Formate-tetrahydrofolate ligase: supplying the cytosolic one-carbon network in roots with one-carbon units originating from glycolate.

10‐formyltetrahydrofolate 10‐formyltetrahydrofolate ligase Arabidopsis thaliana folates glycolate one‐carbon metabolism

Journal

The Plant journal : for cell and molecular biology
ISSN: 1365-313X
Titre abrégé: Plant J
Pays: England
ID NLM: 9207397

Informations de publication

Date de publication:
16 Jul 2024
Historique:
received: 04 05 2022
accepted: 03 07 2024
medline: 16 7 2024
pubmed: 16 7 2024
entrez: 16 7 2024
Statut: aheadofprint

Résumé

The metabolism of tetrahydrofolate (H

Identifiants

pubmed: 39010784
doi: 10.1111/tpj.16933
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : National Science Foundation
ID : MCB-2015828
Organisme : National Science Foundation
ID : MCB-2015843

Informations de copyright

© 2024 The Author(s). The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd.

Références

Atkins, C.A., Smith, P. & Storer, P.J. (1997) Reexamination of the intracellular localization of de novo purine synthesis in cowpea nodules. Plant Physiology, 113, 127–135.
Ayala‐Rodriguez, J., Barrera‐Ortiz, S., Ruiz‐Herrera, L. & Lopez‐Bucio, J. (2017) Folic acid orchestrates root development linked cell elongation with auxin response and acts independently of the TARGET OF RAPAMYCIN signaling in Arabidopsis thaliana. Plant Science, 264, 168–178.
Bao, H., Morency, M., Rianti, W., Saeheng, S., Roje, S., Weber, A.P. et al. (2021) Catalase protects against nonenzymatic decarboxylations during photorespiration in Arabidopsis thaliana. Plant Direct, 5, e366.
Basset, G., Quinlivan, E.P., Ziemak, M.J., de la Garza, R.D., Fischer, M., Schiffmann, S. et al. (2002) Folate synthesis in plants: the first step of the pterin branch is mediated by a unique bimodular GTP cyclohydrolase I. Proceedings of the National Academy of Sciences, 99, 12489–12494.
Bauwe, H. & Kolukisaoglu, Ü. (2003) Genetic manipulation of glycine decarboxylation. Journal of Experimental Botany, 54, 1523–1535.
Besson, V., Rebeille, F., Neuburger, M., Douce, R. & Cossins, E.A. (1993) Effects of tetrahydrofolate polyglutamates on the kinetic parameters of serine hydroxymethyltransferase and glycine decarboxylase from pea leaf mitochondria. Biochemical Journal, 292(2), 425–430.
Boyes, D.C., Zayed, A.M., Ascenzi, R., Mccaskill, A.J., Hoffman, N.E., Davis, K.R. et al. (2001) Growth stage‐based phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants. The Plant Cell, 13, 1499–1510.
Boyes, D.C., Zayed, A.M., Ascenzi, R., McCaskill, A.J., Hoffman, N.E., Davis, K.R. & Gorlach, J. (2001) Growth stage–based phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants. The Plant Cell, 13(7), 1499–1510.
Busch, F.A., Sage, R.F. & Farquhar, G.D. (2018) Plants increase CO2 uptake by assimilating nitrogen via the photorespiratory pathway. Nature Plants, 4, 46–54.
Chen, L., Chan, S.Y. & Cossins, E.A. (1997) Distribution of folate derivatives and enzymes for synthesis of 10‐formyltetrahydrofolate in cytosolic and mitochondrial fractions of pea leaves. Plant Physiology, 115, 299–309.
Clough, S.J. & Bent, A.F. (1998) Floral dip: a simplified method for Agrobacterium‐mediated transformation of Arabidopsis thaliana. The Plant Journal, 16, 735–743.
Cossins, E.A. (1987) Folate biochemistry and the metabolism of one‐carbon units. In: Danvis, D.D. (Ed.) The Biochemistry of plants: a comprehensive treatise. New York: Academic Press.
Czechowski, T., Stitt, M., Altmann, T., Udvardi, M.K. & Scheible, W.‐R. (2005) Genome‐wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiology, 139, 5–17.
Dirk, L.M., Williams, M.A. & Houtz, R.L. (2001) Eukaryotic peptide deformylases. Nuclear‐encoded and chloroplast‐targeted enzymes in Arabidopsis. Plant Physiology, 127, 97–107.
Dorokhov, Y.L., Sheshukova, E.V. & Komarova, T.V. (2018) Methanol in plant life. Frontiers in Plant Science, 9, 1623.
Douce, R., Bourguignon, J., Neuburger, M. & Rébeillé, F. (2001) The glycine decarboxylase system: a fascinating complex. Trends in Plant Science, 6, 167–176.
