The role of photorespiration in redox and energy balance of photosynthetic plant cells: A study with a barley mutant deficient in glycine decarboxylase

Abstract

Protoplasts and mitochondria were isolated from leaves of homozygous barley (Hordeum vulgare L.) mutant deficient in glycine decarboxylase complex (GDC, EC 2.1.2.10) and wild-type plants. The photosynthetic rates of isolated protoplasts from the mutant and wild-type plants under saturating CO2 were similar, but the respiratory rate of the mutant was two-fold higher. Respiration in the mutant plants was much more strongly inhibited by antimycin A than in wild-type plants and a low level of the alternative oxidase protein was found in mitochondria. The activities of NADP- and NAD-dependent malate dehydrogenases were also increased in mutant plants, suggesting an activation of the malate-oxaloacetate exchange for redox transfer between organelles. Mutant plants had elevated activities of NADH- and NADPH-dependent glyoxylate/hydroxypyruvate reductases, which may be involved in oxidizing excess NAD(P)H and the scavenging of glyoxylate. We estimated distribution of pools of adenylates, NAD(H) and NADP(H) between chloroplasts, cytosol and mitochondria. Under photorespiratory conditions, ATP/ADP and NADPH/NADP ratios in the mutant were higher in chloroplasts as compared to wild-type plants. The cytosolic NADH/NAD ratio was increased, whereas the ratio in mitochondria decreased. It is concluded that photorespiration serves as an effective redox transfer mechanism from the chloroplast. Plants with a lowered GDC content are deficient in this mechanism, which leads to over-reduction and over-energization of the chloroplasts.

Genomics-based dissection of the cross-talk of chloroplasts with the nucleus and mitochondria in Arabidopsis

“…In the barley albostrians mutant, the absence of chloroplast activity in an otherwise fully differentiated leaf tissue leads to an increase in mitochondrial gene copy number and an elevated level of mitochondrial transcripts (Hedtke et al, 1999). Vice versa, mutations affecting specific mitochondrial proteins have been analyzed for their effects on chloroplast properties, like gdc of potato (Heineke et al, 2001) and barley (Igamberdiev et al, 2001). Both mutants exhibit a lowered glycine decarboxylase activity and are impaired in photorespiration, leading to an over-reduction and over-energization of the chloroplast.…”

Photorespiration Is Crucial for Dynamic Response of Photosynthetic Metabolism and Stomatal Movement to Altered CO 2 Availability

“…Only the combination of limited CO 2 in conjunction with impaired PR capacity invoked the response. A limitation in CO 2 results in acceptor limitation of photosynthesis and, hence, overreduction of the chloroplasts, which is exaggerated in the absence of a functional PR pathway (Igamberdiev et al, 2001;Scheibe and Dietz, 2012;Keech et al, 2016). To encounter the LC-induced redox stress, the strong mutants induced expression of several protective mechanisms, such as glutathione transferases with antioxidant function (Supplemental Table 3) and the mitochondrial electron valves AOX1A and AOX1D ( Figure 5D), or enhanced NPQ ( Figure 5B) to dissipate excess absorbed light energy.…”

Nuclear Photosynthetic Gene Expression Is Synergistically Modulated by Rates of Protein Synthesis in Chloroplasts and Mitochondria

“…The ncs mutants grow poorly and are characterized by leaves with pale-green or yellow stripes, reflecting defects in chloroplast function. Additional mitochondrial mutants that affect photosynthetic performance include glycine decarboxylase in potato (Solanum tuberosum) (Heineke et al, 2001) and barley (Igamberdiev et al, 2001): here, a reduction in Gly decarboxylase activity impairs photorespiration and leads to excessive reduction and energization of the chloroplast. Furthermore, the tobacco (Nicotiana tabacum) CMSII mutant lacks the major mitochondrial NADH dehydrogenase (Complex I) and exhibits a decrease in the rate of photosynthesis, notably during dark-light transitions or when carbon fixation and photorespiration are simultaneously active (Sabar et al, 2000;Dutilleul et al, 2003a).…”