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Concept: Fraxinus

42

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.

Concepts: Gene, Organism, Virus, Genome, Olive, Fraxinus, Oleaceae, Fraxinus excelsior

28

The emerald ash borer (Agrilus planipennis Fairmaire, EAB) is an alien, invasive wood-boring insect that is responsible for killing millions of ash trees since its discovery in North America in 2002. All North American ash species (Fraxinus spp.) that EAB has encountered have shown various degrees of susceptibility, while Manchurian ash (Fraxinus mandshurica Ruprecht), which shares a co-evolutionary history with this insect, is resistant. Recent studies have looked into constitutive resistance mechanisms in Manchurian ash, concentrating on the secondary phloem, which is the feeding substrate for the insect. In addition to specialized metabolism and defense-related components, primary metabolites and nutritional summaries can also be important to understand the feeding behavior of insect herbivores. Here, we have compared the nutritional characteristics (water content, total protein, free amino acids, total soluble sugars and starch, percent carbon and nitrogen, and macro- and micronutrients) of outer bark and phloem from black, green, white and Manchurian ash to determine their relevance to resistance or susceptibility to EAB. Water content and concentrations of Al, Ba, Cu, Fe, K, Li, tryptophan and an unknown compound were found to separate black and Manchurian ash from green and white ash in a principal component analysis (PCA), confirming their phylogenetic placements into two distinct clades. The traits that distinguished Manchurian ash from black ash in the PCA were water content and concentrations of total soluble sugars, histidine, lysine, methionine, ornithine, proline, sarcosine, tyramine, tyrosol, Al, Fe, K, Na, V and an unknown compound. However, only proline, tyramine and tyrosol were significantly different, and higher, in Manchurian ash than in black ash.

Concepts: Protein, Amino acid, Metabolism, Nutrition, Essential amino acid, Fraxinus, Emerald ash borer, Fraxinus mandschurica

12

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.

Concepts: Gene, Genetics, Gene expression, Bacteria, Evolution, Species, Fraxinus, Fraxinus excelsior

7

Accelerating international trade and climate change make pathogen spread an increasing concern. Hymenoscyphus fraxineus, the causal agent of ash dieback, is a fungal pathogen that has been moving across continents and hosts from Asian to European ash. Most European common ash trees (Fraxinus excelsior) are highly susceptible to H. fraxineus, although a minority (~5%) have partial resistance to dieback. Here, we assemble and annotate a H. fraxineus draft genome, which approaches chromosome scale. Pathogen genetic diversity across Europe and in Japan, reveals a strong bottleneck in Europe, though a signal of adaptive diversity remains in key host interaction genes. We find that the European population was founded by two divergent haploid individuals. Divergence between these haplotypes represents the ancestral polymorphism within a large source population. Subsequent introduction from this source would greatly increase adaptive potential of the pathogen. Thus, further introgression of H. fraxineus into Europe represents a potential threat and Europe-wide biological security measures are needed to manage this disease.

Concepts: DNA, Gene, Genetics, Bacteria, Biology, Europe, Fraxinus, Fraxinus excelsior

7

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.

Concepts: United Kingdom, Europe, British Isles, London, Fraxinus, English Channel, Fraxinus excelsior, Fraxinus ornus

5

Hymenoscyphus fraxineus, an introduced ascomycete fungus and primary causal agent of European ash dieback, was investigated on Fraxinus mandshurica trees in its native range in Primorye region of Far East Russia. This evidence is the first report of H. fraxineus on healthy, asymptomatic F. mandshurica trees. High-throughput sequencing revealed 49 distinct fungal taxa associated with leaves of F. mandshurica, 12 of which were identified to species level. Phyllosphere fungal assemblages were similar among sites despite being largely geographically distant. Many organisms comprising the foliar fungal community on F. mandshurica in Far East Russia have similarity to those reported inhabiting F. excelsior in Europe based on previous studies. However, Mycosphaerella sp., the most dominant species in this study and detected in nearly all samples, was associated only with F. mandshurica. Genetic diversity of H. fraxineus was significantly higher in the Far East Russian population than in Europe. In contrast to its aggressive behaviour on Fraxinus excelsior in Europe, H. fraxineus appears to be a benign associate of indigenous F. mandshurica that initially induces quiescent and asymptomatic infections in healthy trees prior to active host colonization normally associated with modification of host tissue during senescence.

