Transient uncoupling of the Suc-Tre6P-SnRK1 nexus during salt stress associates with biphasic metabolic reprogramming and root plasticity

Soil salinization threatens global agriculture reducing yields, yet the metabolic signals controlling salt-sensitive root plasticity in alfalfa remain unclear. We hypothesize that salinity transiently uncouples the sucrose–trehalose-6-P (Tre6P)– Sucrose non-fermenting kinase 1 (SnRK1) nexus, aligning with a biphasic root metabolic response and altered root architecture. Alfalfa seedlings were grown in a hydroponic system and exposed to 200 mM NaCl, with root samples collected from 1 h to 7 d. While primary root growth and biomass remained unchanged, lateral root development was enhanced under salinity. Early response (1 h–1 d) was characterized by reduced carbon metabolites, low Tre6P, increased malondialdehyde, and SnRK1 activation, with a decline in glycolytic and TCA intermediates. During this phase, sucrose was negatively correlated with both Tre6P and SnRK1. Late response (3–7 d) showed a SnRK1 reactivation, Tre6P recovery, and osmoprotectant accumulation, including increased antioxidant capacity (+75% at 3dpt), proline (+178%), and sucrose (+18%) and starch depletion (−57%) at 7dpt respect to control. These metabolic changes coincided with the enhanced lateral root emergence. These findings indicate a two-phase response: early metabolic downscaling with transient Suc–Tre6P–SnRK1 disruption, followed by recovery with Tre6P restoration, SnRK1 reactivation, osmoprotection, and sustained root plasticity under salinity.