Publications by authors named "Richard J A Buggs"

36 Publications

Resolving phylogeny and polyploid parentage using genus-wide genome-wide sequence data from birch trees.

Mol Phylogenet Evol 2021 Feb 27;160:107126. Epub 2021 Feb 27.

School of Biological and Chemical Sciences, Queen Mary University of London, Mile End Road, London E1 4NS, UK; Royal Botanic Gardens Kew, Richmond, Surrey TW9 3AB, UK. Electronic address:

Numerous plant genera have a history including frequent hybridisation and polyploidisation (allopolyploidisation), which means that their phylogeny is a network of reticulate evolution that cannot be accurately depicted as a bifurcating tree with a single tip per species. The genus Betula, which contains many ecologically important tree species, is a case in point. We generated genome-wide sequence reads for 27 diploid and 36 polyploid Betula species or subspecies using restriction site associated DNA (RAD) sequences. These reads were assembled into contigs with a mean length of 675 bp. We reconstructed the evolutionary relationships among diploid Betula species using both supermatrix (concatenation) and species tree methods. We identified the closest diploid relatives of the polyploids according to the relative rates at which reads from polyploids mapped to contigs from different diploid species within a concatenated reference sequence. By mapping reads from allopolyploids to their different putative diploid relatives we assembled contigs from the putative sub-genomes of allopolyploid taxa. We used these to build new phylogenies that included allopolyploid sub-genomes as separate tips. This approach yielded a highly evidenced phylogenetic hypothesis for the genus Betula, including the complex reticulate origins of the majority of its polyploid taxa. Our phylogeny divides the genus into two well supported clades, which, interestingly, differ in their seed-wing morphology. We therefore propose to split Betula into two subgenera.
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http://dx.doi.org/10.1016/j.ympev.2021.107126DOI Listing
February 2021

The origin of Darwin's "abominable mystery".

Am J Bot 2021 01 22;108(1):22-36. Epub 2021 Jan 22.

Royal Botanic Gardens, Kew, Richmond, Surrey, UK.

The phrase "Darwin's abominable mystery" is frequently used with reference to a range of outstanding questions about the evolution of the plant group today known as the angiosperms. Here, I seek to more fully understand what prompted Darwin to coin the phrase in 1879, and the meaning he attached to it, by surveying the systematics, paleobotanical records, and phylogenetic hypotheses of his time. In the light of this historical research, I argue that Darwin was referring to the origin only of a subset of what are today called angiosperms: a (now obsolete) group equivalent to the "dicotyledons" of the Hooker and Bentham system. To Darwin and his contemporaries, the dicotyledons' fossil record began abruptly and with great diversity in the Cretaceous, whereas the gymnosperms and monocotyledons were thought to have fossil records dating back to the Carboniferous or beyond. Based on their morphology, the dicotyledons were widely seen by botanists in Darwin's time (unlike today) as more similar to the gymnosperms than to the monocotyledons. Thus, morphology seemed to point to gymnosperm progenitors of dicotyledons, but this hypothesis made the monocotyledons, given their (at the time) apparently longer fossil record, difficult to place. Darwin had friendly disagreements about the mystery of the dicotyledons' abrupt appearance in the fossil record with others who thought that their evolution must have been more rapid than his own gradualism would allow. But the mystery may have been made "abominable" to him because it was seen by some contemporary paleobotanists, most notably William Carruthers, the Keeper of Botany at the British Museum, as evidence for divine intervention in the history of life. Subsequent developments in plant systematics and paleobotany after 1879 meant that Darwin's letter was widely understood to be referring to the abrupt appearance of all angiosperms when it was published in 1903, a meaning that has been attached to it ever since.
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http://dx.doi.org/10.1002/ajb2.1592DOI Listing
January 2021

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

Plant J 2021 Mar 6;105(5):1413-1430. Epub 2021 Jan 6.

Sabanci University SUNUM Nanotechnology Research and Application Centre, Istanbul, Turkey.

The European hazelnut (Corylus avellana L.) is a tree crop of economic importance worldwide, but especially for 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. In order to provide a foundation for using the available hazelnut genetic resources for crop improvement, we produced a fully assembled genome sequence and annotation for a hazelnut species, from C. 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 27 270 high-confidence protein-coding genes, over 20 000 of which were functionally annotated based on homology with known plant proteins. We focused particularly on gene families encoding hazelnut allergens, and the Mildew resistance Locus O (MLO) proteins that are an important susceptibility factor for powdery mildew. The complete assembly enabled us to differentiate between members of these families and to identify homologues 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 to develop effective strategies for crop improvement in C. avellana.
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http://dx.doi.org/10.1111/tpj.15099DOI Listing
March 2021

Convergent molecular evolution among ash species resistant to the emerald ash borer.

Nat Ecol Evol 2020 08 25;4(8):1116-1128. Epub 2020 May 25.

School of Biological and Chemical Sciences, Queen Mary University of London, London, UK.

