Biology subjects

McMullan, M.

Publications and source records attributed to McMullan, M..

7 recordsLinked to original sources

bioRxiv2026

Transcriptional signatures underlying divergent lifestyles of endophytic and pathogenic fungi in early colonisation of wheat roots

Wheat take-all is a root disease which devastates crop yields, caused by the ascomycete fungus Gaeumannomyces tritici. The closely related root endophyte, G. hyphopodioides, has been found to induce local host defence responses which confer protection against take-all and reduce disease severity. Chancellor et al. (2024) investigated host transcriptional response to early colonisation by each of these two fungi. Using this RNA-seq dataset in conjunction with newly available Gaeumannomyces reference genomes, we have completed the picture by characterising the fungal transcriptional activity underpinning these different lifestyles. Even at early time points, their transcriptional profiles differ: G. hyphopodioides shows signs of transcriptional reprogramming between 4 and 5 days post inoculation (dpi), mirroring the wheat response, whereas G. tritici expression varied very little between these two time points despite progressing into the vasculature, instead exhibiting a stealthy expression profile dominated by gene downregulation at earlier time points. Moreover, GO term enrichment in this study identified a stress-response unique to G. hyphopodioides, which may explain the formation of its subepidermal vesicles (SEVs), putative resting structures that are a key difference between the pathogen and non-pathogen, alongside upregulation of many putative effectors and CAZymes. The enrichment of a key lignin-degrading CAZyme may contribute to the lack of stress-response identified in G. tritici, allowing fungal hyphae to overcome localised host lignification. These findings highlight the transcriptional basis of colonisation differences and are a step towards understanding how closely related fungi with different lifestyles modulate their interactions within a common host and tissue.

evolutionary biology↗

bioRxiv2024

Starship giant transposable elements cluster by host taxonomy using kmer-based phylogenetics

Starships are a recently established superfamily of giant cargo-mobilising transposable elements in the fungal subphylum Pezizomyotina (phylum Ascomycota). To date, Starship elements have been identified up to [~]700 Kbp in length and carrying hundreds of accessory genes, which can confer both beneficial and deleterious traits to the host genome. Classification of Starship elements has been centred on the tyrosine recombinase gene that mobilises the element, termed the captain. We contribute a new perspective to Starship classification by using an alignment-free kmer-based phylogenetic tree building method, which can infer relationships between elements in their entirety, including both active and degraded elements and irrespective of high variability in element length and cargo content. In doing so we found that relationships between entire Starships differed from those inferred from captain genes and revealed patterns of element relatedness corresponding to host taxonomy. Using Starships from Gaeumannomyces species as a case study, we found that kmer-based relationships correspond with similarity of cargo gene content. Our results suggest that Starship-mediated horizontal transfer events are frequent between species within the same genus but are less prevalent across larger host evolutionary distances. This novel application of a kmer-based phylogenetics approach overcomes the issue of how to represent and compare highly variable Starships elements as a whole, and in effect shifts the perspective from a captain to a cargo-centred concept of Starship identity. SUMMARYWe applied a kmer-based phylogenetic classification approach to giant Starship cargo-mobilising elements from species across the Pezizomycotina (Ascomycota, Fungi). We found Starship elements to frequently cluster according to host taxonomy, suggesting horizontal transfer of elements is less common across larger evolutionary distances. Kmer-based phylogenetics approaches show promise for both element classification and to inform our understanding of the evolution of Starships and other giant cargo-mobilising elements.

evolutionary biology↗

bioRxiv2024

Evolutionary genomics reveals variation in structure and genetic content implicated in virulence and lifestyle in the genus Gaeumannomyces

