Discovery of Key Molecular Pathways of C1 Metabolism and Formaldehyde Detoxification in Maize through a Systematic Bioinformatics Literature Review

Abstract

Computational systems biology approaches provide insights to understand complex molecular phenomena in living systems. Such understanding demands the need to systematically interrogate and review existing literature to refine and distil key molecular pathways. This paper explores a methodological process to identify key molecular pathways from systematic bioinformatics literature review. This process is used to identify molecular pathways for a ubiquitous molecular process in all plant biological systems: C1 metabolism and formaldehyde detoxification, specific to maize. The C1 metabolism is essential for all organisms to provide one-carbon units for methylation and other types of modifications, as well as for nucleic acid, amino acid, and other biomolecule syntheses. Formaldehyde is a toxic one-carbon molecule which is produced endogenously and found in the environment, and whose detoxification is an important part of C1 metabolism. This systematic review involves a five-part process: 1) framing of the research question; 2) literature collection based on a parallel search strategy; 3) relevant study selection based on search refinement; 4) molecular pathway identification; and 5) integration of key molecular pathway mechanisms to yield a well-defined set molecular systems associated with a particular biochemical function. Findings from this systematic review produced three main molecular systems: a) methionine biosynthesis; b) the methylation cycle; and c) formaldehyde detoxification. Specific insights from the resulting molecular pathways indicate that normal C1 metabolism involves the transfer of a carbon group from serine through a folate-mediated pathway to methionine, and eventually the methylation of a biomolecule. In photosynthetic tissues, C1 metabolism often proceeds in reverse towards serine biosynthesis and formate oxidation. C1 metabolism, in maize, appears to be present in the developing embryo and endosperm indicating that these cells are vulnerable to perturbations in formaldehyde detoxification. These insights demonstrate the value of a systematic bioinformatics literature review process from a broad spectrum of domain literature to specific and relevant molecular pathways.

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Deonikar, P. , Kothandaram, S. , Mohan, M. , Kollin, C. , Konecky, P. , Olovyanniko, R. , Zamore, Z. , Carey, B. and Ayyadurai, V. (2015) Discovery of Key Molecular Pathways of C1 Metabolism and Formaldehyde Detoxification in Maize through a Systematic Bioinformatics Literature Review. Agricultural Sciences, 6, 571-585. doi: 10.4236/as.2015.65056.

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1] Khan, K.S., Kunz, R., Kleijnen, J. and Antes, G. (2003) Five Steps to Conducting a Systematic Review. Journal of the Royal Society of Medicine, 96, 118-121.
http://dx.doi.org/10.1258/jrsm.96.3.118
[2] Ayyadurai, V.A.S. and Dewey, C.F. (2011) CytoSolve: A Methodology for Dynamic Integration of Multiple Molecular Pathway Models. Cellular and Molecular Bioengineering, 4, 28-45.
http://dx.doi.org/10.1007/s12195-010-0143-x
[3] Hanson, A.D., Gage, D.A. and Shachar-Hill, Y. (2000) Plant One-Carbon Metabolism and Its Engineering. Trends in Plant Science, 5, 206-213.
http://dx.doi.org/10.1016/S1360-1385(00)01599-5
[4] Hanson, A.D. and Roje, S. (2001) One-Carbon Metabolism in Higher Plants. Annual Review of Plant Physiology and Plant Molecular Biology, 52, 119-137.
http://dx.doi.org/10.1146/annurev.arplant.52.1.119
[5] Ho, M.-W., Saunders, P. and Sirinathsinghji, E. (2013) Science in Society 58 (Institute of Science in Soc).
[6] Giese, M., Bauer-Doranth, U., Langebartels, C. and Sandermann, H. (1994) Detoxification of Formaldehyde by the Spider Plant (ChlorophytumcomosumL.) and by Soybean (Glycine max L.) Cell-Suspension Cultures. Plant Physiology, 104, 1301-1309.
