Functional Mitochondrial Complex I Is Required by Tobacco Leaves for Optimal Photosynthetic Performance in Photorespiratory Conditions and during Transients

Abstract

The importance of the mitochondrial electron transport chain in photosynthesis was studied using the tobacco (Nicotiana sylvestris) mutant CMSII, which lacks functional complex I. Rubisco activities and oxygen evolution at saturating CO 2 showed that photosynthetic capacity in the mutant was at least as high as in wild-type (WT) leaves. Despite this, steady-state photosynthesis in the mutant was reduced by 20% to 30% at atmospheric CO 2 levels. The inhibition of photosynthesis was alleviated by high CO 2 or low O 2 . The mutant showed a prolonged induction of photosynthesis, which was exacerbated in conditions favoring photorespiration and which was accompanied by increased extractable NADP-malate dehydrogenase activity. Feeding experiments with leaf discs demonstrated that CMSII had a lower capacity than the WT for glycine (Gly) oxidation in the dark. Analysis of the postillumination burst in CO 2 evolution showed that this was not because of insufficient Gly decarboxylase capacity. Despite the lower rate of Gly metabolism in CMSII leaves in the dark, the Gly to Ser ratio in the light displayed a similar dependence on photosynthesis to the WT. It is concluded that: (a) Mitochondrial complex I is required for optimal photosynthetic performance, despite the operation of alternative dehydrogenases in CMSII; and (b) complex I is necessary to avoid redox disruption of photosynthesis in conditions where leaf mitochondria must oxidize both respiratory and photorespiratory substrates simultaneously.Plant biomass production is ultimately determined by the ratio between photosynthesis and respiratory CO 2 release, and 30% to 70% of fixed carbon can be rereleased within each 24-h cycle (Lambers, 1997). Therefore, manipulation of respiration is a potential approach to improving agricultural yields (Lewis et al., 2000). One current difficulty is that, quite apart from the roles played by respiration in heterotrophic tissues, the importance of leaf respiration for the process of carbon fixation itself is not yet fully established. Leaf mitochondria may have several functions during photosynthesis (for review, see Krö mer, 1995; Hoefnagel et al., 1998; Gardeströ m et al., 2002). These include oxidation of malate generated by the photosynthetic electron transport chain (Backhausen et al., 1998), production of organic acids for chloroplastic ammonia assimilation (Foyer et al., 2001), and generation of ATP to support UDP-Glc formation for Suc synthesis (Krö mer et al., 1988(Krö mer et al., , 1993. A key function of leaf mitochondria during photosynthesis, particularly in C 3 species, is the oxidation of Gly produced in the photorespiratory pathway (Douce and Neuburger, 1989) through reactions catalyzed by Gly decarboxylase (GDC) and Ser hydroxymethyl transferase, enzymes found in abundance in the mitochondrial matrix (Oliver et al., 1990). Although the importance of these enzymes in photorespiratory carbon recycling is well established (Somerville and Ogren, 1981; Blackwell et al., 1990; Heineke et al., 2001), and although is...

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