All for One, and One for All!
by Mark Martin
Panic grass growing well at a soil temperature
of over 50 °C (123 °F). Source.
When I recently attended the Sixth International Symbiosis Society Congress in Madison, Wisconsin, I was awed by the fascinating forms that symbiotic relationships take among diverse organisms. One talk that particularly intrigued me was from the laboratory of Marilyn Roossinck of the Samuel Roberts Nobel Foundation in Oklahoma, which described the mutualistic relationship between a virus, an endophytic fungus, a monocot, and elevated temperatures in geothermal soils. It also made me consider how readily we seem to associate the word "virus" with pathogenic associations, when nature is often far more subtle when it comes to mutualistic partnerships.
The story began in 2002 when it was found that a type of grass growing in the geothermal zones of Yellowstone National Park—panic grass, Dichanthelium lanuginosum—was able to survive intermittent high temperatures in geothermal soils (up to 65 °C.) due to its association with an endophytic fungus, Curvularia protuberata. The fungus is essential to the plant's ability to tolerate temperatures that are lethal to the non-colonized plant. Panic grass, incidentally, has nothing to do with botanical phobias; instead, the name derives from the Latin panicum, referring to foxtail millet.
The thermal areas of Yellowstone National
Park are home to thermotolerant microbes,
and even a few “macrobes”! Source.
Endophytic fungi are quite common among plants and have been implicated in a number of mutualistic associations that display enhanced stress tolerance. But the story was far stranger than this. It turns out that the "thermal tolerance" trait conferred by the endophytic fungus is actually due to a specific RNA virus onboard. (See the 2007 report in Science.) This dsRNA virus is aptly named "Curvularia thermal tolerance virus" (CThTV). Infected fungal mycelia contain two viral dsRNA molecules: a 2.2 kb dsRNA molecule that encodes two ORFs related to viral replication and a 1.8 kb dsRNA molecule with two ORFs with no similarity to any protein of known function.
It has long been known that viruses can modulate the ability of a fungus to interact pathogenically with a host organism, but this is the first report showing a clear-cut mutualistic interplay. Isolates of C. protuberata "cured" of CThTV by freeze-thaw and desiccation cycles conferred no thermal tolerance on the host plant; re-infection of the virus-free fungus with CThTV restored its ability to confer thermal tolerance to the panic grass.
The Roossinck group went on to show that C. protuberata carrying CThTV could colonize eudicots such as tomato, and even provide some thermal tolerance to the new host plant. However, colonization was not as extensive and the thermal tolerance was not as pronounced as with panic grass. As one might guess, work is continuing to determine the mechanism by which the uncharacterized ORFs within the 1.8 dsRNA of CThTV confer the thermal tolerance in this fungal-plant mutualism.
Panic grass phenotype after laboratory testing of thermotolerance (soil temperature cycling between 65 °C for ten hours a day and 37 °C for fourteen hours a day, for two weeks). Legend: Wt = plant infected with virus-bearing fungi. An = plant infected with previously “cured” fungi carrying reintroduced virus. VF = plant infected with virus-free fungi. NS = plant not infected by fungi. Source.
This kind of fungal-conferred stress tolerance may be much more that a rare oddity. In fact, there is some evidence that the ability of fungi (with or without viral modification) to increase stress tolerance is fairly common, and evolutionarily ancient. The existence of multiple "partners" involved in a mutualism has been described for ants, leeches, and many other associations. This relationship between Dichanthelium lanuginosum, Curvularia protuberata, and CThTV is reminiscent of the interrelationships between bacteriophage, Wolbachia, and insects described here.
Clearly, in what appears to be a warming world, understanding how plants can tolerate and prosper at elevated temperatures is an intriguing topic. To a "symbiophile" like myself, learning that the plant has a fungal partner, and that the fungal partner has a viral passenger—and all are working together in a finely tuned mutualistic dance—is a hot topic indeed!
Mark is associate professor in the Department of Biology, University of Puget Sound, an Associate Blogger for STC, and a passionate advocate for the Small Things.
Marquez, L., Redman, R., Rodriguez, R., & Roossinck, M. (2007). A Virus in a Fungus in a Plant: Three-Way Symbiosis Required for Thermal Tolerance Science, 315 (5811), 513-515 DOI: 10.1126/science.1136237