[7] Xu, Z., Wang, L. and Hou, H. (2011) Formaldehyde Removal by Potted Plant-Soil Systems. Journal of Hazardous Materials, 192, 314-318.
http://dx.doi.org/10.1016/j.jhazmat.2011.05.020
[8] Achkor, H., Díaz, M., Fernández, M.R., Biosca, J.A., Parés, X. and Martínez, M.C. (2003) Enhanced Formaldehyde Detoxification by Overexpression of Glutathione-Dependent Formaldehyde Dehydrogenase from ARABIDOPSIS. Plant Physiology, 132, 2248-2255.
http://dx.doi.org/10.1104/pp.103.022277
[9] Oliver, D.J. (1981) Role of Glycine and Glyoxylate Decarboxylation in Photorespiratory CO2 Release. Plant Physiology, 68, 1031-1034.
http://dx.doi.org/10.1104/pp.68.5.1031
[10] Caperelli, C.A., Benkovic, P.A., Chettur, G. and Benkovicl, S.J. (1980) Purification of a Complex Catalyzing Folate Cofactor Synthesis and Transformylation in de Novo Purine Biosynthesis. Journal of Biological Chemistry, 255, 1885-1890.
[11] Sekhon, R.S., Lin, H., Childs, K.L., et al. (2011) Genome-Wide Atlas of Transcription during Maize Development. The Plant Journal, 66, 553-563.
http://dx.doi.org/10.1111/j.1365-313X.2011.04527.x
[12] Chen, L., Chan, S.Y. and 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.
[13] Hanson, A.D. and Gregory, J.F. (2011) Folate Biosynthesis, Turnover, and Transport in Plants. Annual Review of Plant Biology, 62, 105-125.
http://dx.doi.org/10.1146/annurev-arplant-042110-103819
[14] Rébeillé, F., Stephane, R., Jabrin, S., Douce, R., Storozhenko, S. and Van Der Straeten, D. (2006) Folates in Plants?: Biosynthesis, Distribution, and Enhancement. Physiologia Plantarum, 126, 330-342.
http://dx.doi.org/10.1111/j.1399-3054.2006.00587.x
[15] Appling, D.R. (1991) Compartmentation of Folate-Mediated One-Carbon Metabolism in Eukaryotes. FASEB Jounal, 5, 2645-2651.
[16] Mouillon, J.M., Aubert, S., Bourguignon, J., Gout, E., Douce, R. and Rébeillé, F. (1999) Glycine and Serine Catabolism in Non-Photosynthetic Higher Plant Cells: Their Role in C1 Metabolism. The Plant Journal, 20, 197-205.
http://dx.doi.org/10.1046/j.1365-313x.1999.00591.x
[17] Zhang, W., Tang, L., Sun, H., et al. (2014) C1 Metabolism Plays an Important Role during Formaldehyde Metabolism and Detoxification in Petunia under Liquid HCHO Stress. Plant Physiology and Biochemistry, 83, 327-36.
http://dx.doi.org/10.1016/j.plaphy.2014.08.017
[18] Peacock, D. and Boulter, D. (1970) Kinetic Studies of Formate Dehydrogenase. The Biochemical Journal, 120, 763- 769.
[19] Janave, M.T., Ramaswamy, N.K. and Nair, P.M. (1993) Purification and Characterization of Glyoxylate Synthetase from Greening Potato-Tuber Chloroplasts. European Journal of Biochemistry, 214, 889-896.
http://dx.doi.org/10.1111/j.1432-1033.1993.tb17992.x
[20] Appaji Rao, N., Ambili, M., Jala, V.R., Subramanya, H.S. and Savithri, H.S. (2003) Structure-Function Relationship in Serine Hydroxymethyltransferase. Biochimica et Biophysica Acta (BBA)-Proteins and Proteomics, 1647, 24-29.
http://dx.doi.org/10.1016/S1570-9639(03)00043-8
[21] Kirk, C., Chen, L., Imeson, H.C. and Cossins, E.A. (1995) A 5,10-Methylenetetrahydrofolate Dehydrogenase?: 5,10- Methylenetetrahydrofolate Cyclohydrolase Protein from Pisum sativum. Phytochemistry, 39, 1309-1317.
http://dx.doi.org/10.1016/0031-9422(95)97864-6
[22] Besson, V., Rebeille, F., Neuburger, M., Douce, R. and Cossins, E.A. (1993) Effects of Tetrahydro Folatepolyglutamates on the Kinetic Parameters of Serine Hydroxymethyltransferase and Glycine Decarboxylase from Pea Leaf Mito-chondria. The Biochemical Journal, 292, 425-430.
