Perception and response to gravity in higher fungi--a critical appraisal.

Considering that research on gravitropism in higher fungi has a history of over 100 years, the harvest of established fact is disappointingly meagre. We can be reasonably certain of the following. Hymenomycete 'mushroom' fruit bodies (polypore and agaric) exhibit a number of tropisms of which anemotropism, gravitropism, phototropism and thigmotropism have been clearly demonstrated. At any one time one tropism usually predominates but the inferior tropisms can be demonstrated if the predominating ones can be removed by manipulation of the growth conditions. In ascending order, the hierarchy appears to be: thigmotropism, gravitropism, anemotropism, phototropism. During the course of development of a fruit body different tropisms predominate at different times. The youngest fruit body initials grow perpendicularly away from their substratum. The nature of this tropism is completely unknown but perpendicular growth of fruit body initials has been remarked upon in experiments at a variety of light intensities and in gravitational fields from +/- 0 to 4.5 g. The fruit-body primordium then becomes first positively phototropic but later negative gravitropism predominates. The switch between predominance of the two tropisms has been associated with the onset of sporulation in a number of different studies. The major adjustment of the direction of growth in response to a tropic stimulus is made by the mushroom stem. It is the apex of the stem which makes the most immediate gravitropic response. Gravitropic growth curvatures are limited to the normal growth zones of the stem and seem to depend on re-allocation of available growth resources. If the fruit body is reoriented late in the growth of the stem, it may not be able to respond fully. In these cases gravitropic movements of the cap may still be able to bring the hymenophore back to the vertical. Mechanical forces may influence and contribute to the 'gravitropic' response but this has not been experimentally examined. The hymenophore (gill, tube or tooth) is positively gravitropic and responds independently of the stem. Bracket polypores do not show tropisms but exhibit gravimorphogenetic responses such that gross disturbance leads to renewal of growth to produce and entirely new fruiting structure suitably reoriented to the new spatial position. One experiment performed on an orbiting space station suggests that, in the absence of a light stimulus, gravity may be required for initiation of fruiting in Polyporus brumalis. Otherwise, the indications from both clinostat and space-borne experiments are that the basic form of the mushroom (overall tissue arrangement of stem, cap, gills, hymenium, veil) in agaric and polypore alike is established independently of the gravity vector. Abnormal stem growth has been observed in clinostat cultures of Panus (= Lentinus) tigrinus and Polyporus brumalis, but the morphogenetic event which seems most dependent on gravity is sporulation (in the broadest sense). Cultures of P. brumalis on orbiting space craft fail to produce the poroid hymenophore and in clinostat experiments on the ground even karyogamy was rare in similar cultures. Coprinus cinereus grown on the clinostat was able to produce apparently normal fruit body primordia which failed to produce spores and then aborted, forming a new flush of primordia on the old. Taken together with the clear association between observation of gravitropism and the onset of sporulation, the implication is that commitment to the meiosis-sporulation pathway both requires the gravity vector and couples it in some way to fruit-body growth. There is no convincing evidence for a graviperception mechanism in fungi. There is no evidence for any organised means of communicating the gravitropic stimulus once it has been perceived. Reports of three different experimental studies reveal the authors' conviction that the apparently coordinated expression of gravitropic response is in truth a common, but independent, response by the individual component hyphae of the structure concerned. There is some evidence that in the negatively gravitropic Phycomyces sporangiophore the vacuole floats in the protoplasm. If this is generally true it could affect protoplasmic volumes above and below the vacuole such that a greater proportion of the cell's potential for wall growth was adjacent to the lower wall. This is not only an attractive way of accounting for asymmetric wall growth, but since the relative density of the vacuole can presumably be controlled by regulation of water influx and efflux, it is also an attractive means of accounting for the control of gravitropic responses. Phycomyces also exhibits a response to the mechanical consequences of reorientation which is additional to (and different from) the longer term gravitropic response. [TRUNCATED]