Marker- and genomics-assisted assessments over three decades across Europe reveal substantial genetic diversity and adaptive potential in pedun-culate oak (Quercus robur L.), informing operational conservation strategies
Keywords:
forests, GWAS, high-resolution genomics, landscape genetics, neutral markers, QTLAbstract
This review synthesizes three decades of molecular evidence on the genetic diversity and conservation of pedunculate oak (Quercus robur L.) across Europe. A methodological synthesis delineates three phases of marker evolution: Phase I (1993–2003) – isozymes, RAPD, AFLP and early SSRs establishing popula-tion-genetic baselines; Phase II (2004-2014) – multi-marker integration and QTL analyses linking marker variation to adaptive traits; and Phase III (2015–2026) – the genomic era with WGS, SNP, ddRADseq and GBS systems enabling high-resolution inference of demography and local adaptation. Genetic diversity of Q. robur was assessed using allelic richness, observed and expected heterozygosity, fixation and differen-tiation indices, chloroplast haplotype diversity and SNP-based genomic metrics, consistently showing high within-population diversity, low but significant among-population differentiation maintained by extensive gene flow and spatially structured adaptive variation shaped by postglacial history and environmental gra-dients, confirming strong evolutionary and adaptive capacity across Europe. Integrating SSR, SNP and phenotypic evidence reveals robust adaptive potential to drought and water stress. Based on these findings and EUFORGEN guidance, a tiered conservation strategy is proposed: (i) in situ preservation of large, interbreeding stands; (ii) provenance-based seed transfer within seed zones; (iii) ex situ conservation of marginal populations; and (iv) circa situm management in productive landscapes. This synthesis establishes a marker-informed framework linking evolutionary processes to actionable conservation, thereby strength-ening the adaptive capacity of Q. robur under climate change across Europe.
References
Alberto, F.J., Aitken, S.N., Alía, R., González‐Martínez,
S.C., Hänninen, H., Kremer, A., Lefèvre, F., Lenormand,
T., Yeaman, S., Whetten, R., Savolainen, O., 2013. Po-
tential for evolutionary responses to climate change–evi-
dence from tree populations. Global Change Biology,
19 (6): 1645–1661. https://doi.org/10.1111/gcb.12181
Digital
Annighöfer, P., Beckschäfer, P., Vor, T., Ammer, C., 2015.
Regeneration patterns of European oak species (Quer-
cus petraea (Matt.) Liebl., Quercus robur L.) in depen-
dence of environment and neighborhood. PloS One, 10
(8): e0134935. https://doi.org/10.1371/journal.pone.0134935
Avanzi, C., Bagnoli, F., Romiti, E., Spanu, I., Tsuda, Y., Va-
jana, E., Vendramin, G.G., Piotti, A., 2025. Latitudi-
nal trends in genetic diversity and distinctiveness of
Quercus robur rear edge forest remnants call for new
conservation priorities. Diversity and Distributions, 31
(4): e70018. https://doi.org/10.1111/ddi.70018
Bacilieri, R., Ducousso, A., Kremer, A., 1996. Comparison
of morphological characters and molecular markers for
the analysis of hybridization in sessile and pedunculate
oak. Annales des Sciences Forestières, 53 (2-3): 79–91.
Bakker, E.G., Van Dam, B.C., Van Eck, H.J., Jacobsen, E.,
2001. A discrimination between Quercus robur L. and
Q. petraea (Matt.) Liebl. based on species-indicative
AFLP markers. Silvae Genetica, 50 (2): 61–69.
Baliuckas, V., Pliura, A., 2003. Genetic variation and phe-
notypic plasticity of Quercus robur populations and
open-pollinated families in Lithuania. Scandinavian
Journal of Forest Research, 18 (4): 305–319. https://doi.
org/10.1080/02827580310005153
Ballian, D., Belletti, P., Ferrazzini, D., Bogunić, F., Kaj-
ba, D., 2010. Genetic variability of pedunculate oak (Quer-
cus robur L.) in Bosnia and Herzegovina. Periodicum
Biologorum, 112 (3): 353–362.
Barreneche, T., Bodénès, C., Lexer, C., Trontin, J.-F.,
Fluch, S., Streiff, R., Plomion, C., Roussel, G., Stein-
kellner, H., Burg, K., Favre, J.-M., Glössl, J., Kremer,
A., 1998. A genetic linkage map of Quercus robur L.
based on RAPD, SCAR, microsatellite, minisatellite,
isozyme, and 5S rDNA markers. Theoretical and Ap-
plied Genetics, 97 (6-7): 1090–1103. https://doi.org/10.1007/
s001220050996
Barrès, B., Dutech, C., Saint-Jean, G., Bodénès, C., Burban,
C., Fiévet, V., Lepoittevin, C., Garnier-Géré, P.,
Desprez-Loustau, M-L., 2024. Demographic and ge-
netic impacts of powdery mildew in a young oak (Quer-
cus robur L.) cohort. Annals of Forest Science, 81: 44.
https://doi.org/10.1186/s13595-024-01259-2
Blanc-Jolivet, C., Bakhtina, S., Yanbaev, R., Yanbaev, Y.,
Mader, M., Guichoux, E., Degen, B., 2020. Develop-
ment of new SNPs loci on Quercus robur and Quercus
petraea for genetic studies covering the whole species’
distribution range. Conservation Genetics Resources, 12
(4): 597–600. https://doi.org/10.1007/s12686-020-01141-z
Blanc-Jolivet, C., Liesebach, M., 2015. Tracing the origin
and species identity of Quercus robur and Quercus pet-
raea in Europe: a review. Silvae Genetica, 64 (4): 182–193.
