Heat generation and dissipation in plants: can the alternative oxidative phosphorylation pathway serve a thermoregulatory role in plant tissues other than specialized organs?

Abstract

A number of hypothetical physiological roles have been proposed for the cyanide-insensitive alternative pathway in plants (Palmer, 1976; Laties, 1982; Meeuse, 1984; Purvis and Shewfelt, 1994; Wagner and Krab, 1995). The calorimetric observations of Raskin and co-workers (Ordentlich et al., 1991; Nevo et al., 1992; Moynihan et al., 1995) are significant contributions showing an interesting metabolic, chilling-induced response of the alternative pathway activity and differences in the low-temperature response among species adapted to different climates. Since different oxidative pathways do not have large differences in enthalpy, and observed heat rate increases are insufficient to cause significant temperature increases of physiological importance in nonthermogenic plants, other explanations must be developed for the relationship between the partitioning of electron flow and physiological conditions such as low temperature. The induction and engagement of the alternative respiratory pathway is involved in metabolic stasis, maintaining proper balance between carbon flow, ATP-ADP ratio, and electron flow during fluctuating or extreme temperature conditions. The alternative oxidase is engaged when ATP requirements are adequately met, as discussed by Palmer (1976), Meeuse (1983), Lambers (1985), and Wagner and Krab (1995). The expression and kinetic activity of the alternative oxidase are regulated by concentrations of key metabolites (Day and Wiskich, 1995; Siedow and Umbach, 1995; Wagner and Krab, 1995; Day et al., 1996). Dynamic partitioning of electron flow between Cyt oxidase and the alternative oxidase depends on the kinetic behavior of the two oxidases and the substrate dehydrogenases (Day and Wiskich, 1995; Siedow and Umbach, 1995; Wagner and Krab, 1995; Day et al., 1996). Furthermore, Moynihan et al. (1995) found that Episces cupreata Hook, adapted to the tropics, has very little alternative oxidase activity compared with wheat (Nevo et al., 1992), adapted to a large range of temperature climates. This results is consistent with the general relation between the apparent alternative oxidase activity and the climate of origin of the species.

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