Recent studies show that molecular convergence plays an unexpectedly common role in the evolution of convergent phenotypes. We exploited this phenomenon to find candidate loci underlying resistance to the emerald ash borer (EAB, Agrilus planipennis), the United States' most costly invasive forest insect to date, within the pan-genome of ash trees (the genus Fraxinus). We show that EAB-resistant taxa occur within three independent phylogenetic lineages. In genomes from these resistant lineages, we detect 53 genes with evidence of convergent amino acid evolution. Gene-tree reconstruction indicates that, for 48 of these candidates, the convergent amino acids are more likely to have arisen via independent evolution than by another process such as hybridization or incomplete lineage sorting. Seven of the candidate genes have putative roles connected to the phenylpropanoid biosynthesis pathway and 17 relate to herbivore recognition, defence signalling or programmed cell death. Evidence for loss-of-function mutations among these candidates is more frequent in susceptible species than in resistant ones. Our results on evolutionary relationships, variability in resistance, and candidate genes for defence response within the ash genus could inform breeding for EAB resistance, facilitating ecological restoration in areas invaded by this beetle.
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http://dx.doi.org/10.1038/s41559-020-1209-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7610378PMC
August 2020

FluentDNA: Nucleotide Visualization of Whole Genomes, Annotations, and Alignments.

Front Genet 2020 30;11:292. Epub 2020 Apr 30.

Royal Botanic Gardens Kew, Jodrell Laboratory, Richmond, United Kingdom.

Researchers seldom look at naked genome assemblies: instead the attributes of DNA sequences are mediated through statistics, annotations and high level summaries. Here we present software that visualizes the bare sequences of whole genome assemblies in a zoomable interface. This can assist in detection of chromosome architecture and contamination by the naked eye through changes in color patterns, in the absence of any other annotation. When available, annotations can be visualized alongside or on top of the naked sequence. Genome alignments can also be visualized, laying two genomes side by side in an alignment and highlighting their differences at nucleotide resolution. FluentDNA gives researchers direct visualization of whole genome assemblies, annotations and alignments, for quality control, hypothesis generation, and communicating results.
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http://dx.doi.org/10.3389/fgene.2020.00292DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7203487PMC
April 2020

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

Evol Appl 2020 Jan 24;13(1):161-175. Epub 2019 Nov 24.

Jodrell Laboratory Royal Botanic Gardens, Kew Surrey UK.

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 (). In genome-wide restriction site-associated 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.
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http://dx.doi.org/10.1111/eva.12883DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6935589PMC
January 2020

Genomic basis of European ash tree resistance to ash dieback fungus.

Nat Ecol Evol 2019 12 18;3(12):1686-1696. Epub 2019 Nov 18.

School of Biological and Chemical Sciences,, Queen Mary University of London, London, UK.

Populations of European ash trees (Fraxinus excelsior) are being devastated by the invasive alien fungus Hymenoscyphus fraxineus, which causes ash dieback. We sequenced whole genomic DNA from 1,250 ash trees in 31 DNA pools, each pool containing trees with the same ash dieback damage status in a screening trial and from the same seed-source zone. A genome-wide association study identified 3,149 single nucleotide polymorphisms (SNPs) associated with low versus high ash dieback damage. Sixty-one of the 192 most significant SNPs were in, or close to, genes with putative homologues already known to be involved in pathogen responses in other plant species. We also used the pooled sequence data to train a genomic prediction model, cross-validated using individual whole genome sequence data generated for 75 healthy and 75 damaged trees from a single seed source. The model's genomic estimated breeding values (GEBVs) allocated these 150 trees to their observed health statuses with 67% accuracy using 10,000 SNPs. Using the top 20% of GEBVs from just 200 SNPs, we could predict observed 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 genomic prediction.
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http://dx.doi.org/10.1038/s41559-019-1036-6DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6887550PMC
December 2019

Repeated long-distance dispersal and convergent evolution in hazel.

Sci Rep 2019 11 5;9(1):16016. Epub 2019 Nov 5.

Sabanci University Nanotechnology Research and Application Center (SUNUM), Sabanci University, Orhanlı, 34956, Tuzla, Istanbul, Turkey.

Closely related species with a worldwide distribution provide an opportunity to understand evolutionary and biogeographic processes at a global scale. Hazel (Corylus) is an economically important genus of tree and shrub species found in temperate regions of Asia, North America and Europe. Here we use multiple nuclear and chloroplast loci to estimate a time-calibrated phylogenetic tree of the genus Corylus. We model the biogeographic history of this group and the evolutionary history of tree and shrub form. We estimate that multiple Corylus lineages dispersed long distances between Europe and Asia and colonised North America from Asia in multiple independent events. The geographic distribution of tree versus shrub form of species appears to be the result of 4-5 instances of convergent evolution in the past 25 million years. We find extensive discordance between our nuclear and chloroplast trees and potential evidence for chloroplast capture in species with overlapping ranges, suggestive of past introgression. The important crop species C. avellana is estimated to be closely related to C. maxima, C. heterophylla var. thunbergii and the Colurnae subsection. Our study provides a new phylogenetic hypothesis or Corylus and reveals how long-distance dispersal can shape the distribution of biodiversity in temperate plants.
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http://dx.doi.org/10.1038/s41598-019-52403-2DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6831691PMC
November 2019

Population structure of Betula albosinensis and Betula platyphylla: evidence for hybridization and a cryptic lineage.

Ann Bot 2019 07;123(7):1179-1189

College of Forestry, Shandong Agricultural University, Tai'an city, Shandong province, China.

Background And Aims: Differences in local abundance and ploidy level are predicted to impact the direction of introgression between species. Here, we tested these hypotheses on populations of Betula albosinensis (red birch) and Betula platyphylla (white birch) which were thought to differ in ploidy level, the former being tetraploid and the latter diploid.

