Abstract
The enhanced CO2 release of illuminated leaves transferred into darkness, termed “light enhanced dark respiration (LEDR)”, is often associated with an increase in the carbon isotope ratio of the respired CO2 (δ13CLEDR). The latter has been hypothesized to result from different respiratory substrates and decarboxylation reactions in various metabolic pathways, which are poorly understood so far. To provide a better insight into the underlying metabolic processes of δ13CLEDR, we fed position-specific 13C-labeled malate and pyruvate via the xylem stream to leaves of species with high and low δ13CLEDR values (Halimium halimifolium and Oxalis triangularis, respectively). During respective label application, we determined label-derived leaf 13CO2 respiration using laser spectroscopy and the 13C allocation to metabolic fractions during light–dark transitions. Our results clearly show that both carboxyl groups (C-1 and C-4 position) of malate similarly influence respiration and metabolic fractions in both species, indicating possible isotope randomization of the carboxyl groups of malate by the fumarase reaction. While C-2 position of pyruvate was only weakly respired, the species-specific difference in natural δ13CLEDR patterns were best reflected by the 13CO2 respiration patterns of the C-1 position of pyruvate. Furthermore, 13C label from malate and pyruvate were mainly allocated to amino and organic acid fractions in both species and only little to sugar and lipid fractions. In summary, our results suggest that respiration of both carboxyl groups of malate (via fumarase) by tricarboxylic acid cycle reactions or by NAD-malic enzyme influences δ13CLEDR. The latter supplies the pyruvate dehydrogenase reaction, which in turn determines natural δ13CLEDR pattern by releasing the C-1 position of pyruvate.
Highlights
Transferring light-acclimated leaves into darkness lead to rapid changes in various metabolic processes, causing halt of any photosynthetic activity and increased respiration rates (FlorezSarasa et al, 2012; Griffin and Turnbull, 2012)
To identify the respiratory substrates and enzymatic reactions, determining the species-specific differences in δ13CLEDR at natural isotope abundances in H. halimifolium and in O. triangularis, we fed those plants with different 13C-labeled malate and pyruvate substrates, expecting position- and species-specific differences in 13CO2 respiration during light–dark transitions
13CO2 respiration rates (RLabel) from 13C-1 and 13C-4 malate were low in the light, but steeply increased shortly after darkening during light enhanced dark respiration (LEDR), with a peak of about 0.02 μmol 13CO2 m−2 s−1 (Figures 1 and 2)
Summary
Transferring light-acclimated leaves into darkness lead to rapid changes in various metabolic processes, causing halt of any photosynthetic activity and increased respiration rates (FlorezSarasa et al, 2012; Griffin and Turnbull, 2012) During such light– dark transitions, leaves show enhanced O2 consumption (Stone and Ganf, 1981; Azcon-Bieto et al, 1983) concurrently with enhanced CO2 release (Hill and Bryce, 1992; Atkin et al, 1998). During LEDR the carbon isotope ratio of leaf-respired CO2 (δ13CLEDR) is changing, showing a strong initial increase which is followed by a progressive decrease (Werner et al, 2009; Wegener et al, 2010; Lehmann et al, 2016). The interpretation of this data is still difficult, since its respiratory substrates and associated enzymatic reactions are not fully understood so far (Werner and Gessler, 2011; Ghashghaie and Badeck, 2014)
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