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The biochemical basis for thermoregulation in heat-producing flowers.

Umekawa Y, Seymour RS, Ito K - Sci Rep (2016)

Bottom Line: Here, we show that respiratory control in homeothermic spadices of skunk cabbage (Symplocarpus renifolius) is achieved by rate-determining biochemical reactions in which the overall thermodynamic activation energy exhibits a negative value.Moreover, NADPH production, catalyzed by mitochondrial isocitrate dehydrogenase in a chemically endothermic reaction, plays a role in the pre-equilibrium reaction.We propose that a law of chemical equilibrium known as Le Châtelier's principle governs the homeothermic control in skunk cabbage.

View Article: PubMed Central - PubMed

Affiliation: United Graduate School of Agricultural Science, Iwate University, 3-18-8 Ueda, Morioka, Iwate, 020-8550, Japan.

ABSTRACT
Thermoregulation (homeothermy) in animals involves a complex mechanism involving thermal receptors throughout the body and integration in the hypothalamus that controls shivering and non-shivering thermogenesis. The flowers of some ancient families of seed plants show a similar degree of physiological thermoregulation, but by a different mechanism. Here, we show that respiratory control in homeothermic spadices of skunk cabbage (Symplocarpus renifolius) is achieved by rate-determining biochemical reactions in which the overall thermodynamic activation energy exhibits a negative value. Moreover, NADPH production, catalyzed by mitochondrial isocitrate dehydrogenase in a chemically endothermic reaction, plays a role in the pre-equilibrium reaction. We propose that a law of chemical equilibrium known as Le Châtelier's principle governs the homeothermic control in skunk cabbage.

No MeSH data available.


Model of pre-equilibrium reaction in thermogenic spadices of skunk cabbage.The model comprises one leading equilibrium reaction (k1 and k1′) and one final step of oxygen consumption through mitochondrial terminal oxidases (AOX and COX) (k2). The activation energies of each chemical reaction are indicated as follows: an exothermic reaction with reaction constants k1 (RH2 → R + 2H+ + 2e−) and k2 (1/2 O2 + 2H+ + 2e− → H2O) are expressed as Ea and Ea″, respectively. An endothermic reaction with reaction constant k1′ (R + 2H+ + 2e− → RH2) is indicated as Ea′.
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f2: Model of pre-equilibrium reaction in thermogenic spadices of skunk cabbage.The model comprises one leading equilibrium reaction (k1 and k1′) and one final step of oxygen consumption through mitochondrial terminal oxidases (AOX and COX) (k2). The activation energies of each chemical reaction are indicated as follows: an exothermic reaction with reaction constants k1 (RH2 → R + 2H+ + 2e−) and k2 (1/2 O2 + 2H+ + 2e− → H2O) are expressed as Ea and Ea″, respectively. An endothermic reaction with reaction constant k1′ (R + 2H+ + 2e− → RH2) is indicated as Ea′.

Mentions: To test our hypothesis, we applied the modified Arrhenius model1213 to determine the overall activation energy (Eo) for respiration in an intact thermogenic spadix of skunk cabbage. First, we analysed respiration rates obtained through thermal clamping experiments in the field7, wherein a range of spadix temperatures were artificially enforced and respiration rate measured at equilibrium. Modified Arrhenius plots provided a better fit of the data than classical Arrhenius plots did (Fig. 1a and Supplementary Figs S1 and S2). Moreover, we could calculate the dynamic changes in Eo under various temperatures using the ‘switching temperature’ of 15 °C as the reference temperature (TREF) and other parameters of the model (Fig.1b and Supplementary Table S1). The Eo values of four independent spadices all decreased as the temperature increased, and there was an apparent intersection point around the switching temperature. Significantly, the Eo values in the respiration control range were negative, and rates of respiration decreased as temperature increased (Fig. 1b). There is empirical precedence in chemistry for negative activation energies, where an increase in temperature results in a decrease in chemical reaction rates. Examples include the propagation of anionic polymerization14 and tryptophan-based, bifunctional, thiourea-catalysed asymmetric Mannich reactions15. In contrast, we have found no reports of negative activation energy in biological systems, rather several papers report temperature-dependent changes of Eo in the range of positive values in plant respiration161718. Importantly, negative activation energy in chemistry implicates a complex chemical reaction containing pre-equilibrium reactions19. Namely, a fast reversible step comprises exothermic and endothermic reactions that precede formation of unstable intermediates, and the following rate-limiting reaction determines the entire reaction rate. We propose here that the negative activation energy in homeothermic skunk cabbage could be produced via biochemical pre-equilibrium reactions comprising reversible reactions catalysed by cellular dehydrogenases and a rate-determining reaction catalysed by the mitochondrial terminal oxidases AOX and COX (Fig. 2).


