| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
|
Plant Physiol. (1998) 116: 627-635 Stress Induction of Mitochondrial Formate Dehydrogenase in Potato Leaves1
Institut de Biotechnologie des Plantes, Centre National de la Recherche Scientifique-Equipe en Restructuration 569 Université Paris-Sud, Bâtiment 630, F-91405 Orsay cedex, France (C.H.-C., F.A.-B., R.R., C.C.d.F.-S.); and Laboratoire de Physiologie Cellulaire et Moléculaire des Plantes, Centre National de la Recherche Scientifique-Unité Mixte de Recherche 7632, 2135 Université Pierre et Marie Curie, Tour 53, case 154, 4 Place Jussieu, F-75252 Paris cedex 05, France (F.M., J.D.d.V.)
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 O2 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 C3 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
CO2, 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 In higher plants only NAD-dependent FDHs have been found, and these are
localized in the mitochondrial matrix (Halliwell, 1974 In this paper we describe the expression of potato mitochondrial FDH in
various tissues and under several stresses. The mRNA levels of the
mitochondrial SHMT isoform were studied in parallel because this enzyme
was previously described to be abundant in pea photosynthetic tissues
and scarce in green tissues kept in the dark (Turner et al., 1992 Plant Material and Growth Conditions
RNA Isolation and Northern Analysis Total RNAs were isolated from various potato tissues according to either the procedure of Logemann et al. (1987) or a modified method of
Sambrook et al. (1989). Plant tissues were ground in liquid
N2, and the powder was homogenized in extraction
buffer (8 m guanidium hydrochloride, 20 mm Mes,
pH 7, 20 mm Na4EDTA, and 50 mm 2-mercaptoethanol) and centrifuged for 20 min at 17,000 rpm (rotor SS-34, model RC5C, Sorvall) at 4°C. RNAs were then purified by an overnight centrifugation through a 4-mL 5.7 m CsCl cushion at 20°C at 32,000 rpm (rotor SW41, model
L7-55, Beckman). For each sample, 10 µg of RNA was run on a 3%
formaldehyde, 1.5% agarose gel, transferred by blotting onto nylon
membranes (Hybond-N+, Amersham), and probed with
either an 850-bp potato FDH cDNA (Colas des Francs-Small et al., 1993)
or a 1.5-kb pea (Pisum sativum L.) SHMT cDNA (Turner et al.,
1992). RNA loading on gels was controlled by EtBr staining under UV
light, and transfer efficiency by hybridization with a 2.42-kb wheat
mitochondrial 18S rRNA gene fragment (Bonen and Gray, 1980).
Measurement of Formate Oxidation by Isolated Mitochondria Potato tuber mitochondria were isolated and subsequently purified on Percoll gradients as previously described (Diolez and Moreau, 1985).
O2 uptake and membrane potential were measured simultaneously with an O2 electrode (Hansatech,
Kings Lynn, UK) and a TPP-sensitive electrode (Diolez and Moreau,
1985). Experiments were carried out at 25°C in a medium containing 1 mL (0.5 mg) of mitochondrial protein in 400 mm mannitol, 10 mm K2PO4
buffer, pH 7.2, 100 mm KCl, 5 mm
MgCl2, 1 mg/mL BSA, and 4 µm
TPP+ as final concentrations. Respiration was
initiated with 15 mm formate, and a limiting amount of ADP
(100 µm) was then added to ensure a state 3-to-state 4 transition. Membrane potential was calculated using the equation:
 E is the electrode potential in mV (Kamo et al., 1979). Membrane
potential was collapsed at the end of each experiment run by the
addition of 1 µm carbonylcyanide
m-chlorophenylhydrazone. The calculation of  was
carried out without correction for the probe binding. The mitochondrial
protein concentration was determined according to the method of Lowry
et al. (1951).
