Metabolic and physiological analysis reveals distinct salinity tipping point in Vitis vinifera cv. Syrah to enter a stress response mode

Rising soil salinity threatens Mediterranean viticulture, yet the tipping point and the crosstalk between the physiological, metabolic, and ionic responses to salinity stress are not fully understood. The coordinated metabolic, ionic, and physiological response of Syrah grafted on Sélection Oppenheim 4 (SO4) rootstock was investigated under various salinity levels (control, 1, 1.5, 2, 2.5, and 3 dS m⁻¹) during the growing season. Here we show that salinity stress significantly affected physiological activity, with stomatal conductance (g_s) decreasing rapidly above 1.5 dS m⁻¹, followed by declines in CO₂ assimilation and electron transport rates. Salinity stress induced by NaCl and CaCl₂ significantly affected ion accumulation and nutrient absorption, increasing Na⁺ and Cl⁻ accumulation in the leaf while reducing uptake and translocation of essential ions such as K⁺, Mg²⁺, Fe²⁺, Zn²⁺, and Cu²⁺. This ionic imbalance coincided with Cl⁻ accumulation, often more pronounced than Na⁺ accumulation in Syrah leaves. Critical thresholds were seen for leaf Cl⁻ and Na⁺ concentrations, which exceeded 123 and 65 μmol gDW⁻¹, respectively, that triggered significant reductions in g_s and stem water potential at an electrical conductivity of 1.5 dS m⁻¹. These events were accompanied by increased accumulation of ions and osmoprotectants. Besides decreases in tricarboxylic acid cycle intermediates, such as citrate and malate, salinity stress was explicitly linked to alterations in leaf nitrogen metabolism with the accumulation of free amino acids, including glutamate, proline, and polyamine putrescine, and the non-protein amino acid γ-aminobutyrate. This study provides valuable insights into the complex interplay between physiology, metabolism, and ionic balance in grapevine as a response to salinity stress.