The phosphorylated pathway of serine biosynthesis is essential both for male gametophyte and embryo development and for root growth in Arabidopsis

Cascales - Miñana, Borja; Muñoz-Bertomeu, J.; Flores-Tornero, M.; Anoman, A. D.; Pertusa, J.; Alaiz, M.; Osorio, S.; Fernie, A. R.; Segura, J.; Ros, R.

doi:10.1105/tpc.113.112359

Article (Scientific journals)

The phosphorylated pathway of serine biosynthesis is essential both for male gametophyte and embryo development and for root growth in Arabidopsis

Cascales - Miñana, Borja; Muñoz-Bertomeu, J.; Flores-Tornero, M. et al.

2013 • In Plant Cell, 25 (6), p. 2084-2101

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https://hdl.handle.net/2268/176022

DOI
10.1105/tpc.113.112359

PubMed
23771893

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Keywords :

Arabidopsis protein; PSP1 protein, Arabidopsis; Arabidopsis; Amino Acids; Arabidopsis Proteins; Biosynthetic Pathways; Citric Acid Cycle; Gene Expression Regulation, Developmental; Gene Expression Regulation, Plant; Glycolysis; Green Fluorescent Proteins; Immunoblotting; Microscopy, Electron, Transmission; Microscopy, Fluorescence; Mutation; Phosphoric Monoester Hydrolases; Phosphorylation; Plant Roots; Plants, Genetically Modified; Pollen; Reverse Transcriptase Polymerase Chain Reaction; Seeds; Serine

Abstract :

[en] This study characterizes the phosphorylated pathway of Ser biosynthesis (PPSB) in Arabidopsis thaliana by targeting phosphoserine phosphatase (PSP1), the last enzyme of the pathway. Lack of PSP1 activity delayed embryo development, leading to aborted embryos that could be classified as early curled cotyledons. The embryo-lethal phenotype of psp1 mutants could be complemented with PSP1 cDNA under the control of Pro35S (Pro35S:PSP1). However, this construct, which was poorly expressed in the anther tapetum, did not complement mutant fertility. Microspore development in psp1.1/psp1.1 Pro35S:PSP1 arrested at the polarized stage. The tapetum from these lines displayed delayed and irregular development. The expression of PSP1 in the tapetum at critical stages of microspore development suggests that PSP1 activity in this cell layer is essential in pollen development. In addition to embryo death and male sterility, conditional psp1 mutants displayed a shortroot phenotype, which was reverted in the presence of Ser. A metabolomic study demonstrated that the PPSB plays a crucial role in plant metabolism by affecting glycolysis, the tricarboxylic acid cycle, and the biosynthesis of amino acids. We provide evidence of the crucial role of the PPSB in embryo, pollen, and root development and suggest that this pathway is an important link connecting primary metabolism with development. © 2013 American Society of Plant Biologists. All rights reserved.

Disciplines :

Phytobiology (plant sciences, forestry, mycology...)

Author, co-author :

Cascales - Miñana, Borja ; Departament de Biologia Vegetal, Facultat de Farmàcia, Universitat de València, Burjassot, Valencia, Spain

Muñoz-Bertomeu, J.; Departament de Biologia Vegetal, Universitat de València, 46100 Burjassot (Valencia), Spain, Instituto de Biología Molecular y Celular de Plantas, Departamento Biotecnología, Universidad Politécnica de Valencia-Consejo Superior de Investigaciones Cientificas, C/Ingeniero Fausto Elio, 46022 Valencia, Spain

Flores-Tornero, M.; Departament de Biologia Vegetal, Universitat de València, 46100 Burjassot (Valencia), Spain

Anoman, A. D.; Departament de Biologia Vegetal, Universitat de València, 46100 Burjassot (Valencia), Spain

Pertusa, J.; Departament de Biologia Funcional i Antropologia Física, Universitat de València, 46100 Valencia, Spain

Alaiz, M.; Grupo de Componentes Bioactivos y Funcionales de Productos Vegetales, Departamento de Fisiología y Tecnología de Productos Vegetales, Instituto de la Grasa, Consejo Superior de Investigaciones Científicas, 41012 Seville, Spain

Osorio, S.; Max Planck Institut für Molekulare Pflanzenphysiologie, 14476 Potsdam-Golm, Germany

Fernie, A. R.; Max Planck Institut für Molekulare Pflanzenphysiologie, 14476 Potsdam-Golm, Germany

Segura, J.; Departament de Biologia Vegetal, Universitat de València, 46100 Burjassot (Valencia), Spain

