Theoretical evidence for a multicellular water pump fueled by symplastic osmotic potential gradients in vascular plant roots

The current paradigm of root radial water flow assumes that water only flows of water potential gradients, so that the only way to pump water without lowering xylem relative pressure is by lowering xylem total water potential through solute loading. However, numerous studies report that crops and woody species roots may absorb water despite higher xylem pressure and lower xylem solute concentration, as compared to the root direct environment (i.e. water would flow of water potential gradients). This contradicts the current paradigm of root water acquisition, and seemingly goes against the second law of thermodynamics. We recently found a physiological mechanism solving this enigma with a microhydrological model of water flow across roots, called MECHA. Osmotic gradients between living cells generate pressure gradients driving water through plasmodesmata, with a surprising result: subcellular flow of local water potential gradients may translate into flow of both total and pressure potential gradients between root surface and xylem. This water pumping mechanism means any vascular plant may reduce its xylem water tension and increase its water availability beyond predictions of the current theory. Here, we analyse the water pumping mechanism across a simple cell triplet, then show that the associated upscaled equations hold in 2- and 3-D maize and Arabidopsis hydraulic anatomies, and finally draw perspectives on the implications of such a mechanism on cell-to- cell communication across plasmodesmata