Mitochondrial Protein Analysis Two-dimensional SDS-PAGE of mitochondrial proteins was performed on a Mini Protean II apparatus (Bio-Rad), as described previously (Colas des Francs-Small et al., 1992). The gels were Coomassie blue
stained and the polypeptides were quantified (Scanalytics MasterScan I,
Computer Signal Processing, Billerica, MA) equipped with
two-dimensional gel-analysis software. The polypeptides of interest
were identified by immunodetection with various antibodies after
transfer onto nitrocellulose sheets (Hybond C, Amersham) using the Mini
Trans-Blot cell (Bio-Rad).
FDH and SHMT mRNA Expression in Various Potato Tissues The levels of FDH and SHMT mRNAs were studied in parallel in various tissues from greenhouse-grown potato plants and are presented in Figure 1. The lowest FDH transcript levels were found in leaves and stamen-free flowers, whereas developing tubers exhibited a very high amount of FDH mRNAs (about 100-fold higher than in leaves). Veins, stems, stolons, stamens, and roots showed intermediate amounts of FDH transcripts: about 16-fold higher in stems than in leaves (used as the reference for quantitations), 6-fold higher in veins, 8-fold higher in stamens, 6-fold higher in stolons, and 2.5-fold higher in roots. Compared with FDH, SHMT transcript levels were high in leaves, one-half as abundant in veins and stolons, and very scarce or even undetectable in other tissues. FDH protein amounts followed mRNA levels in the various tissues tested. The histogram of the quantities of FDH, MDH (matrix protein), and -ATPase (membrane
protein) illustrates the variations in FDH and the relatively constant
amounts of MDH and -ATPase in these tissues (Fig.
2).
Formate Oxidation in Potato Tuber Mitochondria From simultaneous measurements of O2 uptake and membrane potential in mitochondria isolated from potato tubers, it could be demonstrated that NAD-linked FDH produced NADH, which was reoxidized by the respiratory chain (Fig. 3). Formate oxidation in state 4 (10.5 ± 0.5 nmol O2 min 1 mg1 protein) was
associated with high values of membrane potential (228 ± 2 mV),
whereas the addition of ADP induced a large depolarization (55 ± 5 mV) (Fig. 3). The rates of formate oxidation (32 ± 2 nmol O2 min1
mg1 protein) were one-half that of those
obtained with malate (64 ± 14 nmol O2
min1 mg1 protein). By
contrast, the ADP-to-O2 ratio found with either formate or malate was identical (2.15 ± 0.35), indicating that formate oxidation was coupled to the three proton translocation sites
in plant mitochondria (see also Oliver, 1981).
The Expression of FDH in Leaves Is Enhanced under Various Environmental Stresses Hypoxia Hypoxia led to a strong FDH mRNA induction. Although no effect was observed after 8 h of hypoxia, the FDH mRNA level increased 8-fold after 16 h (Fig. 4), and remained high after 24 and 48 h of hypoxia (data not shown).
Chilling and Drought Chilling and drought also considerably increased FDH mRNA (respectively, 10- and 24-fold higher than the control) after 24 h of treatment (Fig. 4). Chilling, however, induced a slower response than drought, as the transcript abundance continued to increase for another 24 h.Dark and Dark-to-Light Transition Effects A dramatic increase of FDH mRNA was observed after 16 h of dark treatment (Fig. 4), which continued to increase up to 24 h (17- and 20-fold higher than the control, respectively), remained high after 48 h (data not shown), and started to decrease after 3 d (down to 10-fold higher than the control). Dark induction of FDH mRNAs was almost completely reversible by placing the plants under a 16-h photoperiod for another 24 h (Fig. 4, lanes D24-L24 and D48-L24).Wounding Unlike the previous stress treatments, wounding led to a very rapid FDH mRNA response, as the transcripts were very abundant only 20 min after wounding. They accumulated (13-fold higher than the control) for up to 1 h (Fig. 4), remained high for 24 h, and then decreased between 24 h and 3 d (data not shown).SHMT and FDH Leaf mRNAs Show Opposite Responses to Various Environmental Stresses SHMT mRNA levels were unchanged after chilling or wounding (Fig. 4). On the contrary, they were undetectable after 8 h of hypoxia, 24 h of drought, or 24 h of dark treatment. SHMT mRNAs reappeared when plants kept for 24 to 48 h in the dark were placed back under a 16-h photoperiod for another 24 h. In summary, SHMT and FDH mRNAs showed opposite responses (except for chilling and wounding), demonstrating that we are dealing with specific regulations. In regard to dark and hypoxia stresses, however, the kinetics of the increase or decrease were different, i.e. more rapid and drastic for SHMT transcripts.The Expression of FDH and SHMT mRNAs in Leaves Are Altered Differently by External Addition of Various Metabolites Formate Spraying plants with 10 mm formate (the substrate for FDH) increased FDH mRNAs 13-fold after 24 h, whereas the amount of SHMT mRNAs was unchanged (Fig. 5).
