Information de reference pour ce titreAccession Number: | 00008572-200811040-00011.
|
Author: | Murphy, Alex M. 1,*; Otto, Bettina 1; Brearley, Charles A. 2; Carr, John P. 1; Hanke, David E. 1
|
Institution: | (1)Department of Plant Sciences, University of Cambridge, Downing Street, Cambridge CB2 3EA, UK (2)Department of Biology, University of East Anglia, Norwich NR4 7TJ, UK
|
Title: | |
Source: | Plant Journal. 56(4):638-652, November 2008.
|
Abstract: | Summary: Phytic acid (myo-inositol hexakisphosphate, InsP6) is an important phosphate store and signal molecule in plants. However, low-phytate plants are being developed to minimize the negative health effects of dietary InsP6 and pollution caused by undigested InsP6 in animal waste. InsP6 levels were diminished in transgenic potato plants constitutively expressing an antisense gene sequence for myo-inositol 3-phosphate synthase (IPS, catalysing the first step in InsP6 biosynthesis) or Escherichia coli polyphosphate kinase. These plants were less resistant to the avirulent pathogen potato virus Y and the virulent pathogen tobacco mosaic virus (TMV). In Arabidopsis thaliana, mutation of the gene for the enzyme catalysing the final step of InsP6 biosynthesis (InsP5 2-kinase) also diminished InsP6 levels and enhanced susceptibility to TMV and to virulent and avirulent strains of the bacterial pathogen Pseudomonas syringae. Arabidopsis thaliana has three IPS genes (AtIPS1-3). Mutant atips2 plants were depleted in InsP6 and were hypersusceptible to TMV, turnip mosaic virus, cucumber mosaic virus and cauliflower mosaic virus as well as to the fungus Botrytis cinerea and to P. syringae. Mutant atips2 and atipk1 plants were as hypersusceptible to infection as plants unable to accumulate salicylic acid (SA) but their increased susceptibility was not due to reduced levels of SA. In contrast, mutant atips1 plants, which were also depleted in InsP6, were not compromised in resistance to pathogens, suggesting that a specific pool of InsP6 regulates defence against phytopathogens.
Copyright (C) 2008 Blackwell Publishing Ltd.
|
Author Keywords: | Inositol phosphates; defensive signalling; NahG; sid2.
|
References: | Abelson, P.H. (1999) A potential phosphate crisis. Science, 283, 2015.
AbuQamar, S., Chen, X., Dhawan, R., Bluhm, B., Salmeron, J., Lam, S., Dietrich, R.A. and Mengi, T. (2006) Expression profiling and mutant analysis reveals complex regulatory networks involved in Arabidopsis response to Botrytis infection. Plant J. 48, 28-44.
Alonso, J.M., Stepanova, A.N., Leisse, T.J. et al. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science, 301, 653-657.
Barbara, D.J. and Clark, M.F. (1982) A simple indirect ELISA using F(ab')2 fragments of immunoglobulin. J. Gen. Virol. 58, 315-322.
Bennett, M., Onnebo, S., Azevedo, C. and Saiardi, A. (2006) Inositol pyrophosphates: metabolism and signaling. CMLS Cell. Mol. Life Sci. 63, 552-564.
Bentsink, L., Yuan, K., Koorneef, M. and Vreugdenhil, D. (2003) The genetics of phytate and phosphate accumulation in seeds and leaves of Arabidopsis thaliana, using natural variation. Theor. Appl. Genet. 106, 1234-1243.
Bonaventure, G., Gfeller, A., Proebsting, W.M., Hortensteiner, S., Chetelat, A., Martinoia, E. and Farmer, E.E. (2007) A gain-of-function allele of TPC1 activates oxylipin biogenesis after leaf wounding in Arabidopsis. Plant J. 49, 889-898.
Brearley, C.A. and Hanke, D.E. (1996a) Inositol phosphates in barley (Hordeum vulgare L.) aleurone tissue are stereochemically similar to the products of breakdown of InsP6 in vitro by wheat-bran phytase. Biochem. J. 318, 279-286.
Brearley, C.A. and Hanke, D.E. (1996b) Inositol phosphates in the duckweed Spirodela polyrhiza L. Biochem. J. 314, 215-225.
Brearley, C.A. and Hanke, D.E. (1996c) Metabolic evidence for the order of addition of individual phosphate esters to the myo-inositol moiety of inositol hexakisphosphate in the duckweed Spirodela polyrhiza L. Biochem. J. 314, 227-233.
