How Light Reactions of Photosynthesis in C4 Plants Are Optimized and Protected under High Light Conditions

Abstract

Most C4 plants that naturally occur in tropical or subtropical climates, in high light environments, had to evolve a series of adaptations of photosynthesis that allowed them to grow under these conditions. In this review, we summarize mechanisms that ensure the balancing of energy distribution, counteract photoinhibition, and allow the dissipation of excess light energy. They secure effective electron transport in light reactions of photosynthesis, which will lead to the production of NADPH and ATP. Furthermore, a higher content of the cyclic electron transport components and an increase in ATP production are observed, which is necessary for the metabolism of C4 for effective assimilation of CO₂. Most of the data are provided by studies of the genus Flaveria, where species belonging to different metabolic subtypes and intermediate forms between C3 and C4 are present. All described mechanisms that function in mesophyll and bundle sheath chloroplasts, into which photosynthetic reactions are divided, may differ in metabolic subtypes as a result of the different organization of thylakoid membranes, as well as the different demand for ATP and NADPH. This indicates that C4 plants have plasticity in the utilization of pathways in which efficient use and dissipation of excitation energy are realized.

Keywords: C4 photosynthesis; NAD-ME; NADP-ME; PEPCK subtypes of C4 photosynthesis; bundle sheath chloroplasts; cyclic electron transport; environmental factors; high light intensity; mesophyll chloroplasts; xanthophyll cycle.

Figure 4

The scheme of alterations that take place in bundle sheath chloroplasts (BS) during the evolutionary process from C3 to C4 in the Flaveria genus. As described by Munekage and Taniguchi [38], in species representing C4 photosynthesis, the content of complexes involved in cyclic electron transport increased and the allocation of LHCII trimers as the PSI antenna occurred due to changes in the organization of thylakoid membranes.

Figure 1

(A) Schematic describing the general metabolic pathway of C4 photosynthesis. (B) The requirement for ATP and NADPH per fixed CO₂ in mesophyll and bundle sheath cells of plants representing the NADP-ME, NAD-ME, and PEPCK subtypes of C4 photosynthesis.ATP and NADPH requirements estimated by Edwards and Voznesenskaya [9]. CA: carbonic anhydrase; Chl: chloroplast; DC: decarboxsylase; OAA: oxaloacetate; PCR cycle: photosynthetic carbon reduction cycle; PEP: phosphoenolpyruvate; PEPC: phosphoenolpyruvate carboxylase; PPDK: pyruvate, phosphate dikinase; RuBisCO: ribulose-1,5-bisphosphate carboxylase/oxygenase.

Figure 2

The scheme presents the use of absorbed light energy for photochemical reactions, heat dissipation, and radiation by fluorescence. PAR: photosynthetically active radiation.

Figure 3

The ways of electron transport in the thylakoid membrane under high light intensities and over-reduction of the plastoquinone pool (PQ). The scheme shows linear electron transport (LET), cyclic electron transport (CET), which takes place with the participation of the proteins PGR5 and PGRL1 or/and the NDH complex, and the activity of PTOX in the chlororespiration process. The content of complexes and the activity of the electron transport pathway will differ in the M and BS chloroplasts in particular metabolic subtypes and depending on environmental conditions.

Figure 5

Models of state 1 state 2 transitions in two types of chloroplasts in three subtypes of C4 plants. In maize (NADP-ME) mesophyll chloroplasts, the typical transition from state 1 to state 2 occurs, while in bundle sheath chloroplasts it is permanent state 2 where some pool of LHCII antennas are bound to PSI [41]. For the NAD-ME and PEPCK subtypes, in which the regulation of antenna migration is unknown, the shown model of state transitions is based on the organization of thylakoid membranes and the demand for ATP.