ABA ABA, a compound involved in the response to several stresses such as cold, hypoxia, drought, and wounding, was tested for its ability to regulate FDH or SHMT mRNA levels. Twenty-four hours after spraying 100 µm ABA, the amount of FDH mRNAs was multiplied by five (Fig. 5), and the amount of SHMT mRNAs decreased.Ser and Sarcosine Ser and sarcosine, two products derived from Gly and methylene THF by the action of SHMT and sarcosine dehydrogenase, respectively, induced a 2.5- to 3-fold decrease of SHMT mRNA levels in leaves, whereas the amount of FDH mRNA was increased (about 6-fold higher in both cases) (Fig. 5).Pyruvate, Acetate, and Ethanol Because glycolysis is known to be induced by dark and hypoxia, some products of glycolysis (pyruvate, acetate, and ethanol) were tested. Northern analyses showed an increase of FDH expression level 24 h after spraying 10 mm acetate (5.5-fold) or 10 mm pyruvate (3-fold), and a greater increase (15-fold) 24 h after 10% ethanol treatment (Fig. 5). On the contrary, SHMT mRNAs decreased after spraying acetate or pyruvate (3- and 5-fold, respectively), and disappeared after ethanol treatment (Fig. 5).Methanol Methanol led to a dramatic increase (30-fold higher than the control) of FDH mRNAs (Fig. 5) and a 3-fold decrease of SHMT mRNAs (Fig. 5).Two-Dimensional Analysis of Mitochondrial Polypeptides Figure 6, A and B, shows the polypeptide patterns obtained with mitochondria isolated from tubers and leaves from young, actively growing plants (summer plants). The relative FDH content was 10-fold higher in tubers than in leaves, whereas MDH and - and -ATPase were roughly constant in both
tissues (Fig. 2). However, it was evident that in mitochondria isolated
from the leaves of old, slowly growing plants (winter plants, mostly
grown under artificial light), the relative FDH content observed was
similar to that found in tubers (Fig. 6C). The two-dimensional
mitochondrial protein patterns of tubers from summer and winter plants
were similar (not shown).
Differential Expression of FDH in Various Potato Tissues Our results show that under normal growth conditions, FDH transcript and protein contents are high in nonphotosynthetic tissues (stems, stolons, stamens, tubers, and dark-grown sprouts) and scarce in leaf mitochondria. An exception to this rule is the roots, where FDH content is only slightly higher than in leaves. The fact that formate can be excreted by roots, as reported for oats and maize under poorly oxygenated conditions (Davison, 1951), might explain this discrepancy.
