Plant Biol (Stuttg) 2007; 9(1): 116-126
DOI: 10.1055/s-2006-924542
Research Paper

Georg Thieme Verlag Stuttgart KG · New York

Genetic Variation and Differentiation Within a Natural Community of Five Oak Species (Quercus spp.)

A. L. Curtu1 , O. Gailing1 , L. Leinemann1 , R. Finkeldey1
  • 1Institute of Forest Genetics and Forest Tree Breeding, Georg August University Göttingen, Büsgenweg 2, 37077 Göttingen, Germany
Weitere Informationen

Publikationsverlauf

Received: July 19, 2006

Accepted: August 4, 2006

Publikationsdatum:
17. Oktober 2006 (online)

Abstract

Chloroplast DNA and two categories of nuclear markers - isozymes and microsatellites - were used to examine a very rich natural community of oaks (Quercus spp.) situated in west-central Romania. The community consists of five oak species: Q. robur, Q. petraea, Q. pubescens, and Q. frainetto - that are closely related -, and Q. cerris. A total of five chloroplast haplotypes was identified. Q. cerris was fixed for a single haplotype. The other four species shared the two most common haplotypes. One haplotype was confined to Q. robur and a very rare one was restricted to Q. petraea. Both types of nuclear markers revealed a larger genetic variation for Q. pubescens and Q. petraea than for Q. frainetto and Q. robur, although the differences between species are in most cases not significant. At the nuclear level, Q. cerris could be clearly separated from the other four oak species confirming the taxonomic classification. Regardless of the estimate used, the levels of polymorphism revealed by microsatellites were much higher than those based on isozymes. For the four closely related species the overall genetic differentiation was significant at both categories of nuclear markers. Several loci, such as Acp-C for isozymes, and ssrQpZAG36 and ssrQrZAG96 for microsatellites were very useful to discriminate among species. However, the level of differentiation varied markedly between pairs of species. The genetic affinities among the species may reflect different phylogenetic distances and/or different rates of recurrent gene flow at this site.

