Morphological and molecular analyses of fungal endophytes of achlorophyllous gametophytes of<i>Diphasiastrum alpinum</i>(Lycopodiaceae)

SummaryFungi (Eumycota) form close associations with plants, with which they have co-existed since the dawn of life on land, but their diversity in early terrestrial ecosystems is still poorly understood.We studied petrographic sections of exceptionally well-preserved petrified plants from the 407 million yr-old Rhynie Chert (Scotland, UK). For comparative purposes, we illustrate fungal associations in four extant lower land plants.We document two new endophytes in the plant Horneophyton lignieri: Palaeoglomus boullardii (sp. nov. Glomeromycota) colonizes parenchyma in a discontinuous zone of the outer cortex of the aerial axes, forming arbuscule-like structures, vesicles and spores; Palaeoendogone gwynne-vaughaniae (gen. nov., sp. nov. Mucoromycotina) colonizes parenchyma in the basal part of the plant, where it is present in intercellular spaces and as intracellular coils but absent from rhizoids.Critical comparisons between the newly discovered Horneophyton endophytes, fungi previously described from the Rhynie Chert and fungal colonization in extant lower land plants reveal several features characteristic of both Mucoromycotina and Glomeromycota. A reappraisal of fungal associations in early land plants indicates that they are more diverse than assumed hitherto, overturning the long-held paradigm that the early endophytes were exclusively Glomeromycota.

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“… See our critical interpretation of Diphasiastrum alpinum (Horn et al . () in Supporting Information Notes S1. …”

Section: Resultsmentioning

confidence: 99%

“…S1 Diagram of a spore of P alaeoglomus boullardii showing the layers of the spore wall. Notes S1 Comments concerning fungal associations in D iphasiastrum alpinum (Horn et al ., ).…”

mentioning

confidence: 97%

Fungal associations in Horneophyton ligneri from the Rhynie Chert (c. 407 million year old) closely resemble those in extant lower land plants: novel insights into ancestral plant–fungus symbioses

et al. 2014

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“…The first sequencing study on two gametophytes of Lycopodium hypogeae identified the fungus as a member of the Glomeraceae (following Redecker et al, 2013 for the classification of arbuscular mycorrhizal fungi), a clade also found in other mycoheterotrophic lineages (Merckx et al, 2009;Merckx, 2013). In contrast, a second molecular study found that both ITS and LSU sequences identified the fungus in the gametophytes of Lycopodium alpinum as Sebacinales group B, a basal clade of the agaricomycetes (Basidiomycota) (Horn et al, 2013).…”

Section: Gametophytesmentioning

confidence: 99%

“…Conspicuously absent are any bona fide records of basidiomycetes. The recent report that the main endophyte in gametophytes of Lycopodium alpinum is a basidiomycete (Horn et al, 2013), despite compelling cytological evidence (Bruchmann, 1898;Lang, 1899;Campbell, 1908;Burgeff, 1938;Duckett & Ligrone, 1992;Schmid & Oberwinkler, 1993) and molecular data (Winther & Friedman, 2007a) to the contrary in this and other lycopod gametophytes, is almost certainly due to flawed analysis procedures (see Rimington et al, 2014 for a full critique).…”

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confidence: 99%

Pteridophyte fungal associations: Current knowledge and future perspectives

Pressel

Bidartondo

Field

et al. 2016

J of Sytematics Evolution

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Current understanding of the nature and function of fungal associations in pteridophytes is surprisingly patchy given their key evolutionary position, current research foci on other early-branching plant clades, and major efforts at unravelling mycorrhizal evolution and the mechanisms underlying this key interaction between plants and fungi. Here we provide a critical review of current knowledge of fungal associations across pteridophytes and consider future directions making recommendations along the way. From a comprehensive survey of the literature, a confused picture emerges: suggestions that members of the Lycopsida harbour Basidiomycota fungi contrast sharply with extensive cytological and recent molecular evidence pointing to exclusively Glomeromycota and/or Mucoromycotina associations in this group. Similarly, reports of dark septate, assumingly ascomycetous, hyphae in a range of pteridophytes, advocating a mutualistic relationship, are not backed by functional evidence and the fact that the fungus invariably occupies dead host tissue points to saprotrophy and not mutualism. The best conclusion that can be reached based on current evidence is that the fungal symbionts of pteridophytes belong to the two fungal lineages Mucoromycotina and Glomeromycota. Do symbiotic fungi and host pteridophytes engage in mutually beneficial partnerships? To date, only two pioneering studies have addressed this key question demonstrating reciprocal exchange of nutrients between the sporophytes of Ophioglossum vulgatum and Osmunda regalis and their fungal symbionts. There is a pressing need for more functional investigations also extending to the gametophyte generation and coupled with in vitro isolation and resynthesis studies to unravel the effect of the fungi on their host.

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“…exceptions, such as Diphasiastrum alpinum (Lycopodiaceae) associated with basidiomycetes (Horn et al 2013). Gametophytes grow in divergent habitats ranging from underground, terrestrial on the ground, epilithic on rocks, and epiphytic on tree trunks .…”

Section: Introductionmentioning

confidence: 99%

Arbuscular mycorrhizal colonization in field-collected terrestrial cordate gametophytes of pre-polypod leptosporangiate ferns (Osmundaceae, Gleicheniaceae, Plagiogyriaceae, Cyatheaceae)

et al. 2015

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To determine the mycorrhizal status of pteridophyte gametophytes in diverse taxa, the mycorrhizal colonization of wild gametophytes was investigated in terrestrial cordate gametophytes of pre-polypod leptosporangiate ferns, i.e., one species of Osmundaceae (Osmunda banksiifolia), two species of Gleicheniaceae (Diplopterygium glaucum, Dicranopteris linearis), and four species of Cyatheales including tree ferns (Plagiogyriaceae: Plagiogyria japonica, Plagiogyria euphlebia; Cyatheaceae: Cyathea podophylla, Cyathea lepifera). Microscopic observations revealed that 58 to 97% of gametophytes in all species were colonized with arbuscular mycorrhizal (AM) fungi. Fungal colonization was limited to the multilayered midrib (cushion) tissue in all gametophytes examined. Molecular identification using fungal SSU rDNA sequences indicated that the AM fungi in gametophytes primarily belonged to the Glomeraceae, but also included the Claroideoglomeraceae, Gigasporaceae, Acaulosporaceae, and Archaeosporales. This study provides the first evidence for AM fungal colonization of wild gametophytes in the Plagiogyriaceae and Cyatheaceae. Taxonomically divergent photosynthetic gametophytes are similarly colonized by AM fungi, suggesting that mycorrhizal associations with AM fungi could widely occur in terrestrial pteridophyte gametophytes.

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Morphological and molecular analyses of fungal endophytes of achlorophyllous gametophytes ofDiphasiastrum alpinum(Lycopodiaceae)

Cited by 35 publications

References 99 publications

Fungal associations in Horneophyton ligneri from the Rhynie Chert (c. 407 million year old) closely resemble those in extant lower land plants: novel insights into ancestral plant–fungus symbioses

Fungal associations in Horneophyton ligneri from the Rhynie Chert (c. 407 million year old) closely resemble those in extant lower land plants: novel insights into ancestral plant–fungus symbioses

Pteridophyte fungal associations: Current knowledge and future perspectives

Arbuscular mycorrhizal colonization in field-collected terrestrial cordate gametophytes of pre-polypod leptosporangiate ferns (Osmundaceae, Gleicheniaceae, Plagiogyriaceae, Cyatheaceae)

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