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Temperature gradients assist carbohydrate allocation within trees - PubMed

  • ️Sun Jan 01 2017

Temperature gradients assist carbohydrate allocation within trees

Or Sperling et al. Sci Rep. 2017.

Abstract

Trees experience two distinct environments: thermally-variable air and thermally-buffered soil. This generates intra-tree temperature gradients, which can affect carbon metabolism and water transport. In this study, we investigated whether carbohydrate allocation within trees is assisted by temperature gradients. We studied pistachio (Pistacia integerrima) to determine: (1) temperature-induced variation in xylem sugar concentration in excised branches; (2) changes in carbon allocation in young trees under simulated spring and fall conditions; and (3) seasonal variability of starch levels in mature orchard trees under field conditions. We found that warm branches had less sugar in perfused sap than cold branches due to increasing parenchyma storage. Simulated spring conditions promoted allocation of carbohydrates from cold roots to warm canopy and explained why starch levels surged in canopies of orchard trees during early spring. This driving force of sugar transport is interrupted in fall when canopies are colder than roots and carbohydrate redistribution is compartmentalized. On the basis of these findings, we propose a new mechanistic model of temperature-assisted carbohydrate allocation that links environmental cues and tree phenology. This data-enabled model provides insights into thermal "fine-tuning" of carbohydrate metabolism and a warning that the physiological performance of trees might be impaired by climatic changes.

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Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Figure 1
Figure 1

Apoplastic SC concentrations in perfused branch segments at variable temperatures. 15 cm long and 10 mm in diameter branches were submitted to 12 °C (blue circles), 22 °C (green triangles), and 32 °C (red squares) and perfused with sucrose solution. The solution’s input concentration was 3.42 g L−1 sucrose (red horizontal line) and flow rate was 0.68 g h−1. (A) SC concentration of perfused solution in branches changing temperature every 150 minutes (from 22 °C to 12 °C and then to 32 °C, 450 minutes total). (B) The final SC concentration of perfused solution (after 150 minutes at a given temperature) decreased with temperature in a linear manner (dotted line, R2 = 0.81, df = 16, p = 1.433e−7, grey area denotes 95% confidence intervals). The intercept value of initial SC concentration (i.e. the temperature at zero net uptake of SC) was 14.5 °C and is referred to as the compensation point. (C) The rate of SC uptake from the perfused solution (orange boxes) vs. the rate of SC lost to stem respiration (black panels) during the 150 minutes at each temperature.

Figure 2
Figure 2

Impact of temperature gradients on nonstructural carbohydrates redistribution in young trees. (A) Soluble carbohydrates (SC), (B) starch, and (C) C derived from 13CO2 levels in the leaves, bark at 30 cm from soil, stem at 50, 30, and 5 cm above soil, and roots control trees (25 °Cshoot/25 °Croot, light gray columns), simulated spring (25/10, gray columns), or simulated fall (10/25, dark gray columns). Error bars denote standard errors and lowercase letters denote statistical differences (two-ways Anova and Tukey-HSD, P < 0.005, df = 16).

Figure 3
Figure 3

In-situ representation of seasonal changes in root-to-shoot temperature gradients and starch levels in the canopy of mature orchard trees. (A) Temperature variation and gradients during bud-break, fruit set, vegetative growth, abscission, and dormancy at the canopy (blue line, shaded area denotes SE values of 7 days) and in the roots zone (30 cm deep, red line and shade). Pink line represents the 14.5 °C compensation point (established in experiment #1 with the appropriate 95% confidence intervals). (B) Starch levels in one-year-old branches collected at 11:00 from 5 mature trees. Gray boxes denote the 95% confidence intervals, thick line in the box exhibits the average, and circles show the starch levels at each tree. Dashed vertical lines separate between the phenological stages. (C) A vector illustration to emphasize the magnitude and direction of starch dynamics in the branches at the different phenological stages.

Figure 4
Figure 4

A conceptual model of carbohydrate redistribution due to root-to-canopy temperature gradients. The model summarizes differences observed in experiment #2 between the 25 °Cshoot/10 °Croot (spring) and 10 °Cshoot/25 °Croot (fall) treatments and the control group (25 °Cshoot/25 °Croot). Significant changes (relative to control) in soluble carbohydrates (SC), starch (ST), or 13C derived from new photosynthates following a pulse of 13CO2 are denoted by ± signs. Arrows represent the proposed path for sugar redistribution and the horizontal red line shows an impaired pathway and compartmentalization of NSC transport. Thermal images of the tree demonstrate the temperature gradients from root to canopy.

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