References

  • 1 Aldrich P. R., Parker G. R., Michler C. H., Romero-Severson J.. Whole-tree silvic identifications and the microsatellite genetic structure of a red oak species complex in an Indiana old-growth forest.  Canadian Journal of Forest Research. (2003);  33 2228-2237
  • 2 Bacilieri R., Ducousso A., Kremer A.. Genetic, morphological, ecological and phenological differentiation between Quercus petraea (Matt.) Liebl. and Quercus robur L. in a mixed stand of Northwest of France.  Silvae Genetica. (1995);  44 1-10
  • 3 Bacilieri R., Ducousso A., Petit R. J., Kremer A.. Mating system and asymmetric hybridization in a mixed stand of European oaks.  Evolution. (1996);  50 900-908
  • 4 Bartha D.. Quercus frainetto Ten. Schütt, P., Schuck, H. J., Lang, U. M., and Roloff, A., eds. Enzyklopädie der Holzgewächse: Handbuch und Atlas der Dendrologie. Landsberg am Lech; Ecomed (1998): 1-8
  • 5 Bellarosa R., Simeone M. C., Papini A., Schirone B.. Utility of ITS sequence data for phylogenetic reconstruction of Italian Quercus spp.  Molecular Phylogenetics and Evolution. (2005);  34 355-370
  • 6 Belletti P., Leonardi S., Monteleone I., Piovani P.. Allozyme variation in different species of deciduous oaks from northwestern Italy.  Silvae Genetica. (2005);  54 9-16
  • 7 Bordács S., Popescu F., Slade D., Csaikl U., Lesur I., Borovics A., Kézdy P., König A. O., Gömöry D., Brewer R. A., Burg K., Petit R. J.. Chloroplast DNA variation of white oaks in the northern Balkans and in the Carpathian Basin.  Forest Ecology and Management. (2002);  156 197-209
  • 8 Bruschi P., Vendramin G. G., Bussotti F., Grossoni P.. Morphological and molecular differentiation between Quercus petraea (Matt.) Liebl. and Quercus pubescens Willd. (Fagaceae) in Northern and Central Italy.  Annals of Botany. (2000);  85 325-333
  • 9 Burger W. C.. The species concept in Quercus.  Taxon. (1975);  24 45-50
  • 10 Camus A.. Les Chênes. Monographie du Genre Quercus. Paris; Lechevalier (1936 - 1954)
  • 11 Craft K. J., Ashley M. V., Koenig W. D.. Limited hybridization between Quercus lobata and Quercus douglasii (Fagaceae) in a mixed stand in central coastal California.  American Journal of Botany. (2002);  89 1792-1798
  • 12 Curtu A.-L., Finkeldey R., Gailing O.. Comparative sequencing of a microsatellite locus reveals size homoplasy within and between European oak species (Quercus spp.).  Plant Molecular Biology Reporter. (2004);  22 339-346
  • 13 Degen B., Streiff R., Ziegenhagen B.. Comparative study of genetic variation and differentiation of two pedunculate oak (Quercus robur) stands using microsatellite and allozyme loci.  Heredity. (1999);  83 597-603
  • 14 Demesure B., Sodzi N., Petit R.. A set of universal primers for amplification of polymorphic non-coding regions of mitochondrial and chloroplast DNA in plants.  Molecular Ecology. (1995);  4 129-131
  • 15 Dow B. D., Ashley M. V., Howe H. F.. Characterization of highly variable (GA/CT)n microsatellites in the bur oak, Quercus macrocarpa.  Theoretical and Applied Genetics. (1995);  91 137-141
  • 16 Dumolin S., Demesure B., Petit R.. Inheritance of chloroplast and mitochondrial genomes in pedunculate oak investigated with an efficient PCR method.  Theoretical and Applied Genetics. (1995);  91 1253-1256
  • 17 Dumolin-Lapègue S., Demesure B., Fineschi S., Le Corre V., Petit R.. Phylogeographic structure of white oaks throughout the European continent.  Genetics. (1997);  146 1475-1487
  • 18 El Mousadik A., Petit R. J.. High level of genetic differentiation for allelic richness among populations of the argan tree (Argania spinosa [L.] Skeels) endemic to Morocco.  Theoretical and Applied Genetics. (1996);  92 832-839
  • 19 Estoup A., Jarne P., Cornuet J.-M.. Homoplasy and mutation model at microsatellite loci and their consequences for population genetics analysis.  Molecular Ecology. (2002);  11 1591-1604