[23] Engel, N., Ewald, R., Gupta, K.J., Zrenner, R., Hagemann, M. and Bauwe, H. (2011) The Presequence of Arabidopsis Serine Hydroxymethyltransferase SHM2 Selectively Prevents Import into Mesophyll Mitochondria. Plant Physiology, 157, 1711-1720.
http://dx.doi.org/10.1104/pp.111.184564
[24] Timm, S., Florian, A., Arrivault, S., Stitt, M., Fernie, A.R. and Bauwe, H. (2012) Glycine Decarboxylase Controls Photosynthesis and Plant Growth. FEBS Letters, 586, 3692-3697.
http://dx.doi.org/10.1016/j.febslet.2012.08.027
[25] Hartung, W. and Ratcliffe, R.G. (2002) Utilization of Glycine and Serine as Nitrogen Sources in the Roots of Zea mays and Chamaegigas intrepidus. Journal of Experimental Botany, 53, 2305-2314.
http://dx.doi.org/10.1093/jxb/erf092
[26] Rebeille, F., Neuburger, M. and Douce, R. (1994) Interaction between Glycine Decarboxylase, Serine Hydroxymethyltransferase and Tetrahydrofolate Polyglutamates in Pea Leaf Mitochondria. The Biochemical Journal, 302, 223-228.
[27] Ravanel, S., Block, M.A., Rippert, P., et al. (2004) Methionine Metabolism in Plants: Chloroplasts Are Autonomous for DE NOVO Methionine Synthesis and Can Import S-Adenosylmethionine from the Cytosol. The Journal of Biological Chemistry, 279, 22548-22557.
http://dx.doi.org/10.1074/jbc.M313250200
[28] Stover, P. and Schirch, V. (1992) Enzymatic Mechanism for the Hydrolysis of 5,10-Methenyltetrahydropteroylgluta- mate to 5-Formyltetrahydropteroylglutamate by Serine Hydroxymethyltransferase. Biochemistry, 31, 2155-2164.
http://dx.doi.org/10.1021/bi00122a037
[29] Wong, K.F. and Cossins, E.A. (1966) Occurrence and Some Properties of N-5, N-10-Methylenetetrahydrofolate Dehydrogenase in Plants. Canadian Journal of Biochemistry, 44, 3-6.
http://dx.doi.org/10.1139/o66-159
[30] Lazar, G., Zhang, H. and Goodman, H.M. (1993) The Origin of the Bifunctional Dihydrofolate Reductasethymidylate Synthase Isogenes of Arabidopsis thaliana. The Plant Journal, 3, 657-668.
http://dx.doi.org/10.1111/j.1365-313X.1993.00657.x
[31] Prabhu, V., Chatson, K.B., Lui, H., Abrams, G.D. and King, J. (1998) Effects of Sulfanilamide and Methotrexate on 13C Fluxes through the Glycine Decarboxylase/Serine Hydroxymethyltransferase Enzyme System in Arabidopsis. Plant Physiology, 116,137-144.
http://dx.doi.org/10.1104/pp.116.1.137
[32] Ratnam, S., Delcamp, T.J., Hynes, J.B. and Freisheim, J.H. (1987) Purification and Characterization of Dihydrofolate Reductase from Soybean Seedlings. Archives of Biochemistry and Biophysics, 255, 279-289.
http://dx.doi.org/10.1016/0003-9861(87)90395-X
[33] Samanta, A., Datta, A.K. and Datta, S. (2014) Study on Folate Binding Domain of Dihydrofolate Reductase in Different Plant Species and Human Beings. Bioinformation, 10, 101-104.
http://dx.doi.org/10.6026/97320630010101
[34] Neuburger, M., Rébeillé, F., Jourdain, A., Nakamura, S. and Douce, R. (1996) Mitochondria Are a Major Site for Folate and Thymidylate Synthesis in Plants. The Journal of Biological Chemistry, 271, 9466-9472.
http://dx.doi.org/10.1074/jbc.271.16.9466
[35] Sahr, T., Ravanel, S. and Rébeillé, F. (2005) Tetrahydrofolate Biosynthesis and Distribution in Higher Plants. Bioche- mical Society Transactions, 33, 758-762.
[36] Giovanelli, J., Mudd, S.H. and Datko, A.H. (1985) Quantitative Analysis of Pathways of Methionine Metabolism and Their Regulation in Lemna. Plant Physiology, 78, 555-560.
http://dx.doi.org/10.1104/pp.78.3.555
[37] Kim, D.G., Park, T.J., Kim, J.Y. and Cho, Y.D. (1995) Purification and Characterization of S-Adenosylmethionine Synthetase from Soybean (Glycine Max) Axes. Journal of Biochemistry and Molecular Biology, 28, 100-106.
