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The cost of avoiding freezing in stems: trade-off between xylem resistance to cavitation and supercooling capacity in woody plants

Stems and leaves of Olea europaea L. (olive) avoid freezing damage by substantial supercooling during the winter season. Physiological changes during acclimation to low temperatures were studied in five olive cultivars. Water relations and hydraulic traits, ice nucleation temperature (INT) and temperatures resulting in 50% damage (LT50) were determined. All cultivars showed a gradual decrease in INT and LT50 from the dry and warm summer to the wet and cold winter in Patagonia, Argentina. During acclimation to low temperatures there was an increase in leaf cell wall rigidity and stomatal conductance (gs), as well as a decrease in leaf apoplastic water content, leaf water potential (Ψ), sap flow and stem hydraulic conductivity (ks). More negative Ψ as a consequence of high gs and detrimental effects of low temperatures on root activity resulted in a substantial loss of ks due to embolism formation. Seasonal stem INT decrease from summer to winter was directly related to the xylem resistance to cavitation, determined by the loss of ks across cultivars. Thus the loss of freezable water in xylem vessels by embolisms increased stem supercooling capacity and delayed ice propagation from stems to the leaves. For the first time, a trade-off between xylem resistance to cavitation and stem and leaf supercooling capacity was observed in plants that avoid extracellular freezing by permanent supercooling. The substantial loss of hydraulic function in olive cultivar stems by embolism formation with their high repair costs are compensated by avoiding plant damage at very low subzero temperatures.