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

A. L. Curtu; O. Gailing; L. Leinemann; R. Finkeldey

doi:10.1055/s-2006-924542

Plant Biology, Inhaltsverzeichnis

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

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.

Key words

Genetic variation - differentiation - chloroplast DNA - isozymes - microsatellites - Quercus.

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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