- -

Folate Metabolism Interferes with Plant Immunity through 1C Methionine Synthase-Directed Genome-wide DNA Methylation Enhancement

RiuNet: Institutional repository of the Polithecnic University of Valencia

Share/Send to

Cited by


Folate Metabolism Interferes with Plant Immunity through 1C Methionine Synthase-Directed Genome-wide DNA Methylation Enhancement

Show full item record

González, B.; Vera Vera, P. (2019). Folate Metabolism Interferes with Plant Immunity through 1C Methionine Synthase-Directed Genome-wide DNA Methylation Enhancement. Molecular Plant. 12(9):1227-1242. https://doi.org/10.1016/j.molp.2019.04.013

Por favor, use este identificador para citar o enlazar este ítem: http://hdl.handle.net/10251/159603

Files in this item

Item Metadata

Title: Folate Metabolism Interferes with Plant Immunity through 1C Methionine Synthase-Directed Genome-wide DNA Methylation Enhancement
Author: González, Beatriz Vera Vera, Pablo
UPV Unit: Universitat Politècnica de València. Instituto Universitario Mixto de Biología Molecular y Celular de Plantas - Institut Universitari Mixt de Biologia Molecular i Cel·lular de Plantes
Issued date:
[EN] Plants rely on primary metabolism for flexible adaptation to environmental changes. Here, through a combination of chemical genetics and forward genetic studies in Arabidopsis plants, we identified that the essential ...[+]
Subjects: Folate pathway , Plant immunity , Methionine , DNA methylation
Copyrigths: Reconocimiento (by)
Molecular Plant. (issn: 1674-2052 )
DOI: 10.1016/j.molp.2019.04.013
Publisher version: https://doi.org/10.1016/j.molp.2019.04.013
Project ID:
Ministerio de Ciencia, Innovación y Universidades/RTI2018-098501-B-I00
We acknowledge V. Flors for the determination of SA level, S. Tarraga for the 2D-DIGE analysis and selection of spots proteins, and the SCSIE_University of Valencia Proteomics Unit for MS-MALDI-TOF/TOF and/or LC-MS/MS ...[+]
Type: Artículo


Agorio, A., & Vera, P. (2007). ARGONAUTE4 Is Required for Resistance to Pseudomonas syringae in Arabidopsis. The Plant Cell, 19(11), 3778-3790. doi:10.1105/tpc.107.054494

Ahuja, I., Kissen, R., & Bones, A. M. (2012). Phytoalexins in defense against pathogens. Trends in Plant Science, 17(2), 73-90. doi:10.1016/j.tplants.2011.11.002

Asai, T., Tena, G., Plotnikova, J., Willmann, M. R., Chiu, W.-L., Gomez-Gomez, L., … Sheen, J. (2002). MAP kinase signalling cascade in Arabidopsis innate immunity. Nature, 415(6875), 977-983. doi:10.1038/415977a [+]
Agorio, A., & Vera, P. (2007). ARGONAUTE4 Is Required for Resistance to Pseudomonas syringae in Arabidopsis. The Plant Cell, 19(11), 3778-3790. doi:10.1105/tpc.107.054494

Ahuja, I., Kissen, R., & Bones, A. M. (2012). Phytoalexins in defense against pathogens. Trends in Plant Science, 17(2), 73-90. doi:10.1016/j.tplants.2011.11.002

Asai, T., Tena, G., Plotnikova, J., Willmann, M. R., Chiu, W.-L., Gomez-Gomez, L., … Sheen, J. (2002). MAP kinase signalling cascade in Arabidopsis innate immunity. Nature, 415(6875), 977-983. doi:10.1038/415977a

Beckers, G. J. M., Jaskiewicz, M., Liu, Y., Underwood, W. R., He, S. Y., Zhang, S., & Conrath, U. (2009). Mitogen-Activated Protein Kinases 3 and 6 Are Required for Full Priming of Stress Responses in Arabidopsis thaliana    . The Plant Cell, 21(3), 944-953. doi:10.1105/tpc.108.062158

Berger, S., Papadopoulos, M., Schreiber, U., Kaiser, W., & Roitsch, T. (2004). Complex regulation of gene expression, photosynthesis and sugar levels by pathogen infection in tomato. Physiologia Plantarum, 122(4), 419-428. doi:10.1111/j.1399-3054.2004.00433.x

