Accumulation of an apoplastic solute in the guard-cell wall is sufficient to exert a significant effect on transpiration in Vicia faba leaflets

Accumulation of recently photosynthesized sucrose in the guard-cell wall is the empirical foundation for a hypothesis that links the rates of photosynthesis, translocation, and transpiration (Plant Physiology 114, 109-118). Critical assumptions of this hypothesis were tested by use of Vicia faba, an apoplastic phloem loader. Following measurements of the leaflet-apoplastic-water volume (by P-V isotherm analysis) and the guard-cell wall volume (by 3-D analysis), intact leaflets were fed dilute solutions of mannitol, an impermeant non-toxic osmolyte. Even at bulk-leaflet mannitol concentrations that would have only a negligible osmotic effect on stomata, transpiration at constant temperature, water-vapour pressure, air movement and irradiance was diminished up to 25%, compared with controls. This effect on transpiration, a manifestation of smaller stomatal aperture size, was explained by accumulation of mannitol, up to 350 mol m(-3), in the estimated aqueous volume of the guard-cell wall. The conclusion is that mannitol, a xenobiotic with structural similarity to sucrose, can move throughout the apoplast of a transpiring leaflet and accumulate in an osmotically significant concentration in the guard-cell wall. These data therefore provide support for a new role for sucrose as a signal metabolite that integrates essential functions of the whole leaf. In addition, the results raise questions about the physiological or experimental accumulation of other guard-cell-targeted apoplastic solutes such as plant growth regulators, particularly abscisic acid, and ions.