Bogdan, S., Ivanković, M., Temunović, M., Morić, M.,
Franjić, J., Katičić Bogdan, I., 2017. Adaptive ge-
netic variability and differentiation of Croatian and Aus-
trian Quercus robur L. populations at a drought prone
field trial. Annals of Forest Research, 60 (1): 33–46.
https://doi.org/10.15287/afr.2016.733
Brewer, S., Cheddadi, R., De Beaulieu, J.L., Reille, M.,
2002. The spread of deciduous Quercus throughout Eu-
rope since the last glacial period. Forest Ecology and
Management, 156 (1-3): 27–48. https://doi.org/10.1016/
S0378-1127(01)00646-6
Burger, K. Gailing, O., 2022. Genetic variability of in-
digenous (Quercus robur L.) and late flushing oak (Q.
robur subsp. slavonica) in adult stands compared with
their natural regeneration. European Journal of Forest
Research, 141 (6): 1073–1088. https://doi.org/10.1007/
s10342-022-01491-3
Burger, K., Müller, M., Rogge, M., Gailing, O., 2021.
Genetic differentiation of indigenous (Quercus robur L.)
and late flushing oak stands (Q. robur subsp. slavonica)
in western Germany. European Journal of Forest Re-
search, 140 (6): 1179–1194. https://doi.org/10.1007/
s10342-021-01395-8
Buschbom, J., Yanbaev, Y., Degen, B., 2011. Efficient long-
208
distance gene flow into an isolated relict oak stand. Jour-
nal of Heredity, 102 (4): 464–472. https://doi.org/10.1093/
jhered/esr023
Casasoli, M., Derory, J., Morera-Dutrey, C., Brendel, O.,
Porth, I., Guehl, J.-M., Villani, F., Kremer, A., 2006.
Comparison of quantitative trait loci for adaptive traits
between oak and chestnut based on an expressed se-
quence tag consensus map. Genetics, 172 (1): 533–546.
https://doi.org/10.1534/genetics.105.048439
Chokheli, V., Kozlovsky, B., Sereda, M., Lysenko, V., Fe-
senko, I., Varduny, T., Kapralova, O., Bondarenko,
E., 2016. Preliminary comparative analysis of phenolo-
gical varieties of Quercus robur by ISSR‐markers. Journal
of Botany, 2016 (1): 7910451. https://doi.org/10.1155/2016/
7910451
Coart, E., Lamote, V., De Loose, M., Van Bockstaele, E.,
Lootens, P., Roldán-Ruiz, I., 2002. AFLP markers de-
monstrate local genetic differentiation between two indi-
genous oak species [Quercus robur L. and Q. petraea
(Matt.) Liebl.] in Flemish populations. Theoretical and
Applied Genetics, 105 (3): 431–439. https://doi.org/10.1007/
s00122-002-0920-6
Cortes, L., Zhang, Z., Yu, J., 2021. Status and prospects of
genome-wide association studies in plants. The Plant
Genome, 14 (1): e20077.
Cottrell, J.E., Munro, R.C., Tabbener, H.E., Gillies, A.C.M.,
Forrest, G.I., Deans, J.D., Lowe, A.J., 2002. Distribu-
tion of chloroplast DNA variation in British oaks (Quer-
cus robur and Q. petraea): the influence of postglacial
colonisation and human management. Forest Ecology
and Management, 156 (1-3): 181195. https://doi.org/10.1016/
S0378-1127(01)00642-9
Craciunesc, I., Ciocîrlan, E., Sofletea, N., Curtu, A.L.,
2011. Genetic diversity of pedunculate oak (Quercus ro-
bur L.) in Prejmer natural reserve. Bulletin of the Tran-
silvania University of Brasov. Series II: Forestry - Wood
Industry - Agricultural Food Engineering, 4 (53): 15–20.
Curtu, A.L., Gailing, O. Finkeldey, R., 2007. Evidence for
hybridization and introgression within a species-rich
oak (Quercus spp.) community. BMC Evolutionary Biolo-
gy, 7 (1): 218. https://doi.org/10.1186/1471-2148-7-218
Curtu, A.L., Gailing, O., Finkeldey, R., 2011. Leaf mor-
phological and genetic differentiation between Quercus
robur and Q. pedunculiflora in a mixed stand of the Da-
nube Delta. Annals of Forest Research, 54 (2): 175–188.
