Osmolyte cooperation affects turgor dynamics in plants

Abstract

Scientists have identified turgor-based actuation as a fundamental mechanism in plant movements. Plant cell turgor is generated by water influx due to the osmolyte concentration gradient through the cell wall and the plasma membrane behaving as an osmotic barrier. Previous studies have focused on turgor modulation with respect to potassium chloride (KCl) concentration changes, although KCl is not efficiently retained in the cell, and many other compounds, including L-glutamine (L-Gln) and D-glucose (D-Glc), are present in the cytosol. In fact, the contributions of other osmolytes to turgor dynamics remain to be elucidated. Here, we show the association of osmolytes and their consequent cooperative effects on the time-dependent turgor profile generated in a model cytosol consisting of KCl, D-Glc and L-Gln at experimentally measured plant motor/generic cell concentrations and at modified concentrations. We demonstrate the influence and association of the osmolytes using osmometry and NMR measurements. We also show, using a plant cell-inspired device we previously developed, that osmolyte complexes, rather than single osmolytes, permit to obtain higher turgor required by plant movements. We provide quantitative cues for deeper investigations of osmolyte transport for plant movement, and reveal the possibility of developing osmotic actuators exploiting a dynamically varying concentration of osmolytes.

Arabidopsis tonoplast intrinsic protein and vacuolar H+-adenosinetriphosphatase reflect vacuole dynamics during development of syncytia induced by the beet cyst nematode Heterodera schachtii

“…The mechanism how exactly downregulation of aquaporins might increase the turgor pressure may be related to the complex biology of syncytia. Considering that aquaporins allow water transport in both directions (import/export), the final effect of their action depends on other factors regulating water flux such as osmolytes and their transporters (Argiolas et al 2016). It is also possible that the net effect of aquaporins depends on their activity balance in several subcellular locations.…”

How water flow, geometry, and material properties drive plant movements

“…The van't Hoff law says that in a dilute solution, the osmotic pressure in Pa, P os , is proportional to the A c c e p t e d M a n u s c r i p t 9 temperature in Kelvin, T, and the concentration of the solute in mole, c solute , and R is the ideal gas constant (R= 8.314 J⋅mol −1 ⋅K −1 ). To influence osmosis, the plant can thus modify the flux of ions (in particular potassium and chloride) (Blatt, 2000;Hedrich, 2012;Wang et al, 2017) and make changes in metabolism to alter osmotic compound concentrations (Argiolas et al, 2016) or modify the permeability of the membrane for water through aquaporin gating (Törnroth-Horsefield et al, 2006;Alleva et al, 2012;Maurel et al, 2015;Rodrigues et al, 2017). Brownian motion and diffusion of water and solute will, of course, take place in both chambers but the case against osmosis being driven by diffusion of solvent down a presumed water concentration gradient is nearly sealed, despite occasional counter-arguments leaking through (Nelson, 2017).…”

A variable-stiffness tendril-like soft robot based on reversible osmotic actuation

“…Moreover, plants use the coordinated modulation of intracellular turgor to tune their stiffness and achieve macroscopic movements 10 . The cytosolic osmolyte system is an aqueous gel solution containing proteins and small molecules (including potassium chloride, glucose, and glutamine) 11 , and plant cells actively control osmolyte gradients (also using transmembrane ion-pumping proteins 12 ) to generate reversible movements. Indeed, the osmolyte transport across the cell boundary locally creates differences in concentration between the extracellular fluid (ECF) and the intracellular fluid (ICF), which translates into an osmotic pressure difference Π = Π ICF − Π ECF .…”

“…Indeed, the osmolyte transport across the cell boundary locally creates differences in concentration between the extracellular fluid (ECF) and the intracellular fluid (ICF), which translates into an osmotic pressure difference Π = Π ICF − Π ECF . Given the (hydrostatic) pressure difference P = p ICF− p ECF , the water flow rate (taken as positive towards the ICF) is then driven by Π − P (up to a scaling factor related to the osmotic barrier surface and permeability, and by neglecting correction factors accounting for osmolyte rejection) 10,11 , and the resulting turgor trend also depends on the elastic properties of the cell wall confining the volume variation 10 . Reversibility is then achieved by controlling osmolyte concentration in a cyclic fashion.…”