Abstract
Chloroplast DNA variation was investigated in 42 populations of pedunculate oak, Quercus robur L., in the European part of Russia, Belarus, Poland, Ukraine, the Urals, and the Caucasus. Restriction analysis and sequencing, as well as chloroplast DNA microsatellite loci (cpSSR), were used as genetic markers. For successful amplification and sequencing, new oak-specific primers were designed. For the first time for Q. robur, nucleotide sequences of three fragments (psaA-trnS, psbC-trnD, and trnT-trnF) were obtained with the determination of phylogenetic relationships among 13 identified haplotypes. In the eastern part of the range, several divergent chloroplast DNA lineages were identified. The haplotype groups were characterized by a nonrandom geographic distribution, which probably reflected the history of oak colonization in these regions. Sharp population differentiation in terms of haplotype composition and the level of variation was revealed. Specifically, in the eastern part of the Russian Plain and in the Urals, two haplotypes are widespread, which are disappearing in the west (Northwestern Russia, Belarus, Poland, and Western Ukraine), where nine haplotypes are found that are absent in east. Geographic structure of chloroplast DNA variation in pedunculate oak from Eastern Europe is similar to that in small-leaved lime (Semerikova et al., 2020), another representative of European temperate forests, in which, like in oak in this part of the range, sharp differences between western and eastern populations were observed. It seems likely that this is the result of postglacial colonization by both species from different, long isolated refugia, some of which were located in the east of the studied areas. In the Urals, parallel differentiation of oak and lime between the southern part (Ural River and Belaya River basins) and more northern regions (Ufa River basin and Middle Urals) was revealed, which can be explained by different historical colonization patterns of these regions by broad-leaved vegetation.
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REFERENCES
Denk, T., Grimm, G.W., Manos, P.S., et al., An updated infrageneric classification of the oaks: review of previous taxonomic schemes and synthesis of evolutionary patterns, in Oaks Physiological Ecology: Exploring the Functional Diversity of Genus Quercus L., Gil-Pelegrin, E., Peguero-Pina, J.J., and Sancho-Knapik, D., Eds., Cham, Switzerland: Springer-Verlag, 2017, vol. 7, pp. 13—38.
Kremer, A. and Hipp, A.L., Oaks: an evolutionary success story, New Phytol., 2020, vol. 226, no. 4, pp. 987—1011. https://doi.org/10.1111/nph.16274
Arealy derev’ev i kustarnikov SSSR (Distribution Ranges of Trees and Shrubs of the Soviet Union), Sokolov, S.Ya., Svyazeva, O.A., and Kubli, V.A., Eds., Leningrad: Nauka, 1977, vol. 1.
Dumolin-Lapegue, S., Demesure, B., Fineschi, S., et al., Phylogeographic structure of white oaks throughout the European continent, Genetics, 1997, vol. 146, no. 4, pp. 1475—1487.
Petit, R.J., Csaikl, U.M., Bordacs, S., et al., Chloroplast DNA variation in European white oaks—phylogeography and patterns of diversity based on data from over 2600 populations, For. Ecol. Manage., 2002, vol. 156, nos. 1—3, pp. 5—26. https://doi.org/10.1016/S0378-1127(01)00645-4
Petit, R.J., Brewer, S., Bordacs, S., et al., Identification of refugia and postglacial colonisation routes of European white oaks based on chloroplast DNA and fossil pollen evidence, For. Ecol. Manage., 2002, vol. 156, pp. 49—74. https://doi.org/10.1016/S0378-1127(01)00634-X
Csaikl, U.M., Glaz, I. Baliuckas, V., et al., DNA variation of white oak in the Baltic countries and Poland, For. Ecol. Manage., 2002, vol. 156, nos. 1—3, pp. 211—222. https://doi.org/10.1016/S0378-1127(01)00644-2
Bordacs, S., Popescu, F., Slade, D., et al., Chloroplast DNA variation of white oaks in northern Balkans and in the Carpathian Basin, For. Ecol. Manage., 2002, vol. 156, nos. 1—3, pp. 197—209. https://doi.org/10.1016/S0378-1127(01)00643-0
Brewer, S., Cheddadi, R., de Beaulieu, J.-L., et al., The spread of deciduous Quercus throughout Europe since the last glacial period, For. Ecol. Manage., 2002, vol. 156, nos. 1—3, pp. 27—48. https://doi.org/10.1016/S0378-1127(01)00646-6
Evolyutsiya ekosistem Evropy pri perekhode ot pleistotsena k golotsenu (24—8 tys. l. n.) (Evolution of European Ecosystems during the Pleistocene—Holocene Transition (24—8 kyr BP)), van Kolfschoten, T. and Markova, A.K., Eds., Moscow: KMK, 2008.