  • 20 Excoffier L., Laval G., Schneider S.. Arlequin (version 3.0): an integrated software package for population genetics data analysis.  Evolutionary Bioinformatics Online. (2005);  1 47-50
  • 21 Felsenstein J.. PHYLIP - phylogeny inference package (Version 3.2).  Cladistics. (1989);  5 164-166
  • 22 Finkeldey R.. Genetic variation of oaks (Quercus spp.) in Switzerland. 2. Genetic structures in “pure” and “mixed” forests of pedunculate oak (Q. robur L.) and sessile oak (Q. petraea [Matt.] Liebl.).  Silvae Genetica. (2000);  50 22-30
  • 23 Finkeldey R.. Genetic variation of oaks (Quercus spp.) in Switzerland. 1. Allelic diversity and differentiation at isozyme gene loci.  Forest Genetics. (2001);  8 185-195
  • 24 Gehle T.. Reproduktionssystem und genetische Differenzierung von Stieleichenpopulationen (Quercus robur) in Nordrhein-Westfalen. In 24. Institut für Forstgenetik und Forstpflanzenzüchtung der Universität Göttingen, Göttingen. (1999): 25-35
  • 25 Gömöry D., Yakovlev I., Zhelev P., Jedináková J., Paule L.. Genetic differentiation of oak populations within the Quercus robur/Quercus petraea complex in Central and Eastern Europe.  Heredity. (2001);  86 557-563
  • 26 Goudet J.. FSTAT (Version 1.2): a computer program to calculate F-statistics.  Journal of Heredity. (1995);  86 485-486
  • 27 Guo S., Thompson E.. Performing the exact test of Hardy-Weinberg proportions for multiple alleles.  Biometrics. (1992);  48 361-372
  • 28 Hertel H., Degen B.. Stieleiche von Traubeneiche mit Hilfe von Isoenzymanalysen sicher unterscheiden.  Allgemeine Forstzeitschrift/Der Wald. (1998);  53 246-247
  • 29 Herzog S.. Genetic inventory of European oak populations: consequences for breeding and gene conservation.  Annales des Sciences Forestières. (1996);  53 783-793
  • 30 Kampfer S., Lexer C., Glössl J., Steinkellner H.. Characterization of (GA)n microsatellite loci from Quercus robur.  Hereditas. (1998);  129 183-186
  • 31 Konnert M., Fromm M., Wimmer T.. Anleitung für Isoenzymuntersuchungen bei Stieleiche (Quercus robur) und Traubeneiche (Quercus petraea). Teisendorf; Bayerisches Amt für forstliche Saat- und Pflanzenzucht (ASP) (2004): 1-19
  • 32 Mariette S., Cottrell J., Csaikl U. M., Goikoechea P., König A. O., Lowe A. J., Van Dam B. C., Barreneche T., Bodenes C., Streiff R., Burg K., Groppe K., Munro R. C., Tabbener H., Kremer A.. Comparison of levels of genetic diversity detected with AFLP and microsatellite markers within and among mixed Q. petraea (Matt.) Liebl. and Q. robur L. stands.  Silvae Genetica. (2002);  51 72-79
  • 33 Muir G., Schlötterer C.. Evidence for shared ancestral polymorphism rather than recurrent gene flow at microsatellite loci differentiating two hybridizing oaks (Quercus spp.).  Molecular Ecology. (2005);  14 549-561
  • 34 Müller-Starck G., Zanetto A., Kremer A., Herzog S.. Inheritance of isoenzymes in sessile oak (Quercus petraea [Matt.] Liebl.) and offspring from interspecific crosses.  Forest Genetics. (1996);  3 1-12
  • 35 Müller-Starck G., Ziehe M.. Genetic variation in populations of Fagus sylvatica L., Quercus robur L., and Q. petraea Liebl. in Germany. Müller-Starck, G. and Ziehe, M., eds. Genetic Variation in European Populations of Forest Trees. Frankfurt/M.; Sauerländer's Verlag (1991): 125-140
  • 36 Nei M.. Genetic distance between populations.  The American Naturalist. (1972);  106 283-292
  • 37 Nei M.. Molecular Evolutionary Genetics. New York; Columbia University Press (1987)
  • 38 Nixon K. C.. Infrageneric classification of Quercus (Fagaceae) and typification of sectional names.  Annales des Sciences Forestières. (1993);  50 25-34
  • 39 Peakall R., Smouse P. E.. GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research.  Molecular Ecology Notes. (2006);  6 288-295