https://doi.org/10.1007/s13595-011-0105-z
Degen, B., Yanbaev, R., Yanbaev, Y., 2019. Genetic differen-
tiation of Quercus robur in the South-Ural. Silvae Gene-
tica, 68 (1-2): 111–115. https://doi.org/10.2478/sg-2019-
0019
Degen, B., Yanbaev, Y., Ianbaev, R., Bakhtina, S., Sulta-
nova, R., 2021a. When does habitat fragmentation lead
to changes in populations gene pool of pedunculate oak
(Quercus robur L.)? Forest Ecology and Management,
499: 119617. https://doi.org/10.1016/j.foreco.2021.11961
Degen, B., Blanc-Jolivet, C., Bakhtina, S., Yanbaev, R.,
Yanbaev, Y., Mader, M., Nürnberg, S., Schröder, H.,
2021b. Applying targeted genotyping by sequencing
with a new set of nuclear and plastid SNP and indel loci
for Quercus robur and Q. petraea. Conservation Gene-
tics Resources, 13 (2): 345–347. https://doi.org/10.1007/
s12686-021-01207-6
Degen, B., Yanbaev, Y., Ianbaev, R., Bakhtina, S., Tagiro-
va, A., 2021c. Genetic diversity and differentiation among
populations of the pedunculate oak (Quercus robur) at the
eastern margin of its range based on a new set of 95
SNP loci. Journal of Forestry Research, 32 (5): 2237–
2243. https://doi.org/10.1007/s11676-020-01265-w
Degen, B., Yanbaev, Y., Mader, M., Ianbaev, R., Bakhtina,
S., Schröder, H., Blanc-Jolivet, C., 2021d. Impact
of gene flow and introgression on the range-wide genetic
structure of Quercus robur (L.) in Europe. Forests, 12
(10): 1425. https://doi.org/10.3390/f12101425
Degen, B., Yanbaev, Y., Ianbaev, R., Blanc-Jolivet, C., Ma-
der, M., Bakhtina, S., 2022. Large-scale genetic struc-
ture of Quercus robur in its eastern distribution range
enables assignment of unknown seed sources. Forestry,
95 (4): 531–547. https://doi.org/10.1093/forestry/cpac009
Dyderski, M.K., Páz-Dyderska, S., Jagodziński, A.M., Pu-
chałka, R., 2025. Shifts in native tree species distri-
butions in Europe under climate change. Journal of
Environmental Management, 373: 123504. https://doi.
org/10.1016/j.jenvman.2024.123504
Ducousso, A. Bordacs, S., 2003. EUFORGEN Technical
Guidelines for genetic conservation and use for pedun-
culate and sessile oaks (Quercus robur and Q. petraea).
Rome: International Plant Genetic Resources Institute. 6 p.
Dumolin, S., Demesure, B., Petit, R.J., 1995. Inheritance of
chloroplast and mitochondrial genomes in pedunculate
oak investigated with an efficient PCR method. Theo-
retical and Applied Genetics, 91 (8): 1253–1256. https://
doi.org/10.1007/BF00220937
Eaton, E., Caudullo, G., Oliveira, S., de Rigo, D., 2016.
Quercus robur and Quercus petraea in Europe: distribution,
habitat, usage and threats. In San-Miguel-Ayanz, J.,
de Rigo, D., Caudullo, G., Durrant, T.H., Mauri, A.
(eds). European atlas of forest tree species. Luxembourg:
Publications Office of the European Union, p. e01c6df+
Ehrenmann, F., Jacques-Gustave, A., Labbé, T., Millox, M.,
Plomion, C., Raspail, F., Séverin, R., Soularue, J.-P.,
Kremer, A., 2014. Quercus portal: A web resource for
genetics and genomics of oaks. In Proceedings of the
IUFRO “Genetics of Fagaceae” (Bordeaux, 9–12 Oct 2012).
FAO, 2025a. The second report on the state of the world’s forest
genetic resources (SoW-FGR-2). Rome: FAO Commis-
sion on Genetic Resources for Food and Agriculture As-
sessments. 260 p.
FAO, 2025b. SilvaGRIS – Global information system on forest
genetic resources. Database version 1-2025. Rome:
Food and Agriculture Organization of the United Na-
tions. [cit. 2025-12-3]. https://www.fao.org/silvagris
Gailing, O., Wachter, H., Heyder, J., Schmitt, H.-P., Fin-
keldey, R., 2007. Chloroplast DNA analysis in oak stands
(Quercus robur L.) in North Rhine-Westphalia with pre-
sumably Slavonian origin: Is there an association be-
tween geographic origin and bud phenology? Journal of
Applied Botany and Food Quality, 81 (2): 165–171.
Gömöry, D., Yakovlev, I., Zhelev, P., Jedináková, J., Paule,
L., 2001. Genetic differentiation of oak populations
within the Quercus robur/Quercus petraea complex in
Central and Eastern Europe. Heredity, 86 (5): 557–563.
https://doi.org/10.1046/j.1365-2540.2001.00874.x
Gregorius, H.R., Degen, B., Konig, A., 2007. Problems
in the analysis of genetic differentiation among popu-
lations – a case study in Quercus robur. Silvae Genetica,
56 (3-4): 190–199.
Hall, M., Sunde, J., Franzén, M., Forsman, A., 2025.
Among-individual asynchrony but not genetic diversity
209
is associated with temporal stability of tree growth in
natural Quercus robur oak stands. Biology Letters, 21:
20250180. https://doi.org/10.1098/rsbl.2025.0180
Hoch, G., Stemmelen, A., Béla Eötvös, C., Hinterstoisser,
W., Lanšćak, M., Stojnić, S., Tóth, M., Westergren,
M., Zidar, S., Zlatković, M., Zoric, N., de Groot, M.,
2024. Infestation intensity by the invasive oak lace bug,
Corythucha arcuata (Say) in mixed and pure oak stands.
