The Operation of Two Decarboxylases, Transamination, and Partitioning of C4 Metabolic Processes between Mesophyll and Bundle Sheath Cells Allows Light Capture To Be Balanced for the Maize C4 Pathway

Abstract

The C 4 photosynthesis carbon-concentrating mechanism in maize (Zea mays) has two CO 2 delivery pathways to the bundle sheath (BS; via malate or aspartate), and rates of phosphoglyceric acid reduction, starch synthesis, and phosphoenolpyruvate regeneration also vary between BS and mesophyll (M) cells. The theoretical partitioning of ATP supply between M and BS cells was derived for these metabolic activities from simulated profiles of light penetration across a leaf, with a potential 3-fold difference in the fraction of ATP produced in the BS relative to M (from 0.29 to 0.96). A steady-state metabolic model was tested using varying light quality to differentially stimulate M or BS photosystems. CO 2 uptake, ATP production rate (J ATP ; derived with a low oxygen/chlorophyll fluorescence method), and carbon isotope discrimination were measured on plants under a low light intensity, which is considered to affect C 4 operating efficiency. The light quality treatments did not change the empirical ATP cost of gross CO 2 assimilation (J ATP /GA). Using the metabolic model, measured J ATP /GA was compared with the predicted ATP demand as metabolic functions were varied between M and BS. Transamination and the two decarboxylase systems (NADP-malic enzyme and phosphoenolpyruvate carboxykinase) were critical for matching ATP and reduced NADP demand in BS and M when light capture was varied under contrasting light qualities.

Introgression and repeated co-option facilitated the recurrent emergence of C4photosynthesis among close relatives

“…1983). The acquisition of pck‐1P1_LGT‐C , a gene already adapted for the C 4 context, probably added a PCK shuttle, which alters the stoichiometry of the pathway and the spatial distribution of its energy requirements, increasing its efficiency under some conditions (Bellasio and Griffiths 2014; Wang et al. 2014).…”

Acclimation of C4 metabolism to low light in mature maize leaves could limit energetic losses during progressive shading in a crop canopy

“…PEPCK was assumed to regenerate 20% of the PEP required by PEPC, which is close to the expected value under natural white light (Bellasio and Griffiths, 2014); the remainder was regenerated through PPDK. PEPC rate ( V P ), V C , and V O were calculated with the validated von Caemmerer C 4 model (Table 1), in the light-limited form (von Caemmerer, 2000; Bellasio and Griffiths, 2013).…”

“…We used the validated C 4 model (von Caemmerer, 2000), as recently integrated to describe the C 4 energetics (Bellasio and Griffiths, 2014). The biochemical processes considered are: 3-phosphoglyceric acid (PGA) reduction, starch synthesis, PEP regeneration, ribulose 1,5-bisphosphate (RuBP) regeneration, and glycolate recycling, while the PGA consumed by mitochondrial respiration is subtracted as likely to be consumed by basal metabolism (for derivation see Bellasio and Griffiths, 2014). ATP/ GA B was calculated as: ${\frac{ATP}{GA}}_{\text{B}}=3V_C+\frac{7}{2}{V}_O+\frac{A}{6}+PEPCK+2PPDK-\frac{1}{3}{R}_{LIGHT}$ …”

The Impacts of Fluctuating Light on Crop Performance

“…Before optimal pool sizes are established for a given light intensity, suboptimal CO 2 concentrations near Rubisco would increase rates of oxygenation, leading to increased photorespiration and, thus, incurring the double costs of C 4 carbon pumping and C 3 photorespiration (Fig. 3C;de Veau and Burris, 1989;von Caemmerer and Furbank, 2003;Sage and McKown, 2006;Bellasio and Griffiths, 2014b). The transport mechanisms returning C 3 acids into the mesophyll following decarboxylation in the bundle sheath cell are less clear.…”