Can the progressive increase of C₄ bundle sheath leakiness at low PFD be explained by incomplete suppression of photorespiration?

Abstract

The ability to concentrate CO2 around Rubisco allows C4 crops to suppress photorespiration. However, as phosphoenolpyruvate regeneration requires ATP, the energetic efficiency of the C4 pathway at low photosynthetic flux densities (PFD) becomes a balancing act between primary fixation and concentration of CO2 in mesophyll (M) cells, and CO2 reduction in bundle sheath (BS) cells. At low PFD, retro-diffusion of CO2 from BS cells, relative to the rate of bicarbonate fixation in M cells (termed leakiness f), is known to increase. This paper investigates whether this increase in j could be explained by incomplete inhibition of photorespiration.The PFD response of f was measured at various O2 partial pressures in young Zea mays plants grown at 250 (LL) and 750 mmol m -2 s -1 PFD (HL). f increased at low PFD and was positively correlated with O2 partial pressure. Low PFD during growth caused BS conductance and interveinal distance to be lower in the LL plants, compared to the HL plants, which correlated with lower f. Model analysis showed that incomplete inhibition of photorespiration, especially in the HL plants, and an increase in the relative contribution of mitochondrial respiration at low PFD could explain the observed increases in f.

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

“…Similar conclusions were highlighted by Ubierna et al (2013). This observation is consistent with V P /V C (for Rubisco carboxylation rate) and the optimal x being largely independent of light intensity (von Caemmerer, 2000;Kromdijk et al, 2010), indicating a constant degree of engagement of the CCM even under an apparent F increase. Therefore, care should be taken when the ATP cost (and quantum yield) of C 4 photosynthesis is derived from F, measured either at the leaf or canopy scale, particularly in the vicinity of the light compensation point (Furbank et al, 1990;von Caemmerer, 2000;Tazoe et al, 2008).…”

“…The irradiance of 125 mE m 22 s 21 , characteristic of illumination in the shade, was chosen because ongoing studies on low light and light quality are relevant to the physiology of shading (see "Discussion"). Furthermore, since low light provides a means to directly manipulate C 4 metabolism, a great deal of comparable work has been undertaken both in this laboratory (Kromdijk et al, 2008(Kromdijk et al, , 2010Bellasio and Griffiths, 2013) and by other investigators (Ubierna et al, 2011(Ubierna et al, , 2013 under low irradiances. Reaction rates, shown in the boxes within Figure 1, were obtained by parameterizing the model with the data obtained during the experiment and with the output of the C 4 model (all equations are reported in Supplemental Table S1; see also Bellasio and Griffiths [2013] and refs.…”

“…Shade light has a reduced intensity (typically one-twentieth of full sunlight; Shirley, 1929) and differs in spectral quality from red-rich sunlight: diffuse sky radiation is enriched in blue, whereas canopy-filtered light is enriched in green (Smith, 1982). Under low-light conditions, it has been shown that F may increase both at the leaf (Kromdijk et al, 2010;Bellasio and Griffiths, 2013) and canopy (Kromdijk et al, 2008) levels. Theoretical considerations have associated this F increase with decreased C 4 efficiency and a potential loss of photosynthetic carbon uptake (Furbank et al, 1990;von Caemmerer, 2000;Kromdijk et al, 2008;Tazoe et al, 2008).…”

“…Theoretical considerations have associated this F increase with decreased C 4 efficiency and a potential loss of photosynthetic carbon uptake (Furbank et al, 1990;von Caemmerer, 2000;Kromdijk et al, 2008;Tazoe et al, 2008). Although other studies have compared the effect of light quality on F under low irradiance or under different light qualities (Kromdijk et al, 2010;Sun et al, 2012;Bellasio and Griffiths, 2013;Ubierna et al, 2013), the novelty of the approach presented here has been to couple the measured and predicted ATP supply during assimilation under these conditions. In this experiment, which was specifically optimized to acquire data under low light (Bellasio and Griffiths, 2013), we showed that the total ATP cost of gross assimilation was not significantly influenced by light intensity and underwent a little variation under different light quality (Fig.…”

“…Leakiness (F), the amount of CO 2 retrodiffusing relative to phosphoenolpyruvate (PEP) carboxylation rate, is therefore a proxy for the coordination between the CCM and assimilatory activity (Henderson et al, 1992;Tazoe et al, 2008;Kromdijk et al, 2010;Ubierna et al, 2011;Bellasio and Griffiths, 2013).…”