, Volume 202, Issue 3, pp 324-335

The function of water channels in Chara: The temperature dependence of water and solute flows provides evidence for composite membrane transport and for a slippage of small organic solutes across water channels

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Using the cell pressure probe, the effects of temperature on hydraulic conductivity (Lp; osmotic water permeability), solute permeability (permeability coefficient, Ps), and reflection coefficients (σs) were measured on internodes of Chara corallina, Klein ex Willd., em R.D.W.. For the first time, complete sets of transport coefficients were obtained in the range between 10 and 35 °C which provided evidence about pathways of water and solutes as they move across the plasma membrane (water channel and bilayer arrays). Test solutes used to check for the selectivity of water channels were monohydric alcohols of different molecular size and shape (ethanol, n-propanol, iso-propanol, and tert-butanol) and heavy water (HDO). Within the limits of accuracy, Q10 values for Lp and for the diffusive water permeability (Pd) were identical (Q10 for Lp = 1.29 ± 0.17 (± SD; n = 15 cells) and Q10 for Pd = 1.25 ± 0.16 (n = 5 cells)). The Q10 values were equivalent to activation energies of Ea = 16.8 ± 6.4 and 16.6 ± 10.0 kJ · mol−1, respectively, which is similar to that of self-diffusion or of viscous flow of water. The Q10 values and activation energies for Ps of the alcohols were significantly larger (ethanol: Q10 = 1.68 ± 0.16, Ea = 37.1 ± 5.9 kJ · mol−1; n-propanol: Q10 =  1.75 ± 0.40, Ea = 43.1 ± 15.3 kJ · mol−1; iso-propanol: Q10 = 2.12 ± 0.42, Ea =  52.2 ± 14.6 kJ · mol−1; tert-butanol: Q10 = 2.13 ± 0.56, Ea = 51.6 ± 17.1 kJ · mol−1; ±SD; n = 5 to 6 cells). Effects of temperature on reflection coefficients were most pronounced. With increasing temperature, σs values of the alcohols decreased and those of HDO increased. The data indicate that water and solutes use different pathways when crossing the membrane. Ordinary and isotopic water use water channels and the other test solutes use the bilayer array (composite transport model of membrane). Changes in σs values with temperature were found to be a sensitive measure for the open/closed state of water channels. The decrease of σs with temperature was theoretically predicted from the temperature dependence of Ps and Lp. Differences between predicted and measured values of σs allowed estimation of the bypass flow (slippage) of solutes through water channels which did not completely exclude test solutes. The permeability of channels depended on the structure and size of test solutes. It is concluded that water channels are much less selective than is usually thought. Since water channels represent single-file or no-pass pores, solutes drag along considerable amounts of water as they diffuse across channels. This results in low overall values of σs. The σs of HDO was extremely low. Its response to temperature was opposite to that for the σs of the alcohols. This suggested a stronger effect of temperature on the hydraulic (osmotic) than on the diffusive water flow across individual water channels, i.e. a differential sensitivity of different mechanisms to temperature.

Received: 10 October 1996 / Accepted: 2 December 1996