Regulation of the Expression of the Glycine Decarboxylase Complex during Pea Leaf Development

Vauclare, Pierre; Diallo, N.; Bourguignon, Jacques; Macherel, David; Douce, Roland

doi:10.1104/pp.112.4.1523

Cited by 61 publications

(45 citation statements)

References 33 publications

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“…Then the amount of the transcript progressively decreases to reach the basal level observed in roots or stems. Interestingly, the changes in the level of the HPPK-DHPS mRNA measured during the first 7 d of development match the pattern previously observed for the small subunit of the Rubisco enzyme and the Gly cleavage system (Vauclare et al, 1996). This observation suggests that de novo THF biosynthesis and folate accumulation in leaves are related to photosynthesis.…”

Section: Folate Synthesis In Differentiating Organs During Developmentsupporting

confidence: 83%

“…During leaf development in the light, the expression pattern of the mRNA for HPPK-DHPS follows the accumulation of the transcripts coding proteins involved in photosynthesis and photorespiration, e.g. the small subunit of Rubisco and the constituents of the Gly cleavage system (Vauclare et al, 1996). Also, the HPPK-DHPS protein and folate accumulate gradually during deetiolation (Fig.…”

Section: Discussionmentioning

confidence: 99%

“…4B), i.e. a stage at which the photosynthetic apparatus builds up (Vauclare et al, 1996). High concentration of the vitamin (4-5 nmol g Ϫ1 fresh weight) is then maintained in the mature leaf, which finally contains about three times more folate than other organs.…”

Section: Folate Synthesis In Differentiating Organs During Developmentmentioning

confidence: 99%

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One-Carbon Metabolism in Plants. Regulation of Tetrahydrofolate Synthesis during Germination and Seedling Development

et al. 2003

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Tetrahydrofolate (THF) is a central cofactor for one-carbon transfer reactions in all living organisms. In this study, we analyzed the expression of dihydropterin pyrophosphokinase-dihydropteroate synthase (HPPK-DHPS) in pea (Pisum sativum) organs during development, and so the capacity to synthesize dihydropteroate, an intermediate in the de novo THF biosynthetic pathway. During seedling development, all of the examined organs/tissues contain THF coenzymes, collectively termed folate, and express the HPPK-DHPS enzyme. This suggests that each organ/tissue is autonomous for the synthesis of THF. During germination, folate accumulates in cotyledons and embryos, but high amounts of HPPK-DHPS are only observed in embryos. During organ differentiation, folate is synthesized preferentially in highly dividing tissues and in photosynthetic leaves. This is associated with high levels of the HPPK-DHPS mRNA and protein, and a pool of folate 3-to 5-fold higher than in the rest of the plant. In germinating embryos and in meristematic tissues, the high capacity to synthesize and accumulate folate correlates with the general resumption of cell metabolism and the high requirement for nucleotide synthesis, major cellular processes involving folate coenzymes. The particular status of folate synthesis in leaves is related to light. Thus, when illuminated, etiolated leaves gradually accumulate the HPPK-DHPS enzyme and folate. This suggests that folate synthesis plays an important role in the transition from heterotrophic to photoautotrophic growth. Analysis of the intracellular distribution of folate in green and etiolated leaves indicates that the coenzymes accumulate mainly in the cytosol, where they can supply the high demand for methyl groups.The synthesis of numerous biological compounds and the regulation of many metabolic processes require the addition or removal of one-carbon units (C1 metabolism). Tetrahydrofolate (THF) coenzymes mediate these C1 transfer reactions that are involved in several major cellular processes, including the synthesis of purines and thymidylate, amino acid metabolism, pantothenate synthesis, mitochondrial and chloroplastic protein biogenesis, and Met synthesis (Fig. 1). Met is the direct precursor of S-adenosyl-Met (Ado-Met), which in turn is the source of methyl units for the synthesis of a myriad of molecules such as choline, chlorophyll, or lignin (for reviews, see Cossins, 2000;Scott et al., 2000;Hanson and Roje, 2001). In plants, THF is also involved in the photorespiratory cycle, a specific pathway that occurs at very high rates in green leaves from C3 plants. Photorespiration relies on two THF-dependent enzymes present in the matrix space of leaf mitochondria, the Gly decarboxylase complex (GDC) and Ser hydroxymethyltransferase (SHMT; for reviews, see Oliver, 1994;Douce et al., 2001).THF is composed of three distinct parts, namely a pterin ring, a p-aminobenzoic acid, and a poly-Glu chain of variable length (1-8 residues). Its function is to bind, transport, and donate C1 units that differ i...