Journal of Applied Entomology, 148 (1): 26–33. https://
doi.org/10.1111/jen.13205
Hung, T.H., Formaggia, E., Morley, L., Kirby, K., Sal-
guero-Gómez, R., Sheldon, C.B., MacKay, J.J., 2025.
Genetic diversity and population structure of peduncu-
late oaks (Quercus robur) in Wytham Woods. Plants,
People, Planet, 7: 1789–1802. https://doi.org/10.1002/
ppp3.70042
Jeger, M., Bragard, C., Caffier, D., Candresse, T., Chat-
zivassiliou, E., Dehnen-Schmutz, K., Gilioli, G., Ja-
ques Miret, J.-A., Macleod, A., Navajas Navarro, M.,
Niere, B., Parnell, S., Potting, R., Rossi, V., Urek, G.,
Van Der Werf, W., West, J., Winter, J., Boberg, J.,
Gonthier, P., Pautasso, M., 2018. Pest categorisation
of Bretziella fagacearum. EFSA Journal, 16 (2): e5185.
https://doi.org/10.2903/j.efsa.2018.5185
JP Srbijašume, 2025. Cenovnik osnovnih proizvoda šumarstva
– drvnih sortimenata [Price of basic forestry products –
timber assortments] https://srbijasume.rs/ssume/wp-content/
uploads/2022/08/cenovnik-novi-od-27.08..pdf. (In Ser-
bian).
JP Vojvodinašume, 2025. Cenovnik drvnih sortimenata i os-
talog drveta za ogrev 2025 [Price of timber wood as-
sortments and other fuelwood]. https://www.vojvodina-
sume.rs/wp-content/uploads/2025/10/Cenovnik-drvnih-
sortimenata-i-ostalog-drveta-za-ogrev2025.pdf. (In Serbian).
Jurkšienė, G., Baranov, Y.O., Kagan, I.D., Kovalevič‑Ra-
zumova, A.O., Baliuckas, V., 2020. Genetic diversity
and differentiation of pedunculate (Quercus robur) and
sessile (Q. petraea) oaks. Journal of Forestry Research,
31 (6): 2445–2452. https://doi.org/10.1007/s11676-019-
01043-3
Kampfer, S., Lexer, C., Glössl, J., Steinkellner, H., 1998.
Characterization of (GA)n microsatellite loci from Quercus
robur. Hereditas, 129 (2): 183–186. https://doi.org/10.1111/
j.1601-5223.1998.00183.x
Katičić Bogdan, I., Kajba, D., Šatović, Z., Schüler, S., Bog-
dan, S., 2018. Genetic diversity of pedunculate oak
(Quercus robur L.) in clonal seed orchards in Croatia,
assessed by nuclear and chloroplast microsatellites.
South-east European Forestry, 9: 29–46. https://doi.
org/10.15177/seefor.18-09
Kesić, L., Cseke, K., Orlović, S., Stojanović, D.B., Kostić,
S., Benke, A., Borovics, A., Stojnić, S., Avramidou,
E.V., 2021. Genetic diversity and differentiation of pe-
dunculate oak (Quercus robur L.) populations at the
southern margin of its distribution range–Implications
for conservation. Diversity, 13 (8): 371. https://doi.org/
10.3390/d13080371
Korte, A., Farlow, A., 2013. The advantages and limitations
of trait analysis with GWAS: a review. Plant Methods,
9: 29. https://doi.org/10.1186/1746-4811-9-29
Kremer, A., HIPP, A.L., 2020. Oaks: an evolutionary success
story. New Phytologist, 226 (4): 981–1011. https://doi.org/
10.1111/nph.16274
Kremer, A., Delcamp, A., Lesur, I., Wagner, S., Rellstab, C.,
Guichoux, E., Leroy, T., 2024. Whole-genome screen-
ing for near-diagnostic genetic markers for four western
European white oak species identification. Annals of
Forest Science, 81: 21. https://doi.org/10.1186/s13595-
024-01236-9
Landekić, M., Troha, J., Bakarić, M., 2024. Studij slučaja
javnih nadmetanja prodaje drvnih sortimenata 2022.
godine u Hrvatskoj i Sloveniji [Case study of 2022 pub-
lic auctions for timber assortment sales in Croatia and
Slovenia]. Šumarski List, 1-2: 71–82. https://doi.org/
10.31298/sl.148.1-2.7. (In Croatian).
Le Corre, V., Kremer, A., 2012. The genetic differentiation
at quantitative trait loci under local adaptation. Molecu-
lar Ecology, 21 (7): 1548–1566. https://doi.org/10.1111/
j.1365-294x.2012.05479.x
Lefort, F., Lally, M., Thompson, D., Douglas, G.C., 1998.
Morphological traits, microsatellite fingerprinting and
genetic relatedness of a stand of elite oaks (Q. robur L.)
at Tullynally, Ireland. Silvae Genetica, 47 (5): 257–261.
Lenk, A., Waha, S., Wirth, C., 2025. Elevated tree mortality
as a regeneration niche for oak? Testing different mana-
gement approaches in a meliorated floodplain forest.
Forest Ecology and Management, 586: 122678. https://
doi.org/10.1016/j.foreco.2025.122678
Lepais, O., Léger, V., Gerber, S., 2006. Short note: high
throughput microsatellite genotyping in oak species. Sil-
vae Genetica, 55 (1-6): 238–240.