Methods: We sampled 391 birch individuals from nine localities in China, and classified them into species based on leaf morphology. Twelve nuclear microsatellite markers were genotyped in each sample, and analysed using principal coordinates analysis and STRUCTURE software. We compared the effects of two different methods of scoring polyploid genotypes on population genetic analyses. We analysed the effect of ploidy, local species abundance and latitude on levels of introgression between the species.

Key Results: Leaf morphology divided our samples into red and white birch, but genetic analyses unexpectedly revealed two groups within red birch, one of which was tetraploid, as expected, but the other of which appeared to have diploid microsatellite genotypes. Five individuals were identified as early-generation hybrids or backcrosses between white birch and red birch and five were identified between red birch and 'diploid' red birch. Cline analysis showed that levels of admixture were not significantly correlated with latitude. Estimated genetic differentiation among species was not significantly different between determined tetraploid and undetermined tetraploid genotypes.

Conclusions: Limited hybridization and gene flow have occurred between red birch and white birch. Relative species abundance and ploidy level do not impact the direction of introgression between them, as genetic admixture is roughly symmetrical. We unexpectedly found populations of apparently diploid red birch and this taxon may be a progenitor of allotetraploid red birch populations. Incomplete lineage sorting may explain patterns of genetic admixture between apparently diploid and allotetraploid red birch.
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http://dx.doi.org/10.1093/aob/mcz024DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6612935PMC
July 2019

Genetic diversity maintained among fragmented populations of a tree undergoing range contraction.

Heredity (Edinb) 2018 10 15;121(4):304-318. Epub 2018 Aug 15.

Jodrell Laboratory, Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3DS, UK.

Dwarf birch (Betula nana) has a widespread boreal distribution but has declined significantly in Britain where populations are now highly fragmented. We analyzed the genetic diversity of these fragmented populations using markers that differ in mutation rate: conventional microsatellites markers (PCR-SSRs), RADseq generated transition and transversion SNPs (RAD-SNPs), and microsatellite markers mined from RADseq reads (RAD-SSRs). We estimated the current population sizes by census and indirectly, from the linkage-disequilibrium found in the genetic surveys. The two types of estimate were highly correlated. Overall, we found genetic diversity to be only slightly lower in Britain than across a comparable area in Scandinavia where populations are large and continuous. While the ensemble of British fragments maintain diversity levels close to Scandinavian populations, individually they have drifted apart and lost diversity; particularly the smaller populations. An ABC analysis, based on coalescent models, favors demographic scenarios in which Britain maintained high levels of genetic diversity through post-glacial re-colonization. This diversity has subsequently been partitioned into population fragments that have recently lost diversity at a rate corresponding to the current population-size estimates. We conclude that the British population fragments retain sufficient genetic resources to be the basis of conservation and re-planting programmes. Use of markers with different mutation rates gives us greater confidence and insight than one marker set could have alone, and we suggest that RAD-SSRs are particularly useful as high mutation-rate marker set with a well-specified ascertainment bias, which are widely available yet often neglected in existing RAD datasets.
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http://dx.doi.org/10.1038/s41437-018-0132-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6134035PMC
October 2018

Genome-wide epigenetic variation among ash trees differing in susceptibility to a fungal disease.

BMC Genomics 2018 Jun 28;19(1):502. Epub 2018 Jun 28.

School of Biological and Chemical Sciences, Queen Mary University of London, Mile End Road, London, E1 4NS, UK.

Background: European ash trees (Fraxinus excelsior) are currently threatened by ash dieback (ADB) caused by the fungus Hymenoscyphus fraxineus but a small percentage of the population possesses natural low susceptibility. The genome of a European ash tree has recently been sequenced. Here, we present whole genome DNA methylation data for two F. excelsior genotypes with high susceptibility to ADB, and two genotypes with low susceptibility, each clonally replicated. We also include two genotypes of Manchurian ash (F. mandshurica), an ash species which has co-evolved with H. fraxineus and also has low susceptibility to ADB.

Results: In F. excelsior, we find an average methylation level of 76.2% in the CG context, 52.0% in the CHG context, and 13.9% in the CHH context; similar levels to those of tomato. We find higher methylation in transposable elements as opposed to non-mobile elements, and high densities of Non-Differentially Methylation Positions (N-DMPs) in genes with housekeeping functions. Of genes putatively duplicated in whole genome duplication (WGD) events, an average of 25.9% are differentially methylated in at least one cytosine context, potentially indicative of unequal silencing. Variability in methylation patterns exists among clonal replicates, and this is only slightly less than the variability found between different genotypes. Of twenty genes previously found to have expression levels associated with ADB susceptibility, we find only two of these have differential methylation between high and low susceptibility F. excelsior trees. In addition, we identify 1683 significant Differentially Methylated Regions (DMRs) (q-value< 0.001) between the high and low susceptibility genotypes of F. excelsior trees, of which 665 remain significant when F. mandshurica samples are added to the low susceptibility group.

Conclusions: We find a higher frequency of differentially methylated WGD-derived gene duplicates in ash than other plant species previously studied. We also identify a set of genes with differential methylation between genotypes and species with high versus low susceptibility to ADB. This provides valuable foundational data for future work on the role that epigenetics may play in gene dosage compensation and susceptibility to ADB in ash.
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http://dx.doi.org/10.1186/s12864-018-4874-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6022711PMC
June 2018

Ash leaf metabolomes reveal differences between trees tolerant and susceptible to ash dieback disease.

Sci Data 2017 12 19;4:170190. Epub 2017 Dec 19.

School of Life Sciences, Gibbet Hill Campus, University of Warwick, Coventry CV4 7AL, UK.

