THE ROLE OF VACUOLES

SUMMARY Many plant cells are characterized by the presence of a vacuole (hypertrophied lysosome) occupying a large fraction of the protoplast. The possible benefits of the presence of the vacuole can be divided into those which are related merely to the increased volume of the protoplast, independent of the nature of the vacuolar contents, and those which depend on the nature of the solutes in the vacuole. Increasing the volume of the protoplast per unit volume of cytoplasm increases the total surface area of the cell per unit of cytoplasmic volume. This area amplification has potential benefits in terms of resource acquisition under resource-limiting conditions. At a given chromophore concentration in the cytoplasm, dispersal of a given volume of cytoplasm at the periphery of a vacuole increases the efficiency of photon absorption of an ‘average’ chromophore molecule relative to a comparable non-vacuolate cell, unless the chromophore concentration is low arid/or the cell is very small (no package effect) or the total chromophore per unit projected area is such that almost all light is absorbed, regardless of vacuolation. The area amplification also increases the plasmalemma area per unit cytoplasmic volume through which‘lipid solution’, or mediated transport of chemical resources can occur on a cytoplasmic volume basis and decreases the impediment to resource transfer from a bulk aqueous phase to the cell surface, again on a cytoplasmic volume basis. The increased capacity for uptake of chemical resources from low external concentrations due to vacuolation can increase overall solute acquisition, except in cells of picoplankton size, although other remedies for restricted capacity for chemical nutrient uptake per unit cytoplasmic volume are possible (e.g. evaginations of the cell surface). In addition to these potential benefits of vacuolation which are essentially independent of the contents of the vacuole, and which relate almost entirely to the rate at which resources can be acquired, there are potentially beneficial effects of vacuolation (dependent on specific vacuolar contents) on the acquisition of resources, and on the storage, manipulation and protection of resources which have already been acquired. Effects of vacuolation which involve essentially irreversible deposition (within the life of the cell) of specific solutes in the vacuole embrace the acquisition, manipulation and protection of resources, but not, of course, true (‘reversible’) storage. Deposition-related increases in resource (at least phosphate and iron) acquisition capacity can, in attached rhizophytic macrophytes, result from rhizosphere acidification involving accumulation of cation salts of organic acid anions in the vacuole. Related to resource acquisition (CO2, H2O) in terrestrial halophytes is the disposal of ‘excess’ salt entering the roots by deposition in hypertrophied vacuoles. Resource manipulation involving deposition of salts of organic acid anions occurs as a means of OH− disposal in the reduction of NO3− in the shoot, a process which can increase the photon and water use efficiency of N assimilation. Resource protection in plants often involves the deposition of antibiophage solutes in the vacuoles. The possible osmotic problems engendered by cation organate deposition can be ameliorated by production of insoluble calcium oxalate. Reversible accumulation of solutes in vacuoles is involved in CAM, which can increase the water (and nitrogen? ) use efficiency of carbon assimilation, and may be involved in the storage of fermentation products during temporary anoxia. The storage of soluble compounds in vacuoles during CAM cannot, apparently, be replaced by that of insoluble materia; there is some scope for storage of insoluble waxes during fermentation. Storage of energy and carbon (as reduced carbon), phosphorus and nitrogen often involves soluble low-molecular weight materials in large vacuoles, but can also, in all three cases, involve polymers in smaller vacuoles or in other parts of the cytoplasm. Other potentially beneficial effects of vacuolation include a (mechanistically unexplained) stimulation of the velocity of cytoplasmic streaming in large vacuolate cells and a role in buffering cytoplasmic volume from rapid, large changes in cells (e.g. stomata) undergoing large changes in protoplast volume. Against these putative benefits must be set, in terms of natural selection, the costs of vacuolation. These costs include the costs (energy, solutes) of producing, and those (energy) of maintaining the vacuoles, and the costs (energy, carbon) of synthesizing the extra wall material. The additional costs (all on a unit cytoplasm basis) can be substantial relative to benefits in terms of additional energy and carbon acquisition resulting from vacuolation. Additional costs may be incurred in relation to the energetics of large cells maintaining a constant turgor pressure in environments (e.g. estuaries) with frequent and large changes in external osmolarity, and as colonization opportunities lost if vacuolation reduces desiccation tolerance. The analysis conducted in the paper suggests that the specific growth rate of a cell of a given cytoplasmic volume under optimal growth conditions is decreased if it is vacuolated. Furthermore, the resource acquisition rate of the cell under conditions of low resource availability may be enhanced by vacuolation, even when the resource costs of vacuolation are taken into consideration, although this is not invariably so. Nevertheless, although the cost-benefit analysis of resource acquisition may not always favour vacuolation, the presence of vacuoles may still lead to an increase in inclusive fitness when benefits in relation to the storage, manipulation and protection of resources are also considered. At all events, most phototrophs are vacuolate, the major exception being many planktophytes (where the lack of vacuoles may be rationalized, at least for smaller cells) and essentially all microalga-invertebrate synthesis.