Leroy, T., Roux, C., Villate, L., Bodénès, C., Romiguier, J.,
Paiva, J.A., Dossat, C., Aury, J-M., Plomion, C., Kremer,
A., 2017. Extensive recent secondary contacts between four
European white oak species. New Phytologist, 214 (2):
865–878. https://doi.org/10.1111/nph.14413
Leroy, T., Louvet, J.-M., Lalanne, C., Le Provost, G., Laba-
die, K., Aury, J.-M., Delzon, S., Plomion, C., Kremer,
A., 2020a. Adaptive introgression as a driver of local adap-
tation to climate in European white oaks. New Phytolo-
gist, 226 (4): 1171–1182. https://doi.org/10.1111/nph.16095
Leroy, T., Roux, C., Villate, L., Bodénès, C., Romiguier,
J., Paiva, J.A.P., Dossat, C., Aury, J.-M., Plomion, C.,
Kremer, A., 2020b. Massive post-glacial gene flow be-
tween European white oaks. New Phytologist, 226 (4):
1183–1197. https://doi.org/10.1111/nph.16039
Lesur, I., Rogier, O., Sow, M.D., Boury, C., Duplan, A.,
Garnier, A., Maury, S., 2024. A strategy for studying
epigenetic diversity in natural populations: proof of con-
cept in poplar and oak. Journal of Experimental Botany,
75 (18): 5568–5584. https://doi.org/10.1093/jxb/erae266
Lesur, I., Le Provost, G., Bento, P., Da Silva, C., Leplé,
J.-C., Murat, F., Ueno, S., Bartholomé, J., Lalanne,
C., Ehrenmann, F., Noirot, C., Burban, C., Léger, V.,
Amselem, J., Belser, C., Quesneville, H., Stierschnei-
der, M., Fluch, S., Feldhahn, L., Tarkka, M., Herr-
mann, S., Buscot, F., Klopp, C., Kremer, A., Salse, J.,
Aury, J.-M., Plomion, C., 2015. The oak gene expres-
sion atlas: insights into Fagaceae genome evolution and
the discovery of genes regulated during bud dormancy
release. BMC Genomics, 16 (1): 112. https://doi.org/
10.1186/s12864-015-1331-9
Liang, Y.Y., Liu, H., Lin, Q.Q., Shi, Y., Zhou, B.F., Wang,
J.S., Wang, B., 2025. Pan-genome analysis reveals local
adaptation to climate driven by introgression in oak
species. Molecular Biology and Evolution, 42 (5): msaf088.
https://doi.org/10.1093/molbev/msaf088
Lobo, A., Doonan, J.M., Hansen, J.K., Kosawang, C., Xu,
210
J., Olofsson, J.K., KjÆr, E.D., 2026. Genomic predic-
tion of superior heartwood traits in pedunculate oak
(Quercus robur L.) using GWAS-informed Bayesian
models. Forest Ecology and Management, 609: 123644.
https://doi.org/10.1016/j.foreco.2026.123644
Löf, M., Brunet, J., Filyushkina, A., Lindbladh, M., Skov-
sgaard, J.P., Felton, A., 2015. Management of oak
forests: striking a balance between timber production,
biodiversity and cultural services. International Journal
of Biodiversity Science, Ecosystem Services and Mana-
gement, 12 (1-2): 59–73. https://doi.org/10.1080/21513
732.2015.1120780
Marçais, B., Desprez-Loustau, M.L., 2014. European oak
powdery mildew: impact on trees, effects of environ-
mental factors, and potential effects of climate change.
Annals of Forest Science, 71 (6): 633–642. https://doi.
org/10.1007/s13595-012-0252-x
Mariette, S., Cottrell, J., Csaikl, U.M., Goikoechea, P.,
Konig, A., Lowe, A. J., Van Dam, B.C., Barreneche,
T., Bodénès, C., Streiff, R., Burg, K., Groppe, K., Mun-
ro, R.C., Tabbener, H., Kremer, A., 2002. Comparison
of levels of genetic diversity detected with AFLP and
microsatellite markers within and among mixed Q. pet-
raea (Matt.) Liebl. and Q. robur L. stands. Silvae Geneti-
ca, 51 (2-3): 72–79.
Meger, J., Ulaszewski, B., Chmura, D.J., Burczyk, J., 2024.
Signatures of local adaptation to current and future cli-
mate in phenology-related genes in natural populations
of Quercus robur. BMC Genomics, 25 (1): 78. https://
doi.org/10.1186/s12864-023-09897-y
Müller-Starck, G., Herzog, S., Hattemer, H.H., 1993.
Intra-and interpopulational genetic variation in juvenile
populations of Quercus robur L. and Quercus petraea
Liebl. Annales des Sciences Forestières, 50: 233–244.
https://doi.org/10.1051/forest:19930723
Muir, G., Schlötterer, C., 2005. Evidence for shared an-
cestral polymorphism rather than recurrent gene flow
at microsatellite loci differentiating two hybridizing oaks
(Quercus spp.). Molecular Ecology, 14: 549–561. https://
doi.org/10.1111/j.1365-294x.2004.02418.x
Neophytou, C., 2014. Bayesian clustering analyses for ge-
netic assignment and study of hybridization in oaks:
Effects of asymmetric phylogenies and asymmetric
sampling schemes. Tree Genetics and Genomes, 10:
273–285. https://doi.org/10.1007/s11295-013-0680-2
Neophytou, C., Aravanopoulos, F.A., Fink, S., Dounavi, A.,
2010. Detecting interspecific and geographic differenti-
ation patterns in two interfertile oak species (Quercus
petraea (Matt.) Liebl. and Q. robur L.) using small sets
of microsatellite markers. Forest Ecology and Manage-
ment, 259: 2026–2035. https://doi.org/10.1016/j.foreco.
