Spring bud growth depends on sugar delivery by xylem and water recirculation by phloem Münch flow in Juglans regia

Abstract

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.

Non-structural Carbohydrates in Dormant Woody Perennials; The Tale of Winter Survival and Spring Arrival

“…Modeled NSC depletion from local maintenance respiration in walnut branches was much higher than observed carbohydrate depletion, suggesting a need for the replenishment of reserves from distal locations (Tixier et al, 2017a). Longdistance transport of labeled carbohydrates, grafting, girdling experiments, storage mobilization, and growth measurements also support the hypothesis that carbohydrates are transported from distant locations (Bates et al, 2002;Lacointe et al, 2004;Menora et al, 2015;Tixier et al, 2017b).…”

“…Therefore, NSC requirements also have to be evaluated in terms of the storage size limits in order to quantify the local availability of NSC surrounding the bud. Insufficient NSC in tissues adjacent to a bud-whether they are transported there in spring or stored locally through the winter-can lead to delays in growth and development, decreased leaf area, and the induction of flower abortion (Lebon et al, 2008;Keller and Tarara, 2010;Tixier et al, 2017b).…”

“…Based on experimental observations and modeling, a novel mechanism for the maintenance of spring carbohydrate translocation in woody perennials has been proposed. In the absence of transpiration and prior to leaves' photosynthetic independence, phloem Münch flow would act as a pump to generate water flux in xylem allowing for the transport and mobilization of sugars from distant locations (Tixier et al, 2017b). The accumulation of sugars in xylem sap in response to low temperatures may take part in the transport of NSC, especially when considering thermal gradients at the whole plant scale in spring when roots are colder than the canopy .…”

“…These findings need to be complemented with a holistic approach in understating the synchrony of dormancy breaking which takes into account the whole plant sustaining new bud growth. Indeed, buds require energy (in the form of NSC) for biomass, metabolism, and respiration until they transition from heterotrophy (reserve-dependent growth) to autotrophy (photosynthetic autonomy) Leyhe and Blanke, 1989;Maurel et al, 2004;Vaillant-Gaveau et al, 2011;Tixier et al, 2017b). Bud development, its synchronization at the plant and population levels, and subsequent reproductive success are dependent on the whole plant's ability to supply buds with energy and water (Lebon et al, 2008;Keller and Tarara, 2010).…”

“…Current mechanistic models were developed from the perspective of carbohydrate partitioning and source-sink relationships during the growing season (DeJong et al, 2011;Da Silva et al, 2014). In these models winter biology is usually represented as maintenance respiration, an oversimplification that ignores an entire suite of biological activities related to winter temperature, winter carbohydrate management, transport, and subsequent spring performance (Lacointe et al, 2004;Bonhomme et al, 2005;Pellegrino et al, 2014;Tixier et al, 2017b). On the other hand, models that focus on dormancy such as the chilling hours models (Utah chill models, dynamic model), which were developed to predict bud break in response to winter temperature, are descriptive and empirical in nature (Pérez et al, 2008;Aslamarz et al, 2010;Luedeling and Brown, 2011;Luedeling et al, 2013;Londo and Johnson, 2014).…”