Multiple paths lead to salt tolerance - pre-adaptation vs dynamic responses from two closely related extremophytes

Salt tolerance is a complex trait with much of the underlying genetic variation and integrated response strategies yet to be discovered from stress adapted plants. Schrenkiella parvula and Eutrema salsugineum are salt-tolerant extremophytes related to Arabidopsis thaliana in Brassicaceae. We investigated their response strategies contrasted against the salt-sensitive model, A. thaliana to cope with salt stresses via transcriptomic, metabolomic, and ionomic adjustments. The extremophytes exemplified divergent routes to achieve nutrient balance, build osmotolerance, boost antioxidant capacity, and extend transcriptomic support for modified ion transport and stress signaling. Those led to similar molecular phenotypes adapted to salt stress in the extremophytes, absent in A. thaliana. The predominant transcriptomic signals in all three species were associated with salt stress. However, root architecture modulation mediated by negative regulation of auxin and ABA signaling supported minimally-affected root growth unique to each extremophyte during salt treatments. Overall, E. salsugineum exhibited pre-adapted responses at the metabolome level, whereas S. parvula showed dynamic metabolomic responses coupled to a pre-adapted transcriptome to survive salt stress. Our work shows that the two extremophytes share common salt tolerance features, but differ substantially in pathways leading to the convergent, adaptive traits.