Local adaptation is key for ecotypic differentiation and species evolution. Understanding underlying genomic patterns can allow the prediction of future maladaptation and ecosystem stability. Here, we report the whole-genome resequencing of 874 individuals from 100 range-wide populations of European beech (Fagus sylvatica L.), an important forest tree species in Europe. We show that genetic variation closely mirrors geography with a clear pattern of isolation-by-distance. Genome-wide analyses for genotype-environment associations (GEAs) identify relatively few potentially adaptive variants after correcting for an overwhelming signal of statistically significant but non-causal GEAs. We characterize the single high confidence genomic region and pinpoint a candidate gene possibly involved in winter temperature adaptation via modulation of spring phenology. Surprisingly, allelic variation at this locus does not result in any apparent fitness differences in a common garden. More generally, reciprocal transplant experiments across large climate distances suggest extensive phenotypic plasticity. Nevertheless, we find indications of polygenic adaptation which may be essential in natural ecosystems. This polygenic signal exhibits broad- and fine-scale variation across the landscape, highlighting the relevance of spatial resolution. In summary, our results emphasize the importance, but also exemplify the complexity, of employing natural genetic variation for forest conservation under climate change.

Adaptive divergence is widely accepted as a contributor to speciation and the maintenance of species integrity. However, the mechanisms leading to reproductive isolation, the genes involved in adaptive divergence, and the traits that shape the adaptation of wild species to changes in climate are still largely unknown. In studying the role of ecological interactions and environment-driven selection, trees have emerged as potential model organisms because of their longevity and large genetic diversity, especially in natural habitats. Due to recurrent gene flow among species with different ecological preferences, oaks arose as early as the 1970s as a model for understanding how speciation can occur in the face of interspecific gene flow, and what we mean by “species” when geographically and genomically heterogeneous introgression seems to undermine species’ genetic coherence. In this review, we provide an overview of recent research into the genomic underpinnings of adaptive divergence and maintenance of species integrity in oaks in the face of gene flow. We review genomic and analytical tools instrumental to better understanding mechanisms leading to reproductive isolation and environment-driven adaptive introgression in oaks. We review evidence that oak species are genomically coherent entities, focusing on sympatric populations with ongoing gene flow, and discuss evidence for and hypotheses regarding genetic mechanisms linking adaptive divergence and reproductive isolation. As the evolution of drought- and freezing-tolerance have been key to the parallel diversification of oaks, we investigate the question of whether the same or a similar set of genes are involved in adaptive divergence for drought and stress tolerance across different taxa and sections. Finally, we propose potential future research directions on the role of hybridization and adaptive introgression in adaptation to climate change.

Northern red oak (Quercus rubra L.) is an ecologically and economically important forest tree native to North America. We present a chromosome-scale genome of Q. rubra generated by the combination of PacBio sequences and chromatin conformation capture (Hi-C) scaffolding. This is the first reference genome from the red oak clade (section Lobatae). The Q. rubra assembly spans 739 Mb with 95.27% of the genome in 12 chromosomes and 33,333 protein-coding genes. Comparisons to the genomes of Quercus lobata and Quercus mongolica revealed high collinearity, with intrachromosomal structural variants present. Orthologous gene family analysis with other tree species revealed that gene families associated with defense response were expanding and contracting simultaneously across the Q. rubra genome. Quercus rubra had the most CC-NBS-LRR and TIR-NBS-LRR resistance genes out of the 9 species analyzed. Terpene synthase gene family comparisons further reveal tandem gene duplications in TPS-b subfamily, similar to Quercus robur. Phylogenetic analysis also identified 4 subfamilies of the IGT/LAZY gene family in Q. rubra important for plant structure. Single major QTL regions were identified for vegetative bud break and marcescence, which contain candidate genes for further research, including a putative ortholog of the circadian clock constituent cryptochrome (CRY2) and 8 tandemly duplicated genes for serine protease inhibitors, respectively. Genome–environment associations across natural populations identified candidate abiotic stress tolerance genes and predicted performance in a common garden. This high-quality red oak genome represents an essential resource to the oak genomic community, which will expedite comparative genomics and biological studies in Quercus species.

Norway maple (Acer platanoides L.) is a widespread forest tree species in Central and Northern Europe but with a scattered distribution. In the debate on climate change driven changes in species selection in the forest, Norway maple has recently received raised interest because of its comparatively high drought resistance (higher than in sycamore maple). Therefore, it is an interesting species for sites high in carbonates and where other native tree species have become devastated by pathogens (e.g., elm, ash). In Austria, the demand on saplings is currently rising, while there is only very little domestic reproductive material available (on average more than 95% of saplings are imported from neighboring countries). This study was undertaken to identify genetic diversity and population structure of Norway maple in Austria to lay the foundation for the establishment of respective in situ and ex situ conservation measures. In addition, samples from planted stands and imported reproductive material from other countries were included to study the anthropogenic influence on the species in managed forests. We used 11 novel microsatellites to genotype 756 samples from 27 putatively natural Austrian populations, and 186 samples derived from two planted stands and five lots of forest reproductive material; in addition, 106 samples from other European populations were also genotyped. Cross species amplification of the new markers was tested in 19 Acer species from around the world. Population clustering by STRUCTURE analysis revealed a distinct pattern of population structure in Austria and Europe, but overall moderate differentiation. Sibship analysis identifies several populations with severe founding effects, highlighting the need for proper selection of seed sources of sufficient genetic diversity in the species.

Hundreds of plant lineages have independently evolved dioecy, i.e., separation of female and male flowers on different individuals. In all dioecious plants investigated at the molecular level to date, sex is determined genetically through a sex-determining region (SDR). SDRs have mostly been studied in angiosperms, although dioecy is relatively more common among gymnosperms. Here, we investigate sex determination in the gymnosperm Taxus baccata . We assembled four haplotype-resolved chromosome-level genomes for one female and one male tree, with an average size of 10.04 Gb, and generated resequencing data for 100 phenotypically sexed individuals. Strikingly, k-mer analyses, genome-wide association studies and differential coverage analyses demonstrate the absence of an SDR in the T. baccata genome. This indicates a non-genetic mechanism of sex determination, most likely via a sex-specific epiallele. Given that T. baccata is the first species studied among a large group of conifers, our findings suggest that such a mechanism might be widespread.