FDH Response to Stress Some environmental signals to which tubers are naturally submitted (e.g. dark and hypoxia) and a few other stresses were investigated for their ability to enhance FDH expression in potato leaves, where it is low under normal conditions. The mRNA level of the mitochondrial isoform of SHMT, a key enzyme of C1 metabolism, was studied in parallel as a control. Our results show that FDH mRNA expression is strongly increased by dark, hypoxia, wounding, cold, and drought. We performed western analyses and activity tests for most of these stresses and observed that FDH quantity and activity follow the mRNA increase 1 to 3 d after the stress treatment. In all cases, the final activity was 1.5- to 1.7-fold higher than the control (not shown).FDH Response to Metabolites To elucidate the transduction pathways involved in the FDH plant response to stress, the effects of spraying leaves with various metabolites were studied. The effects of the metabolites should be considered to be qualitative rather than quantitative because of the uncertainties concerning the amount of metabolite actually entering the plant cells. The observation that formate application greatly enhances FDH expression in potato leaves led us to focus on formate biosynthesis. Under normal growth conditions, formate can arise from various pathways (Fig. 7). The photorespiratory origin of formate in leaves was the first to be described (Tolbert et al., 1949), and in a recent review, Fall and
Benson (1996) suggested rapid formate biosynthesis via methanol
metabolism (reactions 2, 3, and 4), with the methanol arising from cell
wall degradation or synthesis. Finally, glycolytic products may
generate glyoxylate from malate (via malate synthase, reaction 15) or
from isocitrate (via isocitrate lyase, reaction 16). This glyoxylate
will give rise to formate in peroxisomes. In stressed plants formate
biosynthesis could result from the enhancement of any of these pathways
or from newly induced ones. Three metabolic pathways thought to be involved in response to stress were studied here.
The Ser and Sarcosine Degradation Pathway Our results show that spraying Ser and sarcosine increases FDH transcription in potato leaves. The catabolism of sarcosine and Ser to formate was first described in yeast and mammals (Barlow and Appling, 1988), but whether plants use sarcosine is not clear. When
photorespiration occurs, the mitochondrial SHMT isoform catalyzes the
synthesis of Ser, whereas the thermodynamic equilibrium of this
reaction is normally in favor of Ser degradation (Rebeillé et
al., 1994). In nongreen tissues Ser is thought to be cleaved by other
isoforms of SHMT to yield Gly, 5,10-methylene THF, and, subsequently,
formate (Schirch, 1984). Furthermore, Ser catabolism was shown to occur
in grapevine leaves under water stress (Morchiladze, 1969). We suggest
that under drought, Ser might be partly metabolized into formate
(reactions 5, 6, 7, 8, 9, and 10) and possibly account for a part of
the FDH induction in potato leaves. The advantages of such a
degradation pathway under stress would be to produce ATP (reaction 10)
and to provide NADH to the respiratory chain (reaction 1). It would be
interesting to study this Ser catabolism in more detail in tissues in
which FDH expression is high.
Glycolysis Dark and hypoxia are known to induce glycolysis, which leads to the production of pyruvate, acetate, and, in the case of hypoxia, ethanol. Spraying acetate and pyruvate increased FDH transcript levels, but less than dark or hypoxia. This suggests that these compounds could be involved in the FDH response to dark or hypoxia, but the concentrations used might not be sufficient to reflect these stresses. On the other hand, 10% ethanol (2 m) led to a higher FDH increase and to total disappearance of SHMT transcripts, close to what was observed under dark and hypoxic stresses. Acetate, pyruvate, and ethanol could act either directly as formate precursors, or indirectly by induction of the enzymes involved in formate biosynthesis. These results suggest that glycolysis may play an important role in the FDH response to dark and hypoxia. The important glycolytic flux that occurs in nonphotosynthetic tissues (germinating tubers, sprouts, germinating pollen, stems, and leaves in the dark) might to a certain extent account for the high FDH levels in such tissues. However, the pathway from glycolytic products to formate remains obscure. We suggest two possibilities: (a) via malate and isocitrate or (b) directly from pyruvate to formate via a pyruvate formate lyase (reaction 17), which has been described in mitochondria from unicellular algae (Kreutzberg, 1984; Kreutzberg et al., 1987) but remains to be
found in higher plants.