2010.02.013
Neophytou, C., Gärtner, S.M., Vargas-Gaete, R., Michiels,
H.-G., 2015. Genetic variation of Central European oaks:
shaped by evolutionary factors and human intervention?
Tree Genetics and Genomes, 11: 79. https://doi.org/10.
1007/s11295-015-0905-7
Pakull, B., Degen, B., Schroeder, H., Riedel, T., Mader,
M., Liesebach, H., Hoffmann, P., Hoppe, S., Euse-
mann, P., 2025. Hybridization, spatial genetic structure
and potential environmental preadaptation in Quercus
robur and Quercus petraea in Germany – results from the
4th National Forest Inventory. Tree Genetics and Geno-
mes, 21 (2): 11. https://doi.org/10.1007/s11295-025-01695-9
Parelle, J., Zapater, M., Scotti-Saintagne, C., Kremer, A.,
Jolivet, Y., Dreyer, E., Brendel, O., 2007. Quanti-
tative trait loci of tolerance to waterlogging in a Euro-
pean oak (Quercus robur L.): Physiological relevance
and temporal effect patterns. Plant, Cell and Environ-
ment, 30 (4): 422–434.
Petit, R.J., Brewer, S., Bordács, S., Burg, K., Cheddadi,
R., Coart, E., Cottrell, J., Csaikl, U.M., van Dam, B.,
Deans, J.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., 2002.
Identification of refugia and post-glacial colonisation
routes of European white oaks based on chloroplast
DNA and fossil pollen evidence. Forest Ecology and
Management, 156 (1-3): 49–74. https://doi.org/10.1016/
S0378-1127(01)00634-X
Petit, R.J., Hampe, A., 2006. Some evolutionary consequen-
ces of being a tree. Annual Review of Ecology, Evolution,
and Systematics, 37 (1): 187–214. https://doi.org/10.1146/
annurev.ecolsys.37.091305.110215
Plomion, C., Aury, J.-M., Amselem, J., Leroy, T., Murat, F.,
Duplessis, S., Faye, S., Francillonne, N., Labadie, K.,
Le Provost, G., Lesur, I., Bartholomé, J., Faivre-Ram-
pant, P., Kohler, A., Leplé, J.-C., Chantret, N., Chen,
J., Diévart, A., Alaeitabar, T., Barbe, V., Belser, C.,
Bergès, H., Bodénès, C., Bogeat-Triboulot, M.-B.,
Bouffaud, M.-L., Brachi, B., Chancerel, E., Cohen,
D., Couloux, A., Da Silva, C., Dossat, C., Ehrenmann,
F., Gaspin, C., Grima-Pettenati, J., Guichoux, E.,
Hecker, A., Herrmann, S., Hugueney, P., Hummel, I.,
Klopp, C., Lalanne, C., Lascoux, M., Lasserre, E.,
Lemainque, A., Desprez-Loustau, M.-L., Luyten, I.,
Madoui, M.-A., Mangenot, S., Marchal, C., Maumus,
F., Mercier, J., Michotey, C., Panaud, O., Picault, N.,
Rouhier, N., Rué, O., Rustenholz, C., Salin, F., So-
ler, M., Tarkka, M., Velt, A., Zanne, A. E., Martin,
F., Wincker, P., Quesneville, H., Kremer, A., Salse,
J., 2018. Oak genome reveals facets of long lifespan.
Nature Plants, 4: 440–452. https://doi.org/10.1038/
s41477-018-0172-3
Popović, M., Katičić Bogdan, I., Varga, F., Šatović, Z.,
Bogdan, S., Ivanković, M., 2023. Genetic diversity in
peripheral pedunculate oak (Quercus robur L.) prove-
nances - potential climate change mitigators in the cen-
ter of distribution despite challenges in natural popu-
lations. Forests, 14 (12): 2290. https://doi.org/10.3390/
f14122290
Rellstab, C., Bühler, A., Graf, R., Folly, C., Gugerli, F.,
2016. Using joint multivariate analyses of leaf morpholo-
gy and molecular-genetic markers for taxon identifica-
tion in three hybridizing European white oak species
(Quercus spp.). Annals of Forest Science, 73 (3): 669–
679. https://doi.org/10.1007/s13595-016-0552-7
Saintagne, C., Bodénès, C., Barreneche, T., Pot, D., Plo-
mion, C., Kremer, A., 2004. Distribution of genomic
regions differentiating oak species assessed by QTL
detection. Heredity, 92 (1): 20–30. https://doi.org/10.1038/
sj.hdy.6800358
Sallmannshofer, M., Chakraborty, D., Vacik, H., Illés, G.,
Löw, M., Rechenmacher, A., Lapin, K., Ette, S., Stoja-
nović, D., Kobler, A., Schueler, S., 2021. Continent-
wide tree species distribution models may mislead re-
211
gional management decisions: a case study in the trans-
boundary Biosphere Reserve Mura-Drava-Danube. Forests,
12: 330. https://doi.org/10.3390/f12030330
Sanchez-Lucas, R., He, J., Chirico, M., Bosanquet, J.L.,
Lehner, A.A.B., Oyesola, K.S., Hart, K., Macken-
zie, R.A., Luna, E., Catoni, M., 2025 (preprint). Epigeno-
mic landscape of oak (Quercus robur) across seasons
and generations [preprint]. bioRxiv. https://doi.org/10.1101/
2025.11.14.688509
Sandurska, E., Ulaszewski, B., Burczyk, J., 2019. Genetic
diversity and differentiation of coexisting populations of
Quercus robur L. and Q. petraea (Matt.) Liebl. Acta Bio-
logica Cracoviensia. Series Botanica, 61 (1): 17–28.
