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Buggs, R. J. A.

Publications and source records attributed to Buggs, R. J. A..

12 recordsLinked to original sources

Genomic diversity of elm trees for future treescapes

O_LIDutch elm disease has devastated the treescapes of Europe and North America, causing large elm trees to become largely absent. Several decades of work are now coming to fruition with the availability of potentially resistant cultivars for restoration. C_LIO_LIWe analysed genome-wide single-nucleotide polymorphisms derived from whole-genome sequences of more than 200 trees, including elm species, British morphological forms, disease-tolerant Spanish selections and cultivars from several breeding programmes. C_LIO_LIWhile confirming many specimen labels and multigenerational crossing records, our results also revealed unexpected misidentifications and origins of some samples. This included past hybridisation in some resistant selections thought to be pure species. We find that within our samples, field elm (Ulmus minor) is more genetically diverse than wych elm (U. glabra). We show that over ten British elm forms sometimes assigned species epithets fall within the genetic range of U. minor, U. glabra or hybrids. C_LIO_LIWith their exotic parentage, many of the elm cultivars introduced into Britain post-epidemic represent a considerable increase in nucleotide diversity over the still numerically large, native U. minor and U. glabra populations. Currently, the cultivars are being planted mainly as ornamentals. Their long-term arboricultural, adaptive and landscape suitability remains to be demonstrated. C_LI

plant biology↗

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↗

European ash pangenome reveals widespread structural variation and a diverse genetic basis for low ash dieback susceptibility

European Ash (Fraxinus excelsior) is a keystone forest tree species, whose populations are being decimated by ash dieback disease (ADB). Uncovering the genetic basis of low susceptibility to this devastating disease relies on a comprehensive understanding of genetic variation present in F. excelsior. A linear reference genome from a single individual cannot contain the total sequence variability within a species, including its genic regions; a pangenome more fully captures total sequence content. In this study, we developed a F. excelsior pangenome reference using a new chromosomal-level phased linear reference genome, and de novo assemblies and long-read data from a geographically diverse set of fifty F. excelsior samples, with particular focus on individuals showing low ADB susceptibility. We identified 362,965 structural variants (SVs) present in more than three individuals, including 174Mb of sequence absent from the linear reference genome (22% of the linear reference size). We demonstrated that failing to explicitly link SVs with gene sequences can lead to substantial overestimation of dispensable genes (those that vary in their presence/absence between individuals) due to variability in the annotation process. Controlling for this reduced the fraction of the genome estimated as dispensable from 35.9% to 8.7%, identifying 3,412 high-confidence dispensable genes, including 141 annotated with gene ontology terms associated with defence response. We used the pangenome to analyse existing genomic data from over 1,200 individuals to identify loci associated with reduced susceptibility to ADB. This revealed 220 single nucleotide polymorphisms (SNPs) showing allele frequency shifts between healthy and highly damaged pools of individuals that are broadly consistent across the mainly UK seed sources sampled, explicitly demonstrating the existence of a shared genetic component to low ADB susceptibility.

genomics↗

Molecular convergence analyses identify candidate genes for low susceptibility to the ash dieback pathogen

Non-native pests and pathogens increasingly threaten global forest ecosystems. An understanding of the genomic basis of low susceptibility in the natural hosts of such pests and pathogens, with which they share a coevolutionary history, can enhance restoration efforts by facilitating the selection of individuals carrying beneficial alleles. Within the genus Fraxinus (ash trees) low susceptibility to the fungal pathogen Hymenoscyphus fraxineus, the causative agent of the ash dieback disease (ADB) epidemic, is observed in three independent lineages of known or plausible natural hosts. Here, we seek to elucidate the genetic basis of this trait, which is key to the future survival of Fraxinus excelsior populations in Europe, using a molecular convergence approach. We analysed 4,300 protein-coding loci for amino acid convergence between lineages with low susceptibility. After filtering for potential false positives, we find 62 genes that have a signal of excess convergence between Fraxinus lineages with low ADB susceptibility. Eleven of these loci have additional evidence for a role in defence against fungal pathogens, with a further 17 linked to more general immunity or defence, or other functions relevant to the response against ADB such as cell wall biogenesis. The candidate loci discovered here complement those reported by previous genomic studies of F. excelsior, and can be targeted in efforts to mitigate the devastation caused by this deadly disease by informing breeding programmes involving hybridisation and marker-assisted back-crossing. Our study demonstrates the benefit of genomic analyses incorporating natural hosts, when seeking to tackle biotic threats to naive host populations. Significance StatementKnowledge of the genomic basis of variation in susceptibility to emerging forest pests and pathogens can provide the foundation for interventions to mitigate such threats, but studies restricted to the analysis of naive host populations may miss relevant genomic loci that could be present in coevolved hosts. Using comparative genomic analyses for the detection of molecular convergence between lineages of ash trees with low susceptibility to ash dieback, incorporating known and plausible natural hosts, we detect novel candidate loci for defence against this disease. Our findings can be used to support efforts to tackle one of the worlds worst forest pathogens and demonstrate the value of integrating genomic data from coevolved hosts when aiming to identify the basis of low susceptibility to biotic threats.