The Metabolism of Methanol Both cell wall growth and degradation lead to methanol production in plants (Fall and Benson, 1996). Methanol catabolism to formate is
particularly interesting, because methanol-treated plants exhibited
very high levels of FDH mRNA. The lack of response of SHMT after
methanol treatment indicates that FDH induction is specific. Moreover,
recent papers demonstrate that the application of methanol to leaves
enhances the yields in a wide range of C3 plants
(unlike C4 plants) (Nonomura and Benson, 1992;
Devlin and al., 1994; Rowe et al., 1994). These authors suggest that an
increase in available CO2 might contribute to
this response. Cossins (1964) showed that methanol is rapidly
metabolized into CO2 in leaves, but although
formaldehyde dehydrogenase and FDH exist in plants, methanol oxidase
has so far only been found in microorganisms. Furthermore, their role
in this metabolic pathway is not yet established (Fall and Benson,
1996). Formaldehyde dehydrogenase, in particular, could be partly or
entirely overshadowed by other pathways, as formaldehyde can also give
rise to formate directly or via methylene THF (Doman and Romanova 1962;
Cossins, 1964). The dramatic induction of FDH after methanol treatment
strongly favors the hypothesis of its participation in methanol
oxidation to CO2. Mutants deficient in one or
more enzymes of this latter pathway would be very helpful for studying
the role of these enzymes in C3 plant growth.
* Corresponding author; e-mail colas{at}ibp.u-psud.fr; fax 33-169-33-63-24. Received May 27, 1997;
accepted October 21, 1997.
Abbreviations:
The authors wish to thank Dr. Steve Rawsthorne for providing the pea SHMT probe and antibody. We are grateful to R. Boyer for taking the photographs and to Drs. Ian Small and Steve Rawsthorne for critical reading of the manuscript. We also thank F. Vedel for his continuous interest in this work.
Allen SJ, Holbrook JJ (1995) Gene 162: 99-104 [CrossRef][Medline] Barlow CK, Appling DR (1988) In vitro evidence for the involvement of mitochondrial folate metabolism in the supply of cytoplasmic one-carbon units. Biofactors 1: 171-176 [Medline]
Bonen L,
Gray MW
(1980)
Organization and expression of mitochondrial genomes of plants. The genes for wheat mitochondrial ribosomal and transfer RNA: evidence for an unusual arrangement.
Nucleic Acid Res
8:
319-335
Colas des Francs-Small C,
Ambard-Bretteville F,
Darpas A,
Sallantin M,
Huet JC,
Pernollet JC,
Rémy R
(1992)
Variation of the polypeptide composition of mitochondria isolated from different potato tissues.
Plant Physiol
98:
273-278
Colas des Francs-Small C, Ambard-Bretteville F, Small ID, Rémy R (1993) Identification of a major soluble protein in mitochondria from nonphotosynthetic tissues as NAD-dependent formate dehydrogenase. Plant Physiol 102: 1171-1177 [Abstract] Cossins EA (1964) The utilization of carbon-1 compounds by plants. I. The metabolism of methanol-C14 and its role in amino-acid biosynthesis. Can J Bot 42: 1793-1802 Cossins EA (1980) One-carbon metabolism. In DD Davies, eds, The Biochemistry of Plants, Vol II. Academic Press, New York, pp 365-418 Davison DC (1951) Studies on formate dehydrogenases. Biochem J 49: 520-526 [Medline] Devlin RM, Bhowmik PC, Karczmarczyk SJ (1994) Influence of methanol on plant growth. Plant Growth Regul Soc Am Q 22: 102-108 Diolez P, Moreau F (1985) Correlations between ATP synthesis, membrane potential and oxidation rate in plant mitochondria. Biochem Biophys Acta 806: 56-63 [CrossRef]
Doman NG,
Romanova AK
(1962)
Transformations of labeled formic acid, formaldehyde, methanol and CO2 absorbed by bean and barley leaves from air.
