Breaking the cycle: how light, CO2 and O2 affect plant respiration

In 1953, Sir Hans Krebs won the Nobel Prize for his classic work elucidating the metabolic steps by which citrate is metabolized within the mitochondria and drives energy recovery from stored carbohydrates. Through an elegant series of reactions fed from a common substrate, the tricarboxylic acid cycle (TCA) creates carbon compounds of various sizes and configurations to support a multitude of metabolic reactions (Krebs 1936). Contemporaneously, physiologists like Bessel Kok, concentrating on photosynthetic metabolism, suggested an in vivo linkage between photosynthesis and respiration that was sensitive to environmental conditions, particularly light (Kok 1948). Many talented scientists from the fields of molecular biology, biochemistry, physiology, and ecology have continued to examine this linkage and the effect of light on it (Hurry et al. 2005). Significant progress has integrated and advanced our knowledge of the biochemical and physiological controls of respiratory metabolism, and now it is well established that even low levels of light can not only decrease respiratory CO2 release but can also cause the long-studied clockwise Krebs cycle to be decidedly non-cyclical (Fig. 1, ‘light’). On pages 2208–2220 of the December issue, Guillaume Tcherkez et al. (2012) use emerging technologies, developing theories and clever experimental manipulations to further advance our knowledge of the structure, function and control of respiratory metabolism in the light.The result is a clearer understanding of the tricarboxylic acid pathway (TCAP – not cycle!) and specifically the dynamic effects of atmospheric CO2 and O2 on respiratory metabolism. Changes in the atmospheric CO2 and/or O2 partial pressure are likely to influence respiratory metabolism during illumination in a variety of ways, though underlying functional controls of these effects are not yet clear. Elevated CO2 conditions can stimulate carboxylation and can decrease oxygenation of ribulose-1,5-bisphosphate (RuBP) in photosynthesis, altering the energy balance and efficiency of carbon fixation and the rate of triose-phosphate production (Sage, Sharkey & Seemann 1990). Kok’s observation of lower mitochondrial CO2 efflux in the light has often been interpreted as a decreased demand for respiratory products when photosynthesis could more directly supply ATP, reductants and reduced sugars. However, increased rates of carbon fixation in elevated CO2 environments have been shown to vary in their influence on the degree of light inhibition of respiration, with studies reporting decreases (Wang et al. 2001; Shapiro et al. 2004) or little effect (Sage et al. 1990; Ayub et al. 2011; Crous et al. 2012). While acknowledging previous interpretations of mechanistic controls on the light inhibition of respiration, Tcherkez et al. view the complexity of plant metabolism in the light under different gaseous environments as a ‘persisting conundrum’ and tackle this issue using an arsenal of techniques. Key to their work is the development of tools to quantitatively follow the flow of individual carbon atoms among the various pools of the TCAP. Such detailed tracing allows for modelling of the probability and kinetics of individual reactions and provides qualitative links to isotopic fluxomics (Tcherkez et al. 2009). The last decade has seen a strong theoretical advancement in our understanding of mitochondrial metabolism in illuminated photosynthetic cells (Hurry et al. 2005; NunesNesi, Sweetlove & Fernie 2007; Leakey et al. 2009). As light impacts the redox state of cells and organelles, the regulation of various enzyme systems leads the TCAP ‘cycle’ to become decidedly less cyclical, opening the sequence of reactions to provide parallel but linked metabolic pathways (Fig. 1). In the dark, Krebs’ classical clockwise view is maintained, and citrate metabolism fed from glycolysis creates carbon substrates, releases CO2 as various intermediates are oxidized and supplies reductant to drive the formation of ATP by the electron transport chain/oxidative phosphorylation. By contrast, in illuminated photosynthetic cells (right panel), TCAP activity is fed directly from stored citrate, bypassing the incorporation of acetyl-coenzyme A, and is used primarily to drive the formation of glutamine/ glutamate rather than participating in the full cycle. Moreover, triose phosphates from the Calvin cycle can feed the formation of phosphoenolpyruvate, which itself can be carboyxlated, and the resulting oxaloacetate can be then transformed into malate or fumarate in the ‘left-hand’ side of the opened cycle. Using a stable isotope pulse-chase experiment, Tcherkez et al. show that the rate of respiration in the light is unaffected by short-term (hours) manipulations of [CO2] and further conclude that CO2 evolution from the TCAP accounts for only 20% of the total decarboxylations. Correspondence: K. L. Griffin. E-mail: griff@ldeo.columbia.edu Plant, Cell and Environment (2012) doi: 10.1111/pce.12039 bs_bs_banner