BILGIN, D. D., ZAVALA, J. A., ZHU, J., CLOUGH, S. J., ORT, D. R., & DeLUCIA, E. H. (2010). Biotic stress globally downregulates photosynthesis genes. Plant, Cell & Environment, 33(10), 1597-1613. doi:10.1111/j.1365-3040.2010.02167.x

Bolton, M. D. (2009). Primary Metabolism and Plant Defense—Fuel for the Fire. Molecular Plant-Microbe Interactions®, 22(5), 487-497. doi:10.1094/mpmi-22-5-0487

Camañes, G., Pastor, V., Cerezo, M., García-Andrade, J., Vicedo, B., García-Agustín, P., & Flors, V. (2011). A Deletion in NRT2.1 Attenuates Pseudomonas syringae-Induced Hormonal Perturbation, Resulting in Primed Plant Defenses    . Plant Physiology, 158(2), 1054-1066. doi:10.1104/pp.111.184424

Cao, H., Glazebrook, J., Clarke, J. D., Volko, S., & Dong, X. (1997). The Arabidopsis NPR1 Gene That Controls Systemic Acquired Resistance Encodes a Novel Protein Containing Ankyrin Repeats. Cell, 88(1), 57-63. doi:10.1016/s0092-8674(00)81858-9

Chen, Y., Zou, T., & McCormick, S. (2016). S-Adenosylmethionine Synthetase 3 Is Important for Pollen Tube Growth. Plant Physiology, 172(1), 244-253. doi:10.1104/pp.16.00774

Coego, A., Ramirez, V., Ellul, P., Mayda, E., & Vera, P. (2005). The H2O2-regulated Ep5C gene encodes a peroxidase required for bacterial speck susceptibility in tomato. The Plant Journal, 42(2), 283-293. doi:10.1111/j.1365-313x.2005.02372.x

Cokus, S. J., Feng, S., Zhang, X., Chen, Z., Merriman, B., Haudenschild, C. D., … Jacobsen, S. E. (2008). Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature, 452(7184), 215-219. doi:10.1038/nature06745

Conrath, U., Beckers, G. J. M., Langenbach, C. J. G., & Jaskiewicz, M. R. (2015). Priming for Enhanced Defense. Annual Review of Phytopathology, 53(1), 97-119. doi:10.1146/annurev-phyto-080614-120132

Denoux, C., Galletti, R., Mammarella, N., Gopalan, S., Werck, D., De Lorenzo, G., … Dewdney, J. (2008). Activation of Defense Response Pathways by OGs and Flg22 Elicitors in Arabidopsis Seedlings. Molecular Plant, 1(3), 423-445. doi:10.1093/mp/ssn019

Dobón, A., Canet, J. V., García-Andrade, J., Angulo, C., Neumetzler, L., Persson, S., & Vera, P. (2015). Novel Disease Susceptibility Factors for Fungal Necrotrophic Pathogens in Arabidopsis. PLOS Pathogens, 11(4), e1004800. doi:10.1371/journal.ppat.1004800

Dong, X. (2004). NPR1, all things considered. Current Opinion in Plant Biology, 7(5), 547-552. doi:10.1016/j.pbi.2004.07.005

Dowen, R. H., Pelizzola, M., Schmitz, R. J., Lister, R., Dowen, J. M., Nery, J. R., … Ecker, J. R. (2012). Widespread dynamic DNA methylation in response to biotic stress. Proceedings of the National Academy of Sciences, 109(32), E2183-E2191. doi:10.1073/pnas.1209329109

Ferrer, J.-L., Ravanel, S., Robert, M., & Dumas, R. (2004). Crystal Structures of Cobalamin-independent Methionine Synthase Complexed with Zinc, Homocysteine, and Methyltetrahydrofolate. Journal of Biological Chemistry, 279(43), 44235-44238. doi:10.1074/jbc.c400325200

Gallardo, K., Job, C., Groot, S. P. C., Puype, M., Demol, H., Vandekerckhove, J., & Job, D. (2002). Importance of methionine biosynthesis for Arabidopsis seed germination and seedling growth. Physiologia Plantarum, 116(2), 238-247. doi:10.1034/j.1399-3054.2002.1160214.x

García-Andrade, J., Ramírez, V., López, A., & Vera, P. (2013). Mediated Plastid RNA Editing in Plant Immunity. PLoS Pathogens, 9(10), e1003713. doi:10.1371/journal.ppat.1003713

