Grapevine leaves contain abundant CaOx crystals located either within the mesophyll in the form of raphides, or in the bundle sheaths as druses. CaOx crystals function as internal carbon pools providing CO2 for a baseline level of photosynthesis, named “alarm photosynthesis”, despite closed stomata; thus, preventing the photoinhibition and the oxidative risk due to carbon starvation under adverse conditions. Structural and functional leaf traits of acclimated grapevine plants (Vitis vinifera L. cv. Assyrtiko) were investigated in response to water availability, in order to evaluate the dynamic functionality of CaOx. Leaf water potential, leaf area, leaf mass per area, stomatal properties, gas exchange parameters and performance index (PI) were decreased in leaves of vines acclimated to water deficit in comparison to the leaves of well-irrigated vines, although the chlorophyll fluorescence parameters showed that the operational efficiency of the photosystem II (PSII) photochemistry (Fv/Fm) did not change, indicating that the photosynthetic apparatus was not subjected to water stress. During the afternoon, more than half of the morning’s existing druses disappeared in the drought-acclimated leaves. Also, the raphides’ area of the drought-acclimated leaves was reduced more than that of the well-watered leaves. The substantial decomposition of druses under water deficit conditions compared to that of the raphides may have important implications for the maintenance of their different though overlapping roles. According to the results, it seems likely that, under water deficit conditions, a mechanism of “alarm photosynthesis” provides an additional tolerance trait in the leaves of Vitis vinifera cv. Assyrtiko; hence, leaf structure relates to function.