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Biology subjects

Denman, S.

Publications and source records attributed to Denman, S..

7 recordsLinked to original sources

Genomic diversity of British native oaks: species differentiation, hybridisation and triploidy

The morphological continuum between Britains two native oak species helped Darwin formulate his "one long argument" in The Origin of Species. Here we comprehensively analyse the genome-wide differentiation of 418 individuals from 60 British oak populations. Using 7 million biallelic SNPs, we find evidence for two species with islands of variation containing 8,230 SNPs of which 2,005 are within gene annotations. We find extensive hybridisation and back-crossing between the species, and this is biased in favour of introgression from Quercus robur into Q. petraea. Chloroplasts are shared between the species, mainly of haplotypes derived from Iberian glacial refugia. Genomic allocation of species and hybrids allows analysis of niche differentiation, showing that a larger Q. robur component is disproportionately found in warmer and more thermally variable environments with alkaline soils, while a larger Q. petraea component is found in more topographically complex terrain with high rainfall. This leads us to emphasise the balance between the opposing forces of hybridisation and niche differentiation in explaining the continuum between the two species. Using long-term field data, we show that stem growth over three decades was higher in Q. robur than in Q. petraea or hybrids, but this difference could be explained by environmental factors. In contrast, the five triploid trees in our sample grew significantly faster than diploids even after accounting for environmental effects, suggesting that triploids could be a valuable economic resource.

evolutionary biology↗

Genomic basis for resistance to acute oak decline and mildew infection in English oak

English oak (Q. robur) in Britain is at risk from a young age due to powdery mildew and at maturity due to acute oak decline (AOD). The contribution of oak genetic diversity to these conditions is a critical question that until recently would have required extensive clonal or family trials of juvenile and mature oak trees. Here we overcome this practical burden with genomic approaches inspired by medicine. We sequence 1868 oak trees from 78 sites and identify 1491 trees exclusively of the species Q. robur, which we analyse. Using single nucleotide polymorphism (SNP) based estimates of heritability ([Formula]), we estimate 20.9% of variation in AOD presence is genetically determined. For mildew symptoms, [Formula] is 27.8%. Using genome-wide association studies, no SNP markers show a significant association with AOD, but 183 are significantly associated with 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 perhaps reflects 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.

evolutionary biology↗

Large-scale culturing of the tree microbiome enables targeted disease suppression

The tree microbiome is essential for host health and pathogen suppression. Synthetic microbial communities (SynComs) are emerging as important tools to understand microbiome dynamics and engineer microbiomes to harness beneficial properties. However, while the rational design, assembly and application of SynComs requires representative microbiota isolate collections combined with functional information, microbial culture collections from tree species such as oak (Quercus) are critically lacking. Here, we generated an oak microbiota culture collection comprising >30,000 isolates from 150 oak trees across Britain, belonging to key bacterial and fungal taxa that represented 61% of the total bacterial sequences and 87% of total fungal sequences as determined by culture-independent sequencing. Over 22,000 isolates were screened for suppression of bacterial species associated with degradation of live stem tissue in trees affected by Acute Oak Decline (AOD), identifying 341 bacterial isolates that suppressed oak pathogens. In vitro screening of 40 randomly assembled SynComs demonstrated that oak microbiota SynComs can suppress oak pathogenic bacteria associated with AOD. Inoculation of a disease-suppressive SynCom into the stem of oak seedlings and logs prior to pathogen challenge reduced the quantities of the bacteria, Brenneria goodwinii and Gibbsiella quercinecans, by 56% and 87%, respectively, in seedlings, and 71% and 95% in logs. This work demonstrates that the tree microbiome can be engineered using disease suppressive SynComs.

microbiology↗

Environment and disease have tissue-specific effects on the tree microbiome

Trees are essential for ecosystem function, but due to their long lifespan, are disproportionately impacted by climate change and disease. Tree-associated microbiota are critical for tree health and resilience, but the composition and function of tree microbiomes across different tissue types, and how environmental factors and disease impact tree microbiomes, is poorly understood. Oak trees are major constituents of forests of the Northern hemisphere, but are increasingly impacted by climate and disease. Here, we studied the oak microbiome across Britain, combining 16S rRNA gene and ITS microbial community profiling and shotgun metagenomics of leaf, stem and root/rhizosphere samples, and developed a three-level occupancy model to describe microbiota distribution across the landscape. We show that oak leaf, stem and root/rhizosphere tissues harbour taxonomically and functionally distinct microbiota and identified differences in tissue-specific effects of environmental variables (e.g. temperature, rainfall, ion deposition) on microbiome composition and function. We generated 1657 bacterial, archaeal and fungal metagenome-assembled genomes representing key members of the oak microbiome. Furthermore, the stem microbiome of oak trees with symptoms of Acute Oak Decline, a complex decline disease driven by abiotic and biotic stressors, exhibited reduced bacterial and fungal richness and altered microbiome function. This work represents the most comprehensive microbiome study of a tree species to date. Understanding how tree-associated microbiota respond to environmental change and disease across different tissues is crucial to predict future climate and disease impacts on tree microbiome function, and inform translational approaches to modulate tree microbiomes for plant health.