Fu, X., Gregory, L.M., Weise, S.E. & Walker, B.J. (2022) Integrated flux and pool size analysis in plant central metabolism reveals unique roles of glycine and serine during photorespiration. Nature Plants, 9, 169–178.
Gorelova, V., Bastien, O., de Clerck, O., Lespinats, S., Rébeillé, F. & van der Straeten, D. (2019) Evolution of folate biosynthesis and metabolism across algae and land plant lineages. Scientific Reports, 9, 5731.
Groth, M., Moissiard, G., Wirtz, M., Wang, H., Garcia‐Salinas, C., Ramos‐Parra, P.A. et al. (2016) MTHFD1 controls DNA methylation in Arabidopsis. Nature Communications, 7, 11640.
Hanson, A.D., Gage, D.A. & Shachar‐Hill, Y. (2000) Plant one‐carbon metabolism and its engineering. Trends in Plant Science, 5, 206–213.
Hanson, A.D. & Gregory, J.F., III. (2011) Folate biosynthesis, turnover, and transport in plants. Annual Review of Plant Biology, 62, 105–125.
Hanson, A.D. & Roje, S. (2001) One‐carbon metabolism in higher plants. Annual Review of Plant Biology, 52, 119–137.
Himes, R.H. & Rabinowitz, J.C. (1962) Formyltetrahydrofolate synthetase II. Characteristics of the enzyme and the enzymic reaction. Journal of Biological Chemistry, 237, 2903–2914.
Hourton‐Cabassa, C., Ambard‐Bretteville, F., Moreau, F., de Virville, J.D., Rémy, R. & Des Francs‐Small, C.C. (1998) Stress induction of mitochondrial formate dehydrogenase in potato leaves. Plant Physiology, 116, 627–635.
Hung, C.‐Y., Fan, L., Kittur, F.S., Sun, K., Qiu, J., Tang, S. et al. (2013) Alteration of the alkaloid profile in genetically modified tobacco reveals a role of methylenetetrahydrofolate reductase in nicotine N‐demethylation. Plant Physiology, 161, 1049–1060.
Iwai, K., Suzuki, N. & Mizoguchi, S. (1967a) The distribution of formyltetrahydrofolate synthetase in plants, and the purification and properties of the enzyme from pea seedlings. Plant and Cell Physiology, 8, 307–325.
Iwai, K., Suzuki, N. & Mizoguchi, S. (1967b) Purification and properties of formyltetrahydrofolate synthetase from spinach. Agricultural and Biological Chemistry, 31, 267–274.
Jefferson, R.A. (1987) Assaying chimeric genes in plants: the GUS gene fusion system. Plant Molecular Biology Reporter, 5, 387–405.
Kirk, C.D., Chen, L.F., Imeson, H.C. & Cossins, E.A. (1995) A 5,10‐methylenetetrahydrofolate dehydrogenase—5,10‐methenyltetrahydrofolate cyclohydrolase protein from Pisum sativum. Phytochemistry, 39, 1309–1317.
Kirk, C.D., Imeson, H.C., Zheng, L.‐L. & Cossins, E.A. (1994) The affinity of pea cotyledon 10‐formyltetrahydrofolate synthetase for polyglutamate substrates. Phytochemistry, 35, 291–296.
Kisaki, T., Yoshida, N. & Imai, A. (1971) Glycine decarboxylase and serine formation in spinach leaf mitochondrial preparation with reference to photorespiration. Plant and Cell Physiology, 12, 275–288.
Konings, E.J. (1999) A validated liquid chromatographic method for determining folates in vegetables, milk powder, liver, and flour. Journal of AOAC International, 82, 119–127.
Kordic, S., Cummins, I. & Edwards, R. (2002) Cloning and characterization of an S‐formylglutathione hydrolase from Arabidopsis thaliana. Archives of Biochemistry and Biophysics, 399, 232–238.
Kunze, M. & Hartig, A. (2013) Permeability of the peroxisomal membrane: lessons from the glyoxylate cycle. Frontiers in Physiology, 4, 204.
Lasok, H., Nziengui, H., Kochersperger, P. & Ditengou, F. (2023) Arabidopsis root development regulation by the endogenous folate precursor para‐aminobenzoic acid, via modulation of the root cycle. Plants, 12, 4076.
Li, R., Moore, M., Bonham‐Smith, P.C. & King, J. (2002) Overexpression of formate dehydrogenase in Arabidopsis thaliana resulted in plants tolerant to high concentrations of formate. Journal of Plant Physiology, 159, 1069–1076.
Li, Y., Luo, J., Chen, R., Zhou, Y., Yu, H., Chu, Z. et al. (2023) Folate shapes plant root architecture by affecting auxin distribution. The Plant Journal, 113, 969–985.
Liu, J.J. & Ward, R.L. (2010) Folate and one‐carbon metabolism and its impact on aberrant DNA methylation in cancer. Advances in Genetics, 71, 79–121.
