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

Abstract

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, ψl, 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 ψl. 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 ψl than (1–3), pointing to the need of an updated definition of hydraulic cost for halophytes under saline conditions.