Mushroom Gravitropism Britt A. Bunyard

The images of Ganoderma applanatum were provided by Patrice Benson who passed away suddenly a few months ago. She is sorely missed by so many in the mycological community.

nce a mushroom is cut or picked, it’s dead right? Wrong! A number of things Otell you that the cells making up the picked mushrooms in your basket or refrigerator are still very much alive. They may continue to “drop” spores for a few days after being picked. (Spore release is actually a very active process— as the name for it, ballistospory, implies—requiring living cells.) Some mushrooms, for example Amanitas, may continue to elongate and bend upwards, away from the surface upon which they are placed. This, of course, ensures the cap is up in the air column so that discharged spores may be carried away on the air currents. Furthermore, the gills (or tubes in boletes and polypores) must be exactly vertical or spores will not drop free of the cap. A growth response to gravity is called gravitropism (sometimes, geotropism). I recall first noting this as an undergrad studying under the mycologist Sam Figure 1a. Mazzer at Kent State University. (Ironically, it was at the same time that to find them—no longer pencil-straight. (See Figure 1; Fig.1a is of Pleurotus I was taking a plant physiology course During the night they had continued to dryinus on a tree; Fig. 1b is of a shiitake with Professor Rollo dela Fuente, one of “grow.” Or so I thought. The stems had growing on a log.) The mushroom’s the co-discoverers of phototropism in become curved with the mushroom hymenophore (be they gills of agarics, plants. Phototropism is the process that caps no longer resting on the table, tubes of boletes and polypores, or teeth causes plants to bend toward sunlight, instead resuming a position above and in hydnoid forms) hang down from the thus more efficiently collecting the horizontal to the surface. cap, indeed they grow perpendicular to sun’s energy on the surfaces of leaves.) I The phenomenon of negative the cap, exhibiting positive gravitropism. had made a nice collection of Amanita gravitropism, wherein the mushroom The cap itself is an ingenious structure, muscaria and brought the specimens stem is moving away from the source for it protects the hymenium of into the lab for all to enjoy. The following of gravity, so to say, is to ensure the Basidiomycetes from rainfall; any day I returned to the table where I had mushroom cap will be in the air column moisture would disable the spore left my mushrooms and was surprised so that the spores may be carried away. discharge mechanism of Basidiomycetes. 26 FUNGI • Volume 5:4 • Fall 2012 Figure 3a.