Lunn, J.E., Feil, R., Hendriks, J.H.M., Gibon, Y., Morcuende, R., Osuna, D. et al. (2006) Sugar‐induced increases in trehalose 6‐phosphate are correlated with redox activiation of ADPglucose pyrophosphorylase and higher rates of starch synthesis in Arabidopsis thaliana. Biochemical Journal, 397, 139–148.
Ma, F., Jazmin, L.J., Young, J.D. & Allen, D.K. (2014) Isotopically nonstationary 13C flux analysis of changes in Arabidopsis thaliana leaf metabolism due to high light acclimation. Proceedings of the National Academy of Sciences, 111, 16967–16972.
Mackenzie, R., Blakely, R. & Benkovic, S. (1984) Folates and pterins. Chemistry and Biochemistry of Folates, 1, 255–306.
Mccormac, A., Elliott, M. & Chen, D. (1998) A simple method for the production of highly competent cells of Agrobacterium for transformation via electroporation. Molecular Biotechnology, 9, 155–159.
Mejillano, M.R., Jahansouz, H., Matsunaga, T.O., Kenyon, G.L. & Himes, R.H. (1989) Formation and utilization of formyl phosphate by N10‐formyltetrahydrofolate synthetase: evidence for formyl phosphate as an intermediate in the reaction. Biochemistry, 28, 5136–5145.
Moreno, J.I., Martín, R. & Castresana, C. (2005) Arabidopsis SHMT1, a serine hydroxymethyltransferase that functions in the photorespiratory pathway influences resistance to biotic and abiotic stress. The Plant Journal, 41, 451–463.
Mouillon, J.M., Aubert, S., Bourguignon, J., Gout, E., Douce, R. & Rebeille, F. (1999) Glycine and serine catabolism in non‐photosynthetic higher plant cells: their role in C1 metabolism. Plant Journal, 20, 197–205.
Neuburger, M., Rébeillé, F., Jourdain, A., Nakamura, S. & Douce, R. (1996) Mitochondria are a major site for folate and thymidylate synthesis in plants (*). Journal of Biological Chemistry, 271, 9466–9472.
Niessen, M., Thiruveedhi, K., Rosenkranz, R., Kebeish, R., Hirsch, H.‐J., Kreuzaler, F. et al. (2007) Mitochondrial glycolate oxidation contributes to photorespiration in higher plants. Journal of Experimental Botany, 58, 2709–2715.
Pelloux, J., Rusterucci, C. & Mellerowicz, E.J. (2007) New insights into pectin methylesterase structure and function. Trends in Plant Science, 12, 267–277.
Peterhansel, C., Horst, I., Niessen, M., Blume, C., Kebeish, R., Kürkcüoglu, S. et al. (2010) Photorespiration. The Arabidopsis book/American Society of Plant Biologists, 8, 1–24.
Prabhu, V., Chatson, K.B., Abrams, G.D. & King, J. (1996) C‐13 nuclear magnetic resonance detection of interactions of serine hydroxymethyltransferase with C1‐tetrahydrofolate synthase and glycine decarboxylase complex activities in Arabidopsis. Plant Physiology, 112, 207–216.
Rabinowitz, J.C. & Pricer, W.E. (1956) Formimino‐tetrahydrofolic acid and methenyltetrahydrofolic acid as intermediates in the formation of N10‐formyltetrahydrofolic acid. Journal of the American Chemical Society, 78, 5702–5704.
Reyes‐Hernandez, B., Srivastava, A., Ugartechea‐Chirino, Y., Shishkova, S., Ramos‐Parra, P., Lira‐Ruan, V. et al. (2014) The root indeterminacy‐to‐determinacy developmental switch is operated through a folate‐dependent pathway in Arabidopsis thaliana. New Phytologist, 202(4), 1223–1236.
Roje, S. (2007) Vitamin B biosynthesis in plants. Phytochemistry, 68, 1904–1921.
Roje, S., Janave, M.T., Ziemak, M.J. & Hanson, A.D. (2002) Cloning and characterization of mitochondrial 5‐formyltetrahydrofolate cycloligase from higher plants. Journal of Biological Chemistry, 277, 42748–42754.
Ros, R., Muñoz‐Bertomeu, J. & Krueger, S. (2014) Serine in plants: biosynthesis, metabolism, and functions. Trends in Plant Science, 19, 564–569.
Rowe, P. (1984) Folates in the biosynthesis and degradation of purines. New York, Ny, USA: John Wiley.
Rzewuski, G., Cornell, K.A., Rooney, L., Bürstenbinder, K., Wirtz, M., Hell, R. et al. (2007) OsMTN encodes a 5′‐methylthioadenosine nucleosidase that is up‐regulated during submergence‐induced ethylene synthesis in rice (Oryza sativa L.). Journal of Experimental Botany, 58, 1505–1514.
