Split roots, unified signals: Electrome and systemic responses reveal priming under recurrent salinity in sorghum

Abstract

Plants can retain information from previous stressful events, adjusting their systemic responses through priming and stress memory. However, the role of bioelectrical signaling in modulating systemic acquired acclimation (SAA) under recurrent salt stress remains poorly understood. Here, we investigated the physiological, biochemical, molecular, and electrophysiological responses of Sorghum bicolor exposed to single and repeated salinity events (120 mM NaCl) using a split-root system, allowing spatial separation of local and systemic stress signaling by selectively salinizing one or both root compartments. Results indicated that recurrent stress (S–S) induced a priming effect. Transpiration and stomatal conductance increased by ∼43% and 46% compared to control (C-C) and other treatments. In contrast, water-use efficiency (A/E) was nearly 90% higher in C–C and non-recurrent stress (S 2nd cycle–S 2nd cycle) than in S–S, while intrinsic (A/gs) was 60% higher in non-recurrent-stressed plants compared to S–S. SOD activity in S–S was 50% higher than in non-recurrent-stressed groups, whereas POD activity in S 2nd cycle–S 2nd cycle, reached 175% above S–S. APX1 expression was strongly downregulated in S–S. Electrophysiological analyses revealed early and transient responses under recurrent stress, with ApEn reaching ∼0.6 within the first 10 min after stimulus and DFA stabilizing around 1.0. In contrast, non-recurrent stress led to delayed responses (>60 min), reduced complexity (ApEn ∼0.2), and higher DFA values (>1.5). Our integrative approach, combining split-root design, electrophysiology, and molecular biology, provides evidence for a dynamic electrome-based memory that enhances stress acclimation.