https://doi.org/10.24425/abcsb.2019.127739
Sanduska, E., Ulaszewski, B., Meyza, K., Sztupecka, E.,
Burczyk, J., 2024. Factors determining fine-scale spatial
genetic structure within coexisting populations of com-
mon beech (Fagus sylvatica L.), pedunculate oak (Quer-
cus robur L.), and sessile oak (Q. petraea (Matt.) Liebl.).
Annals of Forest Science, 81: 3. https://doi.org/10.1186/
s13595-023-01217-4
Scotti-Saintagne, C., Mariette, S., Porth, I., Goicoechea,
P. G., Barreneche, T., Bodénes, C., Burg, K., Kremer,
A., 2004a. Genome scanning for interspecific differentia-
tion between two closely related oak species [Quercus
robur L. and Q. petraea (Matt.) Liebl.]. Genetics, 168 (3):
1615–1626. https://doi.org/10.1534/genetics.104.026849
Scotti-Saintagne, C., Bodénès, C., Barreneche, T., Ber-
tocchi, E., Plomion, C., Kremer, A., 2004b. Detection
of quantitative trait loci controlling bud burst and height
growth in Quercus robur L. Theoretical and Applied Ge-
netics, 109 (8): 1648–1659. https://doi.org/10.1007/s00122-
004-1789-3
Sergeant, K., Spiess, N., Renaut, J., Wilhelm, E., Hausman,
J.F., 2011. One dry summer: a leaf proteome study on
the response of oak to drought exposure. Journal of Pro-
teomics, 74 (8): 1385–1395. https://doi.org/10.1016/j.
jprot.2011.03.011
Siegismund, H.R., Jensen, J.S., 2001. Intrapopulation and in-
terpopulation genetic variation of Quercus in Denmark.
Scandinavian Journal of Forest Research, 16 (2): 103–116.
https://doi.org/10.1080/028275801300088143
Spiess, N., Oufir, M., Matušíková, I., Stierschneider, M.,
Kopecky, D., Homolka, A., Burg, K., Fluch, S., Haus-
man, J.-F., Wilhelm, E., 2012. Ecophysiological and
transcriptomic responses of oak (Quercus robur) to long-
term drought exposure and rewatering. Environmental
and Experimental Botany, 77: 117–126. https://doi.org/
10.1016/j.envexpbot.2011.11.010
Steinkellner, H., Fluch, S., Turetschek, E., Lexer, C.,
Streiff, R., Kremer, A., Burg, K., Glössl, J., 1997.
Identification and characterization of (GA/CT)n – micro-
satellite loci from Quercus petraea. Plant Molecular
Biology, 33 (6): 1093–1096. https://doi.org/10.1023/
A:1005736722794
Stierschneider, M., Gaubitzer, S., Johanna, S., Weichsel-
baum, O., Kopecký, D., Kremer, A., Fluch, S., Molin,
E.M., 2016. The EVOLTREE Repository Centre: a cen-
tral access point for reference material and data of forest
genetic resources. In Kremer, A., Heyes, S., González-
Martínez, C. (eds). Evolution of trees and forest com-
munities: ten years of the EVOLTREE network. PG Edi-
tion, p. 15–19.
Stojnić, S., Kovacević, B., Kebert, M., Vaštag, E., Bojović,
M., Stanković-Nedić, M., Orlović, S., 2019. The use
of physiological, biochemical and morpho-anatomical
traits in tree breeding for improved water-use efficiency
of Quercus robur L. Forest Systems, 28 (3): https://doi.
org/10.5424/fs/2019283-15233
Streiff, R., Labbe, T., Bacilieri, R., Steinkellner, H.,
Glössl, J., Kremer, A., 1998. Within‐population genetic
structure in Quercus robur L. and Quercus petraea (Matt.)
Liebl. assessed with isozymes and microsatellites. Mole-
cular Ecology, 7 (3): 317–328. https://doi.org/10.1046/
j.1365-294X.1998.00360.x
Temunović, M., Garnier-Géré, P., Morić, M., Franjić, J.,
Ivanković, M., Bogdan, S., Hampe, A., 2020. Candi-
date gene SNP variation in floodplain populations of pe-
dunculate oak (Quercus robur L.) near the species’ sou-
thern range margin: Weak differentiation yet distinct
associations with water availability. Molecular Ecology,
29: 2359–2378. https://doi.org/10.1111/mec.15492
Trudić, B., Avramidou, E., Fussi, B., Neophytou, C., Stoj-
nić, S., Pilipović, A., 2021a. Conservation of Quercus
robur L. genetic resources in its south-eastern refugium
using SSR marker system – a case study from Vojvodina
Province, Serbia. Austrian Journal of Forest Science,
138 (2): 117–140.