The biochemical basis for thermoregulation in heat-producing flowers.

Umekawa Y, Seymour RS, Ito K - Sci Rep (2016)

Model of pre-equilibrium reaction in thermogenic spadices of skunk cabbage.The model comprises one leading equilibrium reaction (k1 and k1′) and one final step of oxygen consumption through mitochondrial terminal oxidases (AOX and COX) (k2). The activation energies of each chemical reaction are indicated as follows: an exothermic reaction with reaction constants k1 (RH2 → R + 2H+ + 2e−) and k2 (1/2 O2 + 2H+ + 2e− → H2O) are expressed as Ea and Ea″, respectively. An endothermic reaction with reaction constant k1′ (R + 2H+ + 2e− → RH2) is indicated as Ea′.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4837406&req=5

f2: Model of pre-equilibrium reaction in thermogenic spadices of skunk cabbage.The model comprises one leading equilibrium reaction (k1 and k1′) and one final step of oxygen consumption through mitochondrial terminal oxidases (AOX and COX) (k2). The activation energies of each chemical reaction are indicated as follows: an exothermic reaction with reaction constants k1 (RH2 → R + 2H+ + 2e−) and k2 (1/2 O2 + 2H+ + 2e− → H2O) are expressed as Ea and Ea″, respectively. An endothermic reaction with reaction constant k1′ (R + 2H+ + 2e− → RH2) is indicated as Ea′.
Mentions: To test our hypothesis, we applied the modified Arrhenius model1213 to determine the overall activation energy (Eo) for respiration in an intact thermogenic spadix of skunk cabbage. First, we analysed respiration rates obtained through thermal clamping experiments in the field7, wherein a range of spadix temperatures were artificially enforced and respiration rate measured at equilibrium. Modified Arrhenius plots provided a better fit of the data than classical Arrhenius plots did (Fig. 1a and Supplementary Figs S1 and S2). Moreover, we could calculate the dynamic changes in Eo under various temperatures using the ‘switching temperature’ of 15 °C as the reference temperature (TREF) and other parameters of the model (Fig.1b and Supplementary Table S1). The Eo values of four independent spadices all decreased as the temperature increased, and there was an apparent intersection point around the switching temperature. Significantly, the Eo values in the respiration control range were negative, and rates of respiration decreased as temperature increased (Fig. 1b). There is empirical precedence in chemistry for negative activation energies, where an increase in temperature results in a decrease in chemical reaction rates. Examples include the propagation of anionic polymerization14 and tryptophan-based, bifunctional, thiourea-catalysed asymmetric Mannich reactions15. In contrast, we have found no reports of negative activation energy in biological systems, rather several papers report temperature-dependent changes of Eo in the range of positive values in plant respiration161718. Importantly, negative activation energy in chemistry implicates a complex chemical reaction containing pre-equilibrium reactions19. Namely, a fast reversible step comprises exothermic and endothermic reactions that precede formation of unstable intermediates, and the following rate-limiting reaction determines the entire reaction rate. We propose here that the negative activation energy in homeothermic skunk cabbage could be produced via biochemical pre-equilibrium reactions comprising reversible reactions catalysed by cellular dehydrogenases and a rate-determining reaction catalysed by the mitochondrial terminal oxidases AOX and COX (Fig. 2).

Bottom Line: Here, we show that respiratory control in homeothermic spadices of skunk cabbage (Symplocarpus renifolius) is achieved by rate-determining biochemical reactions in which the overall thermodynamic activation energy exhibits a negative value.Moreover, NADPH production, catalyzed by mitochondrial isocitrate dehydrogenase in a chemically endothermic reaction, plays a role in the pre-equilibrium reaction.We propose that a law of chemical equilibrium known as Le Châtelier's principle governs the homeothermic control in skunk cabbage.

View Article: PubMed Central - PubMed

Affiliation: United Graduate School of Agricultural Science, Iwate University, 3-18-8 Ueda, Morioka, Iwate, 020-8550, Japan.

ABSTRACT
Thermoregulation (homeothermy) in animals involves a complex mechanism involving thermal receptors throughout the body and integration in the hypothalamus that controls shivering and non-shivering thermogenesis. The flowers of some ancient families of seed plants show a similar degree of physiological thermoregulation, but by a different mechanism. Here, we show that respiratory control in homeothermic spadices of skunk cabbage (Symplocarpus renifolius) is achieved by rate-determining biochemical reactions in which the overall thermodynamic activation energy exhibits a negative value. Moreover, NADPH production, catalyzed by mitochondrial isocitrate dehydrogenase in a chemically endothermic reaction, plays a role in the pre-equilibrium reaction. We propose that a law of chemical equilibrium known as Le Châtelier's principle governs the homeothermic control in skunk cabbage.

No MeSH data available.