evolutionary biology↗

Genomic signals of local adaptation and hybridization in Asian white birch

Disentangling the numerous processes that affect patterns of genome-wide diversity in widespread tree species has important implications for taxonomy, conservation, and forestry. Here, we investigate the population genomic structure of Asian white birch (Betula platyphylla) in China and seek to explain it in terms of hybridization, demography and adaptation. We generate whole genome sequence data from 83 individuals across the species range in China. Combining this with an existing dataset for 79 European and Russian white birches, we show a clear distinction between B. pendula and B. platyphylla, which have sometimes been lumped taxonomically. Genomic diversity of B. platyphylla in north-western China and Central Russia is affected greatly by hybridization with B. pendula. Excluding these hybridized populations, B. platyphylla in China has a linear distribution from north-eastern to south-western China, along the edge of the inland mountainous region. Within this distribution, three genetic clusters are found, which we model as long diverged with subsequent episodes of gene flow. Patterns of co-variation between allele frequencies and environmental variables in B. platyphylla suggest the role of natural selection in the distribution of diversity at 7,609 SNPs of which 3,767 were significantly differentiated among the genetic clusters. The putative adaptive SNPs are distributed throughout the genome and span 1,633 genic regions. Of these genic regions, 87 were previously identified as candidates for selective sweeps in Eurasian B. pendula. We use the 7,609 environmentally associated SNPs to estimate the risk of non-adaptedness for each sequenced B. platyphylla individual under a scenario of future climate change, highlighting areas where populations may be under future threat from rising temperatures.

evolutionary biology↗

Introduced crops supplement rather than replace indigenous crops in an African center of agrobiodiversity

O_LICrop diversity plays a major role in underpinning food security. It is especially important to smallholder and subsistence farmers, who often rely on crop diversity for stable and resilient production. Despite this, global expansion of a small pool of major crops and the associated homogenisation of global agricultural systems may decrease on-farm crop diversity. C_LIO_LIWe surveyed 1,369 subsistence farms stratified across climate gradients in the Ethiopian Highlands, to characterise the richness and cultivated area of the 83 edible crops they contained. We further categorise these crops by their period of introduction to Ethiopia. We apply non-metric multidimensional scaling and mixed effects modelling to characterise agrisystem composition and test the impact of crop introductions. C_LIO_LIWe find a significant positive relationship between introduced and indigenous crop richness, suggesting that crop introductions have tended to supplement rather than replace or reduce indigenous crop diversity. Geographically matched farms with higher proportions of introduced crops, had significantly higher overall crop richness. Analysis of socio-economic drivers indicates that both poverty and low accessibility are associated with reduced cultivation of modern introductions. C_LIO_LIWe conclude that global patterns of major crop expansion do not necessarily result in agrobiodiversity loss for subsistence farmers, in our Ethiopian case study. Importantly, socioeconomic factors may strongly influence the farmers propensity to adopt novel species, suggesting targets for agricultural extension policies. Given the rapid climatic, economic and demographic changes impacting global food systems and the threats to food security these entail, robust indigenous agricultural systems supplemented with diverse introduced crops may enhance resilience. C_LI

ecology↗

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↗

A chromosome-scale genome assembly of European Hazel (Corylus avellana L.) reveals targets for crop improvement

European hazelnut (Corylus avellana L.) is a tree crop of economic importance worldwide, but especially to northern Turkey, where the majority of production takes place. Hazelnut production is currently challenged by environmental stresses such as a recent outbreak of severe powdery mildew disease; furthermore, allergy to hazelnuts is an increasing health concern in some regions.\n\nIn order to provide a foundation for utilizing the available hazelnut genetic resources for crop improvement, we produced the first fully assembled genome sequence and annotation for a hazelnut species, from Corylus avellana cv. Tombul, one of the most important Turkish varieties. A hybrid sequencing strategy combining short reads, long reads and proximity ligation methods enabled us to resolve heterozygous regions and produce a high-quality 370 Mb assembly that agrees closely with cytogenetic studies and genetic maps of the 11 C. avellana chromosomes, and covers 97.8% of the estimated genome size. The genome includes 28,409 high-confidence protein-coding genes, over 20,000 of which were functionally annotated based on homology to known plant proteins. We focused particularly on gene families encoding hazelnut allergens, and the MLO proteins that are an important susceptibility factor for powdery mildew. The complete assembly enabled us to differentiate between members of these families and identify novel homologs that may be important in mildew disease and hazelnut allergy. These findings provide examples of how the genome can be used to guide research and develop effective strategies for crop improvement in C. avellana.

