Fungal symbioses in hornworts: a chequered history - PubMed (original) (raw)

Fungal symbioses in hornworts: a chequered history

Alessandro Desirò et al. Proc Biol Sci. 2013.

Abstract

Hornworts are considered the sister group to vascular plants, but their fungal associations remain largely unexplored. The ancestral symbiotic condition for all plants is, nonetheless, widely assumed to be arbuscular mycorrhizal with Glomeromycota fungi. Owing to a recent report of other fungi in some non-vascular plants, here we investigate the fungi associated with diverse hornworts worldwide, using electron microscopy and molecular phylogenetics. We found that both Glomeromycota and Mucoromycotina fungi can form symbioses with most hornworts, often simultaneously. This discovery indicates that ancient terrestrial plants relied on a wider and more versatile symbiotic repertoire than previously thought, and it highlights the so far unappreciated ecological and evolutionary role of Mucoromycotina fungi.

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Figures

Figure 1.

Figure 1.

(a_–_c) Light and (d_–_j) transmission electron micrographs of fungal endophytes in (a,g,h) Folioceros (MA33) and in (b_–_f) Anthoceros (MA29). (a_–_c) Fungal hyphae occur either (a) scattered in the central region of the thallus (arrowed) or (b) in close association with cyanobacterial colonies (CY; arrowed, enlarged in c). (d) Multi-nucleate hypha (N, nucleus) in cell adjacent to a cyanobacterial colony (CY). (e,f) Intracellular hyphae; (e) branched hypha and (f) hypha bridging the walls (arrowed) of two adjacent host cells. (g) Thick-walled fungal structure in mucilage-filled intercellular space (arrowed) adjacent to intracellular collapsed hyphae (CH). (h) Detail of collapsed intracellular hyphae, note the extensive interfacial matrix (IM). (g,j) Intercellular thick-walled fungal structures with internal thin-walled hyphae (arrowed). Scale bars: (a,b) 100 µm, (c) 20 µm, (d_–_g) 5 µm, (h_–_j) 2 µm.

Figure 2.

Figure 2.

Phylogenetic placement of representative Glomeromycota fungi retrieved from hornworts. The tree encompasses different subclades, as in the study by Krüger et al. [37]. The DNA sequences retrieved from hornworts are in bold. Support values are from maximum-likelihood/Bayesian analyses. Dashes instead of numbers imply that the topology was not supported in the respective analysis. Numbers of retrieved sequences belonging to each Glomeromycota family/order are in brackets. The sequences marked with an asterisk were retrieved using fungal primers NS1-EF3 [20,21].

Figure 3.

Figure 3.

Phylogenetic placement of representative _Endogone_-like fungi detected in hornworts within the Mucoromycotina clade. The tree has 13 clades. The DNA sequences retrieved from hornworts are in bold. Support values are from Bayesian/maximum-likelihood analyses. Dashes instead of numbers imply that the topology was not supported in the respective analysis. Numbers of retrieved sequences belonging to each group are in brackets. Sequences marked with an asterisk were retrieved using fungal primers NS1-EF3 [20,21].

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