Aneuraceae

Pressel, Silvia, Bidartondo, Martin I., Ligrone, Roberto & Duckett, Jeffrey G., 2010, Fungal symbioses in bryophytes: New insights in the Twenty First Century, Phytotaxa 9, pp. 238-253 : 245-247

a) Aneuraceae

The Aneuraceae are the only thalloid liverworts found to date to contain basidiomycetous endophytes clearly identified as such by the presence of dolipore septa ( Fig. 4D, F ) ( Bidartondo et al. 2003; Duckett & Ligrone 2008a, b; Ligrone et al. 1993; Nebel et al. 2004; Preussing et al. 2010). The endophyte-host relationships recall those in orchids with the formation of hyphal coils in the colonised cells. These are then digested by the host to be followed by one or more reinfection cycles. As in the Marchantiophyta, the number of cell layers colonized by the fungus varies among taxa: from two to five in Chilean and New Zealand species of Aneura to approximately half the thallus in northern hemisphere A. pinguis (L.) Dumort. to virtually every cell in Cryptothallus .

Whilst this kind of association is also found in Verdoornia R.M.Schust. ( Duckett & Ligrone 2008a) and in nearly all collections of Aneura Dumort. examined to date with the exception of A. pellioides (Horik.) and A. pinguis from California ( Bidartondo & Duckett 2010), the sister genus Riccardia Gray is almost fungus-free. In three Riccardia taxa, all New Zealand endemics, where an endophyte is present the associations appear distinctively different from those in Aneura . Two of these we describe here for the first time ( Fig. 4A–D ), but a third species R. intercellula A.E.Brown is known from but a single collection and has never been refound in nature ( Brown & Braggins 1989). In R. pennata A.E.Brown , prominent basidiomycetous hyphal coils, which show no signs of digestion by the host, fill the ventral epidermal cells ( Fig. 4C ). Even more remarkable is R. cochleata (Hook.f. & Taylor) Kuntze. This species produces achlorophyllous radially symmetrical ‘rhizomes’ ( Brown & Braggins 1989) recalling the ‘roots’ of Haplomitrium but lacking the mucilage investiture of the latter ( Fig. 4A ). While the fleshy surface-growing thalli are fungus-free, the first investigation of the anatomy of the rhizomes revealed that the epidermal cells are packed with hyphal coils ( Fig. 4B ) that undergo digestion cycles.

The fact that the Aneuraceae forms the crown group of an otherwise fungus-free lineage comprising Pleurozia Dumort. , Phyllothallia E.A.Hodgs. and the Metzgeriaceae and the discovery from the initial molecular studies that the fungus from both Aneura and Cryptothallus belongs to the derived genus Tulasnella J.Schröt. ( Bidartondo et al. 2003; Kottke et al. 2003) indicate that the aneuracean associations are of recent origin. Much more extensive sequencing investigations ( Bidartondo & Duckett 2010; Preussing et al. 2010), embracing over one hundred collections of the Aneuraceae , revealed that whilst in the vast majority the fungus is Tulasnella , two gatherings (from Chile and Switzerland) contained Sebacina Tul. , the basidiomycete genus characteristic of leafy liverworts ( Kottke et al. 2003). The molecular diversity discovered within the Tulasnella symbionts ( Bidartondo & Duckett 2010; Preussing et al. 2010), plus the rare occurrence of sebacinoids, in seemingly closely allied aneuracean taxa was at first sight most surprising. However recent molecular studies on the liverworts (Wackowiak et al. 2007; Baczkiewicz et al. 2008; Wickett & Goffinet 2008) have revealed that conservative thallus morphology within the Aneuraceae conceals remarkable genetic diversity. In fact, the diversity in the endophytes closely mirrors that in the hosts and includes noteworthy congruence between the fungal and liverwort phylogenies. Indeed the nesting of Cryptothallus within a single clade of Aneura ( Wickett & Goffinet 2008) , leading to the subsuming of the former into this genus is reinforced by the fungal data. Systematic considerations aside, with wholesale fungal digestion a standard feature of the aneuracean associations compared to those with basidiomycetes in leafy liverworts, it is perhaps not surprising that in this group we find the only achlorophyllose liverworts. Although on the one hand the fungus in the achlorophyllose rhizomes in Riccardia cochleata is most likely an independent acquisition, on the other the rhizomes perhaps provide an example as to how mycoheterotrophy may have evolved in the Aneuraceae .

Figures

FIGURE 4. Basidiomycetes in the Aneuraceae. A-D. Scanning electron micrographs. E, F. Transmission electron micrographs. A, B. Riccardia cochleata. A. Rhizomes extending into the substratum from the lower surface of a thallus (arrowed). B. Hyphal coils in an epidermal cell of a rhizome. C, D. Riccardia pennata. C. Lower epidermal cells almost completely filled by hyphae (h) showing no sign of degeneration. D. Detail of septum with dolipore (d). E, F. Verdoornia succulenta R.M.Schust.. E. Infected cell with healthy (h) and degenerating (dh) hyphae. F. Detail of a typical dolipore septum (d). Scale bars = (A) 500 µm; (B, C, E) 10 µm; (D, F) 2 µm.