A trade-off between allocated resources for photosynthesis and stress tolerance is generally observed in nature. Thus, the search for outlier species breaking this trend is an interesting approach to identity new mechanisms for plant breeding purposes. Hypothetically, outlier extremophyte species present a distinctive arrangement of physiological functions that favor stress tolerance mechanisms without jeopardizing investment allocation into photosynthesis. We explored this trade-off, analyzing twenty-one plant species for desiccation tolerance, and photosynthetic capacity, under the extreme arid environments of the Atacama Desert and the Surire Salar in the Chilean Altiplano. Most of the studied species followed the trade-off tendency, however, we did find one outlier species, Prosopis tamarugo. To study the mechanisms involved in this atypical response, the Prosopis genus was analyzed more deeply. Our results suggest that the outlier response of P. tamarugo is multifactorial. This species presented a high photochemistry activity, associated with a higher synthesis of chlorophylls, photoprotective pigments, and complex antioxidant molecules. Moreover, the synthesis of no-nitrogen osmoprotectant molecules, such as ciceritol and mannitol in P. tamarugo, would allow the allocation of nitrogen to support its high photosynthetic capacity, without compromising its leaf desiccation stress tolerance.

Recent results suggest that metabolism-mediated stomatal closure mechanisms are important to regulate differentially the stomatal speediness between ferns and angiosperms. However, evidence directly linking mesophyll metabolism and the slower stomatal conductance (gs) in ferns is missing. Here we investigated the effect of exogenous application of abscisic acid (ABA), sucrose and mannitol on gs kinetics and carried out a metabolic fingerprinting analysis of ferns and angiosperms leaves harvested throughout a diel course. Ferns stomata did not respond to ABA in the time period analysed. No differences in the relative decrease in gs was observed between ferns and the angiosperm following provision of sucrose or mannitol. However, ferns have slower gs responses to these compounds than angiosperms. Metabolomics analysis highlights that ferns have higher accumulation of secondary rather than primary metabolites throughout the diel course, with the opposite being observed in angiosperms. Our results indicate that metabolism-mediated stomatal closure mechanism is conserved among ferns and angiosperms and that the slower stomatal closure in ferns is associated to a reduced capacity to respond to mesophyll-derived sucrose and to a higher carbon allocation toward secondary metabolism, which likely modulates both photosynthesis-stomatal movements and growth-stress tolerance trade-offs.