Stress Induction of Mitochondrial Formate Dehydrogenase in Potato Leaves1

Abstract

In higher plants formate dehydrogenase (FDH, EC 1.2.1.2.) is a mitochondrial, NAD-dependent enzyme. We previously reported that in potato (Solanum tuberosum L.) FDH expression is high in tubers but low in green leaves. Here we show that in isolated tuber mitochondria FDH is involved in formate-dependent O 2 uptake coupled to ATP synthesis. The effects of various environmental and chemical factors on FDH expression in leaves were tested using the mitochondrial serine hydroxymethyltransferase as a control. The abundance of FDH transcripts is strongly increased under various stresses, whereas serine hydroxymethyltransferase transcripts decline. The application of formate to leaves strongly enhances FDH expression, suggesting that it might be the signal for FDH induction. Our experiments using glycolytic products suggest that glycolysis may play an important role in formate synthesis in leaves in the dark and during hypoxia, and in tubers. Of particular interest is the dramatic accumulation of FDH transcripts after spraying methanol on leaves, as this compound is known to increase the yields of C 3 plants. In addition, although the steady-state levels of FDH transcript increase very quickly in response to stress, protein accumulation is much slower, but can eventually reach the same levels in leaves as in tubers.FDH catalyzes the oxidation of formate into CO 2 , and is a widespread enzyme in bacteria, yeasts, fungi, mammals, and plants. Several types of FDHs have been reported with differing cofactors (NAD or FAD), electron acceptors, substrates, and cellular locations. A wide diversity of FDH types is found in the bacteria, where they are involved in respiration (for review, see Sawers, 1994) and possibly in the maintenance of a reducing environment (Haynes et al., 1995). The NAD-dependent FDHs (EC 1.2.1.2) have been extensively studied in yeast and bacteria over the past decade because the favorable thermodynamics of the reaction, the easy removal of the product (CO 2 ), and the low cost of the substrate (formate) have made this enzyme a good candidate for industrial NADH regeneration (Allen and Holbrook, 1995). In methanol-utilizing yeasts such as Hansenula polymorpha, Candida boidinii, and Pichia pinus, NAD-dependent FDH plays a crucial role, together with formaldehyde dehydrogenase, in providing NADH to the respiratory chain (Van Dijken et al., 1976). Aside from formate, it is possible that S-formylglutathione might also be a substrate for FDH, as was suggested for yeasts (Van Dijken et al., 1976), pea (Uotila and Koivusalo, 1979), and Pseudomonas sp. 101 (Popov and Lamzin, 1994).In higher plants only NAD-dependent FDHs have been found, and these are localized in the mitochondrial matrix (Halliwell, 1974; Oliver, 1981; Colas des Francs-Small et al., 1993). Oliver (1981) showed that isolated leaf mitochondria from spinach (and, to a lesser extent, that from beet and tobacco) can oxidize formate with a tight coupling to oxidative phosphorylation. The first plant FDH cDNA to be published encodes a potato (So...

A Formate Dehydrogenase Confers Tolerance to Aluminum and Low pH

“…In barley roots, the expression of FDH is induced by iron deficiency, an induction that appears to be a secondary effect of the oxygen deficiency resulting from iron deficiency (Suzuki et al, 1998). It has also been proposed that glycolysis may play an important role in the FDH expression in response to abiotic stresses (Hourton-Cabassa et al, 1998). Similarly, we have previously shown that genes involved in glycolysis are repressed, but that genes related to anaerobic respiration are promoted by Al stress in rice bean root apices , implying that hypoxia and glycolysis may be responsible for rice bean VuFDH expression in response to Al stress.…”

“…In plants, FDHs have been reported to be involved in stress responses, because the expression of FDHs was responsive to a wide range of abiotic and biotic stresses (Hourton-Cabassa et al, 1998;David et al, 2010). Recently, Choi et al (2014) reported that FDHs play important role in hypersensitive response-like cell death and defense responses to bacterial pathogens in both peppers (Capsicum annuum) and Arabidopsis.…”

Arabidopsis 10-Formyl Tetrahydrofolate Deformylases Are Essential for Photorespiration

“…A proposed mechanism for the involvement of At4g17360 and At5g47435 as putative folate deformylases in photorespiration is shown in Figure 10. A similar, but not a cyclic, route involving folate interconversion enzymes has previously been postulated to produce formate in plants (Hourton-Cabassa et al, 1998;Hanson et al, 2000;Goyer et al, 2005). (Photorespiration involves a series of cycles to metabolize toxic 2-phosphoglycolate and to prevent both the depletion of intermediates and cofactors and the accumulation of products due to large fluxes.)…”

Peroxisomal Malate Dehydrogenase Is Not Essential for Photorespiration in Arabidopsis But Its Absence Causes an Increase in the Stoichiometry of Photorespiratory CO2 Release

“…In addition, the resulting formate can also be decarboxylated in the peroxisomes by its oxidation via catalase and H 2 O 2 (Halliwel and Butt, 1974) or can be oxidized to CO 2 by formate dehydrogenase in the mitochondrion (Hourton-Cabassa et al, 1998). These potential reactions are shown in Figure 5.…”