Respiratory metabolism of illuminated leaves depends on CO ₂ and O ₂ conditions

Abstract

Day respiration is the process by which nonphotorespiratory CO2 is produced by illuminated leaves. The biological function of day respiratory metabolism is a major conundrum of plant photosynthesis research: because the rate of CO2 evolution is partly inhibited in the light, it is viewed as either detrimental to plant carbon balance or necessary for photosynthesis operation (e.g., in providing cytoplasmic ATP for sucrose synthesis). Systematic variations in the rate of day respiration under contrasting environmental conditions have been used to elucidate the metabolic rationale of respiration in the light. Using isotopic techniques, we show that both glycolysis and the tricarboxylic acid cycle activities are inversely related to the ambient CO2/O2 ratio: day respiratory metabolism is enhanced under high photorespiratory (low CO2) conditions. Such a relationship also correlates with the dihydroxyacetone phosphate/Glc-6-P ratio, suggesting that photosynthetic products exert a control on day respiration. Thus, day respiration is normally inhibited by phosphoryl (ATP/ADP) and reductive (NADH/NAD) poise but is up-regulated by photorespiration. Such an effect may be related to the need for NH2 transfers during the recovery of photorespiratory cycle intermediates.isotope ͉ photosynthesis ͉ regulation ͉ respiration ͉ photorespiration I t has been 70 years since Krebs and Johnson (1, 2) proposed the mechanism by which pyruvic acid is oxidized to CO 2 , which is now called the ''Krebs cycle'' or tricarboxylic acid (TCA) cycle. Whereas the basics of the metabolic reactions involved in leaf respiration are known, intense efforts are still currently devoted to elucidating the regulation of the TCA cycle (and, more generally, of day respiration) in illuminated leaves (for a recent review, see ref.3).Leaf day respiration (nonphotorespiratory CO 2 evolution in the light) is an essential metabolic pathway that accompanies photosynthetic CO 2 assimilation and photorespiration. It is widely accepted that leaf respiration is partly inhibited in the light when compared with darkness (4). This acceptance is based on several strong lines of evidence, ranging from gas-exchange to molecular studies (for a review, see ref. 4): (i) the inhibition is thought to cause the light-enhanced dark respiration (5); (ii) the pyruvate dehydrogenase (PDH) is down-regulated in the light (6, 7); (iii) the metabolic flux through the TCA cycle in the light is reduced in both extracted mitochondria (8) and intact leaves (9, 10); (iv) mitochondria experience high ATP/ADP and NADH/NAD ϩ ratios in the light that inhibit NAD-dependent isocitrate dehydrogenase (11); and (v) carbohydrate molecules such as sucrose (Suc) and glucose (Glc) are prevented from entering glycolysis (9), because of a modification of phosphofructokinase activity by the allosteric effector fructose (Fru)-2,6-bisphosphate (12). Nevertheless, not all leaf cells are photosynthetic (e.g., most epidermal cells, phloem, and xylem) so that some ''heterotrophic'' background respiration in the li...

Measurement of Gross Photosynthesis, Respiration in the Light, and Mesophyll Conductance Using H218O Labeling

“…We found that, at 21% O 2 , respiration was light-inhibited (based on the non-linearity in the 335 light response curve of A net ), as has been commonly found in other experiments (Atkin et al 336 2005;Tcherkez et al 2008;Heskel et al 2013). However, at 2% O 2 , light did not inhibit 337 mitochondrial respiration (i.e.…”

“…Oryza sativa, Ishii and Murata (1978) Tcherkez et al (2008) found that the inhibition of respiration in the light 356 is independent of the CO 2 /O 2 ratio but that under low O 2 conditions, the degree of inhibition may 357 diminish. More recently, suggested that most of the Kok effect could 358 be explained by a variation in C c under limiting irradiances.…”

The Effect of Leaf-Level Spatial Variability in Photosynthetic Capacity on Biochemical Parameter Estimates Using the Farquhar Model: A Theoretical Analysis

“…There is currently no literature on the within-leaf variability of TPU; V TPU has always been considered as a whole-leaf parameter. Effects of variation in R d were not considered in this study outside the light acclimation simulations, but recent studies have suggested that R d could vary within leaves in a manner coupled to the photosynthetic capacity (Tcherkez et al, 2008).…”

Day and night respiration of three tree species in a temperate forest of northeastern China

“…Kirschbaum & Farquhar (1987) showed that RL measured by the Kok method is underestimated because it is assumes that the Ci values remain constant with changing PPFD. However, it has been shown that when PPFD decreases, stomatal closure is altered in response to environmental changes (Tcherkez et al 2008), and Ci gradually increases because of the decreased stomatal conductance. Consequently, a fraction of the respired CO2 is not promptly released and remains involved in the photosynthesis process.…”