Figure 1b. If the cap is repositioned to anything but horizontal (as when a standing tree with perfectly horizontal, the hymenophore brackets falls down) a new bracket is will continue to elongate and bend so formed horizontal to the surface. (See that they will again be vertical. (See two views of Ganoderma in Figure 3.) Amanita species in Figure 2.) In the case of gilled mushrooms, both Bracket fungi probably are more the positive and negative geotropism correctly termed gravimorphogenic, exhibited by the gills and stem, rather than gravitropic, as the entire respectively, ensures that the spores bracket does not bend or reshape. will be ejected from the hymenium (the If repositioned other than perfectly surface of the gills), then fall straight Figure 3b. down without landing on an adjacent gill (see Figure 4, an illustration from A.H.R. Buller, 1909.) Probably all mushrooms demonstrate this while intact. Amanitas demonstrate this beautifully even after being picked or cut (most other mushrooms will wither or dry soon after cutting and don’t show this as dramatically). The Mushroom Handbook by Louis Krieger (1936) is the only book I know of that points out this habit of Amanitas (Figure 5). If you Figure 2a. are involved with setting up wild mushroom displays, you would be wise to store Figure 3c. all Amanita specimens fully How do mushrooms grow “up?” upright, lest As mentioned earlier, plants bend they become towards a light source by a process bent and called phototropism. In a sense, fungal distorted from gravitropism is by a somewhat similar their natural process. In plants, the side of the plant shape found in stem receiving the strongest light Figure 2b. the wild. sends a plant hormone signal (auxin) Fall 2012 • Volume 5:4 • FUNGI 27 the Soviet Union’s unmanned Cosmos enmeshed in proteinaceous actin 690 was the first; Salyut-5 and Salyut-6 filaments that make up the cell’s soon followed. Among the experiments internal “skeleton” (the cytoskeleton). aboard were those to test the effects As these nuclei settle, they tug on actin of space, primarily zero gravity, on filaments, which in turn tug on the cell mushroom fruitbody formation (for walls at their points of attachment. a review see Moore, 1991). A decade This tension triggers cellular changes ago Gruen (1991) performed careful in response to gravity, and on the grafting experiments on developing side of the cell feeling gravity’s Flammulina basidiocarps to test the force, microvesicles begin to fill and effects on gravitropism. In fruitbodies expand, vacuoles expand, and the of Flammulina velutipes growing on entire process causes the expansion of sawdust the mushroom caps were hyphal cells. The net result is that the removed and replaced with either caps, mushroom stem bends away from the or caps with stem apices (and sometimes gravitational sensation. inverted stems) and it was found that And finally, one more note. While the part of the mushroom most sensitive it seems to be common knowledge to gravity’s effects is the apex of the that fungi have no need whatsoever stem. Furthermore, the effects of the for light, there are in fact many fungi Figure 4. various grafts demonstrated “acropetal that show a phototropic response. The to the “darker” side of the stem, and transport” of mycelial metabolites zygomycete Pilobolus is well-known for this induces a physiological change through living hyphae of the stem which “throwing” its “hats” in the direction in the cell walls there. Cells on the induced the bending of the mushroom of light and away from the dung upon dark side of the stem release enzymes stems in response to gravity. Those which it grows. The common stalked called expansins that partially break metabolites—a signal of gravitational polypore Polyporus brumalis will grow down the cell walls of dark side cells, forces—have yet to be elucidated. towards light. And shiitake mushroom allowing those cells to be less rigid and Monzer (1996, 1995) more recently (Lentinula edodes) growers know that to expand. Cells furthest away from proposed a more simple explanation this species will not form mushrooms at the light source receive the strongest for how gravitational sensing is all in the absence of light. Furthermore, auxin signal and expand the most, thus accomplished in fungi. And that it’s very many other mushrooms will fail to form impart a disproportionate elongation similar to the system of otolith organs caps or produce malformed fruitbodies force, causing the plant to bend in the (technically the utricle and saccule) of in the absence of light. opposite direction. Bending towards the humans. Within all of us, deep inside our References Cited light, which is more efficiently captured inner ear, there are organs that contain a by the upper leaf surfaces. liquid filled with tiny stone-like particles Buller, A.H.R. 1909. Researches on Fungal gravitropism was poorly called otoliths or otoconia (they really Fungi. Longman, New York, vol. 1; known until recently (Moore, 1991). are stony, essentially made of limestone 287 pp. A number of experiments, some and a protein) that rub against tiny Gruen, H.E. 1991. Effects of producing inconclusive results, have hairs that line the inside of the otolith grafting on stipe elongation and been published over the past 100 years organ. Most of the time, the particles are pileus expansion in the mushroom uniformly settled Flammulina velutipes. Mycologia 83: telling us which 480-491. way is down. If you Krieger, Louis C.C. 1936. are spun around or The Mushroom Handbook. The shaken like a snow Macmillan Company, New York. globe, the particles Monzer, J. 1996. Cellular move all about graviperception in the basidiomycete giving you a feeling Flammulina velutipes—can the of disorientation, nuclei serve as fungal statoliths? even dizziness. European Journal of Cell Biology And this, Monzer 71(2): 216-220. has concluded, Monzer, J. 1995. Actin filaments are is similar to how involved in cellular graviperception fungal cells sense of the basidiomycete Flammulina Figure 5. gravity. Within velutipes. European Journal of Cell using gravistat devices and centrifuges hyphal cells, nuclei act as fungal Biology 66(2): 151-156. to negate gravity’s effects on mushroom otoliths; their sedimentation within Moore, D. 1991. Perception and formation, and to see the results. the cells in response to the direction of response to gravity in higher fungi—a Mushroom cultures have even been the gravitational forces tells the fungal critical appraisal. New Phytologist taken into Earth’s orbit! In the 1970s, cells which way is up. Thenuclei are 117: 3-23. 28 FUNGI • Volume 5:4 • Fall 2012