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Insights into drought adaptation of two European oak species revealed by nucleotide diversity of candidate genes

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Abstract

Nucleotide diversity, correlations to environmental conditions, and deviations from standard neutral models were examined in eight candidate genes for drought response of European oaks Quercus petraea and Quercus robur. Baseline genetic parameters were calculated and deviation from neutrality was tested using Tajima’s D, and Fu and Li’s D and F statistics. Population structure was investigated using differentiation indices and Bayesian clustering. Similar values of total nucleotide diversity were found in both species with significant higher diversity at non-synonymous sites in Q. robur while the number of haplotypes was significantly higher in Q. petraea. Significant population differentiation was found for three genes in Q. petraea and for one gene in Q. robur. Within four genes, strong correlations were found between the local temperature–precipitation regime and the allele frequencies of six alleles, of which three were private to Q. petraea. Using various population genetic and Bayesian tests for neutrality, four outlier single nucleotide polymorphisms (SNPs) under putative selection were detected in two of the analyzed genes. Significant differentiation and strong allelic correlation to environmental conditions support preceding gene expression profiling experiments, where functional impact of candidate genes in drought response has been revealed. Q. petraea populations were found to be more differentiated as compared to Q. robur—this could be linked to the higher adaptive potential of this species under arid conditions.

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Acknowledgments

The project was funded by the Austrian Federal Ministry of Agriculture, Forestry, Environment and Water Management (LE 2109 GZ LE.3.2.3/0014-IV 2/2005), the Regional Office of Vienna, the Regional Office of Lower Austria (BD1 NU94-2005, LF2-FO-7059/001-05, LF4-A-25/009-2004), the Regional Office of Upper Austria, the Regional Office of Styria (A3-36E4-05/2), and the Regional Office of Burgenland.

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Correspondence to Andreas Homolka.

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Communicated by P. Ingvarsson

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Online Resource 1

Geographical and climatological data of Quercus petraea and Quercus robur sample populations (XLS 76 kb)

Online Resource 2

Allele-specific primers for SNP verification showing primer sequences, location of targeted SNPs, and results of genotyping in a set of four individuals (XLS 39 kb)

Online Resource 3

Nucleotide diversity measures of eight candidate genes for drought response in Quercus petraea (104 individuals) and Quercus robur (105 individuals) (XLS 46 kb)

Online Resource 4

Results of population differentiation tests (F ST) applied to eight candidate genes for drought response in Quercus petraea and Quercus robur (XLS 46 kb)

Online Resource 5

Results of Bayesian clustering implemented in BAPS using mixture of groups of populations mode with a candidate genes and b neutral chloroplast microsatellites. Numbers correspond to the seven distinct climatic regions, ordered by decreasing HMIV (annual heat moisture index during vegetative periods). Regions with the same color belong to one cluster. (JPEG 217 kb)

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(EPS 1111 kb)

Online Resource 6

Results of different neutrality tests applied to eight candidate genes for drought response in Quercus petraea and Quercus robur (XLS 37 kb)

Online Resource 7

Overview of outlier SNP loci detected in eight candidate genes for drought response in Quercus petraea and Quercus robur using three different computation methods (fDist, BayeScan, and Arlequin). Exchanges between base triplets caused by the outlier SNP are shown. Outlier loci detected by more than one method are displayed in red color. (XLS 39 kb)

Online Resource 8

Correlation between the frequency of Quercus petraea private alleles (found in genes ERD8 and LEA14) and heat–moisture index as given by Spearman’s rank coefficient. Black bars show strong correlations (|r>0.39|) (JPEG 347 kb)

High resolution images

(EPS 1419 kb)

Online Resource 9

Correlation coefficients between private or shared alleles and HMIV (annual heat moisture index during vegetative periods). Strong correlations (|r>0.39|) are shown in red color, and blue color denotes differences in correlation coefficients between species higher than 0.25 (XLS 58 kb)

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Homolka, A., Schueler, S., Burg, K. et al. Insights into drought adaptation of two European oak species revealed by nucleotide diversity of candidate genes. Tree Genetics & Genomes 9, 1179–1192 (2013). https://doi.org/10.1007/s11295-013-0627-7

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