European common ash, Fraxinus excelsior, is currently threatened by Ash dieback (ADB) caused by the fungus, Hymenoscyphus fraxineus. To detect and identify metabolites that may be products of pathways important in contributing to resistance against H. fraxineus, we performed untargeted metabolomic profiling on leaves from five high-susceptibility and five low-susceptibility F. excelsior individuals identified during Danish field trials. We describe in this study, two datasets. The first is untargeted LC-MS metabolomics raw data from ash leaves with high-susceptibility and low-susceptibility to ADB in positive and negative mode. These data allow the application of peak picking, alignment, gap-filling and retention-time correlation analyses to be performed in alternative ways. The second, a processed dataset containing abundances of aligned features across all samples enables further mining of the data. Here we illustrate the utility of this dataset which has previously been used to identify putative iridoid glycosides, well known anti-herbivory terpenoid derivatives, and show differential abundance in tolerant and susceptible ash samples.
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http://dx.doi.org/10.1038/sdata.2017.190DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5735976PMC
December 2017

A first assessment of Fraxinus excelsior (common ash) susceptibility to Hymenoscyphus fraxineus (ash dieback) throughout the British Isles.

Sci Rep 2017 11 29;7(1):16546. Epub 2017 Nov 29.

Forest Research, Northern Research Station, Roslin Midlothian, EH25 9SY, UK.

Ash dieback (ADB), caused by Hymenoscyphus fraxineus, has severely damaged a large proportion of ash trees (Fraxinus excelsior) in continental Europe. We have little damage data for the British Isles where the disease was found only five years ago in the Southeast, and is still spreading. A large-scale screening trial to evaluate ADB damage to provenances of F. excelsior sourced from throughout the British Isles was planted in 2013 in the southeast of England. In 2016, we scored trees by their level of ADB damage observed in field at the two worst affected (based on assessments in 2015) of the 14 sites. Significant differences were found in average ADB damage among planting sites and seed source provenances. Trees from certain provenances in Scotland were the least damaged by ADB, whereas trees from Wales and Southeast England were the most badly damaged in both trial sites. Thus the levels of ADB damage currently seen in ash populations in Southeast England may not be an accurate predictor of the damage expected in future throughout the British Isles. Given all provenances contained some healthy trees, a breeding programme to produce genetically variable native ash tree populations with lower ADB susceptibility may be feasible.
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http://dx.doi.org/10.1038/s41598-017-16706-6DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5707348PMC
November 2017

The deepening of Darwin's abominable mystery.

Nat Ecol Evol 2017 May 23;1(6):169. Epub 2017 May 23.

Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3DS, UK.

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http://dx.doi.org/10.1038/s41559-017-0169DOI Listing
May 2017

Genome sequence and genetic diversity of European ash trees.

Nature 2017 01 26;541(7636):212-216. Epub 2016 Dec 26.

School of Biological and Chemical Sciences, Queen Mary University of London, Mile End Road, London E1 4NS, UK.

Ash trees (genus Fraxinus, family Oleaceae) are widespread throughout the Northern Hemisphere, but are being devastated in Europe by the fungus Hymenoscyphus fraxineus, causing ash dieback, and in North America by the herbivorous beetle Agrilus planipennis. Here we sequence the genome of a low-heterozygosity Fraxinus excelsior tree from Gloucestershire, UK, annotating 38,852 protein-coding genes of which 25% appear ash specific when compared with the genomes of ten other plant species. Analyses of paralogous genes suggest a whole-genome duplication shared with olive (Olea europaea, Oleaceae). We also re-sequence 37 F. excelsior trees from Europe, finding evidence for apparent long-term decline in effective population size. Using our reference sequence, we re-analyse association transcriptomic data, yielding improved markers for reduced susceptibility to ash dieback. Surveys of these markers in British populations suggest that reduced susceptibility to ash dieback may be more widespread in Great Britain than in Denmark. We also present evidence that susceptibility of trees to H. fraxineus is associated with their iridoid glycoside levels. This rapid, integrated, multidisciplinary research response to an emerging health threat in a non-model organism opens the way for mitigation of the epidemic.
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http://dx.doi.org/10.1038/nature20786DOI Listing
January 2017

Molecular phylogeny and genome size evolution of the genus Betula (Betulaceae).

Ann Bot 2016 05 11;117(6):1023-35. Epub 2016 Apr 11.

School of Biological and Chemical Sciences, Queen Mary University of London, London E1 4NS, UK,

Background And Aims: Betula L. (birch) is a genus of approx. 60 species, subspecies or varieties with a wide distribution in the northern hemisphere, of ecological and economic importance. A new classification of Betula has recently been proposed based on morphological characters. This classification differs somewhat from previously published molecular phylogenies, which may be due to factors such as convergent evolution, hybridization, incomplete taxon sampling or misidentification of samples. While chromosome counts have been made for many species, few have had their genome size measured. The aim of this study is to produce a new phylogenetic and genome size analysis of the genus.

Methods: Internal transcribed spacer (ITS) regions of nuclear ribosomal DNA were sequenced for 76 Betula samples verified by taxonomic experts, representing approx. 60 taxa, of which approx. 24 taxa have not been included in previous phylogenetic analyses. A further 49 samples from other collections were also sequenced, and 108 ITS sequences were downloaded from GenBank. Phylogenetic trees were built for these sequences. The genome sizes of 103 accessions representing nearly all described species were estimated using flow cytometry.

