Dynamic Modeling of Carbon Metabolism During the Dormant Period Accurately Predicts the Changes in Frost Hardiness in Walnut Trees Juglans regia L.

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 proces...

Full description

Bibliographic Details
Main Authors: Guillaume Charrier, André Lacointe, Thierry Améglio
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-12-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fpls.2018.01746/full
_version_ 1818504367751299072
author Guillaume Charrier
André Lacointe
Thierry Améglio
author_facet Guillaume Charrier
André Lacointe
Thierry Améglio
author_sort Guillaume Charrier
collection DOAJ
description 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.
first_indexed 2024-12-10T21:36:13Z
format Article
id doaj.art-a1d4d189f9ad43168d7535a9ac1debf3
institution Directory Open Access Journal
issn 1664-462X
language English
last_indexed 2024-12-10T21:36:13Z
publishDate 2018-12-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Plant Science
spelling doaj.art-a1d4d189f9ad43168d7535a9ac1debf32022-12-22T01:32:38ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2018-12-01910.3389/fpls.2018.01746410551Dynamic Modeling of Carbon Metabolism During the Dormant Period Accurately Predicts the Changes in Frost Hardiness in Walnut Trees Juglans regia L.Guillaume CharrierAndré LacointeThierry AméglioThe 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.https://www.frontiersin.org/article/10.3389/fpls.2018.01746/fullcarbohydratesdormancyenzymatic activitystarchtree physiologywinter biology
spellingShingle Guillaume Charrier
André Lacointe
Thierry Améglio
Dynamic Modeling of Carbon Metabolism During the Dormant Period Accurately Predicts the Changes in Frost Hardiness in Walnut Trees Juglans regia L.
Frontiers in Plant Science
carbohydrates
dormancy
enzymatic activity
starch
tree physiology
winter biology
title Dynamic Modeling of Carbon Metabolism During the Dormant Period Accurately Predicts the Changes in Frost Hardiness in Walnut Trees Juglans regia L.
title_full Dynamic Modeling of Carbon Metabolism During the Dormant Period Accurately Predicts the Changes in Frost Hardiness in Walnut Trees Juglans regia L.
title_fullStr Dynamic Modeling of Carbon Metabolism During the Dormant Period Accurately Predicts the Changes in Frost Hardiness in Walnut Trees Juglans regia L.
title_full_unstemmed Dynamic Modeling of Carbon Metabolism During the Dormant Period Accurately Predicts the Changes in Frost Hardiness in Walnut Trees Juglans regia L.
title_short Dynamic Modeling of Carbon Metabolism During the Dormant Period Accurately Predicts the Changes in Frost Hardiness in Walnut Trees Juglans regia L.
title_sort dynamic modeling of carbon metabolism during the dormant period accurately predicts the changes in frost hardiness in walnut trees juglans regia l
topic carbohydrates
dormancy
enzymatic activity
starch
tree physiology
winter biology
url https://www.frontiersin.org/article/10.3389/fpls.2018.01746/full
work_keys_str_mv AT guillaumecharrier dynamicmodelingofcarbonmetabolismduringthedormantperiodaccuratelypredictsthechangesinfrosthardinessinwalnuttreesjuglansregial
AT andrelacointe dynamicmodelingofcarbonmetabolismduringthedormantperiodaccuratelypredictsthechangesinfrosthardinessinwalnuttreesjuglansregial
AT thierryameglio dynamicmodelingofcarbonmetabolismduringthedormantperiodaccuratelypredictsthechangesinfrosthardinessinwalnuttreesjuglansregial