Petal photosynthesis and dynamic alterations of carbon metabolism orchestrate floral maturation in Gardenia carinata

During maturation, flowers exhibit complex and finely-coordinated metabolic events facilitating various physiological changes that occur in a short time-span. The floral carbon metabolism underpins a metabolic frame, which provides energy and metabolites to drive the life-processes in flowers. However, studies on floral maturation in the past mostly focused on specialized metabolism or certain metabolite classes of central carbon metabolism. This study aims to provide a detailed insight into the dynamics of floral carbon metabolism and its role in flower maturation; it also addresses a long-standing question on the role of petal photosynthesis in floral maturation. In this report, time-course metabolomic studies were integrated with various physiological, enzymological, histochemical and ultrastructural findings to present a multi-layered investigation on the maturation physiology of Gardenia carinata flowers. This integrated approach revealed the characteristic metabolic features of different floral maturation stages, and also highlighted the metabolic rearrangements that allow each stage to establish their characteristic metabolic state. The photosynthetic bud stages showed metabolism inclined toward active growth and carbon reserve accumulation. A shift to energy-rich metabolism was observed as the flowers unfurled, probably to support energy-demanding events such as flower opening and changes in specialized metabolism. Our study further demonstrates the mechanisms underlining the transition from autotrophic to heterotrophic metabolism during maturation, which also reflects the plasticity in source-sink dynamics of flowers. We envisage that this study could provide a springboard for elucidating the roles of individual metabolites and enzymes in regulating floral maturation.