Ash dieback evolution and population genomics
Analysis of the genetic variation in ash dieback fungal genomes to understand how populations are evolving now.
Hymenoscyphus fraxineus is a fungus that infects the leaves, stems and branches of the ash tree (Fraxinus excelsior). This fungal infection of ash trees is known as ash dieback and is visible first as blackened dead leaves and dark lesions at the base of dead side shoots. The disease will progress over subsequent years leading to dieback of branches in the crown of the tree and often death.
Ash is the UK’s third most common tree species, it supports over 1000 other species and around 150 of these are highly dependent on ash. Work by Richard Bugg and others (Kew Gardens) estimate that 60-100% of these trees will succumb to the disease. Moreover, we will hit a period of peak mortality in the next few years. Our own work on the fungal invasion of Europe suggests that just two individuals were introduced to Europe (from East Asia) and they have gone on to devastate ash populations.
In preliminary analyses of native diversity from a single Japanese wood we showed that genetic diversity was eight times higher there than present across Europe. Genetic diversity is generally assumed to be a proxy for how adaptable a species is and so it is concerning that diversity is so high in a single wood. Given the devastation of the progeny of just two individuals we now want to understand the invasion process itself, could more individuals invade and, if so, what would be the impact of that introduction?
Finally, the adaptive diversity in the genes that interact with the ash host is higher than that of other genes (in Japan). Again this would suggest that further invasions of Europe would introduce genes that could be even worse for our native ash trees. However, new work from a collaborator in Japan (Prof. Tsuyoshi Hosoya) suggests that, there, the fungus might not be a pathogen at all.
Differences in the native range could be due to evolution of the fungus and/or the host, probably both, and we want to understand the causes of these differences using population genetics.
A fungal invasion presents just a snapshot of the diversity present in the native range and this makes it difficult to understand a disease using this diversity alone. Further introductions of genetic diversity can be an important determinant for an increase in severity of invasions and this means it is important to understand the native diversity and the pathogen’s propensity to invade and evolve.
Our work on the population genomics of the ash dieback fungus shows us that the European population passed through an extreme bottleneck and quickly expanded into Europe. Analysis of genetic diversity present in Europe suggests that diversity present in the range from which invaders arrived was high. Preliminary estimates show that native genetic diversity is high and is present as non-synonymous diversity at putative effectors. However, this diversity is estimated based on a single wood in Japan whereas the native range also encoumpases large parts of China and Eastern Russia.
Furthermore, in Europe there is a signal of preservation of genetic diversity which indicates that structural genomic variation may operate to facilitate invasion. Fungi are known to employ numerous mechanisms which can preserve genetic variation through a bottleneck and also generate novel diversity. The implications of this structural genetic variation have generally been associated with rapid adaptation to new hosts. However, this variation may also be important in preserving and generating genetic variation through a bottleneck. It is important that we understand these processes in greater detail because as our climate changes and global trade increases we might have to deal with more fungal invasions.
A combined MP and LMP version 2 assembly of the ash dieback pathogen genome (Hf-v2; see methods in https://www.nature.com/articles/s41559-018-0548-9)
All MP and LMP sequencing data generated for the Hf-v2.0 genome (PRJEB21027)
The annotation built on that of the version 1 using data from the TSL OpenAshDieBack repository
European single isolates
Isolates were collected from across Europe and jointly sequenced at EI and at Edinburgh Genomics. Isolates were also collected from Japan and sequenced at EI. All but one of these were fruiting bodies which are a spore releasing stage and DNA is present from both the parental haplotypes but also their meiotic products. One of these represents a single haploid isolate (PRJEB21027)
McMullan M et al. (2018) Nature Ecology & Evolution 2:1000-1008
The genetic diversity present in Europe suggests just two individuals started this invasion. Mutations are happening at every generation and natural selection may operate on these but the ash dieback pathogen did most of its evolving in its native range and that’s where we are going to study it next. With collaborators in Japan (Prof. Tsuyoshi Hosoya) and China (Prof. Yonglin Wang) we are currently sampling the native range to understand how the fungus adapts to its hosts there.
Considering the devastation already wrought on our native ash trees, it’s important that we have a better understanding of what might lie in store as the ash dieback pathogen evolves. It is also a fascinating opportunity to highlight what makes a fungus pathogenic, by looking into the differences between Europe and Japan, where the ash dieback fungus does not cause disease.
It is important that we understand these processes in greater detail because as our climate changes and global trade increases we might have to deal with more fungal invasions.