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Section: Folate Synthesis In Differentiating Organs During Developmentsupporting

confidence: 83%

Section: Discussionmentioning

confidence: 99%

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One-Carbon Metabolism in Plants. Regulation of Tetrahydrofolate Synthesis during Germination and Seedling Development

et al. 2003

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“…The impressive accumulation of free Gly raises the possibility that Ni depredation is limiting the activity of either Gly decarboxylase or Ser hydroxymethyl transferase, which acts to convert Gly to Ser in the mitochondria. These two enzyme systems comprise about 40% to 50% of the soluble proteins in the mitochondria, with their buildup potentially being dependent on leaf development (Vauclare et al, 1996). Alternatively, the incorporation of Gly into purines could also be blocked.…”

Section: Amino Acidsmentioning

confidence: 99%

Nickel Deficiency Disrupts Metabolism of Ureides, Amino Acids, and Organic Acids of Young Pecan Foliage

2006

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The existence of nickel (Ni) deficiency is becoming increasingly apparent in crops, especially for ureide-transporting woody perennials, but its physiological role is poorly understood. We evaluated the concentrations of ureides, amino acids, and organic acids in photosynthetic foliar tissue from Ni-sufficient (Ni-S) versus Ni-deficient (Ni-D) pecan (Carya illinoinensis [Wangenh.] K. Koch). Foliage of Ni-D pecan seedlings exhibited metabolic disruption of nitrogen metabolism via ureide catabolism, amino acid metabolism, and ornithine cycle intermediates. Disruption of ureide catabolism in Ni-D foliage resulted in accumulation of xanthine, allantoic acid, ureidoglycolate, and citrulline, but total ureides, urea concentration, and urease activity were reduced. Disruption of amino acid metabolism in Ni-D foliage resulted in accumulation of glycine, valine, isoleucine, tyrosine, tryptophan, arginine, and total free amino acids, and lower concentrations of histidine and glutamic acid. Ni deficiency also disrupted the citric acid cycle, the second stage of respiration, where Ni-D foliage contained very low levels of citrate compared to Ni-S foliage. Disruption of carbon metabolism was also via accumulation of lactic and oxalic acids. The results indicate that mouse-ear, a key morphological symptom, is likely linked to the toxic accumulation of oxalic and lactic acids in the rapidly growing tips and margins of leaflets. Our results support the role of Ni as an essential plant nutrient element. The magnitude of metabolic disruption exhibited in Ni-D pecan is evidence of the existence of unidentified physiological roles for Ni in pecan.Relatively little is known about the role of nickel (Ni) in plant nutrition, physiology, and metabolism, especially in woody perennial species, such as pecan (Carya illinoinensis [Wangenh.] K. Koch). Ni was suspected of possessing a metabolic role in plants when discovered as a constituent of plant ash in the early 20th century. Evidence for a key metabolic role was strengthened with observation of field-level growth responses to foliar Ni applications to crops as diverse as wheat (Triticum aestivum), potatoes (Solanum tuberosum), and broad beans (Vicia faba; Roach and Barclay, 1946;Dobrolyubskii and Slavvo, 1957;Welch, 1981).

