneider EL, Hodges SA. Cryptic species in an endangered pondweed community (Potamogeton, Potamogetonaceae) revealed by AFLP markers. American Journal of Botany. 2004;91:2022–2029. PubMed

Wiegleb G, Kaplan Z. An account of the species of Potamogeton L. (Potamogetonaceae) Folia Geobotanica. 1998;33:241–316.

Evolutionary history and patterns of geographical variation, fertility, and hybridization in Stuckenia (Potamogetonaceae)

The endangered Florida pondweed (Potamogeton floridanus) is a hybrid: Why we need to understand biodiversity thoroughly

Multiple horizontal transfers of nuclear ribosomal genes between phylogenetically distinct grass lineages

Genome size as a key to evolutionary complex aquatic plants: polyploidy and hybridization in Callitriche (Plantaginaceae)

Reconstruction of phylogenetic relationships in a highly reticulate group with deep coalescence and recent speciation (Hieracium, Asteraceae)

Intra-individual polymorphism in diploid and apomictic polyploid hawkweeds (Hieracium, Lactuceae, Asteraceae): disentangling phylogenetic signal, reticulation, and noise

Zobrazit více v PubMed

GENBANK
EF174571, EF174572, EF174573, EF174574, EF174575, EF174576, EF174577, EF174578, EF174579, EF174580, EF174581, EF174582, EF174583, EF174584, EF174585, EF174586, EF174587, EF174588, EF174589, EF174590, EF174591, EF174592, EF174593, EF174594, EF174595, EF174596, EF174597