Markova, A.K., Simakova, A.N., and Puzachenko, A.Y., Ecosystems of Eastern Europe at the time of maximum cooling of the Valdai glaciation (24—18 kyr BP) inferred from data on plant communities and mammal assemblages, Quat. Int., 2009, vol. 201, pp. 53—59. https://doi.org/10.1016/j.quaint.2008.05.020
Denisov, A.K., Postglacial dynamics of the northern border of the pedunculate oak range in the USSR and phylocenogenesis of northern oak forests, Lesovedenie, 1980, no. 1, pp. 3—11.
Semerikova, S.A., Isakov, I.Y., and Semerikov, V.L., Chloroplast DNA variation shed light on the history of lime tree (Tilia cordata s. l.) in the eastern part of the range, Russ. J. Genet., 2020, vol. 56, no. 2, pp. 192—203. https://doi.org/10.1134/S1022795420020118
Dering, M., Lewandowski, A., Ufnalski, K., and Kedzierska, A., How far to the east was the migration of white oaks from the Iberian refugium?, Silva Fenn., 2008, vol. 42, no. 3, pp. 327—335. https://doi.org/10.14214/sf.240
Chmielewski, M., Meyza, K., Chybicki, I.J., et al., Chloroplast microsatellites as a tool for phylogeographic studies: the case of white oaks in Poland, iFor.—Biogeosci. For., 2015, vol. 8, pp. 765—771. https://doi.org/10.3832/ifor1597-008
Slade, D., Skvorc, Z., Ballian, D., et al., The chloroplast DNA polymorphisms of white oaks of section Quercus in the Central Balkans, Silvae Genet., 2008, vol. 57, nos. 4—5, pp. 227—234. https://doi.org/10.1515/sg-2008-0035
Curtu, A.L., Sofletea, N., Toader, A.V., and Enescu, M.C., Leaf morphological and genetic differentiation between Quercus robur L. and its closest relative, the drought-tolerant Quercus pedunculiflora K. Koch., Ann. For. Sci., 2011, vol. 68, no. 7, pp. 1163—1172. https://doi.org/10.1007/s13595-011-0105-z
Kovalevich, O.A., Kagan, D.I., and Padutov, V.E., SSRP analysis of chloroplast DNA of pedunculate oak growing in Belarus, Dokl. Nats. Akad. Navuk Belarusi, 2011, vol. 55, no. 6, pp. 100—104.
Kovalevich, O.A., Genogeography of pedunculate oak in Belarus inferred from chloroplast DNA analysis, Extended Abstract of Cand. Sci. Dissertation, Inst. Lesa Nats. Akad. Navuk Belarusi, Gomel’, 2013.
Deguilloux, M.F., Dumolin-Lapegue, S., Gielly, L., et al., A set of primers for the amplification of chloroplast microsatellites in Quercus, Mol. Ecol. Notes, 2003, vol. 3, no. 1, pp. 24—27. https://doi.org/10.1046/j.1471-8286.2003.00339.x
Blanc-Jolivet, C. and Liesebach, M., Tracing the origin and species identity of Quercus robur and Quercus petraea in Europe: a review, Silvae Genet., 2015, vol. 64, no. 4, pp. 182—193. https://doi.org/10.1515/sg-2015-0017
Devey, M.E., Bell, J.C., Smith, D.N., et al., A genetic linkage map for Pinus radiata based on RFLP, RAPD and microsatellite markers, Theor. Appl. Genet., 1996, vol. 92, no. 6, pp. 673—679. https://doi.org/10.1007/BF00226088
Demesure, B., Sodzi, N., and Petit, R.J., A set of universal primers for amplification of polymorphic noncoding regions of mitochondrial and chloroplast DNA in plants, Mol. Ecol., 1995, vol. 4, no. 1, pp. 129—131. https://doi.org/10.1111/j.1365-294X.1995.tb00201.x
Taberlet, P., Gielly, L., Pautou, G., and Bouvet, J., Universal primers for amplification of 3 non-coding regions of chloroplast DNA, Plant Mol. Biol., 1991, vol. 17, no. 5, pp. 1105—1109. https://doi.org/10.1007/BF00037152
Rozen, S. and Skaletsky, H.J., Primer 3 on the WWW for general users and for biologist programmers, in Bioinformatics Methods and Protocols: Methods in Molecular Biology, Krawetz, S. and Misener, S., Eds., Totowa, N.J.: Humana, 2000, pp. 365—386.