[38] Ravanel, S., Gakière, B., Job, D. and Douce, R. (1998) The Specific Features of Methionine Biosynthesis and Metabolism in Plants. Proceedings of the National Academy of Sciences of the United States of America, 95, 7805-7812.
http://dx.doi.org/10.1073/pnas.95.13.7805
[39] James, F., Nolte, K.D. and Hanson, A.D. (1995) Purification and Properties of S-Adenosyl-L-methionine?: L-Methionine S-Methyltransferase from Wollastonia biflora Leaves. The Journal of Biological Chemistry, 270, 22344-22350.
http://dx.doi.org/10.1074/jbc.270.38.22344
[40] Bradbury, L.M.T., Ziemak, M.J., El Badawi-Sidhu, M., Fiehn, O. and Hanson, A.D. (2014) Plant-Driven Repurposing of the Ancient S-Adenosylmethionine Repair Enzyme Homocysteine S-Methyltransferase. Biochemical Journal, 463, 279-286.
http://dx.doi.org/10.1042/BJ20140753
[41] Lyi, S.M., Zhou, X., Kochian, L.V. and Li, L. (2007) Biochemical and Molecular Characterization of the Homocysteine S-Methyltransferase from Broccoli (Brassica oleracea var. Italica). Phytochemistry, 68, 1112-1119.
http://dx.doi.org/10.1016/j.phytochem.2007.02.007
[42] Ranocha, P., Mcneil, S.D., Ziemak, M.J., Li, C., Tarczynski, M.C. and Hanson, A.D. (2001) The S-Methylmethionine Cycle in Angiosperms: Ubiquity, Antiquity and Activity. The Plant Journal, 25, 575-584.
http://dx.doi.org/10.1046/j.1365-313x.2001.00988.x
[43] Kocsis, M.G., Ranocha, P., Gage, D.A., et al. (2003) Insertional Inactivation of the Methionine S-Methyltransferase Gene Eliminates the S-Methylmethionine Cycle and Increases the Methylation Ratio. Plant Physiology, 131, 1808- 1815.
http://dx.doi.org/10.1104/pp.102.018846
[44] Goyer, A., Johnson, T.L., Olsen, L.J., Collakova, E., Shachar-Hill, Y., Rhodes, D. and Hanson, A.D. (2004) Characterization and Metabolic Function of a Peroxisomalsarcosine and Pipecolate Oxidase from Arabidopsis. The Journal of Biological Chemistry, 279, 16947-16953.
http://dx.doi.org/10.1074/jbc.M400071200
[45] Li, R., Moore, M. and King, J. (2003) Investigating the Regulation of One-Carbon Metabolism in Arabidopsis thaliana. Plant & Cell Physiology, 44, 233-241.
http://dx.doi.org/10.1093/pcp/pcg029
[46] Vivancos, P.D., Driscoll, S.P., Bulman, C.A., Ying, L., Emami, K., Treumann, A., Mauve, C., Noctor, G. and Foyer, C.H. (2011) Perturbations of Amino Acid Metabolism Associated with Glyphosate-Dependent Inhibition of Shikimic Acid Metabolism Affect Cellular Redox Homeostasis and Alter the Abundance of Proteins Involved in Photosynthesis and Photorespiration. Plant Physiology, 157, 256-268.
http://dx.doi.org/10.1104/pp.111.181024
[47] Diaz, M., Achkor, H., Titarenko, E. and Martinez, M.C. (2003) The Gene Encoding Glutathione-Dependent Formaldehyde Dehydrogenase/GSNO Reductase Is Responsive to Wounding, Jasmonic Acid and Salicylic Acid. FEBS Letters, 543, 136-139.
http://dx.doi.org/10.1016/S0014-5793(03)00426-5
[48] Kordic, S., Cummins, I. and Edwards, R. (2002) Cloning and Characterization of an S-Formylglutathione Hydrolase from Arabidopsis thaliana. Archives of Biochemistry and Biophysics, 399, 232-238.
