Mycomorphology Part 2:
Basidiocarp Keeps its Balance

© Peter Werner
Original publication: Mycena News, March 2003

In my last column, I discussed how the characteristic umbrella shape of a mushroom is an integral part of a suite of elegant adaptations for the dispersal of spores. These adaptations ensure that the maximum number of spores are successfully released from the hymenophore (that is, the gills, tubes, teeth, etc), and that they fall clear of it into the airstream below.

Figure 1 Gravitropic adjustment over several hours of a basidiocarp placed perpendicular to the direction of gravity.
(Adapted from: Buller AHR. 1909. Researches on fungi. Vol. 1. In: Moore-Landecker E. 1996. Fundamentals of the fungi. 4th ed.)

These adaptations, however, are entirely dependent upon a mushroom's being oriented perfectly upright, with the gills or other hymenophoral elements being completely parallel to the vector of Earth's gravity. Since spores fall along a gravitational vector, any deviation of hymenophore alignment from the normal will lead to an increased number of spores becoming entrapped within the gills. At the beginning of the last century, the eminent fungal physiologist AHR Buller observed that when a basidiocarp of Agaricus campestris was tilted a mere 5 from the normal, spore dispersal was cut in half.

Clearly, a mushroom must have a way of keeping its hymenophoral elements aligned to the normal. However, mushrooms are incapable of locomotion and cannot simply move their gills into the correct position. Mushrooms deal with this problem in a similar way as do plants, through mechanisms known as tropic responses. In a tropic response, the organism grows toward or away from a stimulus rather than moving toward or away from it. Tropic responses include phototropism (response to light), gravitropism (response to gravity), thigmotropism (response to touch or contact), hydrotropism (response to water), and many other such responses. Tropic responses can be either positive (growing toward the stimulus) or negative (growing away from it).

At first, mushroom primordia grow perpendicularly away from the surface from which they arise, independently of the direction of light or gravity, a response that may be some kind of negative thigmotropism or negative hydrotropism. Soon after emergence, gravitropic and (in some species) phototropic responses become active.

The majority of mushroom species exhibit growth that is negatively gravitropic along the stipe and positively gravitropic in the hymenophore. If a mushroom is tilted from the normal, it will grow in such a way that a bend will develop in the stipe until the mushroom is again realigned. This bending is key to the gravitropic response - once the mushroom stipe is aligned away from the normal for a specific time interval (an interval known as the "presentation time", which varies from one species to another), the hyphae on the lower surface of an apical zone on the stipe begin to elongate more rapidly than those of the upper surface, leading to bending of the stem and ultimately the correction of the mushroom's alignment.

In the last decade, it has been discovered that this response actually has two parts involving two apical zones. The initial bending response, which originates at the base of the stipe, often overcompensates and by itself would tend to leave mushrooms tilted in a direction opposite to the initial misalignment. There is therefore a "curvature compensation" growth response which takes place in the upper part of the stipe - this represents a "fine adjustment" and serves to better align the stipe with the normal. The positively gravitropic response of the hymenophoral elements represent a further layer of "fine adjustment".

Figure 2 Diagrammatic model of hypothesized gravity perception mechanism in a fungal cell. Top diagram shows vertical orientation of a cell while the bottom shows horizontal orientation. Stress on microfilament cage stimulates the endomembrane system to release growth (or growth-suppressing) factors, membrane and wall-building materials, and possibly hormones or other signaling factors.
(from: Moore D, et al. 1996. Mycological Research 100:257-273.)

Other tropic responses may modify a mushroom's gravitropic growth. Most mushrooms have some kind of negative thigmotropic response, so that if a mushroom encounters an object as it is growing, responses such as stipe bending, bifurcation, or change in the pattern of pileus growth will cause the mushroom to grow out of the way of the object. (This in contrast to fungi such as Hydnellum that are characterized by indeterminate growth and simply envelop foreign objects within the fruiting body.) Many lignicolous and coprophilous species show strong positive phototropism throughout their fruiting cycle, a response that overrides the gravitropic response. (In one experiment, a Polyporus brumalis basidiocarp was illuminated from below - the stipe curved 180, resulting in an upside- down pileus with tubes growing upward.)

How can we be sure that a mushroom's main tropic responses are in fact responses to gravity? The most obvious way is to deprive them of gravity by placing them in the microgravity conditions of spaceflight. Such an experiment was, in fact, carried out in 1993 when cultures of Flammulina velutipes were sent into orbit on the joint Space Shuttle Columbia/Spacelab D-2 mission. These cultures produced fruiting bodies with a random orientation, while similar control cultures on Earth produced regular verticallyaligned fruiting bodies.

Figure 3 Experiment showing gravitropic orientation of Flammulina velutipes fruiting bodies grown in culture under different gravitational conditions. Top: fruiting bodies grown for 5 days on Earth, as a control for fruiting bodies grown in orbit. Bottom: fruiting bodies grown for 7 days in orbit during Spacelab D-2 mission. Note the regular vertical orientation of the fruiting bodies produced in the control culture (top) and the random orientation of the fruiting bodies produced under conditions of microgravity (bottom).
(from: Kern VD & Hock B. 1996. Advances in Space Research 17:183-186. In: Moore D, et al. 1996. Mycological Research 100: 257-273.)

Since it is clear that mushrooms respond to gravity, how then do they sense it? How do they know "up" from "down"? At present, this is largely unknown, though it has been surmised from what is known about the gravity-sensing mechanisms of animals and plants that it probably involves some kind of statolith. A statolith is an organ or cellular organelle that is more dense than its surrounding matrix and hence tends to exert pressure along a gravitational vector. This pressure is sensed by a network of fibers, hairs, cytoskeletal elements, or the like, which transmit this impulse, and ultimately trigger an ionic, hormonal, or nervous signal.

Our bodies have a complex system of statoliths in our inner ears. This vestibular system consists of small calcium carbonate-filled sacs known as otoliths that are surrounded by a network of nerves and fibers known as the maculae. Pressure on the macula generates nerve impulses, and these signals, when processed by the brain, give us our sense of balance. Vertical and horizontal movements are detected by separate otoliths, known as the saccule and the utricle, respectively. (There are also non-otolithic vestibular organs which contribute to the sensation of movement.)

Plant root cells contain starch granules that act as statoliths - the pressure gradient of these granules upon the plasma membrane is thought to in some way trigger a reaction which leads to the differential distribution of auxin in the root, which stimulates the upper surface to elongate more rapidly, bending the root downward.

The gravitropic mechanisms of fleshy fungi are even less well understood. Fungal hyphae typically do not contain starch granules nor has auxin been shown to play any role in fungal gravitropic bending. Several experiments have demonstrated that the stipes of Flammulina velutipes and Coprinus cinereus show a dramatic decrease in the magnitude and rapidity of gravitropic bending when treated with drugs known as cytochalasins, which act by disrupting the formation of actin microfilaments. This demonstrates that the cytoskeleton likely plays a critical role in gravitropism and points toward an intracellular statolithic mechanism.

Fungal physiologist David Moore has hypothesized that in the fungal cell, the nuclei act as the statoliths. The nuclei bear downward upon a "cage" of actin microfilaments, which are in turn connected to the endomembrane/vacuolar system. Pressure on the microfilament cage could in turn stimulate the release of growth factors and wall and membrane building materials from the endomembrane system in cells at the sites of increased elongation (and possibly growth-suppressing factors in cells at the sites of decreased elongation). The question of how differential cell growth is coordinated throughout the stipe and hymenophore is another open question - it is clear that auxin is not involved, but the hormone or mechanism that is responsible remains to be discovered.

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