The earliest fungal plant pathogen ?

Abstract Nowadays Fungi are recognized as integral to well-functioning ecosystems, and their broader impact on earth systems is widely acknowledged. Remarkable early fossil evidence from the Rhynie chert (Scotland, UK) shows that Fungi were already diverse in terrestrial ecosystems over 407-million-years-ago, yet evidence for the occurrence of Dikarya (the subkingdom of Fungi that includes the phyla Ascomycota and Basidiomycota) in this fossilised geothermal site is scant. Here we used high resolution white light microscopy and confocal laser scanning microscopy to re-examine historic petrographic thin sections of exceptionally well-preserved fossils from the Rhynie chert site. 3D visualizations obtained by confocal laser scanning microscopy were created from the image stacks; this method proved effective for plant tissues and associated fungal remains. We document a new fungus, Potteromyces asteroxylicola that we attribute to Ascomycota incertae sedis (Dikarya). This fungus colonized the aerial axes and leaf-like appendages of the plant Asteroxylon mackiei (Lycopsida). The fungus is represented by a stroma-like structure and by conidiophores originating in tufts from beneath the cuticle. We show that these caused a reaction in the plant that gave rise to dome-shaped surface projections. This suite of features in the fungus together with the plant reaction tissues provides the earliest unequivocal fossil evidence of a plant pathogenic fungus. The newly described fungus belongs to an extinct lineage that could serve as a minimum node age calibration point for the Ascomycota as a whole or perhaps for the Dikarya crown group. This also might apply to Paleopyrenomycites devonicus, and to the hymenial layer bearing polysporus asci that was attributed to Prototaxites taiti, both previously documented in the Rhynie chert. Our finding also supports an affiliation to Ascomycota rather than to Basidiomycota for the origin of fungal plant pathogenicity.