Plant Physiol
37:
833-840
Fall R, Benson AA (1996) Leaf methanol: the simpliest natural product from plants. Trends Plant Sci 1: 296-301 [CrossRef][ISI] Halliwell B (1974) Oxidation of formate by peroxisomes and mitochondria from spinach leaves. Biochem J 138: 77-85 [ISI][Medline] Haynes TS, Klemm DJ, Ruocco JJ, Barton LL (1995) Formate dehydrogenase activity in cells and outer membrane blebs of Desulfovibrio gigas. Anaerobe 1: 175-182 [Medline] Humphery-Smith I, Colas des Francs-Small C, Ambard-Bretteville F, Rémy R (1992) Tissue-specific variations of pea mitochondrial polypeptides detected by computerized image analysis of two-dimensional electrophoresis gels. Electrophoresis 13: 168-172 [Medline] Kamo N, Muratsugu M, Hongoh R, Kobakate Y (1979) Membrane potential of mitochondria measured with an electrode sensitive to tetraphenylphosphonium and relationship between proton electrochemical potential and phosphorylation potential in steady state. J Membr Biol 49: 105-121 [CrossRef][ISI][Medline] Kreutzberg K (1984) Starch fermentation via formate producing pathway in Chlamydomonas reinhardtii, Chlorogonium elongatum, and Chlorella fusca. Physiol Plant 61: 87-94 [CrossRef] Kreutzberg K, Klöck G, Grobheiser D (1987) Subcellular distribution of pyruvate-degrading enzymes in Chlamydomonas reinhardtii studied by an improved protoplast fractionation procedure. Physiol Plant 69: 481-488 Logemann J, Schell J, Willmitzer L (1987) Improved method for the isolation of RNA from plant tissues. Anal Biochem 163: 16-20 [CrossRef][ISI][Medline]
Lowry OH,
Rosenbrough NJ,
Farr AL,
Randall RJ
(1951)
Protein measurement with the Folin phenol reagent.
J Biol Chem
193:
265-275
Morchiladze ZN (1969) Transformation of 3 C14 series in the grapevine. Soobshch Akad Nauk Gruz SSR 54: 705-708
Nonomura AM,
Benson AA
(1992)
The path of carbon in photosynthesis: improved crop yields with methanol.
Proc Natl Acad Sci USA
89:
9794-9798
Norton G (1963) The respiratory pathways in potato tubers. In JD Irvins, FL Milthorpe, eds, The Growth of the Potato. Proceedings of the Tenth Easter School in Agricultural Science. University of Nottingham, Butterworths, London, pp 148-169
Oliver DJ
(1981)
Formate oxidation and oxygen reduction by leaf mitochondria.
Plant Physiol
68:
703-705
Popov VO, Lamzin VS (1994) NAD(+)-dependent formate dehydrogenase. Biochem J 302: 967 Rebeillé F, Neuburger M, Douce R (1994) Interaction between glycine decarboxylase, serine hydroxymethyltransferase and tetrahydrofolate polyglutamates in pea leaf mitochondria. Biochem J 302: 223-228 Rowe RN, Farr DJ, Richards BAJ (1994) Effects of foliar and root applications of methanol or ethanol on the growth of tomato plants (Lycopersicon esculentum Mill.). N Z J Crop Hort Sci 22: 335-337 Sambrook J, Fritsch EF, Manniatis T (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York Sawers G (1994) The hydrogenases and formate dehydrogenases of Escherichia coli. Antonie Van Leeuwenhoek 66: 57-88 [CrossRef][Medline] Schirch L (1984) Folates in serine and glycine metabolism. In RL Blakely, SJ Benkovic, eds, Folates and Pterins. Wiley, New York, pp 399-431
Tolbert NE,
Clagett CO,
Burris RH
(1949)
Products of the oxidation of glycolic acid and lactic acid by enzymes from tobacco leaves.
J Biol Chem
181:
905-914
Turner SR, Hellens R, Ireland R, Ellis N, Rawsthorne S (1993) The organisation and expression of the genes encoding the mitochondrial glycine decarboxylase complex and serine hydroxymethyltransferase in pea (Pisum sativum). Mol Gen Genet 236: 402-408 [CrossRef][Medline]
Turner SR,
Ireland R,
Morgan C,
Rawsthorne S
(1992)
Identification and localization of multiple forms of serine hydroxymethyltransferase in pea (Pisum sativum) and characterization of a cDNA encoding a mitochondrial isoform.
