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, 61 (1), 3-20

The Roots of Plant Frost Hardiness and Tolerance

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The Roots of Plant Frost Hardiness and Tolerance

Valentin Ambroise et al. Plant Cell Physiol.

Abstract

Frost stress severely affects agriculture and agroforestry worldwide. Although many studies about frost hardening and resistance have been published, most of them focused on the aboveground organs and only a minority specifically targets the roots. However, roots and aboveground tissues have different physiologies and stress response mechanisms. Climate models predict an increase in the magnitude and frequency of late-frost events, which, together with an observed loss of soil insulation, will greatly decrease plant primary production due to damage at the root level. Molecular and metabolic responses inducing root cold hardiness are complex. They involve a variety of processes related to modifications in cell wall composition, maintenance of the cellular homeostasis and the synthesis of primary and secondary metabolites. After a summary of the current climatic models, this review details the specificity of freezing stress at the root level and explores the strategies roots developed to cope with freezing stress. We then describe the level to which roots can be frost hardy, depending on their age, size category and species. After that, we compare the environmental signals inducing cold acclimation and frost hardening in the roots and aboveground organs. Subsequently, we discuss how roots sense cold at a cellular level and briefly describe the following signal transduction pathway, which leads to molecular and metabolic responses associated with frost hardening. Finally, the current options available to increase root frost tolerance are explored and promising lines of future research are discussed.

Keywords: Abiotic stress; Cold acclimation; Frost; Hardiness; Roots; Tolerance.

Figures

Fig. 1
Fig. 1
Soil freezing patterns expected in the future. In the future, increased temperature could lead to a decreased snow cover, leading to a less insulated soil and lower soil temperatures. This would decrease the fine root biomass by up to 50% in summer, highly reducing the new aboveground biomass.
Fig. 2
Fig. 2
Sources of damage caused by low temperatures in plants. The main sources of damage during freezing temperatures are intracellular ice formation, which leads to cell death, and extracellular ice formation, which provokes osmotic stress. This osmotic stress mainly causes changes in lipid polymorphism, expansion-induced lysis, which leads to cell death, and an increased ROS production. Light blue, stressors; red, damage done to the membranes; yellow, imbalance in ROS homeostasis; dark blue, alterations in cellular metabolites and macromolecules; purple, physical damages. Skulls mean direct death of the cell via heavy damage to the membranes.
Fig. 3
Fig. 3
Protective mechanisms put in place by freezing-tolerant roots. The plasma membrane is the main site of damage during frost-induced stress. During intense osmotic stress, the plasma membrane and the tonoplast can come into close contact and their lipid bilayers can shift from a lamellar to a hexagonal II phase, leading to cellular leakage. The cell wall plays an important role in frost tolerance, and its strengthening can lead to increased frost tolerance. Antifreeze proteins and fructans decrease the expansion of ice crystal in the apoplast and inhibit the formation of icicles. Simple hexoses and free amino acids accumulate in the cytoplasm where they counterbalance the negative osmotic pressure induced by the presence of ice in the extracellular matrix. Dehydrins, heat shock proteins and polyamines stabilize the membranes and inhibit protein and mRNA denaturation. Trehalose, maltose and glucans stabilize the membranes and inhibit membrane fusion. Antioxidant concentrations increase and counter the increased ROS production with the help of proline and ROS-scavenging sugar alcohols, i.e. raffinose, galactinol, sorbitol. I, ice crystal; N, nucleus; ↗ ROS, increased ROS production.

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