USP Gene Network Modulation and Osmoprotection Define Salt Resilience in Chenopodium quinoa Genotypes

Soil salinity poses a severe threat to global food security, making the halophytic crop Chenopodium quinoa a vital model for sustainable agriculture. While quinoa is known for its extreme salt tolerance, the molecular mechanisms integrating stress perception with metabolic adaptation remain poorly defined. This study employs a multi-level approach, integrating morphological, physiological, biochemical, transcriptomic, and metabolomic analyses, to dissect the complex adaptation strategies across eight advanced quinoa lines. Morphological and physiological screening identified three distinct survival strategies: transient high-productivity, stress-induced optimal performance, and conservative stability. We demonstrated that salt resilience is not merely a survival response but a highly coordinated regulatory program driven by one of the key regulators such as the Universal Stress Protein (USP) gene network. Key physiological findings revealed a progressive decline in photosynthetic efficiency (ΦPSII) and rising oxidative damage (MDA), yet tolerant lines maintained superior photoprotection through highly regulated heat dissipation (ΦNPQ). The cellular defense involved the mobilization of enzymatic scavengers (superoxide dismutase and peroxidase), peaking at the highest stress level. Transcriptomic analysis of the USP gene family showed dynamic, tissue-specific regulation at moderate stress and activation of ion exclusion genes in the roots at 300 mM salinity. Metabolomic profiling identified one variety Q-33 as highly resilient, characterized by coordinated metabolic reprogramming, specifically strong induction of osmolytes and volatile defense compounds. These results define quinoa's salt tolerance as a synergistic strategy combining osmotic adjustment, superior photoprotection, active ROS scavenging, and dynamic transcriptional control of the USP network.