Bregitzer, P. and Raboy, V. (2006) Effects of four independent low-phytate mutations on barley agronomic performance. Crop Sci. 46, 1318-1322.
Carr, J.P. (2004) Tobacco mosaic virus. In Plant-Pathogen Interactions. Annual Plant Reviews (Talbot, N.J., ed.). Oxford: Blackwell, pp. 27-67.
Cecchini, E., Al-Kaff, N., Bannister, A., Giannakou, M., McCallum, D., Maule, A., Milner, J. and Covey, S. (1998) Pathogenic interactions between variants of cauliflower mosaic virus and Arabidopsis thaliana. J. Exp. Bot. 49, 731-737.
Chivasa, S., Murphy, A.M., Naylor, M. and Carr, J.P. (1997) Salicylic acid interferes with Tobacco mosaic virus replication via a novel salicylhydroxamic acid-sensitive mechanism. Plant Cell, 9, 547-557.
Crawford, N.M. and Guo, F.-Q. (2005) New insights into nitric oxide metabolism and regulatory functions. Trends Plant Sci. 10, 195-200.
Dardick, C.D., Golem, S. and Culver, J.N. (2000) Susceptibility and symptom development in Arabidopsis thaliana to Tobacco mosaic virus is influenced by virus cell-to-cell movement. Mol. Plant Microbe Interact. 13, 1139-1144.
Delaney, T.P., Uknes, S., Vernooij, B. et al. (1994) A central role of salicylic acid in plant disease resistance. Science, 266, 1247-1250.
Delledonne, M., Xia, Y., Dixon, R.A. and Lamb, C. (1998) Nitric oxide functions as a signal in plant disease resistance. Nature, 394, 585-588.
Delledonne, M., Zeier, J., Marocco, A. and Lamb, C. (2001) Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proc. Natl Acad. Sci. USA, 98, 13454-13459.
Devoto, A., Ellis, C., Magusin, A., Chang, H., Chilcott, C., Zhu, T. and Turner, J. (2005) Expression profiling reveals COI1 to be a key regulator of genes involved in wound- and methyl jasmonate-induced secondary metabolism, defence, and hormone interactions. Plant Mol. Biol. 58, 497-513.
Dharmasiri, N., Dharmasiri, S. and Estelle, M. (2005) The F-box protein TIR1 is an auxin receptor. Nature, 435, 441-445.
Donahue, T.F. and Henry, S.A. (1981) myo-Inositol-1-phosphate synthase. Characteristics of the enzyme and identification of its structural gene in yeast. J. Biol. Chem. 256, 7077-7085.
Durner, J., Wendehenne, D. and Klessig, D.F. (1998) Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose. Proc. Natl Acad. Sci. USA, 95, 10328-10333.
Ertl, D.S., Young, K.A. and Raboy, V. (1998) Plant genetic approaches to phosphorus management in agricultural production. J. Environ. Qual. 27, 299-304.
Ferrari, S., Plotnikova, J.M., Lorenzo, G.D. and Ausubel, F.M. (2003) Arabidopsis local resistance to Botrytis cinerea involves salicylic acid and camalexin and requires EDS4 and PAD2, but not SID2, EDS5 or PAD4. Plant J. 35, 193-205.
Gaffney, T., Friedrich, L., Vernooij, B., Negrotto, D., Nye, G., Uknes, S., Ward, E., Kessmann, H. and Ryals, J. (1993) Requirement of salicylic acid for the induction of systemic acquired resistance. Science, 261, 754-756.
Garcia-Mata, C., Gay, R., Sokolovski, S., Hills, A., Lamattina, L. and Blatt, M.R. (2003) Nitric oxide regulates K+ and Cl+ channels in guard cells through a subset of abscisic acid-evoked signaling pathways. Proc. Natl Acad. Sci. USA, 100, 11116-11121.
Guo, F.-Q., Okamoto, M. and Crawford, N.M. (2003) Identification of a plant nitric oxide synthase gene involved in hormonal signaling. Science, 302, 100-103.
Hanakahi, L.A., Bartlett-Jones, M., Chappell, C., Pappin, D. and West, S.C. (2000) Binding of inositol phosphate to DNA-PK and stimulation of double-strand break repair. Cell, 102, 721-729.
Handford, M.G. and Carr, J.P. (2007) A defect in carbohydrate metabolism ameliorates symptom severity in virus-infected Arabidopsis thaliana. J. Gen. Virol. 88, 337-341.
