Metabolic network homeostasis and antagonistic stress response drive rootstock-mediated tolerance to combined salinity and water-deficit in grapevine cv. Syrah

Abstract

Water deficit and salinity are major stresses that rarely occur in isolation, yet their combined effects on grapevine remain poorly understood. In a 3-year study, we dissected the response of Vitis vinifera cv. Syrah, a cultivar known for its sensitivity to water-deficit and salinity stress, grafted onto 1103 Paulsen (PL1103) and Sélection Oppenheim 4 (SO4) rootstocks to salinity (2.5 dS m⁻¹) combined with irrigation regimes (66%, 100%, and 133% of control). Water availability primarily defined physiological responses, with subtle rootstock-specific differences. Under water deficit, both rootstocks exhibited substantial physiological impairment (stem water potential < −2.0 MPa, leaf relative water content < 75%, and reduced stomatal conductance). In contrast, salinity induced ion imbalance, with superior Cl⁻ exclusion in SO4-grafts conferring improved physiological performance. Using a comparative framework classifying interactions as additive, synergistic, or antagonistic, we found that SO4-grafts employ an antagonistic mitigation strategy, whereas PL1103-grafts engage in synergistic amplification of stress impacts. This was reflected in a 28% yield advantage of SO4-grafts under combined stress. Central metabolite profiling revealed rootstock-specific divergence. PL1103-grafts displayed condition-driven alterations (up to ±10-fold) in the accumulation of osmoprotective amino acids (proline and GABA) and sugars (glucose and fructose), whereas SO4-grafts showed phenologically regulated, homeostatic stability. Network analysis suggests that tolerance is driven by reduced network connectivity of metabolic architecture rather than increased levels of a few metabolites. Less perturbed network in SO4 (edges reduced from 194 to 168) reflected SO4-grafts’ resilience. Conversely, PL1103-grafts exhibited network expansion under salinity, with increased connectivity from 196 to 267 edges and centrality, indicative of heightened stress perception. Overall, rootstocks appear to actively modulate scion resource allocation rather than passively buffering stress, likely through long-distance signals across the graft union.