The role of chloroplast movement in C4 photosynthesis: a theoretical analysis using a three-dimensional reaction-diffusion model for maize

Abstract

Chloroplasts movement within mesophyll cells in C4 plants is hypothesized to enhance the CO2 concentrating mechanism, but this is difficult to verify experimentally. A three-dimensional (3D) leaf model can help analyse how chloroplast movement influences the operation of the CO2 concentrating mechanism. The first volumetric reaction-diffusion model of C4 photosynthesis that incorporates detailed 3D leaf anatomy, light propagation, ATP and NADPH production, and CO2, O2 and bicarbonate concentration driven by diffusional and assimilation/emission processes was developed. It was implemented for maize leaves to simulate various chloroplast movement scenarios within mesophyll cells: the movement of all mesophyll chloroplasts towards bundle sheath cells (aggregative movement) and movement of only those of interveinal mesophyll cells towards bundle sheath cells (avoidance movement). Light absorbed by bundle sheath chloroplasts relative to mesophyll chloroplasts increased in both cases. Avoidance movement decreased light absorption by mesophyll chloroplasts considerably. Consequently, total ATP and NADPH production and net photosynthetic rate increased for aggregative movement and decreased for avoidance movement compared with the default case of no chloroplast movement at high light intensities. Leakiness increased in both chloroplast movement scenarios due to the imbalance in energy production and demand in mesophyll and bundle sheath cells. These results suggest the need to design strategies for coordinated increases in electron transport and Rubisco activities for an efficient CO2 concentrating mechanism at very high light intensities.

Keywords: 3D leaf anatomy; Biophysical model; CO2 concentrating mechanism; chloroplast movement; gas exchange; leakiness; ray tracing.

Fig. 1.

Three-dimensional leaf anatomy of a maize leaf and the various chloroplast arrangements. The geometries were obtained for the epidermis (Epi), chloroplasts of mesophyll (Mchl) and bundle sheath (BSchl) cells, vacuole (Vac), vascular bundle (Vas), and cytosol (Cyt). (A–C) Default geometry (A), aggregative movement of mesophyll chloroplasts (B), and geometry for avoidance movement (C). (D–F) Light absorbance for the default geometry (D), aggregative movement of mesophyll chloroplasts (E), and avoidance movement of mesophyll chloroplasts (F). The log10 of absorbance is shown in the color bar. Leaf tissue dimensions are 124 × 124 × 200 µm. Scale bar: 50 µm.

Fig. 2.

Validation of light propagation model and the roles of chloroplast arrangement on light propagation and ATP production. (A) Comparison of measured (symbol) and simulated (lines) reflectance (dashed line and pink circle) and transmittance (solid line and black circles) spectra for four maize leaves (Zea mays L.) in the default mesophyll chloroplasts case. (B–D) Simulated fraction of absorbed photons across the leaf depth (B) and just across the depth zone of bundle sheath cells (C) and the response of ATP production to irradiance (I_inc) (D) for the cases of default geometry (solid line), aggregative movement of mesophyll chloroplasts (dashed green line) and the avoidance movement of mesophyll chloroplasts (dashed-dotted red line). The symbols in (D) show the ATP production calculated from experimental data. Inset in (D) shows the total ATP production at low light intensities.

Fig. 3.

Comparison of model prediction of the response of net photosynthesis (A_n) and CO₂ profile in leaf tissue. (A, B) The response of A_n to intercellular CO₂ (C_i) (A) and to irradiance (I_inc) (B). Model predictions are shown by solid lines and experimental data are shown by symbols with error bars. Simulation conditions were irradiance of 1500 µmol m⁻² s⁻¹, ambient CO₂ of 380 µmol mol⁻¹, and oxygen of 210 mmol mol⁻¹ for (A). The response to I_inc (B) was computed at ambient [CO₂] of 250 µmol mol⁻¹ and 210 mmol mol⁻¹ O₂. (C, D) The profiles of CO₂ concentration (µmol mol⁻¹) in the liquid phase (C) and in the intercellular airspace (D). In (A) and (B), the bars show standard error (n = 4). Color bars (C, D) are the CO₂ concentrations (µmol mol⁻¹).

Fig. 4.

The response of net photosynthesis (A_n) (A) and leakiness (Φ) (B) to changes in irradiance (I_inc). The responses are for default geometry (black solid line), aggregative movement of mesophyll chloroplasts (green dashed line), and the avoidance movement of mesophyll chloroplasts (red dash-dotted line). The responses were computed at ambient CO₂ of 250 µmol mol⁻¹ and 210 mmol mol⁻¹ O₂. Symbols (with error bars) in (A) are for measurement data and lines are for model prediction.