The coordination of C4 photosynthesis and the CO2-concentrating mechanism in maize and Miscanthus x giganteus in response to transient changes in light quality

Abstract

Unequal absorption of photons between photosystems I and II, and between bundle-sheath and mesophyll cells, are likely to affect the efficiency of the CO2-concentrating mechanism in C4 plants. Under steady-state conditions, it is expected that the biochemical distribution of energy (ATP and NADPH) and photosynthetic metabolite concentrations will adjust to maintain the efficiency of C4 photosynthesis through the coordination of the C3 (Calvin-Benson-Bassham) and C4 (CO2 pump) cycles. However, under transient conditions, changes in light quality will likely alter the coordination of the C3 and C4 cycles, influencing rates of CO2 assimilation and decreasing the efficiency of the CO2-concentrating mechanism. To test these hypotheses, we measured leaf gas exchange, leaf discrimination, chlorophyll fluorescence, electrochromatic shift, photosynthetic metabolite pools, and chloroplast movement in maize (Zea mays) and Miscanthus × giganteus following transitional changes in light quality. In both species, the rate of net CO2 assimilation responded quickly to changes in light treatments, with lower rates of net CO2 assimilation under blue light compared with red, green, and blue light, red light, and green light. Under steady state, the efficiency of CO2-concentrating mechanisms was similar; however, transient changes affected the coordination of C3 and C4 cycles in M. giganteus but to a lesser extent in maize. The species differences in the ability to coordinate the activities of C3 and C4 cycles appear to be related to differences in the response of cyclic electron flux around photosystem I and potentially chloroplast rearrangement in response to changes in light quality.

Figure 1.

Transitional variation in A_net (µmol m⁻² s⁻¹; A and B), g_s (mol m⁻² s⁻¹; C and D), P_i/P_a (unitless; E and F), Δ¹³C (‰; G and H), and ϕ (I and J) in maize and M. giganteus with changes in light treatment in the light sequence RGB, blue, red, blue, green, blue, and RGB. The light intensity was set to 900 µmol quanta m⁻² s⁻¹ for all light treatments. The CO₂ partial pressure in the leaf chamber was maintained at 38.4 Pa, leaf temperature was 25°C, and relative humidity was between 50% and 70% for all light treatments. Data are reported as means ± se (n = 4).

Figure 2.

Δ¹³C (‰) as a function of P_i/P_a (unitless) for RGB (white circles), red (red circles), green (green circles), and blue (blue circles) light in maize (A) and M. giganteus (B). Solid lines were modeled (Eq. 7) with ϕ of 0.1, 0.2, and 0.3 from bottom to top. Arrows indicate the convergence of ϕ to a constant value in M. giganteus after switching from one light species to another. Data are reported as means ± se (n = 4).

Figure 3.

Modeled transitional variation in x (A and B), P_bs (Pa; C and D), and v_o/v_c (µmol m⁻² s⁻¹; E and F) in maize and M. giganteus with changes in light quality in the order RGB, blue, red, blue, green, blue, and RGB at an irradiance of 900 µmol quanta m⁻² s⁻¹. g_bs was estimated (0.0046 μmol m⁻² s⁻¹ Pa⁻¹ for maize and 0.01 μmol m⁻² s⁻¹ Pa⁻¹ for M. giganteus) using data obtained from the first 1 h of RGB measurements assuming x = 0.4. For the other light treatments, x was solved, assuming g_bs was constant, to minimize the least-square difference between modeled and measured Δ¹³C. The gray areas show the sensitivity of the modeled parameters assuming different values of g_bs (between 0.0069 and 0.0023 μmol m⁻² s⁻¹ Pa⁻¹ for maize and between 0.015 and 0.005 μmol m⁻² s⁻¹ Pa⁻¹ for M. giganteus).

Figure 4.

A_net (A and B) and ϕ (C and D) in response to variation in ϕ_PSII and v_H⁺/LEF under red light (red symbols) and blue light (blue symbols) at 900 µmol quanta m⁻² s⁻¹. Data are reported as means ± se (n = 4–8).

Figure 5.

Transitional variation in pools of the C₄ metabolites OAA (µmol m⁻²; A), pyruvate (µmol m⁻²; B), and PEP (µmol m⁻²; C) and the C₃ metabolites TP (µmol m⁻²; D), RuBP (µmol m⁻²; E), and PGA (µmol m⁻²; F) in maize and M. giganteus when light was switched in the sequence blue, red, and blue at a light intensity of 900 µmol quanta m⁻² s⁻¹. Data are reported as means ± se (n = 4).

Figure 6.

Transitional variation in the ratios of C₃ metabolites (TP + RuBP + PGA) over C₄ metabolites (OAA + PEP + pyruvate; A), TP over PGA (B), RuBP over PGA (C), and PEP over PGA (D) in maize (black circles) and M. giganteus (white circles) when light quality was switched in the sequence blue, red, and blue at a light intensity of 900 µmol quanta m⁻² s⁻¹. Data are reported as means ± se (n = 4).

Figure 7.

Transitional variation in ΔT in maize (black circles) and M. giganteus (white circles) when light treatment was switched in the sequence of RGB, blue, red, blue, and RGB. ΔT is defined as the difference between the initial averaged 5 min of transmittance of a given light quality and the transmittance at a given time point within the 60-min exposure. Data are reported as means ± se (n = 4 for maize; n = 3 for M. giganteus).