Gaeumannomyces tritici is responsible for take-all disease, one of the most important wheat root threats worldwide. High-quality annotated genome resources are sorely lacking for this pathogen, as well as for the closely related antagonist and potential wheat take-all biocontrol agent, G. hyphopodioides. As such, we know very little about the genetic basis of the interactions in this host-pathogen-antagonist system. Using PacBio HiFi sequencing technology we have generated nine near-complete assemblies, including two different virulence lineages for G. tritici and the first assemblies for G. hyphopodioides and G. avenae (oat take-all). Genomic signatures support the presence of two distinct virulence lineages in G. tritici (types A and B), with A strains potentially employing a mechanism to prevent gene copy-number expansions. The CAZyme repertoire was highly conserved across Gaeumannomyces, while candidate secreted effector proteins and biosynthetic gene clusters showed more variability and may distinguish pathogenic and non-pathogenic lineages. A transition from self-sterility (heterothallism) to self-fertility (homothallism) may also be a key innovation implicated in lifestyle. We did not find evidence for transposable element and effector gene compartmentalisation in the genus, however the presence of Starship giant transposable elements likely contributes to genomic plasticity in the genus. Our results depict Gaeumannomyces as an ideal system to explore interactions within the rhizosphere, the nuances of intraspecific virulence, interspecific antagonism, and fungal lifestyle evolution. The foundational genomic resources provided here will enable the development of diagnostics and surveillance of understudied but agriculturally important fungal pathogens.

evolutionary biology↗

bioRxiv2023

Endophytic fungi related to the ash dieback causal agent encode signatures of pathogenicity on European ash

Tree diseases constitute a significant threat to biodiversity worldwide. Pathogen discovery in natural habitats is of vital importance to understanding current and future threats and prioritising efforts towards developing disease management strategies. Ash dieback is a fungal disease of major conservational concern that is infecting common ash trees, Fraxinus excelsior, in Europe. The disease is caused by a non-native fungal pathogen, Hymenoscyphus fraxineus. Other dieback causing-species have not previously been identified in the genus Hymenoscyphus. Here, we discover the pathogenicity potential of two newly identified related species of Asian origin, H. koreanus and H. occultus, and one Europe-native related species, H. albidus. We sequence the genomes of all three Hymenoscyphus species and compare them to that of H. fraxineus. Phylogenetic analysis of core eukaryotic genes identified H. albidus and H. koreanus as sister species, whilst H. occultus diverged prior these and H. fraxineus. All four Hymenoscyphus genomes are of comparable sizes (55-62 Mbp) and GC contents (42-44%) and encode for polymorphic secretomes. Surprisingly, 1,133 predicted secreted proteins are shared between the ash dieback pathogen H. fraxineus and the three related Hymenoscyphus endophytes. Amongst shared secreted proteins are cell death-inducing effector candidates, such as necrosis, and ethylene-inducing peptide 1-like proteins, NLPs, that are upregulated during in planta growth of all Hymenoscyphus species. Indeed, pathogenicity tests showed that all four related Hymenoscyphus species develop pathogenic growth on European ash stems, with native H. albidus being the least virulent. Our results identify the threat Hymenoscypohus species pose to the survival of European ash trees, and highlight the importance of promoting pathogen surveillance in environmental landscapes. Identifying new pathogens and including them in the screening for durable immunity of common ash trees is key to the long-term survival of ash.

plant biology↗

bioRxiv2021

Analysis of wild plant pathogen populations reveals a signal of adaptation in genes evolving for survival in agriculture in the beet rust pathogen (Uromyces beticola)