Gerber, I. B., Laukens, K., De Vijlder, T., Witters, E., & Dubery, I. A. (2008). Proteomic profiling of cellular targets of lipopolysaccharide-induced signalling in Nicotiana tabacum BY-2 cells. Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, 1784(11), 1750-1762. doi:10.1016/j.bbapap.2008.06.012

Giovanelli, J., Mudd, S. H., & Datko, A. H. (1985). Quantitative Analysis of Pathways of Methionine Metabolism and Their Regulation in Lemna. Plant Physiology, 78(3), 555-560. doi:10.1104/pp.78.3.555

Groth, M., Moissiard, G., Wirtz, M., Wang, H., Garcia-Salinas, C., Ramos-Parra, P. A., … Jacobsen, S. E. (2016). MTHFD1 controls DNA methylation in Arabidopsis. Nature Communications, 7(1). doi:10.1038/ncomms11640

Hardham, A. R., Jones, D. A., & Takemoto, D. (2007). Cytoskeleton and cell wall function in penetration resistance. Current Opinion in Plant Biology, 10(4), 342-348. doi:10.1016/j.pbi.2007.05.001

Ishikawa, T., Machida, C., Yoshioka, Y., Kitano, H., & Machida, Y. (2003). TheGLOBULAR ARREST1gene, which is involved in the biosynthesis of folates, is essential for embryogenesis inArabidopsis thaliana. The Plant Journal, 33(2), 235-244. doi:10.1046/j.1365-313x.2003.01621.x

Jones, J. D. G., & Dangl, J. L. (2006). The plant immune system. Nature, 444(7117), 323-329. doi:10.1038/nature05286

Jordá, L., Coego, A., Conejero, V., & Vera, P. (1999). A Genomic Cluster Containing Four Differentially Regulated Subtilisin-like Processing Protease Genes Is in Tomato Plants. Journal of Biological Chemistry, 274(4), 2360-2365. doi:10.1074/jbc.274.4.2360

Kangasjarvi, S., Neukermans, J., Li, S., Aro, E.-M., & Noctor, G. (2012). Photosynthesis, photorespiration, and light signalling in defence responses. Journal of Experimental Botany, 63(4), 1619-1636. doi:10.1093/jxb/err402

Loenen, W. A. M. (2006). S-Adenosylmethionine: jack of all trades and master of everything? Biochemical Society Transactions, 34(2), 330-333. doi:10.1042/bst0340330

Loizeau, K., De Brouwer, V., Gambonnet, B., Yu, A., Renou, J.-P., Van Der Straeten, D., … Ravanel, S. (2008). A Genome-Wide and Metabolic Analysis Determined the Adaptive Response of Arabidopsis Cells to Folate Depletion Induced by Methotrexate. Plant Physiology, 148(4), 2083-2095. doi:10.1104/pp.108.130336

Loizeau, K., Gambonnet, B., Zhang, G.-F., Curien, G., Jabrin, S., Van Der Straeten, D., … Ravanel, S. (2007). Regulation of One-Carbon Metabolism in Arabidopsis: The N-Terminal Regulatory Domain of Cystathionine γ-Synthase Is Cleaved in Response to Folate Starvation. Plant Physiology, 145(2), 491-503. doi:10.1104/pp.107.105379

López, A., Ramírez, V., García-Andrade, J., Flors, V., & Vera, P. (2011). The RNA Silencing Enzyme RNA Polymerase V Is Required for Plant Immunity. PLoS Genetics, 7(12), e1002434. doi:10.1371/journal.pgen.1002434

Luna, E., Bruce, T. J. A., Roberts, M. R., Flors, V., & Ton, J. (2011). Next-Generation Systemic Acquired Resistance    . Plant Physiology, 158(2), 844-853. doi:10.1104/pp.111.187468

Luna, E., Pastor, V., Robert, J., Flors, V., Mauch-Mani, B., & Ton, J. (2011). Callose Deposition: A Multifaceted Plant Defense Response. Molecular Plant-Microbe Interactions®, 24(2), 183-193. doi:10.1094/mpmi-07-10-0149

Martinez-Medina, A., Flors, V., Heil, M., Mauch-Mani, B., Pieterse, C. M. ., Pozo, M. J., … Conrath, U. (2016). Recognizing Plant Defense Priming. Trends in Plant Science, 21(10), 818-822. doi:10.1016/j.tplants.2016.07.009

