Abstract

The leafless period is often considered as inactive, although trees have to actively modulate their metabolism through the cold acclimation/deacclimation processes, to cope with frost exposure during winter and to restore growth ability in spring. Carbon metabolism is a key component of these processes through the osmotic control of extracellular ice formation and the trophic control of bud growth. The influence of temperature on the inter-conversion between starch and soluble carbohydrate has been evidenced for years, but we are currently missing an operational tool to predict starch vs. soluble carbohydrate contents during this period, which should allow to better predict frost hardiness. For this purpose, we exposed 1-year-old branches of Juglans regia to constant temperature for one to 3 weeks and measured the changes in carbohydrate composition at three periods (autumn, winter, and spring). As expected, the temperature significantly affected the changes in carbohydrate composition, but the water content and the sampling period were also relevant. Higher starch hydrolysis was observed at low temperature (<5°C) for all sampling periods. Starch hydrolysis was also observed at warm temperature, but in autumn only. These data were used to compare three modeling approaches simulating the changes in carbohydrate composition through enzymatic analogy. The most empirical and the most mechanistic approach did not succeed to simulate external observations (Root Mean Standard Error of Prediction (RMSEP) > 30 mg.g DM−1, Efficiency (Eff) <0), whereas the intermediate model was more efficient (RMSEP = 15.19 mg.g DM−1, Eff = 0.205 and 16.61 mg.g DM−1, Eff = 0.366, for GFS (Glucose + Fructose + Sucrose) and starch, respectively). The accuracy of the model was further improved when using field data for calibration (RMSEP = 5.86 mg.g DM−1, Eff = 0.962; RMSEP = 10.56 mg.g DM−1, Eff = 0.752, for GFS and starch, respectively). This study provided an operative tool to simulate carbohydrate dynamics over leafless period that could predict frost hardiness with approx. 3.4°C accuracy with temperature, water content and initial starch and soluble carbohydrate measurements. It should now be tested under various meteorological conditions and biological systems.

Highlights

  • In frost-exposed habitats, perennial plants have to cope with freezing stress every winter

  • As the observed variability in carbohydrate composition was reduced after normalization of the daily change in GFS and starch by the initial amount of starch and GFS, respectively (Figures 3A–F; Figures S1–S3; Tables S4–S8), we developed the intermediate model based on the mechanistic assumption that the change in the amount of the product of an enzymatic reaction can be limited by the amount of substrate: GFS(t + 1) = GFS(t) + k1c (t) + k1m(t) · Starch(t)

  • Carbon metabolism is a key component of plant ability to cope with environmental constraints (Hartmann and Trumbore, 2016), especially freezing stress during the dormant period (Gusta et al, 2004; Morin et al, 2007)

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Summary

Introduction

In frost-exposed habitats (i.e., from temperate to boreal areas), perennial plants have to cope with freezing stress every winter. Solute content (i.e., carbohydrates, organic or amino acids) increases and water content decreases in relation to frost hardiness in many perennial species (Reuther, 1971; Levitt, 1980; Guy, 1990; Gusta et al, 2004; Morin et al, 2007; Charrier et al, 2013a, 2015b). The ratio between GFS and water content accurately predict frost hardiness across seasons and organs in walnut trees, according to the osmo-hydric model (Charrier et al, 2013b). The extremely low water potential of ice (−1.16 MPa.K−1 below freezing temperature) pulls water molecules out through the membrane, further increasing solute concentration (Charra-Vaskou et al, 2015; Charrier et al, 2015b; Arora, 2018). Solutes maintain a solvation layer protecting the surface of membranes and the macromolecules (Sakai, 1962; Heber and Santarius, 1973; Steponkus et al, 1977; Yoon et al, 1998, Kasuga et al, 2006, 2007)

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