Ros, R.; Departament de Biologia Vegetal, Universitat de València, 46100 Burjassot (Valencia), Spain

Language :

English

Title :

The phosphorylated pathway of serine biosynthesis is essential both for male gametophyte and embryo development and for root growth in Arabidopsis

Publication date :

2013

Journal title :

Plant Cell

ISSN :

1040-4651

eISSN :

1532-298X

Publisher :

American Society of Plant Biologists, Rockville, United States - Maryland

Volume :

Issue :

Pages :

2084-2101

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 08 January 2015

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Bibliography

Alonso, J.M., et al. (2003). Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657.
Bachelor, M.A., Lu, Y., and Owens, D.M. (2011). L-3-phosphoserine phosphatase (PSPH) regulates cutaneous squamous cell carcinoma proliferation independent of L-serine biosynthesis. J. Dermatol. Sci. 63: 164-172.
Bauwe, H., Hagemann, M., and Fernie, A.R. (2010). Photorespiration: Players, partners and origin. Trends Plant Sci. 15: 330-336.
Boavida, L.C., and McCormick, S. (2007). Temperature as a determinant factor for increased and reproducible in vitro pollen germination in Arabidopsis thaliana. Plant J. 52: 570-582.
Capron, A., Chatfield, S., Provart, N., and Berleth, T. (2009). Embryogenesis: Pattern formation from a single cell. The Arabidopsis Book 7: e0126, doi/10.1199/tab.0126.
Clough, S.J., and Bent, A.F. (1998). Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16: 735-743.
Colcombet, J., Boisson-Dernier, A., Ros-Palau, R., Vera, C.E., and Schroeder, J.I. (2005). Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASES1 and 2 are essential for tapetum development and microspore maturation. Plant Cell 17: 3350-3361.
Curtis, M.D., and Grossniklaus, U. (2003). A Gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol. 133: 462-469.
Czechowski, T., Stitt, M., Altmann, T., Udvardi, M.K., and Scheible, W.R. (2005). Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol. 139: 5-17.
Devic, M. (2008). The importance of being essential: EMBRYODEFECTIVE genes in Arabidopsis. C. R. Biol. 331: 726-736.
Douce, R., Bourguignon, J., Neuburger, M., and Rébeillé, F. (2001). The glycine decarboxylase system: A fascinating complex. Trends Plant Sci. 6: 167-176.
Eichler, H.G., Hubbard, R., and Snell, K. (1981). The role of serine hydroxymethyltransferase in cell proliferation: DNA synthesis from serine following mitogenic stimulation of lymphocytes. Biosci. Rep. 1: 101-106.
Ge, X., Chang, F., and Ma, H. (2010). Signaling and transcriptional control of reproductive development in Arabidopsis. Curr. Biol. 20: R988-R997.
Grienenberger, E., Besseau, S., Geoffroy, P., Debayle, D., Heintz, D., Lapierre, C., Pollet, B., Heitz, T., and Legrand, M. (2009). A BAHD acyltransferase is expressed in the tapetum of Arabidopsis anthers and is involved in the synthesis of hydroxycinnamoyl spermidines. Plant J. 58: 246-259.
Handford, J., and Davies, D.D. (1958). Formation of phosphoserine from 3-phopho-glycerate in higher plants. Nature 182: 532-533.
Hanson, A.D., and Gregory, J.F., III., (2011). Folate biosynthesis, turnover, and transport in plants. Annu. Rev. Plant Biol. 62: 105-125.
Hanson, A.D., and Roje, S. (2001). One-carbon metabolism in higher plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52: 119-137.
Ho, C.L., Noji, M., and Saito, K. (1999a). Plastidic pathway of serine biosynthesis. Molecular cloning and expression of 3-phosphoserine phosphatase from Arabidopsis thaliana. J. Biol. Chem. 274: 11007-11012.
Ho, C.L., Noji, M., Saito, M., and Saito, K. (1999b). Regulation of serine biosynthesis in Arabidopsis. Crucial role of plastidic 3- phosphoglycerate dehydrogenase in non-photosynthetic tissues. J. Biol. Chem. 274: 397-402.
