Photosynthesis is well-known to not only occur in leaves but also other tissues like stems, sepals, and fruits. Fruit photosynthesis has been documented in cucumber, tomatoes, satsuma mandarins, prickly pear, wheat, and apple. Fruit photosynthesis occurs in these instances not only to contribute to carbon assimilation but to support other metabolic processes, the synthesis of metabolites, and seed development. Early fruit growth in apple is regulated by energy-intensive cell division that lasts for approximately five weeks before switching to a phase of predominantly cell expansion-driven growth. Thus, fruit photosynthesis during early fruit development in apple could function to fulfill the resource and energy requirements necessary for the growth and development of fruit tissues. To examine this potential contribution of photosynthesis to apple fruit metabolism, shade bags made of 30%, 65%, and 80% shade cloth were placed on fruitlets at 16 days after full bloom. The effects of fruit shading on fruit tissue plastid ultrastructure, metabolite composition and tissue transcriptomes were analyzed. Using transmission electron microscopy (TEM), we found that plastids in the peel and cortex overall resembled that of photosynthetically active plastids; they contained stromal and granal thylakoids similar to those found in leaves. Spatially, pith plastids displayed unique hypergranal features , with increased granal thylakoids and a significantly reduced presence of stromal thylakoids. When compared to the control, 80% shaded peel plastids contained more plastoglobuli, and 80% shaded pith plastids displayed prolamellar bodies, which are indicative of disassembly. Further, significantly lower chlorophyll a concentration was observed in shaded fruit. Metabolite analyses indicated that sorbitol was significantly greater in shaded fruit than in the control. Transcriptome analyses indicated substantial changes associated with carbohydrate metabolism in the fruit cortex and peel in response to fruit shading. Together, these analyses indicate a significant contribution of fruit photosynthesis to early fruit growth and development in apple.
