Genomic prediction of resistance to Hymenoscyphus fraxineus in common ash (Fraxinus excelsior L.) populations.

The increase in introduced insect pests and pathogens due to anthropogenic environmental changes has become a major concern for tree species worldwide. Common ash (Fraxinus excelsior L.) is one of such species facing a significant threat from the invasive fungal pathogen Hymenoscyphus fraxineus. Some studies have indicated that the susceptibility of ash to the pathogen is genetically determined, providing some hope for accelerated breeding programs that are aimed at increasing the resistance of ash populations. To address this challenge, we used a genomic selection strategy to identify potential genetic markers that are associated with resistance to the pathogen causing ash dieback. Through genome-wide association studies (GWAS) of 300 common ash individuals from 30 populations across Poland (ddRAD, dataset A), we identified six significant SNP loci with a p-value ≤1 × 10-4 associated with health status. To further evaluate the effectiveness of GWAS markers in predicting health status, we considered two genomic prediction scenarios. Firstly, we conducted cross-validation on dataset A. Secondly, we trained markers on dataset A and tested them on dataset B, which involved whole-genome sequencing of 20 individuals from two populations. Genomic prediction analysis revealed that the top SNPs identified via GWAS exhibited notably higher prediction accuracies compared to randomly selected SNPs, particularly with a larger number of SNPs. Cross-validation analyses using dataset A showcased high genomic prediction accuracy, predicting tree health status with over 90% accuracy across the top SNP sets ranging from 500 to 10,000 SNPs from the GWAS datasets. However, no significant results emerged for health status when the model trained on dataset A was tested on dataset B. Our findings illuminate potential genetic markers associated with resistance to ash dieback, offering support for future breeding programs in Poland aimed at combating ash dieback and bolstering conservation efforts for this invaluable tree species.

Relatives reproduce in synchrony: kinship and individual condition shape intraspecific variation in masting phenotype.

Masting (synchronous and interannually variable seed production) is frequently called a reproductive strategy; yet it is unclear whether the reproductive behaviour of individuals has a heritable component. To address this, we used 22 years of annual fruit production data from 110 Sorbus aucuparia L. trees to examine the contributions of genetic factors to the reproductive phenotype of individuals, while controlling for environmental variation. Trees sharing close genetic relationships and experiencing similar habitat conditions exhibited similar levels of reproductive synchrony. Trees of comparable sizes displayed similar levels of year-to-year variation in fruiting, with relatedness contributing to this variation. External factors, such as shading, influenced the time intervals between years with abundant fruit production. The effects of genetic relatedness on the synchrony of reproduction among trees and on interannual variation provide long-awaited evidence that the masting phenotype is heritable, and can respond to natural selection.

Signatures of local adaptation to current and future climate in phenology-related genes in natural populations of Quercus robur.

BACKGROUND: Local adaptation is a key evolutionary process that enhances the growth of plants in their native habitat compared to non-native habitats, resulting in patterns of adaptive genetic variation across the entire geographic range of the species. The study of population adaptation to local environments and predicting their response to future climate change is important because of climate change. RESULTS: Here, we explored the genetic diversity of candidate genes associated with bud burst in pedunculate oak individuals sampled from 6 populations in Poland. Single nucleotide polymorphism (SNP) diversity was assessed in 720 candidate genes using the sequence capture technique, yielding 18,799 SNPs. Using landscape genomic approaches, we identified 8 FST outliers and 781 unique SNPs in 389 genes associated with geography, climate, and phenotypic variables (individual/family spring and autumn phenology, family diameter at breast height (DBH), height, and survival) that are potentially involved in local adaptation. Then, using a nonlinear multivariate model, Gradient Forests, we identified vulnerable areas of the pedunculate oak distribution in Poland that are at risk from climate change. CONCLUSIONS: The model revealed that pedunculate oak populations in the eastern part of the analyzed geographical region are the most sensitive to climate change. Our results might offer an initial evaluation of a potential management strategy for preserving the genetic diversity of pedunculate oak.

A novel synthesis of two decades of microsatellite studies on European beech reveals decreasing genetic diversity from glacial refugia.