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“…This enzyme also contains a lipoic acid moiety, can account for up to 50% of matrix protein, and is responsible for the most prominent metabolic activity in the mitochondria of illuminated leaves, photorespiration (10). GDC is a multienzyme complex composed of four component enzymes, the P-, H-, T-, and L-proteins and is responsible for the conversion of glycine produced in the peroxisome to serine in the mitochondria during operation of the photorespiratory cycle (11). The H-protein plays a pivotal role as a mobile substrate that commutes between the other subunits, allowing its lipoic acid "arm" to visit the active sites of the other three components (10).…”

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confidence: 99%

Environmental Stress Causes Oxidative Damage to Plant Mitochondria Leading to Inhibition of Glycine Decarboxylase

Taylor¹,

Day²,

Millar³

2002

Journal of Biological Chemistry

176

145

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A cytotoxic product of lipid peroxidation, 4-hydroxy-2-nonenal (HNE), rapidly inhibited glycine, malate/ pyruvate, and 2-oxoglutarate-dependent O 2 consumption by pea leaf mitochondria. Dose-and timedependence of inhibition showed that glycine oxidation was the most severely affected with a K 0.5 of 30 M. Several mitochondrial proteins containing lipoic acid moieties differentially lost their reactivity to a lipoic acid antibody following HNE treatment. The most dramatic loss of antigenicity was seen with the 17-kDa glycine decarboxylase complex (GDC) H-protein, which was correlated with the loss of glycine-dependent O 2 consumption. Paraquat treatment of pea seedlings induced lipid peroxidation, which resulted in the rapid loss of glycine-dependent respiration and loss of Hprotein reactivity with lipoic acid antibodies. Pea plants exposed to chilling and water deficit responded similarly. In contrast, the damage to other lipoic acidcontaining mitochondrial enzymes was minor under these conditions. The implication of the acute sensitivity of glycine decarboxylase complex H-protein to lipid peroxidation products is discussed in the context of photorespiration and potential repair mechanisms in plant mitochondria.The polyunsaturated fatty acids of membrane lipids are susceptible to reactive oxygen species (ROS) 1 -induced peroxidation yielding various aldehydes, alkenals, and hydroxyalkenals, including the cytotoxic compounds malonaldehyde (MDA) and 4-hydroxy-2-nonenal (HNE). These two end products are commonly measured in studies of lipid peroxidation by the thiobarbituric acid-reactive substances (TBARS) assay (1). Interest in the biological effect of HNE was stimulated by studies showing cytotoxicity due to rapid reaction with sulfydryl groups via Michael addition (2). A number of stress conditions, including cardiac reperfusion injury, increase ROS production and the rate of membrane peroxidation and ultimately lead to inhibition of the respiratory rate in mammals (3). HNE has been shown to directly inhibit respiration of isolated mammalian mitochondria through modification of the lipoic acid moieties of 2-oxo acid dehydrogenases, forming HNE-Michael adducts ( Fig. 1) (4). These targets have also been shown to be damaged in vivo under conditions that induce lipid peroxidation (5).A range of biotic and abiotic stresses also raise ROS levels in plants due to perturbations of chloroplastic and mitochondrial metabolism and the generation of ROS in defense responses (6). Such accumulation of ROS in plants will clearly result in a wide variety of deleterious effects through oxidation reactions involving proteins, lipids, and nucleic acids. Lipid peroxidation in plants has been known for many years, but direct evidence of the pathways involved and the identification of HNE production in plants has only been reported recently (7). However, the exact molecular targets, the relative sensitivity of target enzymes, the mechanisms of repair, and the impact on plant function have not been extensively investigated.Research o...

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Regulation of the Expression of the Glycine Decarboxylase Complex during Pea Leaf Development

Cited by 61 publications

References 33 publications

One-Carbon Metabolism in Plants. Regulation of Tetrahydrofolate Synthesis during Germination and Seedling Development

One-Carbon Metabolism in Plants. Regulation of Tetrahydrofolate Synthesis during Germination and Seedling Development

Nickel Deficiency Disrupts Metabolism of Ureides, Amino Acids, and Organic Acids of Young Pecan Foliage

Environmental Stress Causes Oxidative Damage to Plant Mitochondria Leading to Inhibition of Glycine Decarboxylase

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