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 (M) cells in C4 plants is hypothesized to enhance the CO2 concentrating mechanism (CCM), but this is difficult to verify experimentally. A three-dimensional (3-D) leaf model can help analyze how chloroplast movement influences the operation of CCM. The first volumetric reaction-diffusion model of C4 photosynthesis that incorporates: detailed 3-D leaf anatomy, light propagation, ATP and NADPH production and CO2, O2 and bicarbonate concentration driven by diffusional and assimilation/emission processes, was developed and implemented for maize leaves to simulate various chloroplast movement scenarios within M cells : the movement of all M chloroplasts towards bundle-sheath (BS) cells (aggregative movement) and movement of only those of interveinal M cells towards BS cells (avoidance movement). Light absorbed by bundle-sheath (BS) chloroplasts relative to M chloroplasts increased in both cases. Avoidance movement decreased light absorption by M chloroplasts considerably. Consequently, total ATP and NADPH production and net photosynthesis rate increased for aggregative movement and decreased for avoidance movement case compared to 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 M and BS cells. These results suggest the need to design strategies for coordinated increases in electron transport and Rubisco activities for an efficient CCM at very high light intensities.