Key Results: As expected for a gene tree of a genus where hybridization and allopolyploidy occur, the ITS tree shows clustering, but not resolved monophyly, for the morphological subgenera recently proposed. Most sections show some clustering, but species of the dwarf section Apterocaryon are unusually scattered. Betula corylifolia (subgenus Nipponobetula) unexpectedly clusters with species of subgenus Aspera Unexpected placements are also found for B. maximowicziana, B. bomiensis, B. nigra and B. grossa Biogeographical disjunctions were found within Betula between Europe and North America, and also disjunctions between North-east and South-west Asia. The 2C-values for Betula ranged from 0·88 to 5·33 pg, and polyploids are scattered widely throughout the ITS phylogeny. Species with large genomes tend to have narrow ranges.

Conclusions: Betula grossa may have formed via allopolyploidization between parents in subgenus Betula and subgenus Aspera. Betula bomiensis may also be a wide allopolyploid. Betula corylifolia may be a parental species of allopolyploids in the subsection Chinenses Placements of B. maximowicziana, B. michauxii and B. nigra need further investigation. This analysis, in line with previous studies, suggests that section Apterocaryon is not monophyletic and thus dwarfism has evolved repeatedly in different lineages of Betula Polyploidization has occurred many times independently in the evolution of Betula.
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http://dx.doi.org/10.1093/aob/mcw048DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4866320PMC
May 2016

Unidirectional diploid-tetraploid introgression among British birch trees with shifting ranges shown by restriction site-associated markers.

Mol Ecol 2016 Jun 11;25(11):2413-26. Epub 2016 May 11.

School of Biological and Chemical Sciences, Queen Mary University of London, London, E1 4NS, UK.

Hybridization may lead to introgression of genes among species. Introgression may be bidirectional or unidirectional, depending on factors such as the demography of the hybridizing species, or the nature of reproductive barriers between them. Previous microsatellite studies suggested bidirectional introgression between diploid Betula nana (dwarf birch) and tetraploid B. pubescens (downy birch) and also between B. pubescens and diploid B. pendula (silver birch) in Britain. Here, we analyse introgression among these species using 51 237 variants in restriction site-associated (RAD) markers in 194 individuals, called with allele dosages in the tetraploids. In contrast to the microsatellite study, we found unidirectional introgression into B. pubescens from both of the diploid species. This pattern fits better with the expected nature of the reproductive barrier between diploids and tetraploids. As in the microsatellite study, introgression into B. pubescens showed clear clines with increasing introgression from B. nana in the north and from B. pendula in the south. Unlike B. pendula alleles, introgression of B. nana alleles was found far from the current area of sympatry or allopatry between B. nana and B. pubescens. This pattern fits a shifting zone of hybridization due to Holocene reduction in the range of B. nana and expansion in the range of B. pubescens.
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http://dx.doi.org/10.1111/mec.13644DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4999052PMC
June 2016

Molecular markers for tolerance of European ash (Fraxinus excelsior) to dieback disease identified using Associative Transcriptomics.

Sci Rep 2016 Jan 13;6:19335. Epub 2016 Jan 13.

Department of Biology, University of York, York, UK.

Tree disease epidemics are a global problem, impacting food security, biodiversity and national economies. The potential for conservation and breeding in trees is hampered by complex genomes and long lifecycles, with most species lacking genomic resources. The European Ash tree Fraxinus excelsior is being devastated by the fungal pathogen Hymenoscyphus fraxineus, which causes ash dieback disease. Taking this system as an example and utilizing Associative Transcriptomics for the first time in a plant pathology study, we discovered gene sequence and gene expression variants across a genetic diversity panel scored for disease symptoms and identified markers strongly associated with canopy damage in infected trees. Using these markers we predicted phenotypes in a test panel of unrelated trees, successfully identifying individuals with a low level of susceptibility to the disease. Co-expression analysis suggested that pre-priming of defence responses may underlie reduced susceptibility to ash dieback.
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http://dx.doi.org/10.1038/srep19335DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4725942PMC
January 2016

250 years of hybridization between two biennial herb species without speciation.

AoB Plants 2015 Jul 17;7. Epub 2015 Jul 17.

School of Biological and Chemical Sciences, Queen Mary University of London, Mile End Road, London E1 4NS, UK

Hybridization between plant species can generate novel morphological diversity and lead to speciation at homoploid or polyploid levels. Hybrids between biennial herbs Tragopogon pratensis and T. porrifolius have been studied in experimental and natural populations for over 250 years. Here we examine their current status in natural populations in southeast England. All hybrids found were diploid; they tended to grow taller and with more buds than their parental species; many showed partial fertility; a few showed evidence of backcrossing. However, we found no evidence to suggest that the hybrids are establishing as a new species, nor can we find literature documenting speciation of these hybrids elsewhere. This lack of speciation despite at least 250 years of hybridization contrasts with the fact that both parental species have formed new allopolyploid species through hybridization with another diploid, T. dubius. Understanding why hybrids often do not speciate, despite repeated opportunities, would enhance our understanding of both the evolutionary process and risk assessments of invasive species.
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http://dx.doi.org/10.1093/aobpla/plv081DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4571729PMC
July 2015

Speciation by genome duplication: Repeated origins and genomic composition of the recently formed allopolyploid species Mimulus peregrinus.

Evolution 2015 Jun 27;69(6):1487-1500. Epub 2015 May 27.

Department of Biology, College of William and Mary, Williamsburg, Virginia, 23185.