Schmitz, J., Hüdig, M., Meier, D., Linka, N. & Maurino, V.G. (2020) The genome of Ricinus communis encodes a single glycolate oxidase with different functions in photosynthetic and heterotrophic organs. Planta, 252, 1–12.
Scrimgeour, K. & Vitols, K.S. (1966) The reduction of folate by borohydride. Biochemistry, 5, 1438–1443.
Serero, A., Giglione, C. & Meinnel, T. (2001) Distinctive features of the two classes of eukaryotic peptide deformylases1. Journal of Molecular Biology, 314, 695–708.
Smith, A.G., Croft, M.T., Moulin, M. & Webb, M.E. (2007) Plants need their vitamins too. Current Opinion in Plant Biology, 10, 266–275.
Song, Z.B., Xiao, S.Q., You, L., Wang, S.S., Tan, H., Li, K.Z. et al. (2013) C1 metabolism and the C alvin cycle function simultaneously and independently during HCHO metabolism and detoxification in Arabidopsis thaliana treated with HCHO solutions. Plant, Cell & Environment, 36, 1490–1506.
Srivastava, A., Ramos‐Parra, P., Bedair, M., Robledo‐Hernandez, A., Tang, Y., Sumner, L. et al. (2011) The folypolyglutamate synthetase plastidial isoform is required for postembryonic root development in Arabidopsis. Plant Physiology, 155, 1237–1251.
Staben, C. & Rabinowitz, J. (1984) Formation of formylmethionyl‐tRNA and initiation of protein synthesis. Folates and Pterins, 1, 457–495.
Strong, W., Joshi, G., Lura, R., Muthukumaraswamy, N. & Schirch, V. (1987) 10‐Formyltetrahydrofolate synthetase. Evidence for a conformational change in the enzyme upon binding of tetrahydropteroylpolyglutamates. The Journal of Biological Chemistry, 262, 12519–12525.
Suzuki, N. & Iwai, K. (1974) The occurrence and properties of methylenetetrahydrofolate dehydrogenase in pea seedlings, and intracellular distribution of some folate‐linked enzymes in the plant. Journal of Nutritional Science and Vitaminology (Tokyo), 20, 89–96.
Timm, S., Florian, A., Arrivault, S., Stitt, M., Fernie, A.R. & Bauwe, H. (2012) Glycine decarboxylase controls photosynthesis and plant growth. FEBS Letters, 586, 3692–3697.
Walkup, A.S. & Appling, D.R. (2005) Enzymatic characterization of human mitochondrial C1‐tetrahydrofolate synthase. Archives of Biochemistry and Biophysics, 442, 196–205.
Wei, Z. & Roje, S. (2011) A high‐performance liquid chromatography‐based fluorometric method for assaying serine hydroxymethyltransferase toward serine formation. Analytical Biochemistry, 409, 156–158.
Wei, Z., Sun, K., Sandoval, F.J., Cross, J.M., Gordon, C., Kang, C. et al. (2013) Folate polyglutamylation eliminates dependence of activity on enzyme concentration in mitochondrial serine hydroxymethyltransferases from Arabidopsis thaliana. Archives of Biochemistry and Biophysics, 536, 87–96.
Wingler, A., Lea, P.J. & Leegood, R.C. (1999) Photorespiratory metabolism of glyoxylate and formate in glycine‐accumulating mutants of barley and Amaranthus edulis. Planta, 207, 518–526.
Xie, Z., Yu, L., Yu, H. & Deng, Q. (2012) Application of a fluorescent derivatization reagent 9‐chloromethyl anthracene on determination of carboxylic acids by HPLC. Journal of Chromatographic Science, 50, 464–468.
Xu, Y., Fu, X., Sharkey, T.D., Shachar‐Hill, Y. & Walker, B.J. (2021) The metabolic origins of non‐photorespiratory CO2 release during photosynthesis: a metabolic flux analysis. Plant Physiology, 186, 297–314.
Zhang, Y., Sun, K. & Roje, S. (2008) An HPLC‐based fluorometric assay for serine hydroxymethyltransferase. Analytical Biochemistry, 375, 367–369.
Zhang, Y., Sun, K., Sandoval, F.J., Santiago, K. & Roje, S. (2010) One‐carbon metabolism in plants: characterization of a plastid serine hydroxymethyltransferase. Biochemical Journal, 430, 97–105.
Zhang, Y., Zhang, C., Man, X., Men, Y., Ren, X., Li, X. et al. (2023) Functional characterization of the SiFPGS2 gene of foxtail millet in folate accumulation and root development. Plant Growth Regulation, 99, 137–147.
Zimmermann, S.E., Benstein, R.M., Flores‐Tornero, M., Blau, S., Anoman, A.D., Rosa‐Téllez, S. et al. (2021) The phosphorylated pathway of serine biosynthesis links plant growth with nitrogen metabolism. Plant Physiology, 186, 1487–1506.

