Monday, July 25, 2011

What are “saprophytic” plants all about?

Those of us who penetrate the depths of our local forests in Summer inevitably come across plants which have no chlorophyll. They are always white. Indian pipe (Monotropa uniflora) is the most common of these in B.C., and is just flowering now in late July of 2011. But there are others, including the rare phantom orchid (which is also flowering now in one of our local forest Parks). Such plants, having no chlorophyll, have generally been called saprophytic plants, the assumption being that since they can’t make their own food by photosynthesis, they must be absorbing nutrition from the decaying remains of other organisms in the soil (as, for example, many fungi do). We have recently learned that this is not the case, and that none of these achlorophyllous plants are, in fact, saprophytic. So what is really going on?

The somewhat weird relationships between the non-photosynthesizing flowering plants in a strange sub-group of the heather, Arbutus and Rhododendron family (Ericaceae), known as the Monotropoideae, and others like the phantom orchid, have recently been clarified, in particular by the work of Martin Bidartondo and his associates in California.

The roots of Monotropa have a fungal mantle outside and something resembling a Hartig net of fungal hyphae inside. The one distinguishing morphological feature is that the fungus sends a single haustorium-like peg into each root cell. So you might think that the plant was in a normal mycorrhizal relationship (such as that between many fungi and Douglas-fir). But since this plant cannot photosynthesize, it has no energy-rich carbon compounds to give the fungus. This eventually led mycologists to suspect that the plant might in fact be parasitic on the fungus. This turned out to be the case. The plant is indeed taking food from the fungus.

The main fungi so far identified as being associated with Monotropa are species of the mushroom genus Russula and some other mushrooms in the Family Russulaceae, and the association is often extremely specific and exclusive.
The monotropoid genera Allotropa and Pityopus have victims in the mushroom genus Tricholoma, and other monotropoid genera are tied to different fungi. For example, the genus Pleuricospora has associates in Gautieria, while Sarcodes and Pterospora have associates in Rhizopogon (Gautieria and Rhizopogon are both hypogeous basidiomycetes - genera which fruit underground). Hemitomes and Monotropopsis associate with Hydnellum,(a tooth fungus) while Cheilotheca and Monotropastrum are associated with members of the Russulaceae.
Whatever the morphology suggests, the fact is that the achlorophyllous Monotropaceae are taking food from the fungi, and no-one knows if they are giving anything at all in exchange.

The key to the situation is that the food in question has been found to be coming from a large neighbouring plant (a green one this time) with which the fungus in question has a normal ectomycorrhizal relationship. So we are looking at a tripartite relationship. Coniferous trees, such as Douglas-fir, make sugars and pass them to Russula. Russula translocates them through its mycelium in the soil, and then, for reasons unknown, hands over part to the Monotropa, which thus seems to exploit the fungus directly, and the conifer at second hand as an epiparasite.
Pseudotsuga ---> Russula ---> Monotropa

So, despite what you read in even the most up-to-date dictionary (and the one I have, the Canadian Oxford Dictionary, was published in 1998), Monotropa is not a saprophyte, and can more correctly be described as parasitic on its associated fungus. Interestingly, mycologists have known this since 1960. It makes me wonder about lexicologists.

How did this strange group of plants and its even stranger fungal relationships evolve? I suspect that it all began in a regular ectomycorrhizal relationship (to judge by the way the fungus still grows around and into the roots of the plant) and somehow became turned around, possibly when the ancestor of the plant group lost its ability to produce chlorophyll, and found that the fungus had another source of food, and could be exploited. Even in normal ectomycorrhizal fungi, food moves back and forth between plant and fungus depending on the needs of each partner. Sometimes the mycorrhizal mantle is a food bank for the tree, and sometimes the root is a food bank for the fungus. So you can see how it might start...

J.R. Leake (2005) presented a wide-ranging discussion of plants which are now known to be parasitic on fungi - the antithesis of a mycorrhizal symbiosis. Leake notes that this phenomenon extends to over 400 achlorophyllous plants in 87 genera. The fungi exploited by these plants represent a wide taxonomic spectrum: Glomeromycota (arbuscular mycorrhizal fungi), basidiomycetes in the Ceratobasidiales, Sebacinales, Tulasnellales, resupinate Aphyllophorales, Russulales, Boletales and Agaricales, as well as ascomycetes in the Pezizales (cup fungi and truffles).

1 comment:

  1. They seem to be coming up early this year here on Maryland's Eastern Shore. We've had much more rain her than normal. Does this explain the early emergence, or have I just been too dim-witted to notice them come up this early before?

    Bill Peak