Naganishia liquefaciensARY7, a Psychrophilic Yeast Endophyte Improves Plant Low Temperature Acclimation Through Auxin and Salicylic Acid Signaling

Understanding how plant-associated yeasts mediate plant fitness under environmental stress remains mostly elusive. Here, the role of auxin and salicylic acid (SA)-producing psychrophilic yeast endophyte Naganishia liquefaciens strain ARY7, isolated from the roots of cold-desert plant Arnebia euchroma, was investigated for low temperature (LT; 10°C) tolerance in Arabidopsis thaliana. ARY7-inoculated plants had higher biomass, exhibited higher photosynthetic efficiency, starch accumulation, and reduced stress-responsive parameters at 10°C than their non-inoculated controls. ARY7-inoculation in the Arabidopsis enhanced auxin signaling in the roots, leading to more lateral roots and root hair development at 10°C. Increased exopolysaccharide (EPS) accumulation around roots and root colonization by ARY7 at 10°C also suggested its role in cold tolerance. The SA-production ability of ARY7 was supported by the elevated SA levels and upregulation of key SA biosynthesis genes (SID2 and PBS3) in ARY7-inoculated plants at 10°C. In addition, an improved seedling phenotype in ARY7-inoculated sid2 (SA-deficient) mutants of Arabidopsis further confirmed the role of ARY7-produced SA-mediated plant fitness. The downregulated expression of key cold-responsive genes (CBF, COR, RD29A, and P5CS1) in the leaves of ARY7-inoculated plants indicated reduced sensitivity to LT. This study established that the ARY7-mediated plant cold tolerance is due to the increased ARY7-root colonization through EPS production and involves auxin and SA signaling. This study provides valuable insights to explore plant-associated psychrophilic yeasts for protecting plants from various abiotic stresses, including cold temperature.