Whole genome duplication (polyploidization) is a mechanism of "instantaneous" species formation that has played a major role in the evolutionary history of plants. Much of what we know about the early evolution of polyploids is based upon studies of a handful of recently formed species. A new polyploid hybrid (allopolyploid) species Mimulus peregrinus, formed within the last 140 years, was recently discovered on the Scottish mainland and corroborated by chromosome counts. Here, using targeted, high-depth sequencing of 1200 genic regions, we confirm the parental origins of this new species from M. x robertsii, a sterile triploid hybrid between the two introduced species M. guttatus and M. luteus that are naturalized and widespread in the United Kingdom. We also report a new population of M. peregrinus on the Orkney Islands and demonstrate that populations on the Scottish mainland and Orkney Islands arose independently via genome duplication from local populations of M. x robertsii. Our data raise the possibility that some alleles are already being lost in the evolving M. peregrinus genomes. The recent origins of a new species of the ecological model genus Mimulus via allopolyploidization provide a powerful opportunity to explore the early stages of hybridization and genome duplication in naturally evolved lineages.
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http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5033005PMC
http://dx.doi.org/10.1111/evo.12678DOI Listing
June 2015

The legacy of diploid progenitors in allopolyploid gene expression patterns.

Philos Trans R Soc Lond B Biol Sci 2014 Aug;369(1648)

Department of Biology, Reed College, Portland, OR 97202, USA.

Allopolyploidization (hybridization and whole-genome duplication) is a common phenomenon in plant evolution with immediate saltational effects on genome structure and gene expression. New technologies have allowed rapid progress over the past decade in our understanding of the consequences of allopolyploidy. A major question, raised by early pioneer of this field Leslie Gottlieb, concerned the extent to which gene expression differences among duplicate genes present in an allopolyploid are a legacy of expression differences that were already present in the progenitor diploid species. Addressing this question necessitates phylogenetically well-understood natural study systems, appropriate technology, availability of genomic resources and a suitable analytical framework, including a sufficiently detailed and generally accepted terminology. Here, we review these requirements and illustrate their application to a natural study system that Gottlieb worked on and recommended for this purpose: recent allopolyploids of Tragopogon (Asteraceae). We reanalyse recent data from this system within the conceptual framework of parental legacies on duplicate gene expression in allopolyploids. On a broader level, we highlight the intellectual connection between Gottlieb's phrasing of this issue and the more contemporary framework of cis- versus trans-regulation of duplicate gene expression in allopolyploid plants.
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http://dx.doi.org/10.1098/rstb.2013.0354DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4071527PMC
August 2014

Molecular footprints of the Holocene retreat of dwarf birch in Britain.

Mol Ecol 2014 Jun 16;23(11):2771-82. Epub 2014 May 16.

School of Biological and Chemical Sciences, Queen Mary University of London, London, E1 4NS, UK.

Past reproductive interactions among incompletely isolated species may leave behind a trail of introgressed alleles, shedding light on historical range movements. Betula pubescens is a widespread native tetraploid tree species in Britain, occupying habitats intermediate to those of its native diploid relatives, B. pendula and B. nana. Genotyping 1134 trees from the three species at 12 microsatellite loci, we found evidence of introgression from both diploid species into B. pubescens, despite the ploidy difference. Surprisingly, introgression from B. nana, a dwarf species whose present range is highly restricted in northern, high-altitude peat bogs, was greater than introgression from B. pendula, which is morphologically similar to B. pubescens and has a substantially overlapping range. A cline of introgression from B. nana was found extending into B. pubescens populations far to the south of the current B. nana range. We suggest that this genetic pattern is a footprint of a historical decline and/or northwards shift in the range of B. nana populations due to climate warming in the Holocene. This is consistent with pollen records that show a broader, more southerly distribution of B. nana in the past. Ecological niche modelling predicts that B. nana is adapted to a larger range than it currently occupies, suggesting additional factors such as grazing and hybridization may have exacerbated its decline. We found very little introgression between B. nana and B. pendula, despite both being diploid, perhaps because their distributions in the past have rarely overlapped. Future conservation of B. nana may partly depend on minimization of hybridization with B. pubescens, and avoidance of planting B. pendula near B. nana populations.
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http://dx.doi.org/10.1111/mec.12768DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4237149PMC
June 2014

Genome sequence of dwarf birch (Betula nana) and cross-species RAD markers.

Mol Ecol 2013 Jun 21;22(11):3098-111. Epub 2012 Nov 21.

School of Biological and Chemical Sciences, Queen Mary University of London, Mile End Road, London, E1 4NS, UK.

New sequencing technologies allow development of genome-wide markers for any genus of ecological interest, including plant genera such as Betula (birch) that have previously proved difficult to study due to widespread polyploidy and hybridization. We present a de novo reference genome sequence assembly, from 66× short read coverage, of Betula nana (dwarf birch) - a diploid that is the keystone woody species of subarctic scrub communities but of conservation concern in Britain. We also present 100 bp PstI RAD markers for B. nana and closely related Betula tree species. Assembly of RAD markers in 15 individuals by alignment to the reference B. nana genome yielded 44-86k RAD loci per individual, whereas de novo RAD assembly yielded 64-121k loci per individual. Of the loci assembled by the de novo method, 3k homologous loci were found in all 15 individuals studied, and 35k in 10 or more individuals. Matching of RAD loci to RAD locus catalogues from the B. nana individual used for the reference genome showed similar numbers of matches from both methods of RAD locus assembly but indicated that the de novo RAD assembly method may overassemble some paralogous loci. In 12 individuals hetero-specific to B. nana 37-47k RAD loci matched a catalogue of RAD loci from the B. nana individual used for the reference genome, whereas 44-60k RAD loci aligned to the B. nana reference genome itself. We present a preliminary study of allele sharing among species, demonstrating the utility of the data for introgression studies and for the identification of species-specific alleles.
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http://dx.doi.org/10.1111/mec.12131DOI Listing
June 2013

Monkeying around with ploidy.