Hall, T.A., BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows95/98/NT, Nucleic Acids Symp. Ser., 1999, vol. 41, pp. 95—98. https://doi.org/10.1111/jbi.12867
Ronquist, F. and Huelsenbeck, J.P., MrBayes 3: Bayesian phylogenetic inference under mixed models, Bioinformatics, 2003, vol. 19, no. 12, pp. 1572—1574. https://doi.org/10.1093/bioinformatics/btg180
Swofford, D.L., PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods): Version 4.0 beta 10, Sunderland: Sinauer Associates, 2002.
Sork, V.L., Fitz-Gibbon, S.T., Puiu, D., et al., First draft assembly and annotation of the genome of a California endemic oak Quercus lobata Nee (Fagaceae), Genes Genomes Genet., 2016, vol. 6, no. 11, pp. 3485—3495. https://doi.org/10.1534/g3.116.030411
Pham, K.K., Hipp, A.L., Manos, P.S., and Cronn, R.C., A time and a place for everything: phylogenetic history and geography as joint predictors of oak plastome phylogeny, Genome, 2017, vol. 60, no. 9, pp. 720—732. https://doi.org/10.1139/gen-2016-0191
Bandelt, H.J., Forster, P., and Röhl, A., Median-joining networks for inferring intraspecific phylogenies, Mol. Biol. Evol., 1999, vol. 16, no. 1, pp. 37—48. https://doi.org/10.1093/oxfordjournals.molbev.a026036
Nei, M., Molecular Evolutionary Genetics, New York: Columbia Univ. Press, 1987.
Librado, P. and Rozas, J., DnaSP v5: a software for comprehensive analysis of DNA polymorphism data, Bioinformatics, 2009, vol. 25, pp. 1451—1452. https://doi.org/10.1093/bioinformatics/btp187
Excoffier L., Lischer H. ARLEQUIN ver. 3.5: An Integrated Software Package for Population Genetics Data Analysis. Bern: Computational and Molecular Population Genetics Lab (CMPG). Institute of Ecology and Evolution, Univ. Bern, Bern, Switzerland, 2011.
Dupanloup, I., Schneider, S., and Excoffier, L., A simulated annealing approach to define the genetic structure of populations, Mol. Ecol., 2002, vol. 11, no. 12, pp. 2571—2581. https://doi.org/10.1046/j.1365-294X.2002.01650.x
Semerikov, L.F., Populyatsionnaya struktura drevesnykh rastenii (na primere vidov duba evropeiskoi chasti SSSR i Kavkaza) (Population Structure of Arboraceous Plants (Exemplified by Oak Species of the European Part of the USSR and the Caucasus), Moscow: Nauka, 1986.
Gomory, D., Yakovlev, I., Zhelev, P., et al., Genetic differentiation of oak populations within the Quercus robur/Quercus petraea complex in Central and Eastern Europe, Heredity, 2001, vol. 86, pp. 557—563. https://doi.org/10.1046/j.1365-2540.2001.00874.x
Gabitova, A.A., Yanbaev, Yu.A., and Red’kina, N.N., High genetic polymorphism of pedunculate oak populations on the western macroslope of the Southern Urals, Vestn. Bashk. Univ., Ser. Biol., 2015, vol. 20, no. 3, pp. 854—856.
Degen, B., Yanbaev, R., Yanbaev, Y., Genetic differentiation of Quercus robur in the South-Ural, Silvae Genet., 2019, vol. 68, no. 1, pp. 111—115. https://doi.org/10.2478/sg-2019-0019
Ekhvaia, J., Simeone, M.C., Silakadze, N., and Abdaladze, O., Morphological diversity and phylogeography of the Georgian durmast oak (Q. petraea subsp. iberica) and related Caucasian oak species in Georgia (South Caucasus), Tree Genet. Genom., 2018, vol. 14, no. 2. https://doi.org/10.1007/s11295-018-1232-6
ACKNOWLEDGMENTS
We thank L.I. Agafonov, B.K. Gannibal, G.Yu. Konechnaya, N.V. Semerikov, A.H. Sozontov, E.G. Filippov, and Yu.Ya. Khrunyk for participation in the collection of oak accessions, A.I. Tsivilev and K.A. Panikovskaya for help in laboratory analyses, and an anonymous reviewer for constructive comments.
Funding
This study was performed within the framework of the state contract of the Institute of Plant and Animal Ecology of the Ural Branch of the Russian Academy of Sciences and was supported by the Russian Foundation for Basic Research (grant no. 18-04-01061A).
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Semerikova, S.A., Isakov, I.Y. & Semerikov, V.L. Chloroplast DNA Variation and Phylogeography of Pedunculate Oak Quercus robur L. in the Eastern Part of the Range. Russ J Genet 57, 47–60 (2021). https://doi.org/10.1134/S1022795421010130
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DOI: https://doi.org/10.1134/S1022795421010130