Hawkins, P.T., Poyner, D.R., Jackson, T.R., Letcher, A.J., Lander, D.A. and Irvine, R.F. (1993) Inhibition of iron-catalysed hydroxyl radical formation by inositol polyphosphates: a possible physiological function for myo-inositol hexakisphosphate. Biochem. J. 294, 929-934.
Heath, M.C. (2000) Nonhost resistance and nonspecific plant defenses. Curr. Opin. Plant Biol. 3, 315-319.
Irvine, R.F. and Schell, M.J. (2001) Back in the water: the return of the inositol phosphates. Mol. Cell. Biol. 2, 327-338.
Johnson, M.D. (1994) The Arabidopsis thaliana myo-inositol 1-phosphate synthase (EC 5.5.1.4). Plant Physiol. 105, 1023-1024.
Johnson, M.D. and Wang, X. (1996) Differentially expressed forms of 1L-myo-inositol-1-phosphate synthase (EC) in Phaseolus vulgaris. J. Biol. Chem. 271, 17215-17218.
Jongbloed, A.W. and Lenis, N.P. (1998) Environmental concerns of animal manure. J. Anim. Sci. 76, 2641-2648.
Keller, R., Brearley, C.A., Trethewey, R.N. and Muller-Rober, B. (1998) Reduced inositol content and altered morphology in transgenic potato plants inhibited for 1D-myo-inositol 3-phosphate synthase. Plant J. 16, 403-410.
Kepinski, S. and Leyser, O. (2005) The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature, 435, 446-451.
Knoester, M., van Loon, L.C., van den Heuvel, J., Hennig, J., Bol, J.F. and Linthorst, H.J.M. (1998) Ethylene-insensitive tobacco lacks nonhost resistance against soil-borne fungi. Proc. Natl Acad. Sci. USA, 95, 1933-1937.
Kus, J.V., Zaton, K., Sarkar, R. and Cameron, R.K. (2002) Age-related resistance in arabidopsis is a developmentally regulated defense response to Pseudomonas syringae. Plant Cell, 14, 479-490.
Lackey, K.H., Pope, P.M. and Johnson, M.D. (2003) Expression of 1L-myo-inositol-1-phosphate synthase in organelles. Plant Physiol. 132, 2240-2247.
Larson, S.R., Rutger, J.N., Young, K.A. and Raboy, V. (2000) Isolation and genetic mapping of a non-lethal rice (Oryza sativa L.) low phytic acid 1 mutation. Crop Sci. 40, 1397-1405.
Lemtiri-Chlieh, F., MacRobbie, E.A.C. and Brearley, C.A. (2000) Inositol hexakisphosphate is a physiological signal regulating the K+-inward rectifying conductance in guard cells. Proc. Natl Acad. Sci. USA, 97, 8687-8692.
Lemtiri-Chlieh, F., MacRobbie, E.A.C., Webb, A.A.R., Manison, N.F., Brownlee, C., Skepper, J.N., Chen, J., Prestwich, G.D. and Brearley, C.A. (2003) Inositol hexakisphosphate mobilizes an endomembrane store of calcium in guard cells. Proc. Natl Acad. Sci. USA, 100, 10091-10095.
Levine, A., Pennell, R.I., Alvarez, M.E., Palmer, R. and Lamb, C. (1996) Calcium-mediated apoptosis in a plant hypersensitive disease resistance response. Curr. Biol. 6, 427-437.
Lewsey, M., Robertson, F.C., Canto, T., Palukaitis, P. and Carr, J.P. (2007) Selective targeting of miRNA-regulated plant development by a viral counter-silencing protein. Plant J. 50, 240-252.
Loewus, F.A. and Loewus, M.W. (1983) myo-inositol: its biosynthesis and metabolism. Annu. Rev. Plant Physiol. 34, 137-161.
Loewus, F.A. and Murthy, P.P.N. (2000) myo-Inositol metabolism in plants. Plant Sci. 150, 1-19.
Lott, J.N.A., Ockenden, I., Raboy, V. and Batten, G.D. (2000) Phytic acid and phosphorus in crop seeds and fruits: a global estimate. Seed Sci. Res. 10, 11-33.
Love, A.J., Yun, B.W., Laval, V., Loake, G.J. and Milner, J.J. (2005) Cauliflower mosaic virus, a compatible pathogen of Arabidopsis, engages three distinct defense-signaling pathways and activates rapid systemic generation of reactive oxygen species. Plant Physiol. 139, 935-948.