Mol Ecol 2012 Nov;21(21):5159-61

School of Biological and Chemical Sciences, Queen Mary University of London, London, E1 4NS, UK.

Inferences of whole genome duplication (WGD) events accompany the annotation of every newly sequenced plant genome, but much remains unknown about the evolutionary processes and pathways relating to WGD (Soltis et al. 2010). What ecological, biogeographical and genetic factors cause WGD to occur in nature? How does WGD affect gene expression? How do genomes evolve after WGD? New species that have arisen recently through WGD are good places to seek answers to such questions. These could be relatively common in nature, but reliably demonstrating their recent origin requires documentary evidence, which can be very hard to come by. Thus far, records of species introductions and meticulous botanizing have demonstrated six new natural allopolyploids in just four genera: Tragopogon miscellus and T. mirus, Senecio cambrensis and S. eboracensis, Spartina anglica and Cardamine schultzii (Abbott & Rieseberg 2012; Ainouche et al. 2009; Soltis & Soltis 2009). It is risky to generalize about a universal feature of plant evolution from such a small sample; more examples are needed, in different genera. It is therefore of considerable interest that Mario Vallejo-Marin of University of Stirling has this year named a new allopolyploid species of monkey flower, Mimulus peregrinus, and presented evidence that it is <140 years old (Vallejo-Marin 2012). This discovery is particularly timely as the monkey flower genus is developing rapidly as a model system for ecological genetics (Wu et al. 2008), and in the current issue of Molecular Ecology, Jennifer Modliszewski and John Willis of Duke University present new data showing high genetic diversity in another recently discovered monkey flower allopolyploid, M. sookensis (Modliszewski & Willis 2012).
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http://dx.doi.org/10.1111/mec.12005DOI Listing
November 2012

Next-generation sequencing and genome evolution in allopolyploids.

Am J Bot 2012 Feb 20;99(2):372-82. Epub 2012 Jan 20.

School of Biological and Chemical Sciences, Queen Mary University of London, Mile End Road, London, E1 4NS, UK.

Premise Of The Study: Hybridization and polyploidization (allopolyploidy) are ubiquitous in the evolution of plants, but tracing the origins and subsequent evolution of the constituent genomes of allopolyploids has been challenging. Genome doubling greatly complicates genetic analyses, and this has long hindered investigation in that most allopolyploid species are "nonmodel" organisms. However, recent advances in sequencing and genomics technologies now provide unprecedented opportunities to analyze numerous genetic markers in multiple individuals in any organism.

Methods: Here we review the application of next-generation sequencing technologies to the study of three aspects of allopolyploid genome evolution: duplicated gene loss and expression in two recently formed Tragopogon allopolyploids, intergenomic interactions and chromosomal evolution in Tragopogon miscellus, and repetitive DNA evolution in Nicotiana allopolyploids.

Key Results: For the first time, we can explore on a genomic scale the evolutionary processes that are ongoing in natural allopolyploids and not be restricted to well-studied crops and genetic models.

Conclusions: These approaches can be easily and inexpensively applied to many other plant species-making any evolutionarily provocative system a new "model" system.
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http://dx.doi.org/10.3732/ajb.1100395DOI Listing
February 2012

Rapid, repeated, and clustered loss of duplicate genes in allopolyploid plant populations of independent origin.

Curr Biol 2012 Feb 19;22(3):248-52. Epub 2012 Jan 19.

Department of Biology, University of Florida, Gainesville, FL 32611, USA.

The predictability of evolution is debatable, with recent evidence suggesting that outcomes may be constrained by gene interaction networks [1]. Whole-genome duplication (WGD; polyploidization-ubiquitous in plant evolution [2]) provides the opportunity to evaluate the predictability of genome reduction, a pervasive feature of evolution [3, 4]. Repeated patterns of genome reduction appear to have occurred via duplicated gene (homeolog) loss in divergent species following ancient WGD [5-9], with evidence for preferential retention of duplicates in certain gene classes [8-10]. The speed at which these patterns arise is unknown. We examined presence/absence of 70 homeologous loci in 59 Tragopogon miscellus plants from five natural populations of independent origin; this allotetraploid arose ~80 years ago via hybridization between diploid parents and WGD [11]. Genes were repeatedly retained or lost in clusters, and the gene ontology categories of the missing genes correspond to those lost after ancient WGD in the same family (Asteraceae; sunflower family) [6] and with gene dosage sensitivity [8]. These results provide evidence that the outcomes of WGD are predictable, even in 40 generations, perhaps due to the connectivity of gene products [8, 10, 12]. The high frequency of single-allele losses detected and low frequency of changes fixed within populations provide evidence for ongoing evolution.
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http://dx.doi.org/10.1016/j.cub.2011.12.027DOI Listing
February 2012

Transcriptomic shock generates evolutionary novelty in a newly formed, natural allopolyploid plant.

