Microbiome analysis and epigenetic patterns revealed distinct differences between two elm species with contrasting Dutch elm disease resistance.

Abstract

Background: Dutch elm disease (DED), caused by the fungus Ophiostoma novo-ulmi, has devastated elm species in Europe and North America for over a century. While the Chinese elm (Ulmus parvifolia) frequently displays notable resistance to DED, the European wych elm (Ulmus glabra) remains highly susceptible. Understanding microbiome interaction and epigenetic factors might help to explain this contrasting resilience and subsequently improve disease management.

Results: Seedlings of both elm species were germinated and maintained under identical environmental conditions. Comparative metabarcoding revealed distinct differences in bacterial and eukaryotic microbiomes, as well as in their associations with lichenized fungi and their photobiont algae. In U. parvifolia, 24 eukaryotic and 14 bacterial taxa were identified as the most differentially abundant microbiome components, and exhibited significantly different levels compared to U. glabra. In particular, Leotiomycetes fungi and Rhizobiales bacteria, both previously implicated in resistance to pathogens, were strongly enriched in U. parvifolia. Lichenized fungi and chlorophyte algae were likewise more abundant in U. parvifolia. In U. glabra, 11 eukaryotic and 16 bacterial taxa were significantly more abundant, including Nocardioides bacteria and Leptospora fungi. Ultra-performance liquid chromatography coupled with mass spectrometry revealed that, compared to U. glabra, U. parvifolia exhibited higher levels of 5-(hydroxymethyl)-2'-deoxycytidine and lower levels of 5-methyl-2'-deoxycytidine and N6-methyl-2'-deoxyadenosine in DNA, as well as increased amounts of 5-methylcytidine, N6-methyladenosine, and 5-hydroxymethyluridine in RNA. The elevated levels of well-established epigenetic markers in DNA and RNA are remarkable. However, it remains unclear what part of the holobiont may be responsible for this effect.

Conclusions: The contrasting susceptibility of Chinese and European elms to DED correlates with pronounced differences in their associated microbial communities and lichens, as well as in patterns of epigenetic nucleoside modifications. In particular, the enrichment of specific stress-associated microbiome components, together with lichen associations and elevated levels of modified DNA and RNA nucleosides in U. parvifolia, may underlie its increased tolerance to DED. Although this study did not identify the factors responsible for DED resistance, it provides valuable insights into microbiomic and epigenetic features that could contribute to the development of new approaches to combat DED. Video Abstract.