Ho, C.L., Noji, M., Saito, M., Yamazaki, M., and Saito, K. (1998). Molecular characterization of plastidic phosphoserine aminotransferase in serine biosynthesis from Arabidopsis. Plant J. 16: 443-452.
Ho, C.L., and Saito, K. (2001). Molecular biology of the plastidic phosphorylated serine biosynthetic pathway in Arabidopsis thaliana. Amino Acids 20: 243-259.
Hunt, E., Gattolin, S., Newbury, H.J., Bale, J.S., Tseng, H.M., Barrett, D.A., and Pritchard, J. (2010). A mutation in amino acid permease AAP6 reduces the amino acid content of the Arabidopsis sieve elements but leaves aphid herbivores unaffected. J. Exp. Bot. 61: 55-64.
Kalhan, S.C., and Hanson, R.W. (2012). Resurgence of serine: An often neglected but indispensable amino acid. J. Biol. Chem. 287: 19786-19791.
Kawanabe, T., Ariizumi, T., Kawai-Yamada, M., Uchimiya, H., and Toriyama, K. (2006). Abolition of the tapetum suicide program ruins microsporogenesis. Plant Cell Physiol. 47: 784-787.
Kleczkowski, L.A., and Givan, C.V. (1988). Serine formation in leaves by mechanisms other than the glycolate pathway. J. Plant Physiol. 132: 641-652.
Lam, H.M., Coschigano, K.T., Oliveira, I.C., Melo-Oliveira, R., and Coruzzi, G.M. (1996). The molecular-genetics of nitrogen assimilation into amino acids in higher plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47: 569-593.
Larsson, C., and Albertsson, E. (1979). Enzymes related to serine synthesis in spinach chloroplasts. Physiol. Plant. 45: 7-10.
Lisec, J., Schauer, N., Kopka, J., Willmitzer, L., and Fernie, A.R. (2006). Gas chromatography mass spectrometry-based metabolite profiling in plants. Nat. Protoc. 1: 387-396.
Locasale, J.W., et al. (2011). Phosphoglycerate dehydrogenase diverts glycolytic flux and contributes to oncogenesis. Nat. Genet. 43: 869-874.
Matsuhara, S., Jingu, F., Takahashi, T., and Komeda, Y. (2000). Heat-shock tagging: A simple method for expression and isolation of plant genome DNA flanked by T-DNA insertions. Plant J. 22: 79-86.
Maurino, V.G., and Peterhansel, C. (2010). Photorespiration: Current status and approaches for metabolic engineering. Curr. Opin. Plant Biol. 13: 249-256.
Michard, E., Lima, P.T., Borges, F., Silva, A.C., Portes, M.T., Carvalho, J.E., Gilliham, M., Liu, L.H., Obermeyer, G., and Feijó, J.A. (2011). Glutamate receptor-like genes form Ca2+ channels in pollen tubes and are regulated by pistil D-serine. Science 332: 434-437.
Mothet, J.P., Parent, A.T., Wolosker, H., Brady, R.O., Jr., Linden, D.J., Ferris, C.D., Rogawski, M.A., and Snyder, S.H. (2000). D-serine is an endogenous ligand for the glycine site of the N-methyl-D-aspartate receptor. Proc. Natl. Acad. Sci. USA 97: 4926-4931.
Muñoz-Bertomeu, J., Anoman, A.D., Toujani, W., Cascales- Miñana, B., Flores-Tornero, M., and Ros, R. (2011a). Interactions between abscisic acid and plastidial glycolysis in Arabidopsis. Plant Signal. Behav. 6: 157-159.
Muñoz-Bertomeu, J., Bermúdez, M.A., Segura, J., and Ros, R. (2011b). Arabidopsis plants deficient in plastidial glyceraldehyde-3- phosphate dehydrogenase show alterations in abscisic acid (ABA) signal transduction: interaction between ABA and primary metabolism. J. Exp. Bot. 62: 1229-1239.
Muñoz-Bertomeu, J., Cascales-Miñana, B., Alaiz, M., Segura, J., and Ros, R. (2010a). A critical role of plastidial glycolytic glyceraldehyde- 3-phosphate dehydrogenase in the control of plant metabolism and development. Plant Signal. Behav. 5: 67-69.
Muñoz-Bertomeu, J., Cascales-Miñana, B., Irles-Segura, A., Mateu, I., Nunes-Nesi, A., Fernie, A.R., Segura, J., and Ros, R. (2010b). The plastidial glyceraldehyde-3-phosphate dehydrogenase is critical for viable pollen development in Arabidopsis. Plant Physiol. 152: 1830-1841.