Genetic diversity influences the evolutionary potential of forest trees under changing environmental conditions, thus indirectly the ecosystem services that forests provide. European beech (Fagus sylvatica L.) is a dominant European forest tree species that increasingly suffers from climate change-related die-back. Here, we conducted a systematic literature review of neutral genetic diversity in European beech and created a meta-data set of expected heterozygosity (He) from all past studies providing nuclear microsatellite data. We propose a novel approach, based on population genetic theory and a min-max scaling to make past studies comparable. Using a new microsatellite data set with unprecedented geographic coverage and various re-sampling schemes to mimic common sampling biases, we show the potential and limitations of the scaling approach. The scaled meta-dataset reveals the expected trend of decreasing genetic diversity from glacial refugia across the species range and also supports the hypothesis that different lineages met and admixed north of the European mountain ranges. As a result, we present a map of genetic diversity across the range of European beech which could help to identify seed source populations harboring greater diversity and guide sampling strategies for future genome-wide and functional investigations of genetic variation. Our approach illustrates how to combine information from several nuclear microsatellite data sets to describe patterns of genetic diversity extending beyond the geographic scale or mean number of loci used in each individual study, and thus is a proof-of-concept for synthesizing knowledge from existing studies also in other species. Supplementary Information: The online version contains supplementary material available at 10.1007/s11295-022-01577-4.

Phylogeny of Maleae (Rosaceae) Based on Complete Chloroplast Genomes Supports the Distinction of Aria, Chamaemespilus and Torminalis as Separate Genera, Different from Sorbus sp.

Several genera formerly contained within the genus Sorbus L. sensu lato have been proposed as separate taxa, including Aria, Chamaemespilus and Torminalis. However, molecular evidence for such distinctions are rather scarce. We assembled the complete chloroplast genome of Sorbus aucuparia, another representative of Sorbus s.s., and performed detailed comparisons with the available genomes of Aria edulis, Chamaemespilus alpina and Torminalis glaberrima. Additionally, using 110 complete chloroplast genomes of the Maleae representatives, we constructed the phylogenetic tree of the tribe using Maximum Likelihood methods. The chloroplast genome of S. aucuparia was found to be similar to other species within Maleae. The phylogenetic tree of the Maleae tribe indicated that A. edulis, C. alpina and T. glaberrima formed a concise group belonging to a different clade (related to Malus) than the one including Sorbus s.s. (related to Pyrus). However, Aria and Chamaemespilus appeared to be more closely related to each other than to Torminalis. Our results provide additional support for considering Aria, Chamaemespilus and Torminalis as separate genera different from Sorbus s.s.

Complete Chloroplast Genomes of Fagus sylvatica L. Reveal Sequence Conservation in the Inverted Repeat and the Presence of Allelic Variation in NUPTs.

Growing amounts of genomic data and more efficient assembly tools advance organelle genomics at an unprecedented scale. Genomic resources are increasingly used for phylogenetic analyses of many plant species, but are less frequently used to investigate within-species variability and phylogeography. In this study, we investigated genetic diversity of Fagus sylvatica, an important broadleaved tree species of European forests, based on complete chloroplast genomes of 18 individuals sampled widely across the species distribution. Our results confirm the hypothesis of a low cpDNA diversity in European beech. The chloroplast genome size was remarkably stable (158,428 ± 37 bp). The polymorphic markers, 12 microsatellites (SSR), four SNPs and one indel, were found only in the single copy regions, while inverted repeat regions were monomorphic both in terms of length and sequence, suggesting highly efficient suppression of mutation. The within-individual analysis of polymorphisms showed >9k of markers which were proportionally present in gene and non-gene areas. However, an investigation of the frequency of alternate alleles revealed that the source of this diversity originated likely from nuclear-encoded plastome remnants (NUPTs). Phylogeographic and Mantel correlation analysis based on the complete chloroplast genomes exhibited clustering of individuals according to geographic distance in the first distance class, suggesting that the novel markers and in particular the cpSSRs could provide a more detailed picture of beech population structure in Central Europe.

Genomic signatures of natural selection at phenology-related genes in a widely distributed tree species Fagus sylvatica L.

