A pump/leak model of growth: the biophysics of cell elongation in higher plants revisited

Abstract

Current concepts of growth hydraulics in higher plants are critically revisited, and it is concluded that they partly fail to interpret the experimental data adequately, particularly in the case of hydroponics-grown roots. Theoretical considerations indicate that the growth rate in roots is controlled by the extensibility of the cell wall, excluding water availability (i.e. hydraulic conductance) as a major constraint. This is supported by the findings that the growth rate does not scale with turgor, and that no radial nor axial water potential gradients have been observed in the root elongation zone. Nevertheless, a water potential deficit ranging from –0.2 to –0.6 MPa has repeatedly been reported for growing cells that by far exceeds the shallow trans-membrane water potential difference required for the uptake of growth water. Unexpectedly, growth was also shown to depend on the hydraulic conductance (LP) of the plasma membrane of root cells, even though LP should generally be too large to have an impact on growth. For leaves, similar observations have been reported, but the interpretation of the data is less straightforward. Inconsistencies associated with the current model of growth hydraulics prompt the author to suggest a revised model that comprises, in addition to a passive mechanism of water transport across the plasma membrane of growing cells mediated by aquaporins (‘leak’) a secondary active water transport (‘pump’), in analogy to a mechanism previously demonstrated for mammalian epithelia and postulated for xylem parenchyma cells in roots. Water is hypothesised to be secreted against a trans-membrane water potential difference by cotransport with solutes (salts, sugars, and/or amino acids), taking advantage of the free energy released by this transport step. The solute concentration gradient is supposed to be maintained by a subsequent retrieval of the solutes from the apoplast and back-transport at the expense of metabolic energy. Water secretion tends to reduce the turgor pressure and retards growth, but turgor and, in turn, growth can be upregulated very rapidly independent from any adjustment in the osmolyte deposition rate by increasing LP and/or reducing secondary active water transport, e.g. when the root is exposed to mild osmotic stress, as confirmed by experimental studies.