Nonstructural carbohydrate (NSC) storage plays a critical role in tree function and survival, but understanding and predicting local NSC storage dynamics is challenging because NSC storage pools are dispersed throughout the complex architecture of trees and continuously exchange carbon between source and sink organs at different time scales. To address these knowledge gaps, characterization and understanding of NSC diel variation are necessary. Here, we analyzed diurnal NSC dynamics in the overall architecture of almond (Prunus dulcis) trees. We also analyzed the allocation of newly assimilated carbon using isotopic labeling. We show that both components of NSC (i.e. soluble carbohydrates and starch) are highly dynamic at the diurnal time scale and that these trends are influenced by tissue type, age, and/or position within the canopy. In leaves, starch reserves can be depleted completely during the night, while woody tissue starch levels may vary by more than 50% over a daily cycle. Recently assimilated carbon showed a dispersed downward allocation across the entire tree. NSC diurnal fluctuations within the tree's structure in combination with dispersed carbon allocation patterns provide evidence for the presence of vertical mixing and suggest that the xylem acts as a secondary NSC redistribution pathway.
During spring, bud growth relies on long-distance transport of remotely stored carbohydrates. A new hypothesis suggests this transport is achieved by the interplay of xylem and phloem. During the spring, carbohydrate demand of developing buds often exceeds locally available storage, thus requiring the translocation of sugars from distant locations like limbs, stems and roots. Both the phloem and xylem have the capacity for such long-distance transport, but their functional contribution is unclear. To address this ambiguity, the spatial and temporal dynamics of carbohydrate availability in extension shoots of Juglans regia L. were analyzed. A significant loss of extension shoot carbohydrates in remote locations was observed while carbohydrate availability near the buds remained unaffected. This pattern of depletion of carbohydrate reserves supports the notion of long-distance translocation. Girdling and dye perfusion experiments were performed to assess the role of phloem and xylem in the transport of carbohydrate and water towards the buds. Girdling caused a decrease in non-structural carbohydrate concentration above the point of girdling and an unexpected concurrent increase in water content associated with impeded xylem transport. Based on experimental observations and modeling, we propose a novel mechanism for maintenance of spring carbohydrate translocation in trees where xylem transports carbohydrates and this transport is maintained with the recirculation of water by phloem Münch flow. Phloem Münch flow acts as a pump for generating water flux in xylem and allows for transport and mobilization of sugars from distal locations prior to leaves photosynthetic independence and in the absence of transpiration.
Despite non-structural carbohydrate (nSc) importance for tree productivity and resilience, little is known about their seasonal regulations and trade-off with growth and reproduction. We characterize the seasonal dynamics of nSc in relation to the aboveground phenology and temporal growth patterns of three deciduous Mediterranean species: almond (Prunus dulcis (Mill.) D. A. Webb), walnut (Juglans regia L.) and pistachio (Pistacia vera L.). Seasonal dynamics of nSc were synchronous between wood tissues from trunk, branches and twigs. Almond had almost identical levels and patterns of nSc variation in twigs, branches and trunks whereas pistachio and walnut exhibited clear concentration differences among plant parts whereby twigs had the highest and most variable NSC concentration, followed by branches and then trunk. While phenology had a significant influence on NSC seasonal trends, there was no clear trade-off between NSC storage and growth suggesting that both were similarly strong sinks for NSC. A temporal trade-off observed at the seasonal scale was influenced by the phenology of the species. We propose that late senescing species experience C allocation trade-off at the end of the growing season because of c-limiting thermal conditions and priority allocation to storage in order to survive winter. Rising temperatures due to global climate change are associated with significant shifts in tree phenology, while the increase in the frequency and intensity of drought events threatens their survival 1-4. The shifts in temperature combined with drought events not only disturb non-structural carbohydrate (NSC, starch and soluble sugars) accumulation in summer but also their remobilization during winter and spring 5-8. As remobilization of stored NSC allows plants to buffer periods of carbon (C) deficit when supply by photosynthesis is not sufficient to sustain maintenance, growth and defense, they play a key role in tree survival through periods of stress and winter dormancy and allow for resumption of growth in spring 9-15. Hence, the disturbance of evolved seasonal patterns of NSC due to climate change may lead to an overall NSC reserve depletion, leaving trees highly vulnerable to mortality 16. As NSC reserve depletion remains debated, another option is that strong C demand of a storage sink could reduce C supply to growth or reproduction, leading to reduction in productivity of natural populations and agroecosystems with dramatic consequences for ecosystems and food production 17-19. It is therefore critical to understand how perennial plants integrate multiannual, seasonal and short-term NSC regulation in response to short-term stress, seasonal environmental signals and long-term global change in order to fully predict and potentially mitigate impact of climate change. The classical view of storage formation as the accumulation of resources when supply exceeds demand is now supplanted by the understanding of storage as a competing C sink 16,20,21. In fact, a classical model of C allocation presented as a static ...
Deciduous trees mostly rely on non-structural carbohydrates (NSC—soluble carbohydrates and starch) stored prior to dormancy to sustain both spring bloom and the initial phase of spring growth prior to the transition of leaves from sink to source. Winter management of NSC, their loss due to respiration, reallocation patterns and remobilization during spring, seems to be key to a timely and synchronous bloom. To assess tree dependence on NSC during dormancy, we tested whether the interruption of local branch NSC accumulation prior to dormancy by defoliation and the interruption of NSC translocation by phloem girdling influence spring phenology in three major deciduous Mediterranean nut crop species: Prunus dulcis (Mill.) D.A Webb, a hybrid between Pistacia integerrima (J. L. Stewart ex Brandis) and P. atlantica Desf. (referred to as P. integerrima), and Juglans regia L. Defoliation treatments had different effects on NSC concentration in different species depending on the time of application. However, despite the significant initial impact (increase or decrease of NSC concentration), with time this impact diminished resulting in overall similar concentrations between control and defoliated branches suggesting the presence of NSC reallocation during dormancy. Phloem girdling in P. dulcis and P. integerrima resulted in reduced export activity and greater NSC concentrations, while in J. regia girdling resulted in lower NSC concentrations, indicating that this species requires a net import of NSC during dormancy. Bud break was distinctly delayed by both defoliation and phloem girdling in all the three species, providing evidence of the significant roles that fall NSC accumulation and winter NSC management play in priming trees for spring growth resumption.
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