David Moore's World of Fungi: where mycology starts

Monotropoid mycorrhizas

Until fairly recently the mycorrhizal association formed by plants of the Montropaceae were classified as arbutoid.  However, fundamental differences were noted and resulted in a new category of mycorrhiza being created.

Typical arbutoid mycorrhizas such as Arbustus and Pyrola show extensive intracellular penetration, with coils of hyphae filling large volumes in many cells. In contrast, fungi colonising achlorophylous plants in the Monotropaceae family (but now included within the Ericaceae), such as Monotropa hypopitys (in Europe) and M. uniflora (North America) shown in Fig. 1, never actually penetrate the plant cell walls. This feature was sufficiently distinct to warrant the creation of a new class of mycorrhizas: the monotropoid mycorrhizas.

Fig. 1. Monotropa uniflora (also known as the Ghost Plant, Indian Pipe, or Corpse Plant, is a herbaceous perennial plant, formerly classified in the family Monotropaceae, but now included within the Ericaceae). It lacks chlorophyll and parasitises its mycorrhizal partner.  © Charles Lewallen with permission.

The Monotropaceae are also unusual in that all 10 genera in the family are entirely achlorophyllous.  This means they contain no chlorophyll, and hence are unable to photosynthesise and produce carbohydrates.  Instead, they use their mycorrhizas not only to obtain minerals and nutrients, but also to tap the carbon supplies of nearby plants via their roots.

These neighbouring plants can include beech, oak and cedar but more usually they are pine, spruce and fir, since Monotropa species are most commonly found in coniferous forests. Fungi in forest soils form ectomycorrhizal associations with trees and also monotropoid associations with the Monotropa species. Carbohydrates pass from conifer to Monotropa via their common mycorrhizal partner, in what is termed a source-sink relationship (demonstrated by supplying conifer trees with sucrose labeled with the radioactive isotope ¹⁴C.  Monotropa was subsequently shown  to have absorbed the radiolabelled carbon).

The tree, already providing energy to the fungus, is probably physiologically 'unaware' of the additional loss of carbon and it is likely that it is the fungus that controls the passage of carbon to Monotropa. Monotropa may supply a different source of carbon to the fungus, or nothing at all, and whether there is a net carbon gain by Monotropa over the course of a season is not yet known. Radiolabelled phosphorus (³²P) injected into Monotropa has been recovered in neighbouring trees and so this relationship may not be entirely one-sided.

Fig. 2. The fungi involved in monotropoid associations belong to the Basidiomycota. Several Boletus spp. such as Boletus edulis, (shown here) have been identified by comparison with pure cultures.  Boletus spp. form ectomycorrhizas with a wide range of tree species, and this may explain how Monotropa is itself associated with many different tree species. Boletus edulis image © Michael Wood with permission.

Monotropa and other Montropaceae species such as Pterospora and Sarcodes are often the only higher plants growing in the herb layer of forests, since the dense shading oftens excludes most chlorophyllous plants, which rely on light to produce carbohydrates.

The root system of Monotropa is highly adapted to gaining all its nutrients via mycorrhizas.  Its roots are surrounded in a dense fungal sheath, from which hyphae spread into the soil. In Monotropa and Pterospora, the sheath encloses the root apex, whilst in Sarcodes sanguinea the apex remains free. In all 3 genera, a Hartig net surrounds the outer epidermal layer, but does not penetrate into the underlying cortex.  However, individual hyphae do grow out of the Hartig net into the outer cortical cells, the walls of which invaginate to accomodate the growing hypha.  These intrusions from the hartig net into the cortical cell walls are known as fungal pegs (Figs 3 - 5). Small protuberances or wall ingrowths begin to develop and extend from the invaginated plant cell wall into the cortical cell (i.e. intracellularly). These protuberances are arrowed red in the electronmicrograph shown as Fig. 4).

Fig. 3. Diagram of m ycorrhiza in Monotropa hypopitys showing fungal peg.  From Werner (1992) Symbiosis of Plants and Microbes.  © 1998 with kind permission from Kluwer Academic Publishers.	Fig. 4. Fungal pegs in Pterospora, with numerous protruberances (red arrows). Reprinted from Smith & Read (1997) Mycorrhizal Symbiosis  by permission of the publisher Academic Press London.	Fig. 5. Fungal peg entering plant cell. From Kendrick (1999) The Fifth Kingdom. © Mycologue Publications with permission.

As the growth proliferate, the surface area within the cell increases massively, producing a structure analagous to a 'transfer cell'.  Transfer cells are found widely in the plant kingdom and are particularly associated with tissues that are involved in nutrient exchange. Eventually, the tip of the fungal peg opens or 'bursts' and a membraneous sac extends from the peg into the cell cytoplasm.  Contents of the fungal peg fill the membraneous sac, but never directly enter the plant cell cytoplasm. A ring of highly osmiophyllic material forms a neckband behind the peg opening, and it is suggested that this prevents backflow of material into the peg.

The bursting of the fungal peg was first thought to facilitate the transfer of materials from fungus to plant.  However, in Pterospora, Sarcodes and Monotropa, the sac material showed no resemblence to the cytoplasmic contents of the fungus, and light microscopy shows that the fungal peg is not empty, but still contains cytoplasm and organelles after 'bursting'. Linear arrays of fibrils (possibly microtubules) and membrane-bounded vesicles can be seen in the sac cytoplasm. It must be concluded that the contents of the membraneous sac is not identical to the contents of the fungal peg.

The number of fungal pegs produced by a monotropoid mycorrhiza is heavily linked to season. The maximum period of peg formation coincides with elongation of the flowering scape in June, whilst the 'bursting' occurs from July to August, when seeds are released. This suggests that during expansion of the flowering scape Monotropa has a high demand for nutrients, especially carbohydrates. The production of transfer cells, stimulated by the advancing fungal pegs, also suggests that rapid nutrient mobilisation is occurring. The 'bursting' could also provide a late surge of nutrients to boost seed production just before the scape senesces.