The Complementary Roles of Chloroplast Cyclic Electron Transport and Mitochondrial Alternative Oxidase to Ensure Photosynthetic Performance

Chloroplasts use light energy and a linear electron transport (LET) pathway for the coupled generation of NADPH and ATP. It is widely accepted that the production ratio of ATP to NADPH is usually less than required to fulfill the energetic needs of the chloroplast. Left uncorrected, this would quickly result in an over-reduction of the stromal pyridine nucleotide pool (i.e., high NADPH/NADP+ ratio) and under-energization of the stromal adenine nucleotide pool (i.e., low ATP/ADP ratio). These imbalances could cause metabolic bottlenecks, as well as increased generation of damaging reactive oxygen species. Chloroplast cyclic electron transport (CET) and the chloroplast malate valve could each act to prevent stromal over-reduction, albeit in distinct ways. CET avoids the NADPH production associated with LET, while the malate valve consumes the NADPH associated with LET. CET could operate by one of two different pathways, depending upon the chloroplast ATP demand. The NADH dehydrogenase-like pathway yields a higher ATP return per electron flux than the pathway involving PROTON GRADIENT REGULATION5 (PGR5) and PGR5-LIKE PHOTOSYNTHETIC PHENOTYPE1 (PGRL1). Similarly, the malate valve could couple with one of two different mitochondrial electron transport pathways, depending upon the cytosolic ATP demand. The cytochrome pathway yields a higher ATP return per electron flux than the alternative oxidase (AOX) pathway. In both Arabidopsis thaliana and Chlamydomonas reinhardtii, PGR5/PGRL1 pathway mutants have increased amounts of AOX, suggesting complementary roles for these two lesser-ATP yielding mechanisms of preventing stromal over-reduction. These two pathways may become most relevant under environmental stress conditions that lower the ATP demands for carbon fixation and carbohydrate export.

The Physiological Functionality of PGR5/PGRL1-Dependent Cyclic Electron Transport in Sustaining Photosynthesis

The cyclic electron transport (CET), after the linear electron transport (LET), is another important electron transport pathway during the light reactions of photosynthesis. The proton gradient regulation 5 (PGR5)/PRG5-like photosynthetic phenotype 1 (PGRL1) and the NADH dehydrogenase-like complex pathways are linked to the CET. Recently, the regulation of CET around photosystem I (PSI) has been recognized as crucial for photosynthesis and plant growth. Here, we summarized the main biochemical processes of the PGR5/PGRL1-dependent CET pathway and its physiological significance in protecting the photosystem II and PSI, ATP/NADPH ratio maintenance, and regulating the transitions between LET and CET in order to optimize photosynthesis when encountering unfavorable conditions. A better understanding of the PGR5/PGRL1-mediated CET during photosynthesis might provide novel strategies for improving crop yield in a world facing more extreme weather events with multiple stresses affecting the plants.

The Significance of Chloroplast NAD(P)H Dehydrogenase Complex and Its Dependent Cyclic Electron Transport in Photosynthesis

Chloroplast NAD(P)H dehydrogenase (NDH) complex, a multiple-subunit complex in the thylakoid membranes mediating cyclic electron transport, is one of the most important alternative electron transport pathways. It was identified to be essential for plant growth and development during stress periods in recent years. The NDH-mediated cyclic electron transport can restore the over-reduction in stroma, maintaining the balance of the redox system in the electron transfer chain and providing the extra ATP needed for the other biochemical reactions. In this review, we discuss the research history and the subunit composition of NDH. Specifically, the formation and significance of NDH-mediated cyclic electron transport are discussed from the perspective of plant evolution and physiological functionality of NDH facilitating plants’ adaptation to environmental stress. A better understanding of the NDH-mediated cyclic electron transport during photosynthesis may offer new approaches to improving crop yield.

The chloroplast NADH dehydrogenase-like complex influences the photosynthetic activity of the moss Physcomitrella patens

Alternative electron pathways contribute to regulation of photosynthetic light reactions to adjust to metabolic demands in dynamic environments. The chloroplast NADH dehydrogenase-like (NDH) complex mediates the cyclic electron transport pathway around PSI in different cyanobacteria, algae, and plant species, but it is not fully conserved in all photosynthetic organisms. In order to assess how the physiological role of this complex changed during plant evolution, we isolated Physcomitrella patens lines knocked out for the NDHM gene that encodes a subunit fundamental for the activity of the complex. ndhm knockout mosses indicated high PSI acceptor side limitation upon abrupt changes in illumination. In P. patens, pseudo-cyclic electron transport mediated by flavodiiron proteins (FLVs) was also shown to prevent PSI over-reduction in plants exposed to light fluctuations. flva ndhm double knockout mosses had altered photosynthetic performance and growth defects under fluctuating light compared with the wild type and single knockout mutants. The results showed that while the contribution of NDH to electron transport is minor compared with FLV, NDH still participates in modulating photosynthetic activity, and it is critical to avoid PSI photoinhibition, especially when FLVs are inactive. The functional overlap between NDH- and FLV-dependent electron transport supports PSI activity and prevents its photoinhibition under light variations.

Optimal reorganization of photosynthesis after the evolution of C4

The evolution of C4 photosynthesis evolved numerous times independently in the grasses over tens of millions of years, and each event required the development of distinct biochemistry and anatomy. Recent theoretical, anatomical and phylogenetic studies made great progress in reconstructing the evolutionary processes leading to the formation of the C4 carbon concentration mechanism (CCM) in grasses. After the formation of the full CCM, C4 physiology continued to diverge between C3 and C4 grasses, presumably as selection optimized photosynthetic function. In this study, we combine optimality modeling, physiological measurements and phylogenetic analysis to examine how various aspects of C4 photosynthetic machinery were reorganized within a lineage and as compared to closely-related C3 grasses. Both model and empirical results support a strong, and comparatively rapid, reorganization in resource allocation between the Calvin-Benson cycle and light reactions in C4, as determined by a higher maximal electron transport to maximal Rubisco carboxylation rate (Jmax/Vcmax). Our model, chlorophyll a/b ratios, and fluorescence-based electron transport measurements all suggest that linear electron transport represents a lower proportion (approximately 67%) of total electron transport in C4, and that the impetus for increased cyclic-electron transport is to balance ATP:NADPH stoichiometry, as opposed to decreasing O2 in the bundle sheath cells. Finally, the tight coordination between RuBP carboxylation and PEP carboxylation occurred coincidently with the evolution of the C4 CCM, with a relatively constant maximal PEP carboxylation rate and Vcmax (Vpmax/Vcmax).

Influence of elevated temperature on electron flows in chloroplasts of barley

The efficiency of electron carriers in thylakoid membranes untreated and exposed to heat 7-day-old barley seedlings was evaluated with PAM fluorescence. Darkness–light transitional states in chloroplasts after heat exposure are studied. Thermoinduced changes in linear and cyclic electron transport chain of chloroplasts are revealed. The activation of NADPH-dependent electron flux after exposure to elevated temperatures is shown. We assumed that ΔрН of thylakoid membranes employed the regulatory role in the distribution of electron flows and the adaptation of the photosynthetic apparatus to stressful effects.