Trudić, B., Draškić, G., Le Provost, G., Stojnić, S., Pili-
pović, A., Ivezić, A., 2021b. Expression profiles of 11
candidate genes involved in drought tolerance of pe-
dunculate oak (Quercus robur L.). Possibilities for ge-
netic monitoring of the species. Silvae Genetica, 70 (2):
226–234. https://doi.org/10.2478/sg-2021-0020
Trudić, B., Stojnić, S., Avramidou, E. V., Malliarou, E.,
Ivezić, A., Bojović, M., Pilipović, A., 2024. Recent
global (bio)technological advancements in the service
of forest genetic resources protection under climate
change. Topola, 213: 17–31. https://doi.org/10.5937/
topola2413017T
Utkina, I.A., Rubtsov, V.V., 2017. Studies of phenological
forms of pedunculate oak. Contemporary Problems
of Ecology, 10: 804–811. https://doi.org/10.1134/S199542
5517070101
Vakkari, P., Blom, A., Rusanen, M., Raisio, J., Toivonen, H.,
2006. Genetic variability of fragmented stands of pe-
dunculate oak (Quercus robur) in Finland. Genetica,
127 (1): 231–241. https://doi.org/10.1007/s10709-005-
4014-7
Vakkari, P., Rusanen, M., Heikkinen, J., Huotari, T., Kär-
kkäinen, K., 2020. Patterns of genetic variation in leading-
edge populations of Quercus robur: genetic patchiness
due to family clusters. Tree Genetics and Genomes, 16
(5): 73. https://doi.org/10.1007/s11295-020-01465-9
Vastag, E., Cocozza, C., Orlović, S., Kesić, L., Kresoja,
M., Stojnić, S., 2020. Half-sib lines of pedunculate
oak (Quercus robur L.) respond differently to drought
through biometrical, anatomical and physiological traits.
Forests, 11 (2): 153. https://doi.org/10.3390/f11020153
Vranckx, G.U.Y., Jacquemyn, H., Muys, B., Honnay, O.,
2012. Meta‐analysis of susceptibility of woody plants to
loss of genetic diversity through habitat fragmentation.
Conservation Biology, 26 (2): 228–237. https://doi.org/
10.1111/j.1523-1739.2011.01778.x
Vranckx, G., Jacquemyn, H., Mergeay, J., Cox, K., Kint,
V., Muys, B., Honnay, O., 2014a. Transmission of ge-
netic variation from the adult generation to naturally es
tablished seedling cohorts in small forest stands of pe-
212
dunculate oak (Quercus robur L.). Forest Ecology and
Management, 312: 19–27. https://doi.org/10.1016/j.foreco.
2013.10.027
Vranckx, G., Mergeay, J., Cox, K., Muys, B., Jacquemyn,
H., Honnay, O., 2014b. Tree density and population
size affect pollen flow and mating patterns in small frag-
mented forest stands of pedunculate oak (Quercus robur
L.). Forest Ecology and Management, 328: 254–261.
https://doi.org/10.1016/j.foreco.2014.05.044
Yakovlev, I.A., Kleinschmit, J., 2002. Genetic differentiation
of pedunculate oak (Quercus robur L.) in the European
part of Russia based on RAPD markers. Russian Journal
of Genetics, 38 (2): 148–155. https://doi.org/10.1023/
A:1014330010233
Yücedağ, C., Gailing, O., 2013. Morphological and genetic
variation within and among four Quercus petraea and Q.
robur natural populations. Turkish Journal of Botany, 37
(4): 619–629. https://doi.org/10.3906/bot-1205-18
Zanetto, A., Roussel, G., Kremer, A., 1994. Geographic
variation of inter-specific differentiation between Quercus
robur L. and Quercus petraea (Matt.) Liebl. Forest Ge-
netics, 1 (2): 111–123.
Zlatković, M., Sallmannshofer, M., Schueler, S., Cech,
T.L., Djilas, M., Hoch, G., Lapin, K., Ogris, N., Piškur,
B., Schwanda, K., Stojnić, S., Westergren, M., Orlo-
vić, S., 2024. Tubakia spp., Didymella macrostoma and
Apiognomonia errabunda causing leaf spot and anthrac-
nose of Quercus robur in the Mura-Drava-Danube Bio-
sphere Reserve. Frontiers in Forests and Global Change,
7: 1363141. https://doi.org/10.3389/ffgc.2024.1363141
Zlatković, M., Wingfield, M.J., Jami, F., Slippers, B., 2018.
Host specificity of co-infecting Botryosphaeriaceae on
ornamental and forest trees in the Western Balkans. Forest
Pathology, 48: e12410. https://doi.org/10.1111/efp.12410
Żukowska, W.B., Wawrzyniak, M.K., Lewandowski, A.,
Suszka, J., Chmielarz, P., 2025. Long-term storage
does not affect the genetic diversity of pedunculate oak
acorns; instead, the collection process is crucial. Forest
Ecology and Management, 585: 122664. https://doi.org/
10.1016/j.foreco.2025.122664
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