BACKGROUND: Diversity among phenology-related genes is predicted to be a contributing factor in local adaptations seen in widely distributed plant species that grow in climatically variable geographic areas, such as forest trees. European beech (Fagus sylvatica L.) is widespread, and is one of the most important broadleaved tree species in Europe; however, its potential for adaptation to climate change is a matter of uncertainty, and little is known about the molecular basis of climate change-relevant traits like bud burst. RESULTS: We explored single nucleotide polymorphisms (SNP) at candidate genes related to bud burst in beech individuals sampled across 47 populations from Europe. SNP diversity was monitored for 380 candidate genes using a sequence capture approach, providing 2909 unlinked SNP loci. We used two complementary analytical methods to find loci significantly associated with geographic variables, climatic variables (expressed as principal components), or phenotypic variables (spring and autumn phenology, height, survival). Redundancy analysis (RDA) was used to detect candidate markers across two spatial scales (entire study area and within subregions). We revealed 201 candidate SNPs at the broadest scale, 53.2% of which were associated with phenotypic variables. Additive polygenic scores, which provide a measure of the cumulative signal across significant candidate SNPs, were correlated with a climate variable (first principal component, PC1) related to temperature and precipitation availability, and spring phenology. However, different genotype-environment associations were identified within Southeastern Europe as compared to the entire geographic range of European beech. CONCLUSIONS: Environmental conditions play important roles as drivers of genetic diversity of phenology-related genes that could influence local adaptation in European beech. Selection in beech favors genotypes with earlier bud burst under warmer and wetter habitats within its range; however, selection pressures may differ across spatial scales.

A Chromosome-Level Genome Assembly of the European Beech (Fagus sylvatica) Reveals Anomalies for Organelle DNA Integration, Repeat Content and Distribution of SNPs.

The European Beech is the dominant climax tree in most regions of Central Europe and valued for its ecological versatility and hardwood timber. Even though a draft genome has been published recently, higher resolution is required for studying aspects of genome architecture and recombination. Here, we present a chromosome-level assembly of the more than 300 year-old reference individual, Bhaga, from the Kellerwald-Edersee National Park (Germany). Its nuclear genome of 541 Mb was resolved into 12 chromosomes varying in length between 28 and 73 Mb. Multiple nuclear insertions of parts of the chloroplast genome were observed, with one region on chromosome 11 spanning more than 2 Mb which fragments up to 54,784 bp long and covering the whole chloroplast genome were inserted randomly. Unlike in Arabidopsis thaliana, ribosomal cistrons are present in Fagus sylvatica only in four major regions, in line with FISH studies. On most assembled chromosomes, telomeric repeats were found at both ends, while centromeric repeats were found to be scattered throughout the genome apart from their main occurrence per chromosome. The genome-wide distribution of SNPs was evaluated using a second individual from Jamy Nature Reserve (Poland). SNPs, repeat elements and duplicated genes were unevenly distributed in the genomes, with one major anomaly on chromosome 4. The genome presented here adds to the available highly resolved plant genomes and we hope it will serve as a valuable basis for future research on genome architecture and for understanding the past and future of European Beech populations in a changing climate.

A reference genome of the European beech (Fagus sylvatica L.).

Background: The European beech is arguably the most important climax broad-leaved tree species in Central Europe, widely planted for its valuable wood. Here, we report the 542 Mb draft genome sequence of an up to 300-year-old individual (Bhaga) from an undisturbed stand in the Kellerwald-Edersee National Park in central Germany. Findings: Using a hybrid assembly approach, Illumina reads with short- and long-insert libraries, coupled with long Pacific Biosciences reads, we obtained an assembled genome size of 542 Mb, in line with flow cytometric genome size estimation. The largest scaffold was of 1.15 Mb, the N50 length was 145 kb, and the L50 count was 983. The assembly contained 0.12% of Ns. A Benchmarking with Universal Single-Copy Orthologs (BUSCO) analysis retrieved 94% complete BUSCO genes, well in the range of other high-quality draft genomes of trees. A total of 62,012 protein-coding genes were predicted, assisted by transcriptome sequencing. In addition, we are reporting an efficient method for extracting high-molecular-weight DNA from dormant buds, by which contamination by environmental bacteria and fungi was kept at a minimum. Conclusions: The assembled genome will be a valuable resource and reference for future population genomics studies on the evolution and past climate change adaptation of beech and will be helpful for identifying genes, e.g., involved in drought tolerance, in order to select and breed individuals to adapt forestry to climate change in Europe. A continuously updated genome browser and download page can be accessed from beechgenome.net, which will include future genome versions of the reference individual Bhaga, as new sequencing approaches develop.