Metabolic Responses to Waterlogging Differ between Roots and Shoots and Reflect Phloem Transport Alteration in Medicago truncatula.

Jérémy Lothier,Guillaume Tcherkez,Anis M. Limami,Caroline Cukier,Houssein Diab

doi:10.3390/plants9101373

Abstract

Root oxygen deficiency that is induced by flooding (waterlogging) is a common situation in many agricultural areas, causing considerable loss in yield and productivity. Physiological and metabolic acclimation to hypoxia has mostly been studied on roots or whole seedlings under full submergence. The metabolic difference between shoots and roots during waterlogging, and how roots and shoots communicate in such a situation is much less known. In particular, the metabolic acclimation in shoots and how this, in turn, impacts on roots metabolism is not well documented. Here, we monitored changes in the metabolome of roots and shoots of barrel clover (Medicago truncatula), growth, and gas-exchange, and analyzed phloem sap exudate composition. Roots exhibited a typical response to hypoxia, such as γ-aminobutyrate and alanine accumulation, as well as a strong decline in raffinose, sucrose, hexoses, and pentoses. Leaves exhibited a strong increase in starch, sugars, sugar derivatives, and phenolics (tyrosine, tryptophan, phenylalanine, benzoate, ferulate), suggesting an inhibition of sugar export and their alternative utilization by aromatic compounds production via pentose phosphates and phosphoenolpyruvate. Accordingly, there was an enrichment in sugars and a decline in organic acids in phloem sap exudates under waterlogging. Mass-balance calculations further suggest an increased imbalance between loading by shoots and unloading by roots under waterlogging. Taken as a whole, our results are consistent with the inhibition of sugar import by waterlogged roots, leading to an increase in phloem sugar pool, which, in turn, exert negative feedback on sugar metabolism and utilization in shoots.

Highlights

Flooding is currently one of the most severe factors that reduces crop productivity [1,2].It is believed that at least 10% of arable fields can be affected by flooding (FAOSTAT, www.fao.org).As such, it concerns many cultivated species, including major crops, like wheat, and alternative agricultural practices have to be found to overcome this problem.Flooding leads to occasional or prolonged root submergence
There was a significant negative effect of waterlogging on photosynthesis (Figure 1a), due to lower stomatal conductance (Figure 1b). This effect was not more pronounced after 21 d suggesting that leaf photosynthesis partly acclimated to waterlogging conditions
Our results show that roots and leaves have distinct metabolic responses, driven by the effect of oxygen shortage, and by the side effect of root hypoxia on sap homeostasis

Summary

Introduction

Flooding is currently one of the most severe factors that reduces crop productivity [1,2].It is believed that at least 10% of arable fields can be affected by flooding (FAOSTAT, www.fao.org).As such, it concerns many cultivated species, including major crops, like wheat, and alternative agricultural practices have to be found to overcome this problem (reviewed in Manik et al, 2019 [3]).Flooding leads to occasional or prolonged root submergence (waterlogging). Flooding is currently one of the most severe factors that reduces crop productivity [1,2]. It is believed that at least 10% of arable fields can be affected by flooding (FAOSTAT, www.fao.org). As such, it concerns many cultivated species, including major crops, like wheat, and alternative agricultural practices have to be found to overcome this problem (reviewed in Manik et al, 2019 [3]). O2 deprivation is the most important biochemical factor during waterlogging [4]: when air spaces that are normally present in soil are filled with water, root environment becomes hypoxic due to O2 consumption by Plants 2020, 9, 1373; doi:10.3390/plants9101373 www.mdpi.com/journal/plants. The well-known effects of hypoxia relate to energy limitation (i.e. reduction in respiratory ATP production due to O2 shortage) and cytoplasm acidification due to a decline in plasma membrane H+ -ATPase activity as well as organic acid generation by metabolism [5]

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