Regulation of thermogenesis in flowering Araceae: The role of the alternative oxidase

Abstract

The inflorescences of several members of the Arum lily family warm up during flowering and are able to maintain their temperature at a constant level, relatively independent of the ambient temperature. The heat is generated via a mitochondrial respiratory pathway that is distinct from the cytochrome chain and involves a cyanide-resistant alternative oxidase (AOX). In this paper we have used flux control analysis to investigate the influence of temperature on the rate of respiration through both cytochrome and alternative oxidases in mitochondria isolated from the appendices of intact thermogenic Arum maculatum inflorescences. Results are presented which indicate that at low temperatures, the dehydrogenases are almost in full control of respiration but as the temperature increases flux control shifts to the AOX. On the basis of these results a simple model of thermoregulation is presented that is applicable to all species of thermogenic plants. The model takes into account the temperature characteristics of the separate components of the plant mitochondrial respiratory chain and the control of each process. We propose that 1) in all aroid flowers AOX assumes almost complete control over respiration, 2) the temperature profile of AOX explains the reversed relationship between ambient temperature and respiration in thermoregulating Arum flowers, 3) the thermoregulation process is the same in all species and 4) variations in inflorescence temperatures can easily be explained by variations in AOX protein concentrations.

Identification of a Gene for Pyruvate-Insensitive Mitochondrial Alternative Oxidase Expressed in the Thermogenic Appendices in Arum maculatum

“…The extent to which other organic acids, such as succinate, are able to stimulate AmAOX1e and SgAOX remains to be investigated. However, it would be tempting to speculate that homoeothermic plants such as skunk cabbage and sacred lotus utilize their metabolites for fine control of the AOX-mediated oxygen consumption and also that the metabolic pathways that regulate the mitochondrial pool of pyruvate or succinate may play an important role in thermoregulation in these plants, whereas in A. maculatum and S. guttatum, the expression levels of pyruvate-insensitive AOX protein per se regulate their thermogenic activities, as proposed previously (Wagner et al, 2008). Alternatively, because pyruvate has been shown recently to stabilize the active conformation of purified AOX, which supports an exclusive effect of pyruvate on the enzyme's apparent V max in the mitochondria of A. maculatum (Carré et al, 2011), cellular metabolites including pyruvate may have a more general role to protect and/or stabilize the active conformation of AOX protein.…”

“…In contrast to the cytochrome c oxidase, AOX does not pump protons (Moore et al, 1978), and this allows the dramatic drop in free energy between ubiquinol and oxygen to be dissipated as heat (Vanlerberghe and McIntosh, 1997;Albury et al, 2009). Electron paramagnetic resonance studies have shown that the AOX active site comprises a binuclear iron center (Berthold et al, 2002;Moore et al, 2008), and persuasive Fourier transform infrared analysis has further indicated that the AOX belongs to the class of membrane-bound diiron carboxylate proteins (Berthold et al, 2002;Berthold and Stenmark, 2003;Maréchal et al, 2009).…”

Metabolic Control of Redox and Redox Control of Metabolism in Plants

“…As mentioned earlier, this protein, similar to the UCP, provides a means to relax the coupling between respiration and ATP production and it appears to be particularly important under stress (359). A small number of thermogenic plants use AOX in order to generate heat from respiration (228,370,377); however, given the limited range of plants possessing this capacity, the function of AOX should differ from this in most species. Specific AOX gene family members are strongly induced at the transcript and protein level by complex III or complex IV dysfunction (167,361), suggesting that AOX expression is highly responsive to insufficient cytochrome pathway capacity downstream of the ubiquinone pool.…”

In the heat of the night – alternative pathway respiration drives thermogenesis in Philodendron bipinnatifidum

“…Importantly, transcript abundance is not necessarily correlated with protein abundance or enzyme activity, and expression of AOX and pUCP in nonthermogenic and thermogenic tissues of P. bipinnatifidum has not been investigated. Coexpression of both pUCP and AOX proteins has been reported in thermogenic tissues of some other aroids, suggesting the possibility that both may play a role in thermogenesis (Onda et al, 2008;Wagner et al, 2008).…”

“…Araceae; Lance, 1974). The Araceae contains more thermogenic species than any other family (Meeuse, 1975;Meeuse & Raskin, 1988;Gibernau et al, 2005), and has attracted much attention from researchers aiming to understand heating mechanisms (Wagner et al, 1998(Wagner et al, , 2008Ito et al, 2003a,b;Crichton et al, 2005;Ito & Seymour, 2005;Onda et al, 2008), or to characterize the ecological significance of thermogenesis in plant-pollinator interactions (Gottsberger, 1999;Gibernau & Barabé, 2002). Among thermogenic arums, the capacity for heat generation differs markedly, from approx.…”