genomics↗

Genomic assessment of local adaptation in dwarf birch to inform assisted gene flow

When populations of a rare species are small, isolated and declining under climate change, some populations may become locally maladapted. Detecting this maladaptation may allow effective rapid conservation interventions, even if based on incomplete knowledge. Population maladaptation may be estimated by finding genome-environment associations (GEA) between allele frequencies and environmental variables across a local species range, and identifying populations whose allele frequencies do not fit with these trends. We can then design assisted gene flow strategies for maladapted populations, to adjust their allele frequencies, entailing lower levels of intervention than with undirected conservation action. Here, we investigate this strategy in Scottish populations of the montane plant dwarf birch (Betula nana). In genome-wide single nucleotide polymorphism (SNP) data we found 267 significant associations between SNP loci and environmental variables. We ranked populations by maladaptation estimated using allele frequency deviation from the general trends at these loci; this gave a different prioritization for conservation action than the Shapely Index, which seeks to preserve rare neutral variation. Populations estimated to be maladapted in their allele frequencies at loci associated with annual mean temperature were found to have reduced catkin production. Using an environmental niche modelling (ENM) approach, we found annual mean temperature (35%), and mean diurnal range (15%), to be important predictors of the dwarf birch distribution. Intriguingly, there was a significant correlation between the number of loci associated with each environmental variable in the GEA, and the importance of that variable in the ENM. Together, these results suggest that the same environmental variables determine both adaptive genetic variation and species range in Scottish dwarf birch. We suggest an assisted gene flow strategy that aims to maximize the local adaptation of dwarf birch populations under climate change by matching allele frequencies to current and future environments.

evolutionary biology↗

Genomic basis of European ash tree resistance to ash dieback fungus

Populations of European ash trees (Fraxinus excelsior) are being devastated by the invasive alien fungus Hymenoscyphus fraxineus, which causes ash dieback (ADB). We sequenced whole genomic DNA from 1250 ash trees in 31 DNA pools, each pool containing trees with the same ADB damage status in a screening trial and from the same seed-source zone. A genome-wide association study (GWAS) identified 3,149 single nucleotide polymorphisms (SNPs) associated with low versus high ADB damage. Sixty-one of the 203 most significant SNPs were in, or close to, genes with putative homologs already known to be involved in pathogen responses in other plant species. We also used the pooled sequence data to train a genomic prediction (GP) model, cross-validated using individual whole genome sequence data generated for 75 healthy and 75 damaged trees from a single seed source. Using the top 30% of our genomic estimated breeding values from 200 SNPs, we could predict tree health with over 90% accuracy. We infer that ash dieback resistance in F. excelsior is a polygenic trait that should respond well to both natural selection and breeding, which could be accelerated using GP.

evolutionary biology↗

Genetic diversity and domestication of hazelnut (Corylus avellana) in Turkey

O_LIAssessing and describing genetic diversity in crop plants is a crucial first step towards their improvement. The European hazelnut, Corylus avellana, is one of the most economically important tree nut crops worldwide. It is primarily produced in Turkey where rural communities depend on it for their livelihoods. Despite this we know little about hazelnuts domestication history and the genetic diversity it holds.\nC_LIO_LIWe use double digest Restriction-site Associated DNA (ddRAD) sequencing to produce genome-wide dataset containing wild and domesticated hazelnut. We uncover patterns of population structure and diversity, determine levels of crop-wild gene flow and estimate the timing of key divergence events.\nC_LIO_LIWe find that genetic clusters of cultivars do not reflect their given names and that there is limited evidence for a reduction in genetic diversity in domesticated individuals. Admixture has likely occurred multiple times between wild and domesticated hazelnut. Domesticates appear to have first diverged from their wild relatives during the Mesolithic.\nC_LIO_LIWe provide the first genomic assessment of Turkish hazelnut diversity and suggest that it is currently in a partial stage of domestication. Our study provides a platform for further research that will protect this crop from the threats of climate change and an emerging fungal disease.\nC_LI

evolutionary biology↗