SnRK1 subcellular localization is linked to TOR signaling, chloroplast function, and salt stress tolerance in mature Arabidopsis leaves

Abstract

Soil salinity can impair carbon fixation and ultimately decrease crop yield. To counteract this detrimental effect and maintain cellular homeostasis and productivity under stress, plants rely on metabolic and growth adaptations. Sucrose non-fermenting Related Kinase 1 (SnRK1) and Target of Rapamycin (TOR) kinases coordinate cellular metabolism and stress signaling. Despite substantial progress, major gaps persist regarding how SnRK1 subcellular localization affects TOR activity, chloroplast function, and overall metabolic balance under salinity in source leaves. We analyzed Arabidopsis mature leaves of plants expressing SnRK1α1 targeted to the nucleus (NLS-α1) or membrane/myristoylation (βMYR-α1) subjected to prolonged salinity (150 mM NaCl, 14 days). Under control conditions, SnRK1 activity was low during the light period in wild-type (WT) leaves, however under salinity, both total and nuclear SnRK1 activity rose markedly at midday. Remarkably, the NLS-α1 plants exhibited increased tolerance, showing 10% less shoot biomass reduction than WT plants under salt stress. This may be related to the fact that mature leaves of NLS-α1 genotype showed intact chloroplast ultrastructure, higher photosynthetic performance, and elevated levels of threonine and stress-related metabolites under NaCl long-term exposure. Conversely, βMYR-α1 plants exhibited misregulated TOR activity, disrupted thylakoid structure with reduced photosynthetic efficiency and photodamage at PSII level, and the accumulation of photorespiratory intermediates. Overall, SnRK1 localization emerges as a spatial factor associated with organelle performance, metabolic reprogramming, and TOR signaling patterns during salt stress. Modulating SnRK1 intracellular distribution may, therefore, be a useful strategy for breeding or biotechnological approaches toward plant salinity tolerance.