Xylem-phloem hydraulic coupling explains multiple osmoregulatory responses to salt stress

Salinity is known to affect plant productivity by limiting leaf-level carbon exchange, root water uptake, and carbohydrates transport in the phloem. However, the mechanisms through which plants respond to salt exposure by adjusting leaf gas exchange and xylem-phloem flow are still mostly unexplored. A physically based model coupling xylem, leaf, and phloem flows is here developed to explain different osmoregulation patterns across species. Hydraulic coupling is controlled by leaf water potential, ψ_l , and determined under four different maximization hypotheses: water uptake (1), carbon assimilation (2), sucrose transport (3), or (4) profit function - i.e. carbon gain minus hydraulic risk. All four hypotheses assume that finite transpiration occurs, providing a further constraint on ψ_l . With increasing salinity, the model captures different transpiration patterns observed in halophytes (nonmonotonic) and glycophytes (monotonically decreasing) by reproducing the species-specific strength of xylem-leaf-phloem coupling. Salt tolerance thus emerges as plant's capability of differentiating between salt- and drought-induced hydraulic risk, and to regulate internal flows and osmolytes accordingly. Results are shown to be consistent across optimization schemes (1-3) for both halophytes and glycophytes. In halophytes, however, profit-maximization (4) predicts systematically higher ψ_l than (1-3), pointing to the need of an updated definition of hydraulic cost for halophytes under saline conditions.