  • 40 Petit R., Brewer S., Bordács S., Burg K., Cheddadi R., Coart E., Cottrell J., Csaikl U., van Dam B., Deans D., Espinel S., Fineschi S., Finkeldey R., Glaz I., Goicoechea P. G., Jensen J. S., König A. O., Lowe A. J., Madsen S. F., Mátyás G., Munro R. C., Popescu F., Slade D., Tabbener H., de Vries S. G. M., Ziegenhagen B., de Beaulieu J.-L., Kremer A.. Identification of refugia and post-glacial colonisation routes of European white oaks based on chloroplast DNA and fossil pollen evidence.  Forest Ecology and Management. (2002 a);  156 49-74
  • 41 Petit R., Csaikl U., Bordács S., Burg K., Coart E., Cottrell J., van Dam B., Deans D., Dumolin-Lapègue S., Fineschi S., Finkeldey R., Gillies A., Glaz I., Goicoechea P. G., Jensen J. S., König A. O., Lowe A. J., Madsen S. F., Mátyás G., Munro R. C., Olalde M., Pemonge M.-H., Popescu F., Slade D., Tabbener H., Taurchini D., de Vries S. G. M., Ziegenhagen B., Kremer A.. Chloroplast DNA variation in European white oaks. Phylogeography and patterns of diversity based on data from over 2600 populations.  Forest Ecology and Management. (2002 b);  156 5-26
  • 42 Petit R., El Mousadik A., Pons O.. Identifying populations for conservation on the basis of genetic markers.  Conservation Biology. (1998);  12 844-855
  • 43 Petit R. J., Bodenes C., Ducousso A., Roussel G., Kremer A.. Hybridization as a mechanism of invasion in oaks.  New Phytologist. (2004);  161 151-164
  • 44 Raymond M., Rousset F.. GENEPOP (Version 1.2): population genetics software for exact tests and ecumenicism.  Journal of Heredity. (1995);  86 248-249
  • 45 Schwarz O.. Monographie der Eichen Europas und des Mittelmeergebietes, I. Textband. Berlin-Dahlem; (1937): 1-200
  • 46 Scotti-Saintagne C., Mariette S., Porth I., Goicoechea P. G., Barreneche T., Bodenes C., Burg K., Kremer A.. Genome scanning for interspecific differentiation between two closely related oak species (Quercus robur L. and Q. petraea [Matt.] Liebl.).  Genetics. (2004);  168 1615-1626
  • 47 Slatkin M.. A measure of population subdivision based on microsatellite allele frequencies.  Genetics. (1995);  139 457-462
  • 48 Stanciu A.. Cercetari taxonomice, morfologice si ecologice privind hibrizii genului Quercus din Rezervatia Stiintifica Bejan-Deva, judetul Hunedoara. Teza de Doctorat, Universitatea Transilvania. (1995)
  • 49 Steinkellner H., Fluch S., Turetschek E., Lexer C., Streiff R., Kremer A., Burg K., Glössl J.. Identification and characterization of (GA/CT)n-microsatellite loci from Quercus petraea.  Plant Molecular Biology. (1997 a);  33 1093-1096
  • 50 Steinkellner H., Lexer C., Turetschek E., Glössl J.. Conservation of (GA)n microsatellite loci between Quercus species.  Molecular Ecology. (1997 b);  6 1189-1194
  • 51 Streiff R., Labbe T., Bacilieri R., Steinkellner H., Glössl J., Kremer A.. Within-population genetic structure in Quercus robur L. and Quercus petraea (Matt.) Liebl. assessed with isozymes and microsatellites.  Molecular Ecology. (1998);  7 317-328
  • 52 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
  • 53 Valbuena-Carabana M., Gonzalez-Martinez S. C., Sork V. L., Collada C., Soto A., Goicoechea P. G., Gil L.. Gene flow and hybridisation in a mixed oak forest (Quercus pyrenaica Willd. and Quercus petraea [Matts.] Liebl.) in central Spain.  Heredity. (2005);  95 457-465
  • 54 Weir B. S., Cockerham C. C.. Estimating F-statistics for the analysis of population structure.  Evolution. (1984);  38 1358-1370
  • 55 Zanetto A., Kremer A., Müller-Starck G., Hattemer H. H.. Inheritance of isozymes in pedunculate oak (Quercus robur L.).  Journal of Heredity. (1996);  87 364-370
  • 56 Zanetto A., Roussel G., Kremer A.. Geographic variation of inter-specific differentiation between Quercus robur L. and Quercus petraea (Matt.) Liebl.  Forest Genetics. (1994);  1 111-123

R. Finkeldey

Institute of Forest Genetics and Forest Tree Breeding
Georg August University Göttingen

Büsgenweg 2

37077 Göttingen

Germany

eMail: rfinkel@gwdg.de

Editor: F. Salamini