Effects of Temperature on H + Uptake And Release During Circadian Rhythmic Movements of Excised Samanea Motor Organs

Abstract

A previous study revealed that Samanea saman leaflets open more completely and close less completely as temperature is increased. We now demonstrate that, as temperature is increased, extensor cells release more HI during their swelling phase (opening), but flexor motor cells release less HI during their swelling phase (closure). Leaflets of Samanea saman open and close with a circadian rhythm during a prolonged dark period. These movements are due to the rhythmic expansion and shrinkage of cortical cells in the motor organ (pulvinus), in turn dependent upon circadian rhythms in ion fluxes (mainly K + and Cl-) accompanied by water fluxes. Cells in the extensor region of the pulvinus take up K+, Cl-, and water during leaflet opening and lose both ions and water during closure, while cells in the opposing (flexor) region behave in the reverse manner (7). Rhythmic leaflet opening is promoted by an increase in temperature , while rhythmic leaflet closure is promoted by a decrease in temperature (7). These effects were originally interpreted in terms of a 'tension/relaxation' hypothesis, i.e. the 'open' phase requires metabolic energy generation but the 'closed' phase does not (5-7). However, it is difficult to reconcile this interpretation with data indicating that K+ and Cl-accumulate in flexor cells during closure (7), since the accumulation of K + and Cl-utilizes metabolic energy, directly or indirectly. Even if K+ enters motor cells passively, for example by diffusion through a channel in the plasma membrane, energy would be required to establish an electrochemical gradient that favors inward diffusion. We recently reported rhythmic changes in H + fluxes from excised motor tissue (3) and suggested that rhythmic changes in the proton-motive force established by the H + pump may energize rhythms in the uptake of K + and Cl-. This 'chemiosmotic' hypothesis predicts that the effect of temperature on leaflet movement is mediated by the effect of temperature on the proton motive force. It acknowledges that metabolic energy is utilized during both opening and closure, in contrast to predictions of a tension/relaxation hypothesis. We now describe effects of temperature on H + fluxes in excised extensor and flexor tissue during rhythmic leaflet opening I Supported by National Science Foundation grant DMB 83-04613 to R. L. S. and closure. Our data are consistent with a chemiosmotic explanation for rhythmic leaflet movement.