Centenary review: Gravimorphogenesis in agarics

The shape changes which occur in agaric fruit bodies in response to change in the direction of gravity, usually referred to as gravitropism, are morphogenetic changes. Our interest in what we prefer to call gravimorphogenesis is to use it to examine morphogenesis experimentally. We are examining two agarics, Coprinus cinereus and Flammulina velutipes, and applying the best available technologies, including video analysis, all forms of electron microscopy, computer-aided image analysis and experiments in orbit in Spacelab. Responses to gravity of the two organisms differ in ways which can be related to their ecological and structural adaptations. C. cinereus reacts extremely rapidly; its fruit body can regain the vertical within 3 h of being placed horizontal, whereas F. velutipes requires 12 h to bend through 90 degrees. The fungi also differ in the bulk of tissue involved in the response. In Coprinus, a zone extending several cm down from the apex is normally involved in bending. In Flammulina, gravisensing is limited to a region just a few mm immediately below the cap, although curvature is performed in a zone of up to 2 cm below. Flammulina cultures were flown on the Spacelab D-2 mission in 1993, and fruit body disorientation in orbit provides the first definitive proof that 'gravitropism' really is a response to the unidirectional gravity vector. Experiments with different clinostat rotation rates in Flammulina indicate that the perception threshold is about 10(-4) x g. Analysis of different times of exposure to an altered gravity vector prior to clinorotation in Coprinus reveals that the perception time is 7 minutes and that continued response requires continued exposure. Cell size determinations in Coprinus demonstrate that cells of the stem increase in length, not diameter, to produce the growth differential. In Flammulina a unique population of highly electron-transparent microvacuoles changes in distribution; decreasing in upper cells and increasing in the lower cells in a horizontal fruit body within a few minutes of disorientation. These are thought to contribute to vacuolar expansion which accompanies/drives cell elongation. Application of a variety of metabolic inhibitors indicates that the secondary messenger calcium is also involved in regulating the growth differentials of gravimorphogenesis but that gravity perception is unaffected by inhibitors of calcium signalling. In both Flammulina and Coprinus, gravity perception seems to be dependent on the actin cytoskeleton since cytochalasin treatment suppresses gravitropic curvature in Flammulina and, in Coprinus, significantly delays curvature without affecting stem extension. This, together with altered nuclear motility observed in living hyphae during reorientation suggests that gravity perception involves statoliths (possibly nuclei) acting on the actin cytoskeleton and triggering specific vesicle/microvacuole release from the endomembrane system.