Improvements in crop resistance to pathogens can reduce yield losses and address global malnourishment today. Gene-for-gene -type interactions can identify new sources of resistance but genetic resistance is often short lived. Ultimately an understanding of how pathogens rapidly adapt will allow us to both increase resistance gene durability and more effectively target chemical treatments. Until recently all agricultural pathogens were living on wild hosts. To understand crop pathogen evolution, we compared genetic diversity in agricultural and wild populations. Wild reservoirs may be the source of emergent pathogen lineages, but here we outline a strategy for comparison of wild and agricultural pathogen populations to highlight genes adapting to agriculture. To address this, we have selected and developed the beet rust system (Beta vulgaris, Uromyces beticola, respectively) as our wild-agricultural model. Our hypothesis is that pathogen adaptation to agricultural crops will be evident as divergence in comparisons of wild and agricultural plant pathogen populations. We sampled isolates in both the wild and agriculture, sequenced and assembled and annotated a large fungal genome and analysed genetic diversity in 42 re-sequenced rust isolates. We found population differentiation between isolates in the wild compared to a predominantly agricultural group. Fungal effector genes are co-evolving with host resistance and are important for successful colonisation. We predicted (and found) that these exhibit a greater signal of diversification and adaptation and more importantly displayed increased wild agricultural divergence. Finding a signal of adaptation in these genes highlights this as an important strategy to identify genes which are key to pathogen success, that analysis of agricultural isolates alone cannot. Author SummaryAs quickly as we develop new strategies for crop defence, pathogens evolve to circumvent them. Novel crop pathogen strains emerge periodically and sweep through the agricultural system. However, because of the (often) clonal nature of these crop pathogens it is difficult to identify the trait that is key to their success. In other words, if there is a trait that is key for success in agriculture, all agricultural isolates will have it (or die without it). What we need is a case and control system where we identify genes important to pathogen success in agricultural by comparing them to pathogens that live in the wild. Here we exemplify this strategy by focussing on genes already known to specifically adapt for the successful colonisation of the host, the fungal effector genes. We find that these genes appear to be evolving quickly and that they are more different between the wild and agriculture than other non-effector genes. These differences between wild and agricultural pathogens suggest we are observing adaptation to agriculture. We do this work in the sugar beet rust system because of its tractability to sample but this understanding about how to identify genetic variation that is key to pathogen success in agriculture is applicable to crop systems where pathogen reservoirs exist as well as other pathogen reservoir systems (e.g. zoonoses).

evolutionary biology↗

bioRxiv2019

Distinct life histories impact dikaryotic genome evolution in the rust fungus Puccinia striiformis causing stripe rust in wheat

Stripe rust of wheat, caused by the obligate biotrophic fungus Puccinia striiformis f. sp. tritici, is a major threat to wheat production world-wide with an estimated yearly loss of US $1 billion. The recent advances in long-read sequencing technologies and tailored-assembly algorithms enabled us to disentangle the two haploid genomes of Pst. This provides us with haplotype-specific information at a whole-genome level. Exploiting this novel information, we perform whole genome comparative genomics of two P. striiformis f. sp. tritici isolates with contrasting life histories. We compare one isolate of the old European lineage (PstS0), which has been asexual for over 50 years, and a Warrior isolate (PstS7 lineage) from a novel incursion into Europe in 2011 from a sexual population in the Himalayan region. This comparison provides evidence that long-term asexual evolution leads to genome expansion, accumulation of transposable elements, and increased heterozygosity at the single nucleotide, structural and allele levels. At the whole genome level, candidate effectors are not compartmentalized and do not exhibit reduced levels of synteny. Yet we were able to identify two subsets of candidate effector populations. About 70% of candidate effectors are invariant between the two isolates while 30% are hypervariable. The latter might be involved in host adaptation on wheat and explain the different phenotypes of the two isolates. Overall this detailed comparative analysis of two haplotype-aware assemblies of P. striiformis f. sp. tritici are the first steps in understanding the evolution of dikaryotic rust fungi at a whole genome level.

evolutionary biology↗

bioRxiv2017

The ash dieback invasion of Europe was founded by two individuals from a native population with huge adaptive potential

Accelerating international trade and climate change make pathogen spread an increasing concern. Hymenoscyphus fraxineus, the causal agent of ash dieback is one such pathogen, moving across continents and hosts from Asian to European ash. Most European common ash (Fraxinus excelsior) trees are highly susceptible to H. fraxineus although a small minority (~5%) evidently have partial resistance to dieback. We have assembled and annotated a draft of the H. fraxineus genome which approaches chromosome scale. Pathogen genetic diversity across Europe, and in Japan, reveals a tight bottleneck into Europe, though a signal of adaptive diversity remains in key host interaction genes (effectors). We find that the European population was founded by two divergent haploid individuals. Divergence between these haplotypes represents the 'shadow' of a large source population and subsequent introduction would greatly increase adaptive potential and the pathogen's threat. Thus, EU wide biological security measures remain an important part of the strategy to manage this disease.

genomics↗