Muñoz-Bertomeu, J., Cascales-Miñana, B., Mulet, J.M., Baroja- Fernández, E., Pozueta-Romero, J., Kuhn, J.M., Segura, J., and Ros, R. (2009). Plastidial glyceraldehyde-3-phosphate dehydrogenase deficiency leads to altered root development and affects the sugar and amino acid balance in Arabidopsis. Plant Physiol. 151: 541-558.
Muralla, R., Lloyd, J., and Meinke, D. (2011). Molecular foundations of reproductive lethality in Arabidopsis thaliana. PLoS ONE 6: e28398.
Pfaffl, M.W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29: e45.
Pollari, S., Käkönen, S.M., Edgren, H., Wolf, M., Kohonen, P., Sara, H., Guise, T., Nees, M., and Kallioniemi, O. (2011). Enhanced serine production by bone metastatic breast cancer cells stimulates osteoclastogenesis. Breast Cancer Res. Treat. 125: 421-430.
Possemato, R., et al. (2011). Functional genomics reveal that the serine synthesis pathway is essential in breast cancer. Nature 476: 346-350.
Riens, B., Lohaus, G., Heineke, D., and Heldt, H.W. (1991). Amino acid and sucrose content determined in the cytosolic, chloroplastic, and vacuolar compartments and in the phloem sap of spinach leaves. Plant Physiol. 97: 227-233.
Sanders, P.M., Bui, A.Q., Weterings, K., McIntire, N., Hsu, Y.-C., Lee, P.Y., Truong, M.T., Beals, T.B., and Goldberg, R.B. (1999). Anther developmental defects in Arabidopsis thaliana male-sterile mutants. Sex. Plant Reprod. 11: 297-322.
Scholl, R.L., May, S.T., and Ware, D.H. (2000). Seed and molecular resources for Arabidopsis. Plant Physiol. 124: 1477-1480.
Slaughter, J.C., and Davies, D.D. (1968). The isolation and characterization of 3-phosphoglycerate dehydrogenase from peas. Biochem. J. 109: 743-748.
Smyth, D.R., Bowman, J.L., and Meyerowitz, E.M. (1990). Early flower development in Arabidopsis. Plant Cell 2: 755-767.
Till, B.J., et al. (2003). Large-scale discovery of induced point mutations with high-throughput TILLING. Genome Res. 13: 524-530.
Timm, S., Mielewczik, M., Florian, A., Frankenbach, S., Dreissen, A., Hocken, N., Fernie, A.R., Walter, A., and Bauwe, H. (2012). High-to-low CO2 acclimation reveals plasticity of the photorespiratory pathway and indicates regulatory links to cellular metabolism of Arabidopsis. PLoS ONE 7: e42809.
Tolbert, N.E. (1980). Photorespiration. In The Biochemistry of plants, D.D. Davies, ed (New York: Academic Press), pp. 488-525.
Tolbert, N.E. (1997). The C2 oxidative photosynthetic carbon cycle. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48: 1-25.
Walton, N.J., and Woolhouse, H.W. (1986). Enzymes of serine and glycine metabolism in leaves and nonphotosynthetic tissues of Pisum sativum L. Planta 167: 119-128.
Winter, D., Vinegar, B., Nahal, H., Ammar, R., Wilson, G.V., and Provart, N.J. (2007). An "Electronic Fluorescent Pictograph" browser for exploring and analyzing large-scale biological data sets. PLoS ONE 2: e718.
Yamaoka, Y., Yu, Y., Mizoi, J., Fujiki, Y., Saito, K., Nishijima, M., Lee, Y., and Nishida, I. (2011). PHOSPHATIDYLSERINE SYNTHASE1 is required for microspore development in Arabidopsis thaliana. Plant J. 67: 648-661.
Yang, C., Vizcay-Barrena, G., Conner, K., and Wilson, Z.A. (2007). MALE STERILITY1 is required for tapetal development and pollen wall biosynthesis. Plant Cell 19: 3530-3548.
Yoshida, K., Furuya, S., Osuka, S., Mitoma, J., Shinoda, Y., Watanabe, M., Azuma, N., Tanaka, H., Hashikawa, T., Itohara, S., and Hirabayashi, Y. (2004). Targeted disruption of the mouse 3-phosphoglycerate dehydrogenase gene causes severe neurodevelopmental defects and results in embryonic lethality. J. Biol. Chem. 279: 3573-3577.
Zhang, Y., Sun, K., Sandoval, F.J., Santiago, K., and Roje, S. (2010). One-carbon metabolism in plants: Characterization of a plastid serine hydroxymethyltransferase. Biochem. J. 430: 97-105.