Gating of aquaporins by low temperature in roots of chilling-sensitive cucumber and chilling-tolerant figleaf gourd

Abstract

Effects of low temperature (8°C) on the hydraulic conductivity of young roots of a chilling-sensitive (cucumber, Cucumis sativus L.) and a chilling-resistant (figleaf gourd, Cucurbita ficifolia Bouché) crop have been measured at the levels of whole root systems (root hydraulic conductivity, Lpr) and of individual cortical cells (cell hydraulic conductivity, Lp). Exposure of roots to low temperature (LRT) for up to 6 d caused a stronger suberization of the endodermis in cucumber compared with figleaf gourd, but no development of exodermal Casparian bands in either species. Changes in anatomy after 6 d of LRT treatment corresponded with a reduction in hydrostatic root Lpr of cucumber roots by a factor of 24, and by a factor of 2 in figleaf gourd. In figleaf gourd, there was a reduction only in hydrostatic Lpr but not in osmotic Lpr suggesting that the activity of water channels was not much affected by LRT treatment in this species. Changes in cell Lp in response to chilling and recovery were similar to the root levels, although they were more intense at the root level. Activation energies (E a) and Q10 of water flow as measured at the cell level were high in cucumber (Ea=109±13 KJ mol-1; Q 10=4.8±0.7; n=6-10 cells), but small in figleaf gourd (E a=11±2 KJ mol-1; Q10=1.2±0.1; n=6-10 cells). Roots of figleaf gourd recovered better from LRT treatment than those of cucumber. In figleaf gourd, recovery (at both the root and cell level) often resulted in Lp and Lpr values which were even bigger than the original, i.e. there was an overshoot in hydraulic conductivity. These effects were larger for osmotic (representing the cell-to-cell passage of water) than for hydrostatic Lpr. After a short-term (1 d) exposure to 8°C followed by 1 d at 20°C, hydrostatic Lpr of cucumber nearly recovered and that of figleaf gourd still remained higher due to the overshoot. By contrast, osmotic Lpr and cell Lp in both species remained high by a factor of 3 compared with the control, possibly due to an increased activity of water channels. After preconditioning of roots at LRT, increased hydraulic conductivity was completely inhibited by HgCl2 at both the root and cell levels. Different from figleaf gourd, recovery from chilling was not complete in cucumber after longer exposure to LRT. It is concluded that at LRT, both changes in the activity of aquaporins (AQPs) and alterations of root anatomy determine the water uptake in both species. The high temperature dependence of cell Lp in cucumber suggests conformational changes of AQPs during LRT treatment which result in channel closure and in a strong gating of AQP activity by low temperature. This mechanism is thought to be different from that in figleaf gourd where AQPs reacted in the conventional way, i.e. low temperature affected the mobility of water molecules in AQPs rather than their open/closed state, and Q10 was low. © The Author [2005]. Published by Oxford University Press [on behalf of the Society for Experimental Biology]. All rights reserved.