Mauch-Mani, B., Baccelli, I., Luna, E., & Flors, V. (2017). Defense Priming: An Adaptive Part of Induced Resistance. Annual Review of Plant Biology, 68(1), 485-512. doi:10.1146/annurev-arplant-042916-041132

McCullough, J. L., & Maren, T. H. (1973). Inhibition of Dihydropteroate Synthetase from Escherichia coli by Sulfones and Sulfonamides. Antimicrobial Agents and Chemotherapy, 3(6), 665-669. doi:10.1128/aac.3.6.665

Návarová, H., Bernsdorff, F., Döring, A.-C., & Zeier, J. (2012). Pipecolic Acid, an Endogenous Mediator of Defense Amplification and Priming, Is a Critical Regulator of Inducible Plant Immunity. The Plant Cell, 24(12), 5123-5141. doi:10.1105/tpc.112.103564

Noutoshi, Y., Ikeda, M., Saito, T., Osada, H., & Shirasu, K. (2012). Sulfonamides identified as plant immune-priming compounds in high-throughput chemical screening increase disease resistance in Arabidopsis thaliana. Frontiers in Plant Science, 3. doi:10.3389/fpls.2012.00245

Pato, M. L., & Brown, G. M. (1963). Mechanisms of resistance of Escherichia coli to sulfonamides. Archives of Biochemistry and Biophysics, 103(3), 443-448. doi:10.1016/0003-9861(63)90435-1

Pavet, V., Quintero, C., Cecchini, N. M., Rosa, A. L., & Alvarez, M. E. (2006). ArabidopsisDisplays Centromeric DNA Hypomethylation and Cytological Alterations of Heterochromatin Upon Attack byPseudomonas syringae. Molecular Plant-Microbe Interactions®, 19(6), 577-587. doi:10.1094/mpmi-19-0577

Pieterse, C. M. J., Van der Does, D., Zamioudis, C., Leon-Reyes, A., & Van Wees, S. C. M. (2012). Hormonal Modulation of Plant Immunity. Annual Review of Cell and Developmental Biology, 28(1), 489-521. doi:10.1146/annurev-cellbio-092910-154055

Prabhu, V., Lui, H., & King, J. (1997). Arabidopsis dihydropteroate synthase: General properties and inhibition by reaction product and sulfonamides. Phytochemistry, 45(1), 23-27. doi:10.1016/s0031-9422(96)00793-5

Ramírez, V., González, B., López, A., Castelló, M. J., Gil, M. J., Zheng, B., … Vera, P. (2018). A 2′-O-Methyltransferase Responsible for Transfer RNA Anticodon Modification Is Pivotal for Resistance to Pseudomonas syringae DC3000 in Arabidopsis. Molecular Plant-Microbe Interactions®, 31(12), 1323-1336. doi:10.1094/mpmi-06-18-0148-r

Ramírez, V., López, A., Mauch-Mani, B., Gil, M. J., & Vera, P. (2013). An Extracellular Subtilase Switch for Immune Priming in Arabidopsis. PLoS Pathogens, 9(6), e1003445. doi:10.1371/journal.ppat.1003445

Ravanel, S., Block, M. A., Rippert, P., Jabrin, S., Curien, G., Rébeillé, F., & Douce, R. (2004). Methionine Metabolism in Plants. Journal of Biological Chemistry, 279(21), 22548-22557. doi:10.1074/jbc.m313250200

Ravanel, S., Gakiere, B., Job, D., & Douce, R. (1998). The specific features of methionine biosynthesis and metabolism in plants. Proceedings of the National Academy of Sciences, 95(13), 7805-7812. doi:10.1073/pnas.95.13.7805

Rocha, P. S. C. F., Sheikh, M., Melchiorre, R., Fagard, M., Boutet, S., Loach, R., … Furner, I. (2005). The Arabidopsis HOMOLOGY-DEPENDENT GENE SILENCING1 Gene Codes for an S-Adenosyl-l-Homocysteine Hydrolase Required for DNA Methylation-Dependent Gene Silencing. The Plant Cell, 17(2), 404-417. doi:10.1105/tpc.104.028332

Roje, S. (2006). S-Adenosyl-l-methionine: Beyond the universal methyl group donor. Phytochemistry, 67(15), 1686-1698. doi:10.1016/j.phytochem.2006.04.019

