21st Century Guidebook to Fungi, SECOND EDITION, by David Moore, Geoffrey D. Robson and Anthony P. J. Trinci

Table of Contents

1. Chapter 2: Evolutionary origins
2. Chapter 3: Natural classification of fungi
   1. The members of the Kingdom
   2. The Chytrids
   3. Neocallimastigomycota
   4. Blastocladiomycota
   5. The traditional zygomycetes
   6. Glomeromycotina
   7. Ascomycota
   8. Basidiomycota
   9. The species concept in fungi
   10. The untrue fungi
   11. Ecosystem mycology
   12. Chapter 3 References and further reading
   13. Buy a PDF of Chapter 3
3. Chapter 4: Hyphal cell biology and growth on solid substrates

3.6 Glomeromycotina

Until recently, arbuscular mycorrhizal (AM) fungi have generally been classified in the ‘Zygomycota’ (in the Order Glomales), but they do not form the zygospores characteristic of zygomycetes, and all ‘glomalean’ fungi form mutualistic symbioses with plants, known as arbuscular mycorrhizas; there is one exception, the genus Geosiphon, which is a symbiont of cyanobacteria in the genus Nostoc. The fungi are dependent on carbohydrates derived from their photoautotrophic symbiotic partners and represent a significant carbon sink in terrestrial ecosystems. In return, AM fungi provide inorganic nutrients (mainly phosphorus) to the plants and are therefore essential for plant nutrition. Because most land plants form AM, these fungi must be considered as vital components of terrestrial ecosystems. Initial molecular studies suggested a separate phylum was appropriate for the AM fungi, the ‘Glomeromycota’ (Redecker & Raab, 2006), consisting of the four orders Diversisporales, Glomerales, Archaeosporales and Paraglomerales (Redecker et al., 2013; Redecker & Schüßler (2014). More recently, based on genome-scale data, these four orders have been placed in class Glomeromycetes in a newly-erected subphylum Glomeromycotina, which replaces the name ‘Glomeromycota’. Glomeromycotina being a subphylum of phylum Mucoromycota (Spatafora et al., 2016; and see Section 3.5).

Traditionally, taxonomy of AM fungi has been based on characteristics of the relatively large (80 to 500 µm diameter) multinucleate spores. There is no evidence that the Glomeromycotina reproduce sexually. Studies using molecular marker genes have detected little or no genetic recombination, although it has been shown that Glomus species contain 51 genes encoding all the tools necessary for meiosis (Halary et al., 2011), which might imply that Glomus species have a cryptic sexual cycle (Halary et al., 2013; Kück & Pöggeler, 2009). Clearly, there is a severe limit to the morphology that can be used in taxonomy and fewer than 200 species (or morphotypes) are recognisable; however, combined morphological and molecular analyses have led to the description of three classes, five orders, 14 families and 29 genera (Oehl et al., 2011). The spores have a layered wall and features of this can be used to describe morphospecies. Similarly, spores may be formed singly, in clusters or aggregated in so-called sporocarps and the mode of spore formation has been important in describing genera and families (CLICK HERE for illustration of most of these morphologies).

This is a very challenging group to study. Arbuscular mycorrhiza (AM) fungi are obligate symbionts and none of them has been cultivated without their plant hosts; most probably because AM fungi depend on their host plants to synthesise lipids that they cannot make for themselves (Luginbuehl et al., 2017). This is one of several metabolic abilities that are not found in the AM genome, though there are many transporters and secreted proteins, implying evolutionary adaptation to mutualistic obligate biotrophy (Tang et al., 2016). Genomic data from AM fungi have now revealed indirect evidence of sexual reproduction, such as intact sets of meiotic genes, and homologues of the mating type genes found in other fungi (Corradi & Brachmann, 2017). Nevertheless, pure AM biomass can be obtained only from cultures in transformed plant roots that can be cultivated in tissue culture, but only a small number of AM species are available in this form. Most samples from nature are DNA sample of ‘cryptic species’ that cannot be cultivated even in this way. Consequently, there is an on-going controversy about the definition, dispersal and distribution of species in this clade. The controversy is far from being settled, but it has been well described by Bruns et al. (2017).

Yet, in ecological terms, this is possibly the most important group of fungi because AM fungi form endomycorrhizal associations with about 80% of land plants. The association is essential for plant ecosystem function because the plants depend on it for their mineral nutrient uptake, which is efficiently performed by the mycelium of the fungal symbionts that extends outside the roots. Within root cells AM fungi form hyphal coils or the typical tree-like structures, the arbuscules.

Some also produce storage organs, termed vesicles (hence, another frequently used name for them: vesicular-arbuscular mycorrhizas or VAM-fungi). In phylogenetic terms they are important because they are the oldest unambiguous filamentous fungi known from the fossil record (see the Fossil Fungi section in Chapter 2). Put these two facts together and you get the suggestion that early colonisation of the land surface on Earth was promoted by the success of this plant-fungal symbiosis. Phylogenomics of fungi has established the Glomeromycotina in a basal position of the Mucoromycota as a sister group of Asco- and Basidiomycota (see the cladogram illustrated in Chapter 2).

Ten genera are recognised currently in the Glomeromycotina. Names to look out for include Glomus, which is the largest genus in the phylum, with more than 70 morphospecies (spores, typically with layered wall structure, are formed by budding from a hyphal tip), placed in the Family Glomeraceae, Order Glomerales. It might be appropriate here to explain a specific point of nomenclature: why is Glomus classified in the Glomerales? The International Code of Botanical Nomenclature requires the name of a family or order to be formed from the genitive singular of the name of an included genus. The genitive of Glomus is Glomeris, and so, by International agreement, the name of the Family should be Glomeraceae and the Order Glomerales (rather than ‘Glomales’). For a reminder of the characteristic word-endings used for the principal taxonomic ranks of fungi today visit our ‘Some terminology explained’ Resources Box CLICK HERE.

Gigaspora and Scutellospora are closely related genera in the family Gigasporaceae; their spores form on a bulbous sporogenous cell and germinate through a newly formed opening in the spore wall. These two genera do not form vesicles within roots, and the mycelium external to the root bears ‘auxiliary cells’ of unknown function. For the family Acaulosporaceae the diagnostic feature is the formation of spores next to a ‘saccule’ that collapses during spore maturation and eventually disappears; the included genera are Acaulospora and Entrophospora.

Geosiphon pyriformis (family Geosiphonaceae) is the only member of the phylum that is symbiotic with a cyanobacterium. It forms an endosymbiosis with Nostoc punctiforme, the photobionts being harboured in fungal bladders up to 2 mm in size (Redecker & Raab, 2006).

Because of the difficulties (outlined above) resulting from their obligate symbiosis and our inability to culture them, there is no clear notion of what constitutes a species in the Glomeromycotina at the moment. Environmental studies using molecular markers have revealed a great deal of diversity suggesting that the number of 200 or so described morphospecies might considerably underestimate the true diversity of the Glomeromycotina.

Updated July, 2019