Auteurs

Sompop Saeheng (S)

Institute of Biological Chemistry, Washington State University, Pullman, Washington, USA.
Center of Excellence for Biochemistry, Faculty of Science, Prince of Songkla University, Hat Yai, 90110, Thailand.
Plant Cell and Physiology for Sustainable Agriculture Research Unit, Faculty of Science, Prince of Songkla University, Hat Yai, 90110, Thailand.

Clayton Bailes (C)

Institute of Biological Chemistry, Washington State University, Pullman, Washington, USA.

Han Bao (H)

Department of Energy-Michigan State University Plant Research Laboratory, Michigan State University, East Lansing, Michigan, USA.

Kelem Gashu (K)

Department of Energy-Michigan State University Plant Research Laboratory, Michigan State University, East Lansing, Michigan, USA.
Department of Plant Biology, Michigan State University, East Lansing, Michigan, USA.

Matt Morency (M)

Department of Energy-Michigan State University Plant Research Laboratory, Michigan State University, East Lansing, Michigan, USA.
Department of Plant Biology, Michigan State University, East Lansing, Michigan, USA.

Tana Arlynn (T)

Institute of Biological Chemistry, Washington State University, Pullman, Washington, USA.

Andrei Smertenko (A)

Institute of Biological Chemistry, Washington State University, Pullman, Washington, USA.

Berkley James Walker (BJ)

Department of Energy-Michigan State University Plant Research Laboratory, Michigan State University, East Lansing, Michigan, USA.
Department of Plant Biology, Michigan State University, East Lansing, Michigan, USA.

Sanja Roje (S)

Institute of Biological Chemistry, Washington State University, Pullman, Washington, USA.

Classifications MeSH