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Abstract
Fruit growth and development consists of general phases of cell division, cell expansion, maturation, and ripening. In apple, growth during early fruit development is largely mediated by rapid cell division, while growth at later stages is achieved through cell expansion. Resource availability, intrinsic capacity for growth, and internal atmosphere are major factors that influence growth, particularly during early stages of fruit development. Fruit growth is substantially reliant on carbohydrates transported from nearby leaves via the vascular tissues, into the fruit. However, non-foliar photosynthesis is commonly noted in organs such as stems, petioles, petals, sepals, seeds, and fruits. The capacity for fruit photosynthesis and its contribution to early fruit growth are not well understood in apple. In this study, fruit-shading was used to understand the contribution of fruit photosynthesis to early apple fruit growth. Fruit tissues, particularly the peel and cortex, display chloroplast ultrastructure and chlorophyll pigment characteristics consistent with capacity for fruit photosynthesis. Shading resulted in enhanced degradation of plastid components, particularly in the pith. The decrease in fruit photosynthesis by shading did not reduce early fruit growth or fruit retention. However, it affected fruit metabolism resulting in reduced consumption of C resources as indicated by metabolite and transcriptome analysis. Transcriptome analyses also indicated enhanced stress responses upon fruit shading. Analyses of the regulation of fruit growth were performed by comparing fruit populations differing in relative growth rates (RGR). During early development, fruit with high RGR were associated with enhanced cell production as indicated by sustained expression of multiple cell division-related genes. Early fruit development in apple was also associated with chronic hypoxia development, which was associated with high rates of respiration. While chronic hypoxia was partially alleviated by a decrease in fruit respiration at later stages, this was not consistent across cultivars, indicating that other factors such as tissue pore space development also influences hypoxia development during apple fruit development. Together, data from these studies indicate that fruit photosynthesis may be dispensable for early fruit growth but alters fruit metabolism and stress response in apple. Further, early fruit development is associated with intensive cell production, the extent of which can influence fruit RGR. Additionally, chronic hypoxia develops in internal tissues during early fruit development, potentially owing to the high respiration rates observed during this period.