Schreiber, K., Ckurshumova, W., Peek, J., & Desveaux, D. (2008). A high-throughput chemical screen for resistance to Pseudomonas syringae in Arabidopsis. The Plant Journal, 54(3), 522-531. doi:10.1111/j.1365-313x.2008.03425.x

Shen, Y., Issakidis-Bourguet, E., & Zhou, D.-X. (2016). Perspectives on the interactions between metabolism, redox, and epigenetics in plants. Journal of Experimental Botany, 67(18), 5291-5300. doi:10.1093/jxb/erw310

Slaughter, A., Daniel, X., Flors, V., Luna, E., Hohn, B., & Mauch-Mani, B. (2011). Descendants of Primed Arabidopsis Plants Exhibit Resistance to Biotic Stress    . Plant Physiology, 158(2), 835-843. doi:10.1104/pp.111.191593

Storozhenko, S., Navarrete, O., Ravanel, S., De Brouwer, V., Chaerle, P., Zhang, G.-F., … Van Der Straeten, D. (2007). Cytosolic Hydroxymethyldihydropterin Pyrophosphokinase/Dihydropteroate Synthase from Arabidopsis thaliana. Journal of Biological Chemistry, 282(14), 10749-10761. doi:10.1074/jbc.m701158200

Torres, M. A. (2010). ROS in biotic interactions. Physiologia Plantarum, 138(4), 414-429. doi:10.1111/j.1399-3054.2009.01326.x

Tóth, R., & van der Hoorn, R. A. L. (2010). Emerging principles in plant chemical genetics. Trends in Plant Science, 15(2), 81-88. doi:10.1016/j.tplants.2009.11.005

Urich, M. A., Nery, J. R., Lister, R., Schmitz, R. J., & Ecker, J. R. (2015). MethylC-seq library preparation for base-resolution whole-genome bisulfite sequencing. Nature Protocols, 10(3), 475-483. doi:10.1038/nprot.2014.114

Van Loon, L. C., Rep, M., & Pieterse, C. M. J. (2006). Significance of Inducible Defense-related Proteins in Infected Plants. Annual Review of Phytopathology, 44(1), 135-162. doi:10.1146/annurev.phyto.44.070505.143425

Vlot, A. C., Dempsey, D. A., & Klessig, D. F. (2009). Salicylic Acid, a Multifaceted Hormone to Combat Disease. Annual Review of Phytopathology, 47(1), 177-206. doi:10.1146/annurev.phyto.050908.135202

Wildermuth, M. C., Dewdney, J., Wu, G., & Ausubel, F. M. (2001). Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature, 414(6863), 562-565. doi:10.1038/35107108

Yu, A., Lepere, G., Jay, F., Wang, J., Bapaume, L., Wang, Y., … Navarro, L. (2013). Dynamics and biological relevance of DNA demethylation in Arabidopsis antibacterial defense. Proceedings of the National Academy of Sciences, 110(6), 2389-2394. doi:10.1073/pnas.1211757110

ZEIER, J. (2013). New insights into the regulation of plant immunity by amino acid metabolic pathways. Plant, Cell & Environment, 36(12), 2085-2103. doi:10.1111/pce.12122

Zhang, H., Deng, X., Miki, D., Cutler, S., La, H., Hou, Y.-J., … Zhu, J.-K. (2012). Sulfamethazine Suppresses Epigenetic Silencing in Arabidopsis by Impairing Folate Synthesis. The Plant Cell, 24(3), 1230-1241. doi:10.1105/tpc.112.096149

Zhang, X., Yazaki, J., Sundaresan, A., Cokus, S., Chan, S. W.-L., Chen, H., … Ecker, J. R. (2006). Genome-wide High-Resolution Mapping and Functional Analysis of DNA Methylation in Arabidopsis. Cell, 126(6), 1189-1201. doi:10.1016/j.cell.2006.08.003

Zhou, H.-R., Zhang, F.-F., Ma, Z.-Y., Huang, H.-W., Jiang, L., Cai, T., … He, X.-J. (2013). Folate Polyglutamylation Is Involved in Chromatin Silencing by Maintaining Global DNA Methylation and Histone H3K9 Dimethylation in Arabidopsis. The Plant Cell, 25(7), 2545-2559. doi:10.1105/tpc.113.114678




This item appears in the following Collection(s)

Show full item record