Integrated transcriptomic and metabolomic analysis reveals that SiGPX1 enhances saline-alkali tolerance in foxtail millet through the glutathione metabolism pathway

Soil saline-alkalization represents a critical global environmental threat and severely impairs plant physiological processes, causing substantial yield losses and even complete crop failure. It is essential to understand the molecular mechanisms underlying plant saline-alkali tolerance and identify the key genetic determinants for developing stress-tolerant crops, enhancing agricultural productivity on saline-alkali lands, and ensuring ecological sustainability. Foxtail millet is a naturally stress-tolerant crop with exceptionally high drought resistance and adaptability to saline-alkali conditions. This study employed a integrated transcriptomic and metabolomic analysis approach to investigate the mechanisms for salt-alkali (seawater) tolerance in foxtail millet with two genetically distinct varieties, 'Jikegu 3 hao' (JK3; highly saline-alkali tolerant) and 'Baogu 175' (B175; saline-alkali sensitive). Metabolomic profiling identified 1,539 differentially expressed metabolites. JK3 exhibited significant enrichment of key osmoregulators (citric acid, γ-aminobutyric acid, and betaine) for coordinated upregulation of some critical metabolic pathways, including alanine, aspartate and glutamate metabolism, glutathione metabolism, galactose metabolism, and the TCA cycle under saline-alkali stress. Integrated transcriptomic-metabolomic analysis pinpointed glutathione metabolism as the central regulatory pathway for saline-alkali tolerance. Transient silencing of SiGPX1 disrupted cellular ion homeostasis, impaired reactive oxygen species (ROS) scavenging capacity (indicated by reduced H2O2 clearance), and elevated malondialdehyde accumulation, ultimately resulting in growth retardation under stress conditions. The results indicated that SiGPX1 is a master positive regulator of saline-alkali tolerance in foxtail millet by maintaining redox homeostasis and cellular integrity. This study establishes SiGPX1 as a promising genetic target for precise breeding of saline-alkali tolerant foxtail millet varieties.