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

Abstract

C4 plants have a biochemical carbon-concentrating mechanism that increases CO2 concentration around Rubisco in the bundle sheath. Under low light, the activity of the carbon-concentrating mechanism generally decreases, associated with an increase in leakiness (ϕ), the ratio of CO2 retrodiffusing from the bundle sheath relative to C4 carboxylation. This increase in ϕ had been theoretically associated with a decrease in biochemical operating efficiency (expressed as ATP cost of gross assimilation, ATP/GA) under low light and, because a proportion of canopy photosynthesis is carried out by shaded leaves, potential productivity losses at field scale. Maize plants were grown under light regimes representing the cycle that leaves undergo in the canopy, whereby younger leaves initially developed under high light and were then re-acclimated to low light (600 to 100 μE·m(-2)·s(-1) photosynthetically active radiation) for 3 weeks. Following re-acclimation, leaves reduced rates of light-respiration and reached a status of lower ϕ, effectively optimizing the limited ATP resources available under low photosynthetically active radiation. Direct estimates of respiration in the light, and ATP production rate, allowed an empirical estimate of ATP production rate relative to gross assimilation to be derived. These values were compared to modelled ATP/GA which was predicted using leakiness as the sole proxy for ATP/GA, and, using a novel comprehensive biochemical model, showing that irrespective of whether leaves are acclimated to very low or high light intensity, the biochemical efficiency of the C4 cycle does not decrease at low photosynthetically active radiation.

Keywords: Bundle sheath; PPFD.; efficiency; irradiance; isotopic discrimination; leakiness; low light; mesophyll; Δ 13C.

Fig. 1.

Maize responses to decreasing light intensities for plants grown under high light (HL), low light (LL) or LL following HL (HLLL). (A) Net assimilation (A). The curves were fitted to calculate the LCP (Table 2). The inset shows a magnification at the lowest PAR. (B) Total ATP production rate (J _ATP), measured with the low O₂-ETR method (see Materials and methods section on gas exchange measurements). (C) Online isotopic discrimination during photosynthesis (Δ). Error bars represent one SE (n = 6).

Fig. 2.

(A) Stomatal conductance and (B) C _i/C _a responses to decreasing light intensity, under different light qualities, for plants grown under high light (HL), low light (LL), or LL following HL (HLLL) measured by gas exchange. (C) Response of C _BS to decreasing light intensity, under different light qualities, estimated by the C₄ model. Error bars represent one SE (n = 6).

Fig. 3.

Leakiness (ϕ) resolved from online isotopic discrimination during photosynthesis (Δ) by means of a full isotopic discrimination model for HL plants (squares), LL plants (triangles), and HLLL plants (diamonds). Error bars represent one SE (n = 6).

Fig. 4.

Measured ATP cost of net assimilation (J _ATP/A) for HL plants (squares), LL plants (triangles), and HLLL plants (diamonds). Error bars represent one SE (n = 6).

Fig. 5.

ATP cost of gross assimilation, representing C₄ biochemical operating efficiency for HL plants (A), LL plants (B), and HLLL plants (C). The empirical values for J _ATP/GA (empty symbols) were compared to predicted values for ATP/GA (solid symbols) calculated with two different approaches. ATP/GA was calculated using ϕ as the sole proxy for operating efficiency (ϕ approach; solid squares) or using a comprehensive calculation summing the ATP cost of all processes contributing to assimilation (B approach; solid circles). Note that both calculations were based on the same dataset, presented in Figs 1–3 and Table 2. Error bars represent one SE; n = 6 plants per condition.