http://dx.doi.org/10.1006/abbi.2002.2772
[49] Martinez, M.C., Achkor, H., Perssonz, B., Fernandez, M.R., Shafqat, J. and Farres, J. (1996) Arabidopsis Formaldehyde Dehydrogenase Molecular Properties of Plant Class III Alcohol Dehydrogenase Provide Further Insights into the Origins , Structure and Function of Plant Class P and Liver Class I Alcohol Dehydrogenases. European Journal of Biochemistry, 241, 849-857.
http://dx.doi.org/10.1111/j.1432-1033.1996.00849.x
[50] Wippermann, U., Fliegmann, J., Bauw, G., Langebartels, C., Maier, K. and Sandermann, H. (1999) Maize Glutathione- Dependent Formaldehyde Dehydrogenase: Protein Sequence and Catalytic Properties. Planta, 208, 12-18.
http://dx.doi.org/10.1007/s004250050529
[51] Loizeau, K., Gambonnet, B., Zhang, G.F., et al. (2007) Regulation of One-Carbon Metabolism in Arabidopsis: The N-Terminal Regulatory Domain of Cystathionine Gamma-Synthase Is Cleaved in Response to Folate Starvation. Plant Physiology, 145,491-503.
http://dx.doi.org/10.1104/pp.107.105379
[52] Prabhu, V., Chatson, K.B., Abrams, G.D. and King, J. (1996) 13C 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.
http://dx.doi.org/10.1104/pp.112.1.207
[53] Collakova, E., Goyer, A., Naponelli, V., et al. (2008) Arabidopsis 10-Formyl Tetrahydrofolate Deformylases Are Essential for Photorespiration. The Plant Cell, 20, 1818-1832.
http://dx.doi.org/10.1105/tpc.108.058701
[54] Cummins, I., Mcauley, K., Fordham-skelton, A., et al. (2006) Unique Regulation of the Active Site of the Serine Esterase S-Formylglutathione Hydrolase. Journal of Molecular Biology, 359,422-432.
http://dx.doi.org/10.1016/j.jmb.2006.03.048
[55] Fliegmann, J. and Sandermann, H. (1997) Maize Gluta-thione-Dependent Formaldehyde Dehydrogenase cDNA: A Novel Plant Gene of Detoxification. Plant Molecular Biology, 34, 43-54.
http://dx.doi.org/10.1023/A:1005872222490
[56] Haslam, R., Rust, S., Pallett, K., Cole, D. and Coleman, J. (2002) Cloning and Characterisation of S-Formylglutathione Hydrolase from Arabidopsis thaliana?: A Pathway for Formaldehyde Detoxification. Plant Physiology and Biochemistry, 40, 281-288.
http://dx.doi.org/10.1016/s0981-9428(02)01378-5
[57] Chen, J., Zeng, B., Zhang, M., et al. (2014) Dynamic Transcriptome Landscape of Maize Embryo and Endosperm Development. Plant Physiology, 166, 252-264.
http://dx.doi.org/10.1104/pp.114.240689
[58] Lawrence, C.J., Dong, Q., Polacco, M.L., Seigfried, T.E. and Brendel, V. (2004) MaizeGDB, the Community Database for Maize Genetics and Genomics. Nucleic Acids Research, 32, D393-D397.
http://dx.doi.org/10.1093/nar/gkh011
[59] Li, G., Wang, D., Yang, R., et al. (2014) Temporal Patterns of Gene Expression in Developing Maize Endosperm Identified through Transcriptome Sequencing. Proceedings of the National Academy of Sciences of the United States of America, 111, 7582-7587.
http://dx.doi.org/10.1073/pnas.1406383111
[60] Walley, J.W., Shen, Z., Sartor, R., et al. (2013) Reconstruction of Protein Networks from an Atlas of Maize Seed Proteotypes. Proceedings of the National Academy of Sciences of the United States of America, 110, E4808-E4817.
http://dx.doi.org/10.1073/pnas.1319113110
[61] Wippermann, U., Fliegmann, J., Bauw, G., Langebartels, C., Maier, K. and Sandermann, H. (1999) Maize Glutathione-Dependent Formaldehyde Dehydrogenase: Protein Sequence and Catalytic Properties. Planta, 208, 12-18.
http://dx.doi.org/10.1007/s004250050529
[62] Ravanel, S., Gambonnet, B., Douce, R. and Rébeillé, F. (2003) One-Carbon Metabolism in Plants. Regulation of Tetra-hydrofolate Synthesis during Germination and Seedling Development. Plant Physiology, 131, 1431-1439.
http://dx.doi.org/10.1104/pp.016915

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