Basidiomycetous endophytes in jungermannialean (leafy) liverworts have novel cytology and species-specific host ranges: a cytological and experimental study

This article reviews published data on the likely occurrence of basidiomycetous endophytes in jungermannialean (leafy) liverworts and presents a new overview based on observations on freshly collected specimens supplemented with confirmation, by transmission electron microscopy, of dolipore septa in representative taxa. These associations are widespread in the Lophoziaceae and Arnelliaceae and sporadic in the Jungermanniaceae, Scapaniaceae, and Geocalycaceae. They are almost exclusively confined to taxa growing on well-drained, humus-rich substrata and are absent from epiphytes and species from bare rocks and waterlogged habitats. Cross-infection experiments between axenically cultured liverworts (Lophozia, Nardia, Diplophyllum, Southbya, and Aneura in the Metzgeriales) and their mycobionts revealed the associations to be host specific, in striking contrast with the wide host ranges previously recorded for rhizoidal ascomycetes in the Cephaloziaceae and other families. More vigorous growth of resynthesized basidiomycete associations compared with their axenic counterparts is indicative of nutritional benefits to the liverworts. The fungi enter their hosts via the tips of the rhizoids and develop distinctive distributions within the liverwort stem. In the Arnelliaceae, this comprises a central medullary strand; in the Lophoziaceae and Scapaniaceae, the ventral medulla contains a mosaic of infected and noninfected cells. In the latter, pegs of host wall material overgrow penetrating hyphae. Electron microscopy revealed that all of the endophytes have straight imperforate parenthesomes typical of heterobasidiomycetes. The fungi form hyphal coils that outlive the host cytoplasm, and digestion of the mycobionts, as seen in Aneuraceae and orchidaceous mycorrhizas, are absent. Closely similar mosaic infection patterns in Lophoziaceae and Scapaniaceae strenghten the link between the two families based on molecular data, but the present cross-infection and ultrastructural data indicate that the Calypogeia endophyte is ascomycetous rather than a member of the Sebacinaceae as reported previously. The distribution of basidiomycete associations in liverworts suggests that these probably arose several times and are more recent in origin than associations with glomeromycotean fungi.