A light and electron microscope study of rhizoid–ascomycete associations and flagelliform axes in British hepatics with observations on the effects of the fungi on host morphology

Abstract

SUMMARYAscomycetous fungi, identified by the presence of simple septa and Woronin bodies, form a range of highly specialized associations with the unicellular rhizoids of 46 {16*2 °.Q) of the 284 species of British liverworts. The majority of these are in the two jungermannialian suborders Lepidoziineae and Cephaloziineae, Thirt\-three species (11'6 "o) also possess flagelliform axes. These extend to depths of 20-30 cnn in peaty substrata and in most species bear abundant fungus-infected rhizoids. When grown in sand or water culture, isolated from their natural substrata (sandstone rocks, peat, Sphagnum, rotten wood), the hepatics are free from rhizoid infections. On returning the plants to their native substrata, the rhizoid-fungus associations are re-established.Each rhizoid or fascicie of rhizoids is infected independently and a continuous strand of fungus-containing cells is absent. Internally the flagelliform axes contain elongate parenchyma cells with abundant plasmodesmata in their transverse end walls. The apices of the axes are invested by mucilage and subapical amyloplasts appear to act as graviperceptive particles.The morphology of the flagelliform axes and the ultrastructure of the rhizoid-fungus association varies greatly between taxa. The Lepidoziaceae and Calypogeiaceae produce fascicles of rhizoids from the bases of rudimentary leaves whereas the flagelliform axes in the Cephaloziaceae are leafless. In Cladopodiella the fungus forms a pseudoparenchymatous sheath around the tips of swollen rhizoids. Development of swollen rhizoids precedes fungal mfection in Lepidozia, Kurzia and Telaranea but not in other genera. Hyphae penetrating the basal walls of the rhizoids in Cephalozia, Nozvellia, Calypogeia and Odontoschisma are ensheathed by host wal! material. These diverse patterns of fungal infection suggest independent, and probably relatively recent, evolution in the various genera.The flagelliform axes in hepatics appear to be major organs of assimilation and perennation structurally and functionally analogous in the former capacity to vascular plant mycorrhizas and particularly the hairs roots in Ericaceae.

Widespread association between the ericoid mycorrhizal fungus Rhizoscyphus ericae and a leafy liverwort in the maritime and sub‐Antarctic

“…Williams et al (1994) concluded that the fungal structures observed in C. varians resembled those described as mycorrhizas or mycothalli. The current study indicates that the latter term is the more appropriate, because of the apparent systemic growth of the fungus and the fact that C. varians lacks flagelliform axes, which might be considered to function in an analogous way to roots (Duckett et al, 1991). In other liverwort-fungal associations the fungal partner does not grow systemically, but proliferates in particular regions, such as in the rhizoids of other members of the Cephaloziaceae or in the inner stem region of members of the Lophoziaceae, Arnelliaceae and Scapaniaceae (Read et al, 2000).…”

“…In other liverwort-fungal associations the fungal partner does not grow systemically, but proliferates in particular regions, such as in the rhizoids of other members of the Cephaloziaceae or in the inner stem region of members of the Lophoziaceae, Arnelliaceae and Scapaniaceae (Read et al, 2000). Fungal hyphae within tissues of British Cephaloziella species similarly appear to be restricted to rhizoid cells and are not present in the walls between the contiguous bases of colonized rhizoids (Duckett et al, 1991).…”

“…In a study of British hepatics, species of the leafy liverwort genus Cephaloziella were found to possess fungal associations restricted to rhizoids, with over half the rhizoid tips colonized (Duckett et al ., 1991). Fungal colonization of rhizoids is characterized by dense intracellular growth that appears analogous to ericoid mycorrhizal coils (Selosse, 2005).…”

The use of the fluorescent dye, 3,3′‐dihexyloxacarbocyanine iodide, for selective staining of ascomycete fungi associated with liverwort rhizoids and ericoid mycorrhizal roots

“…8), a genus closely allied to Calypogeia and Cephalozia, the hyphae both external to and within the rhizoids fluoresced with the same intensity. In Odontoschisma (Figs 10, 11) funguscontaining rhizoids are largely restricted to leafless flagelliform axes (Duckett et al, 1991). Not only did DiOC6(3) pick out individual hyphae in rhizoid tips and shafts (Fig.…”

Association of Glomus tenue (Greenall) Hall with the hepatic Mannia fragrans (Balb.)Frye & Clark

“…Endophytic fungal associations have also been reported in hornworts and liverworts (Duckett et al 1991;Read et al 2000;Ligrone et al 2007). Almost 400 species of bryophilous fungi have been described (Ptaszynska et al2009) but the number is very low if we consider that there probably exist 1.5 million species of fungi (Webster and Weber 2007) and each year about 1500 new species are added by scientists.…”