Myco-Heterotrophs: Hacking the Mycorrhizal Network

© Peter Werner
Original publication: Mycena News, March 2006

In discussions of symbiosis, it is often pointed out that close mutualistic relationships (in which both partners benefit) and parasitic relationships (in which one partner benefits at the expense of the other) are fundamentally similar and only differ in the degree of overall benefit to the host. In this view, a symbiont can shift from a parasitic to a mutualistic relationship with its host over evolutionary time. Sometimes, a symbiont may even be mutualistic or parasitic at different phases of its life cycle or that of the host.

This has been an important question in the study of the evolution of mycorrhizas—did any of the various types of mycorrhizal fungi evolve from parasitic ancestors? And do mutualistic fungi ever switch gears and become parasites. Recent study of monotropoid and orchid mycorrhizas have demonstrated that parasitism does take place in these systems, but from an unexpected source—the plant partner in the mycorrhizal symbiosis.

For over a century, it’s been observed that some plants did not contain chlorophyll and therefore needed to get their food heterotrophically (that is, from another organism, living or dead). Such plants were termed “saprophytes” and were thought to get their food from the breakdown of soil organic matter. (Until recently, the term “saprophyte” was also used to describe fungi that obtained food in this way, though the suffix “-phyte” means plant. Such fungi are now more accurately called “saprotrophs” or “saprobes”.) Other authors hypothesized that the roots of these saprotrophs directly parasitized the roots of other plants, though no direct root-toroot contact was ever demonstrated.

Though evidence of “myco-heterotrophic” or epiparasitic (that is, parasitic upon another parasite) nature of Monotropa was first noted by Franz Kamienski in 1881 and again by pioneering mycorrhizist AB Frank in 1892, this hypothesis was largely ignored for the better part of a century until 1960, when Erik Björkmann conducted radioisotope experiments demonstrating the movement of carbon from spruce trees to Monotropa, and that fungi were involved in this carbon flow. Further investigation into the nature of mycorrhizas with monotropes and achlorophyllous orchids and the fungal species involved did not begin until the mid-1980s.

Since this time, new tools have become available to aid investigators in better understanding the nature of the relationship between epiparasitic plants and their fungal associates. DNA sequencing and other molecular techniques have made it possible to identify root and soil fungi that may lack fruiting bodies or other clear morphological features that mycologist have traditionally used to identify fungi. Also, analysis of stable isotopes (non-radioactive isotopes of various elements, such as carbon-13 or nitrogen-15) has become increasingly sophisticated and now allows researchers to track the flow of nutrients through an ecosystem.

Myco-heterotrophy has been found to be more widespread that previously thought. All achlorophyllous plant species studies so far have been shown to be completely dependent upon parasitized fungi as a carbon source. Additionally, a number of species of chlorophyllous plants found in low-light habitats (including chlorophyllous orchids, gentians, and the gametophytes of several species of liverworts, lycophytes, and ferns) have been found to be at least partially mycoheterotrophic.

In most cases, the fungi involved are also engaged in a mycorrhizal relationship with other plants. Many ectomycorrhizal species, including Russula and Tricholoma, have been observed to be parasitized by myco-heterotrophs, and several years ago epiparasitism of arbuscular mycorrhizae (by gentians) was observed for the first time. Also, a few cases of mycoheterotrophs parasitizing major plant pathogens likeArmillaria have been reported. It is therefore the case that these epiparasitic plants are ultimately drawing carbon from the rest of the plant community.

This epiparasitism can be seen as a very clever adaptation on the part of the plant. Carbon is often shared between plants sharing the same fungal symbionts as part of a “common mycorrhizal network”. Plants are adapted to allow infection by a large number of mycorrhizal fungi and to sometimes allow the net flow of carbon to other plants. They are ill-equipped to detect “cheaters” in this system—plants that take carbon but never return it. As long as the epiparasitic plant does not end up compromising the fitness of the fungus, the long-term stability of their food source is assured. The ancestors of myco-heterotrophs, like most plants, are likely to have been mycorrhizal; the loss of chlorophyll and the resulting “cheating” of the common mycorrhizal network came later.

Several studies have found that the relationship between myco-heterotrophs and their fungal symbionts is very specific, with a single plant species or group of species associated with a similarly small group of fungi. For example, the bright red snow plant (Sarcodes sanguinea) of the Sierra Nevada is associated exclusively with Rhizopogon ellenae, while sugar stick (Allotropa virgata) is associated exclusively with matsutake mycelium. (The blooming of sugar stick in spring is therefore a useful indicator of where matsutake may fruit in fall.) A recent study by Martín Bidartondo and Tom Bruns indicates that in the case of pinedrop (Pterospora andromedea), different co-occurring phenotypes within the same population are each associated with symbiosis with different species of Rhizopogon.

There is still much to be learned concerning the plant (and fungal?) parasitism of mycorrhizas and mycorrhizal networks. How widespread is partial myco-heterotrophy in the plant kingdom? Do fungi ever “cheat” the mycorrhizal system? What feedbacks (if any) are present in the mycorrhizal network to discourage cheating? These are all questions that will need to be addressed in order to more deeply understand the role that mycorrhizas play in plant communities.