Temperature-induced Changes in Hill Activity of Chloroplasts Isolated from Chilling-sensitive and Chilling-resistant Plants

Abstract

The effect of temperature on Hill activity has been compared in chilling-sensitive and chilling-resistant plants. The Arrhenius activation energy (Ea) for the photorednction of 2,6-dichlorophenolindophenol by chloroplasts isolated from two chilling-sensitive plants, mung bean (Vigna radiata L. var. Mungo) and maize (Zea mays L. cv. PX 616), increased at low temperatures, below 17 C for mung bean and below 11 C for maize. However, the Ea for this reaction in pea ( (6, throughout 13). It has been reported that a fundamental difference in the response to these low temperatures exists between mitochondrial and other cellular membranes of chilling-sensitive plants and membranes of plants which are resistant to chilling temperatures (7,13,14). The Ea' of membrane-bound respiratory enzymes in mitochondria of chilling-sensitive plants increased below a critical chilling temperature, typically between 10 C to 15 C (7), and this change was correlated with a temperature-induced change in the molecular ordering of the mitochondrial lipids as detected with the aid of spin-labeled compounds (16). The membrane lipids of chloroplasts from chilling-sensitive plants also exhibited similar changes below the chilling temperature (14,15) and there was an increase in Ea for photoreduction of NADP+ although not of other Hill oxidants (18). Neither mitochondria nor chloroplasts isolated from chilling-resistant plants showed any of the temperature-dependent changes in membrane properties at temperatures close to or within the chilling-temperature range (7,13).Recently, we have investigated the effect of temperature on the Hill activity of chloroplasts isolated from barley (12). Although barley is a chilling-resistant plant, the Ea for photoreduc-I Abbreviations: DCIP: 2,6-dichlorophenolindophenol; Ea: Arrhenius activation energy. tion of either DCIP or ferricyanide increased at temperatures below 9 C. The change was reversible and additional changes in Ea took place at 20 and 29 C. Thus, there were at least four different values of Ea as the temperature was varied within the physiological temperature range for growth of barley. The alterations in Ea of Hill activity by the temperature became apparent only when a rate-limiting reaction in coupled barley chloroplasts was circumvented by the addition of uncouplers or by other means.Since the studies with barley indicated that changes in membrane properties and function induced by low temperatures were, at least for chloroplasts, not confined to chilling-sensitive plants, the effect of temperature on Hill activity was compared in two chilling-sensitive plants, mung bean and maize, and another chilling-resistant plant, pea. Chloroplasts isolated from all of these plants showed a distinct increase in the Ea for Hill activity at low temperatures, as well as another change in Ea at temperatures above 25 C. These results, together with those previously obtained with barley (12), showed that the Ea for Hill activity was not constant as the temperature was varied throughout the physiologi...

Effect of Temperature on Proton Efflux from Isolated Chloroplast Thylakoids

“…This temperature is close to that at which several electron transport activities showed a temperature-induced change in Ea when thylakoids from a different variety of barley were utilized (14). Table I (12,13). A change in Ea for electron transport by mung bean thylakoids occurs at approximately 12.9 C (Fig.…”

“…IC). This temperature is somewhat lower than that at which thylakoids from a different variety of mung bean showed a temperature-induced change in Ea of electron transport activity (13).…”

“…sitive plants (4,9,(12)(13)(14)21). Although the presence or absence of temperature-induced changes in mitochondrial membranes correlates with the chilling-sensitivity or resistance, respectively, of the plant species from which the mitochondria were isolated, the results obtained using chloroplast membranes do not show such a straightforward correlation.…”

“…Reaction rates were determined by measuring acidification of the reaction mixtures accompanying ferricyanide reduction. The uncoupler gramicidin D was included in the reaction mixtures as it has been shown previously that temperature-induced changes in electron transport are not observed at low temperatures in these plants when electron transport is rate-limited (12)(13)(14). Figure IA shows that a change in Ea of electron transport activity of barley thylakoids occurs at approximately 10.3 C. (The temperature cited for a temperature-induced change is an approximation and is the temperature midway between the two straightline segments.)…”

Thermal Behavior and Lipid Composition of Cauliflower Plasma Membranes in Relation to ATPase Activity and Chilling Sensitivity

“…Furthermore, some membrane-associated enzymes from chilling-resistant plants also exhibit nonlinear Arrhenius plots, e.g. the photoreduction of DCIP by chloroplasts from barley (17) and pea (18), assayed in the presence ofuncouplers. However, no phase separation (21) or change in lipid ordering (24) occurs in the membranes of these plants at temperatures coincident with the altered activation energies and such changes are more likely a direct effect of temperature on the uncoupler-enzyme-substrate complex.…”