Curr Biol 2011 Apr 17;21(7):551-6. Epub 2011 Mar 17.

Department of Biology, University of Florida, Gainesville, FL 32611, USA.

New hybrid species might be expected to show patterns of gene expression intermediate to those shown by parental species. "Transcriptomic shock" may also occur, in which gene expression is disrupted; this may be further modified by whole genome duplication (causing allopolyploidy). "Shock" can include instantaneous partitioning of gene expression between parental copies of genes among tissues. These effects have not previously been studied at a population level in a natural allopolyploid plant species. Here, we survey tissue-specific expression of 144 duplicated gene pairs derived from different parental species (homeologs) in two natural populations of 40-generation-old allotetraploid Tragopogon miscellus (Asteraceae) plants. We compare these results with patterns of allelic expression in both in vitro "hybrids" and hand-crossed F(1) hybrids between the parental diploids T. dubius and T. pratensis, and with patterns of homeolog expression in synthetic (S(1)) allotetraploids. Partitioning of expression was frequent in natural allopolyploids, but F(1) hybrids and S(1) allopolyploids showed less partitioning of expression than the natural allopolyploids and the in vitro "hybrids" of diploid parents. Our results suggest that regulation of gene expression is relaxed in a concerted manner upon hybridization, and new patterns of partitioned expression subsequently emerge over the generations following allopolyploidization.
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http://dx.doi.org/10.1016/j.cub.2011.02.016DOI Listing
April 2011

Tissue-specific silencing of homoeologs in natural populations of the recent allopolyploid Tragopogon mirus.

New Phytol 2010 Apr;186(1):175-83

Department of Biology, University of Florida, Gainesville, FL 32611, USA.

Recent years have seen rapid advances in our knowledge of the transcriptomic consequences of allopolyploidy, primarily through the study of polyploid crops and model systems. However, few studies have distinguished between homoeologs and between tissues, and still fewer have examined young natural allopolyploid populations of independent origin, whose parental species are still present in the same location. Here, we examined the expression of 13 homoeolog pairs in seven tissues of 10 plants of allotetraploid Tragopogon mirus from two natural populations formed by independent polyploidizations between Tragopogon dubius and Tragopogon porrifolius c. 40 generations ago. We compare these with patterns of expression in the diploid parental species from the same locality. Of the 910 assays in T. mirus, 576 (63%) showed expression of both homoeologs, 63 (7%) showed no expression of either homoeolog, 186 (20%) showed nonexpression of one homoeolog across all tissues of a plant, and 72 (8%) showed non-expression of a homoeolog in a particular tissue within a plant. We found two cases of reciprocal tissue-specific expression between homoeologs, potentially indicative of subfunctionalization. Our study shows that tissue-specific silencing, and even apparent subfunctionalization, can arise rapidly in the early generations of natural allopolyploidy.
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http://dx.doi.org/10.1111/j.1469-8137.2010.03205.xDOI Listing
April 2010

Characterization of duplicate gene evolution in the recent natural allopolyploid Tragopogon miscellus by next-generation sequencing and Sequenom iPLEX MassARRAY genotyping.

Mol Ecol 2010 Mar;19 Suppl 1:132-46

Department of Biology, University of Florida, Gainesville, 32611, USA.

Tragopogon miscellus (Asteraceae) is an evolutionary model for the study of natural allopolyploidy, but until now has been under-resourced as a genetic model. Using 454 and Illumina expressed sequence tag sequencing of the parental diploid species of T. miscellus, we identified 7782 single nucleotide polymorphisms that differ between the two progenitor genomes present in this allotetraploid. Validation of a sample of 98 of these SNPs in genomic DNA using Sequenom MassARRAY iPlex genotyping confirmed 92 SNP markers at the genomic level that were diagnostic for the two parental genomes. In a transcriptome profile of 2989 SNPs in a single T. miscellus leaf, using Illumina sequencing, 69% of SNPs showed approximately equal expression of both homeologs (duplicate homologous genes derived from different parents), 22% showed apparent differential expression and 8.5% showed apparent silencing of one homeolog in T. miscellus. The majority of cases of homeolog silencing involved the T. dubius SNP homeolog (164/254; 65%) rather than the T. pratensis homeolog (90/254). Sequenom analysis of genomic DNA showed that in a sample of 27 of the homeologs showing apparent silencing, 23 (85%) were because of genomic homeolog loss. These methods could be applied to any organism, allowing efficient and cost-effective generation of genetic markers.
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http://dx.doi.org/10.1111/j.1365-294X.2009.04469.xDOI Listing
March 2010

Does hybridization between divergent progenitors drive whole-genome duplication?

Mol Ecol 2009 Aug 14;18(16):3334-9. Epub 2009 Jul 14.

Department of Biology, University of Florida, Gainesville, FL 32611, USA.

Hybridization and whole-genome duplication are both potential mechanisms of rapid speciation which sometimes act in concert. Recent surveys, showing that homoploid hybrid species tend to be derived from parents that are less evolutionarily divergent than parents of polyploid hybrid species (allopolyploids), have been interpreted as supporting a hypothesis that high divergence between hybridizing species drives whole-genome duplication. Here, we argue that such conclusions stem from problems in sampling (especially the omission of autopolyploids) and null model selection, and underestimate the importance of selection. The data simply demonstrate that hybridization between divergent parents has a higher probability of successfully producing a species if followed by polyploidization.
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http://dx.doi.org/10.1111/j.1365-294X.2009.04285.xDOI Listing
August 2009