microbiology↗

Chemical cues from beetle larvae trigger proliferation and virulence of a plant pathogen

Agricultural crop productivity and global forest biomes are coming under increasing threat from insect pests and microbial pathogens. This impact is worsened by inter- kingdom insect-microbe interactions that can increase transmission and disease severity in affected plants. Whilst bacterial chemical cues have been shown to directly influence insect behaviour, the impact of insect-derived compounds on phytopathogens is poorly understood. Here, we investigated the chemical basis for interactions between beetle larvae and bacteria in acute oak decline (AOD), a disease characterised by inner bark necrosis and involving a polymicrobial consortium including Brenneria goodwinii and larval galleries of Agrilus biguttatus. We found that A. biguttatus larval extracts contain chemical elicitors that increase bacterial growth rate and final cell density during in vitro culture, and stimulate the differential expression of [~]600 genes, including the Type III Secretion System and its effectors, which are major virulence factors in plant pathogens. Chemical compounds from closely related insect species did not have this effect. These findings highlight the importance of inter-kingdom interactions in plant disease and suggests a novel mode-of-action for insect-derived chemical elicitors in facilitating the virulence of phytopathogens.

ecology↗

Leaf susceptibility of Macaronesian laurel forest species to Phytophthora ramorum

Phytophthora ramorum (Pr) is an invasive oomycete in Europe and North America and the causal agent of sudden oak death (SOD), which occurs along the coastal fog belt of California and southwestern Oregon, and it also causes sudden larch death in the UK. The Macaronesian laurel forest (MLF), a relict subtropical evergreen forest of the North Atlantic islands, shares climatic and some taxonomic affinities with those areas affected by SOD. To assess the disease risk, we tested the foliage susceptibility of MLF species and their capacity to sustain Pr sporulation and compared the climatic suitability with other areas where the pathogen is established. Detached leaves of 15 species were inoculated with zoospores and mycelium (through wounding) with five Pr isolates belonging to the EU1 and NA1 clonal lineages. MLF species showed diverse responses to Pr, ranging from extensive necroses on Viburnum tinus to asymptomatic sporulation on Picconia excelsa. Eleven species developed necrotic lesions to different degrees through zoospore inoculation while this increased to 13 species through wound treatment. Overall, small necrotic lesions (i.e. tolerance) were predominant, but Pr was rather aggressive to V. tinus, Arbutus canariensis and Ilex canariensis. Although the mean sporangial production was generally low (25-201 sporangia) in all species, the number of sporangia per leaf in five MLF species was similar to those reported for Umbellularia californica, a key host driving the SOD epidemics in California. Climatic suitability indexes in MLF areas were similar to those where SOD is found in California. Our results indicate a moderate to high risk of Pr establishment if the pathogen is introduced in the MLF.

plant biology↗

Genomic structure and diversity of oak populations in British Parklands

The two predominant oak species in Britain are Quercus robur (English or pedunculate oak) and Q. petraea (sessile oak). We sequenced the whole genomes of 386 oak trees from four British parkland sites and found over 50 million nuclear single nucleotide polymorphisms (SNPs), allowing us to identify 360 Q. robur, ten Q. petraea and 16 hybrid individuals using clustering methods. Comparing Q. robur and Q. petraea trees from Attingham Park, we found that the nuclear genomes of the two species are largely undifferentiated but identified 81 coding regions exhibiting strong interspecific differentiation. The nuclear genomes of our 360 Q. robur individuals showed no clear differentiation among the four parkland sites. Scans for selective sweeps in Q. robur highlighted regions containing genes with putative involvement in stress tolerance, one of which was moderately differentiated from Q. petraea. Reconstructions of past effective population sizes suggested a long population size decline in both Q. robur and Q. petraea over the Pleistocene, but population growth after the last glacial maximum. We assembled the whole chloroplast genomes of 287 Q. robur, 8 Q. petraea and 14 hybrid trees. In a phylogenetic network, these fell into five major haplotypes, which were shared among species but differed in frequency among parkland sites. We matched our chloroplast genome haplotypes to restriction enzyme fragment haplotypes identified in older studies that had surveyed ancient woodlands in Britain and much of Europe. This suggested that the parkland populations in our study derive from local seed sources.

genomics↗