Acute Oak Decline (AOD) is complex syndrome affecting Britain’s keystone native oak species, (Quercus robur L. and Q. petraea L. (Matt.) Liebl.), in some cases causing mortality within five years of symptom development. The most distinguishable symptom is weeping stem lesions, from which four species of bacteria have been isolated: Brenneria goodwinii, Gibbsiella quercinecans, Lonsdalea britannica and Rahnella victoriana. We do not yet know where else these bacteria exist, and little is known about the relationship of the wider oak leaf microbiome (phyllosphere) to acute oak decline. Here we investigate whether incidental evidence from a large oak genome re-sequencing dataset could be used to detect these bacteria in oak foliage, and whether bacterial incidence co-varied with AOD status or location. Oak leaves and buds were sampled from 421 trees at five sites in England. Whole genomic DNA from these samples was shot-gun sequenced with short reads. Non-oak reads were extracted from these data and queried to microbial databases. Reads uniquely matching AOD-associated bacterial genomes were found to be present on trees from all five sites and included trees with active lesions, trees with historic lesions and trees without AOD symptoms. The abundance of the AOD-associated bacteria did not differ between tree health categories but did differ among sites. We conclude that the AOD-associated bacteria may be members of the normal oak microbiome, whose presence on a tree is not sufficient to cause AOD symptoms.

Acute Oak Decline (AOD) is complex syndrome affecting Britain’s keystone native oak species, (Quercus robur L. and Q. petraea L. (Matt.) Liebl.), in some cases causing mortality within five years of symptom development. The most distinguishable symptom is weeping stem lesions, from which four species of bacteria have been isolated: Brenneria goodwinii, Gibbsiella quercinecans, Lonsdalea britannica and Rahnella victoriana. We do not yet know where else these bacteria exist, and little is known about the relationship of the wider oak leaf microbiome (phyllosphere) to acute oak decline. Here we investigate whether incidental evidence from a large oak genome re-sequencing dataset could be used to detect these bacteria in oak foliage, and whether bacterial incidence co-varied with AOD status or location. Oak leaves and buds were sampled from 421 trees at five sites in England. Whole genomic DNA from these samples was shot-gun sequenced with short reads. Non-oak reads were extracted from these data and queried to microbial databases. Reads uniquely matching AOD-associated bacterial genomes were found to be present on trees from all five sites and included trees with active lesions, trees with historic lesions and trees without AOD symptoms. The abundance of the AOD-associated bacteria did not differ between tree health categories but did differ among sites. We conclude that the AOD-associated bacteria may be members of the normal oak microbiome, whose presence on a tree is not sufficient to cause AOD symptoms.

Oak trees are of major economic and ecological importance globally. In England the main oak species is Quercus robur (English oak). Establishment and growth of Q. robur has suffered from the spread of the powdery mildew, a fungal foliar disease, over the past century, which affects trees of all ages. In recent decades, acute oak decline (AOD) has damaged many mature Q. robur populations; this is a complex syndrome in which predisposing environmental factors, a beetle, and four bacterial species have been implicated. Little is known about genetic factors contributing to AOD and mildew symptoms. Here we analyse the population structure of British oak populations using the whole genomes of 1868 oak trees from 78 sites. Retaining 1491 trees exclusively of the species Q. robur , we investigate the genetic component of AOD and mildew susceptibility, and its architecture. Using single nucleotide polymorphism (SNP) based estimates of heritability, we estimate 20.9% of variation in AOD presence is genetically determined. For mildew symptoms, this figure is higher, at 27.8%. Using genome-wide association studies, no SNP markers cross significance thresholds for AOD, but 183 are significant for mildew. Genomic prediction models for AOD and its symptoms, using thousands of loci, give low to moderate accuracies, ranging from 0.187 to 0.617. These results suggest a highly polygenic heritable component of susceptibility to AOD, which is not surprising given the number of biotic and abiotic factors known to contribute to it. In contrast, powdery mildew, caused by a single fungus, has an oligogenic heritable component controlled by fewer loci of large effect. These results could be used to inform breeding programs to develop trees more resistant to AOD and mildew.

Black alder ( Alnus glutinosa ) is a native tree species in the British Isles, which it colonised after the last glaciation from continental refugia. It is now a widespread pioneer species, thriving on wetlands and riverbanks. We present whole genome sequence data for 324 alder seedlings grown from seed collected from 44 populations across the UK. Among these we found two triploids and one sample with trisomy at chromosome five. Removing these, we found little population genetic structure apart from diverging northern populations with lower diversity. Using Latent-Factor Mixed Models (LFMM) analyses we identified 1,364 loci whose allele frequencies were significantly associated with environmental variables. Of these loci, 93% were associated with the number of snow days. In contrast, the greatest total genomic signal (variance in SNP effect sizes of 7.38 million SNP loci) was observed for mean temperature of the wettest quarter and annual number of frost days. Estimates of maladaptation using 1.49 million SNPs, predicted that northern populations are worst adapted to present and future worst-case climates. Our results suggest that similarity of source-site temperature variables should be prioritised when choosing seed sources for new planting, and northern populations could benefit from assisted gene flow from the south.

The two native British oak species Quercus robur (pedunculate oak) and Q. petraea (sessile oak) are widespread and of ecological, cultural and economic value. Here we sequence whole genomic DNA of 418 individuals from 60 natural oak populations, most of which were previously monitored in a Forest Condition Survey that ran from 1987 to 2007 across Great Britain. Variant calling identifies 146,995,863 single nucleotide polymorphisms (SNPs) and 28,275,691 indels. Analysing population genetic structure at 7,112,139 biallelic SNPs, we find two groups, indicating that Q. robur is more common in the south and east of Britain, and Q. petraea in the north and west. The species distributions show niche differentiation in that Q. robur prefers warmer and more thermally variable environments with alkaline soils, while Q. petraea prefers rainy environments with more topographically complex terrain. We show extensive hybridisation and back-crossing between the two species. This is biased in favour of introgression from Q. robur into Q. petraea . By analysis of allele balance, we find five triploid trees among our samples, two belonging to each species and one being hybridised. We find little population genetic structure within species. Despite genome-wide introgression, we find islands of genomic differentiation between species, particularly in chromosome two. These differentiated regions contain 8,230 SNPs of which 2,005 are within gene annotations. We also show widespread chloroplast haplotype sharing between species. Between 1990 and 2019, mean stem growth was higher in Q. robur than in Q. petraea and hybrids, due to environmental factors. Triploids grew significantly faster than diploids even when environmental factors were accounted for.