Concepts: Biology, Fungus, Ascomycota, Russia, Fraxinus, Fraxinus mandschurica, Fraxinus excelsior, Russian Far East

3

Since its accidental introduction from Asia, the emerald ash borer (EAB), Agrilus planipennis Fairmaire (Coleoptera: Buprestidae), has killed millions of ash trees in North America. As it continues to spread, it could functionally extirpate ash with devastating economic and ecological impacts. Little was known about EAB when it was first discovered in North America in 2002, but substantial advances in understanding of EAB biology, ecology, and management have occurred since. Ash species indigenous to China are generally resistant to EAB and may eventually provide resistance genes for introgression into North American species.EABis characterized by stratified dispersal resulting from natural and human-assisted spread, and substantial effort has been devoted to the development of survey methods. Early eradication efforts were abandoned largely because of the difficulty of detecting and delineating infestations. Current management is focused on biological control, insecticide protection of high-value trees, and integrated efforts to slow ash mortality. Expected final online publication date for the Annual Review of Entomology Volume 59 is January 07, 2014. Please see http://www.annualreviews.org/catalog/pubdates.aspx for revised estimates.

Concepts: Biology, United States, North America, Indigenous peoples of the Americas, Fraxinus, Emerald ash borer, Agrilus, Buprestidae

2

Tree diseases are on the increase in many countries and the implications of their appearance can be political, as well as ecological and economic. Preventative policy approaches to tree diseases are difficult to formulate because dispersal pathways for pest and pathogens are numerous, poorly known and likely to be beyond human management control. Genomic techniques could offer the quickest and most predictable approach to developing a disease tolerant native ash. The population of European Ash (Fraxinus Excelsior) has suffered major losses in the last decade, due to the onset of Hymenoscyphus fraxineus (previously called Chalara Fraxinea) commonly known in the UK as ash dieback. This study presents evidence on the public acceptability of tree-breed solutions to the spread of Chalara, with the main aim to provide science and policy with an up-stream ‘steer’ on the likely public acceptability of different tree breeding solutions. The findings showed that whilst there was a firm anti-GM and ‘we shouldn’t tamper with nature’ attitude among UK publics, there was an equally firm and perhaps slightly larger pragmatic attitude that GM (science and technology) should be used if there is a good reason to do so, for example if it can help protect trees from disease and help feed the world. The latter view was significantly stronger among younger age groups (Millennials), those living in urban areas and when the (GM)modified trees were destined for urban and plantation, rather than countryside settings. Overall, our findings suggest that the UK government could consider genomic solutions to tree breeding with more confidence in the future, as large and influential publics appear to be relaxed about the use of genomic techniques to increase tolerance of trees to disease.

Concepts: Disease, Poverty, United Kingdom, Forestry, Wood, Trees, Fraxinus, Fraxinus excelsior

2

During post glacial colonization, loss of genetic diversity due to leading edge effects may be attenuated in forest trees because of their prolonged juvenile phase, allowing many migrants to reach the colonizing front before populations become reproductive. The northern range margins of temperate tree taxa in Europe are particularly suitable to study the genetic processes that follow colonization because they have been little affected by northern refugia. Here we examined how post glacial range dynamics have shaped the genetic structure of common ash (Fraxinus excelsior L.) in its northern range compared to its central range in Europe. We used four chloroplast and six nuclear microsatellites to screen 42 populations (1099 trees), half of which corresponded to newly sampled populations in the northern range and half of which represented reference populations from the central range obtained from previously studies. We found that northern range populations of common ash have the same chloroplast haplotypes as south-eastern European populations, suggesting that colonization of the northern range took place along a single migration route, a result confirmed by the structure at the nuclear microsatellites. Along this route, diversity strongly decreased only in the northern range, concomitantly with increasing population differentiation and complex population substructures, a pattern consistent with a leading edge colonization model. Our study highlights that while diversity is maintained in the central range of common ash due to broad colonizing fronts and high levels of gene flow, it profoundly decreases in the northern range, where colonization was unidirectional and probably involved repeated founder events and population fluctuations. Currently, common ash is threatened by ash dieback, and our results on northern populations will be valuable for developing gene conservation strategies.

Concepts: DNA, Genetics, Demography, Population, Immigration, Population genetics, Fraxinus, Fraxinus excelsior

1

We examined the suitability of cultivated olive, Olea europaea L., as a host for emerald ash borer, Agrilus planipennis Fairmaire. In a bioassay using cut stems from a field-grown olive tree (cv. ‘Manzanilla’) we found that 45% of larvae that had emerged from eggs used to inoculate stems, were recovered alive, many as larvae or prepupae, during periodic debarking of a subset of stems. Three intact stems that 19 larvae successfully entered were exposed to a simulated overwintering treatment. Four live adults emerged afterwards, and an additional pupa and several prepupae were discovered after debarking these stems. Cultivated olive joins white fringetree as one of the two species outside of the genus Fraxinus capable of supporting the development of emerald ash borer from neonate to adult.

Concepts: Olive, Medicinal plants, Fraxinus, Emerald ash borer, Oleaceae, Olea, Agrilus, Buprestidae