J Biol Chem
267:
13528-13534
Uotila L, Koivusalo M (1979) Purification of formaldehyde and formate dehydrogenases from pea seeds by affinity chromatography and S-formylglutathione as the intermediate of formaldehyde metabolism. Arch Biochem Biophys 196: 33-45 [CrossRef][ISI][Medline] Van Dijken JP, Oostra-Demkes GT, Otto R, Harder W (1976) S-Formylglutathione: the substrate for formate dehydrogenase in methanol-utilizing yeasts. Arch Microbiol 111: 77-83 [Medline]
Copyright Clearance Center: 0032-0889/98/116/0627/09
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
|
|
 |
|
  A. B. Cousins, I. Pracharoenwattana, W. Zhou, S. M. Smith, and M. R. Badger Peroxisomal Malate Dehydrogenase Is Not Essential for Photorespiration in Arabidopsis But Its Absence Causes an Increase in the Stoichiometry of Photorespiratory CO2 Release Plant Physiology, October 1, 2008; 148(2): 786 - 795. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 C. P. Lee, H. Eubel, N. O'Toole, and A. H. Millar Heterogeneity of the Mitochondrial Proteome for Photosynthetic and Non-photosynthetic Arabidopsis Metabolism Mol. Cell. Proteomics, July 1, 2008; 7(7): 1297 - 1316. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 E. Collakova, A. Goyer, V. Naponelli, I. Krassovskaya, J. F. Gregory III, A. D. Hanson, and Y. Shachar-Hill Arabidopsis 10-Formyl Tetrahydrofolate Deformylases Are Essential for Photorespiration PLANT CELL, July 1, 2008; 20(7): 1818 - 1832. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. Goyer, T. L. Johnson, L. J. Olsen, E. Collakova, Y. Shachar-Hill, D. Rhodes, and A. D. Hanson Characterization and Metabolic Function of a Peroxisomal Sarcosine and Pipecolate Oxidase from Arabidopsis J. Biol. Chem., April 23, 2004; 279(17): 16947 - 16953. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
N. V. Bykova, A. Stensballe, H. Egsgaard, O. N. Jensen, and I. M. Moller Phosphorylation of Formate Dehydrogenase in Potato Tuber Mitochondria J. Biol. Chem., July 3, 2003; 278(28): 26021 - 26030. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. S. AMTHOR Efficiency of Lignin Biosynthesis: a Quantitative Analysis Ann. Bot., May 1, 2003; 91(6): 673 - 695. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. Li, M. Moore, and J. King Investigating the Regulation of One-carbon Metabolism in Arabidopsis thaliana Plant Cell Physiol., March 15, 2003; 44(3): 233 - 241. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. Gout, S. Aubert, R. Bligny, F. Rébeillé, A. R. Nonomura, A. A. Benson, and R. Douce Metabolism of Methanol in Plant Cells. Carbon-13 Nuclear Magnetic Resonance Studies Plant Physiology, May 1, 2000; 123(1): 287 - 296. [Abstract] [Full Text]
|
|
|
|
|
|
S. D. McNeil, M. L. Nuccio, D. Rhodes, Y. Shachar-Hill, and A. D. Hanson Radiotracer and Computer Modeling Evidence that Phospho-Base Methylation Is the Main Route of Choline Synthesis in Tobacco Plant Physiology, May 1, 2000; 123(1): 371 - 380. [Abstract] [Full Text]
|
|
|
|
 |
|
 E.S. Dennis, R. Dolferus, M. Ellis, M. Rahman, Y. Wu, F.U. Hoeren, A. Grover, K.P. Ismond, A.G. Good, and W.J. Peacock Molecular strategies for improving waterlogging tolerance in plants J. Exp. Bot., January 1, 2000; 51(342): 89 - 97. [Abstract] [Full Text] [PDF]
|
|
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Top
Abstract
Introduction