Martin, A.M., y Poch, H.L.C., Herrera, D.M. and Ponz, F. (1999) Resistances to turnip mosaic potyvirus in Arabidopsis thaliana. Mol. Plant Microbe Interact. 12, 1016-1021.
Mauch-Mani, B. and Mauch, F. (2005) The role of abscisic acid in plant-pathogen interactions. Curr. Opin. Plant Biol. 8, 409-414.
Mendoza, C., Viteri, F.E., Lonnerdal, B., Young, K.A., Raboy, V. and Brown, K.H. (1998) Effect of genetically modified, low-phytic acid maize on absorption of iron from tortillas. Am. J. Clin. Nutr. 68, 1123-1127.
Mitsuhashi, N., Ohnishi, M., Sekiguchi, Y., Kwon, Y.-U., Chang, Y.-T., Chung, S.-K., Inoue, Y., Reid, R.J., Yagisawa, H. and Mimura, T. (2005) Phytic acid synthesis and vacuolar accumulation in suspension-cultured cells of Catharanthus roseus induced by high concentration of inorganic phosphate and cations. Plant Physiol. 138, 1607-1614.
Murphy, A.M., Chivasa, S., Singh, D.P. and Carr, J.P. (1999) Salicylic acid-induced resistance to viruses and other pathogens: a parting of the ways? Trends Plant Sci. 4, 155-160.
Murphy, A.M., Holcombe, L. and Carr, J.P. (2000) Characteristics of salicylic acid-induced delay in disease caused by a necrotrophic fungal pathogen in tobacco. Physiol. Mol. Plant Pathol. 57, 47-54.
Navarro, L., Dunoyer, P., Jay, F., Arnold, B., Dharmasiri, N., Estelle, M., Voinnet, O. and Jones, J.D.G. (2006) A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science, 312, 436-439.
Nishizawa, A., Yabuta, Y., Yoshida, E., Maruta, T., Yoshimura, K. and Shigeoka, S. (2006) Arabidopsis heat shock transcription factor A2 as a key regulator in response to several types of environmental stress. Plant J. 48, 535-547.
Otegui, M.S., Capp, R. and Staehelin, L.A. (2002) Developing seeds of Arabidopsis store different minerals in two types of vacuoles and in the endoplasmic reticulum. Plant Cell, 14, 1311-1327.
Palukaitis, P. and Garcia-Arenal, F. (2003) Cucumoviruses. Adv. Virus Res. 62, 241-323.
Raboy, V. (2001) Seeds for a better future: 'low phytate' grains help to overcome malnutrition and reduce pollution. Trends Plant Sci. 6, 458-462.
Raboy, V. (2003) myo-Inositol-1,2,3,4,5,6-hexakisphosphate. Phytochemistry, 64, 1033-1043.
Raboy, V., Gerbasi, P.F., Young, K.A., Stoneberg, S.D., Pickett, S.G., Bauman, A.T., Murthy, P.P.N., Sheridan, W.F. and Ertl, D.S. (2000) Origin and seed phenotype of maize low phytic acid 1-1 and low phytic acid 2-1. Plant Physiol. 124, 355-368.
Rajamaki, M.L., Maki-Valkama, T., Makinen, K. and Valkonen, J.P.T. (2004) Infection with potyviruses. In Plant-Pathogen Interactions. Annual Plant Reviews (Talbot, N.J., ed.). Oxford: Blackwell, pp. 68-91.
Rasmussen, S.K. and Hatzack, F. (1998) Identification of two low-phytate barley (Hordeum vulgare L.) grain mutants by TLC and genetic analysis. Hereditas, 129, 107-112.
Rate, D.N. and Greenberg, J.T. (2001) The Arabidopsis aberrant growth and death2 mutant shows resistance to Pseudomonas syringae and reveals a role for NPR1 in suppressing hypersensitive cell death. Plant J. 27, 203-211.
Regierer, A.B. (1998) Molekulargenetische Ansaetze zur Veraenderung der Phosphat Nutzungseffizienz von Hoeheren Pflanzen [Molecular Genetic Approaches for Modifying the Phosphate Utilization Efficiency of Higher Plants]. Berlin: P+H Wissenschaftlicher Verlag.
Schoelz, J. and Shepherd, R. (1988) Host range control of cauliflower mosaic virus. Virology, 162, 30-37.
Shen, X.T., Xiao, H., Ranallo, R., Wu, W.H. and Wu, C. (2003) Modulation of ATP-dependent chromatin-remodeling complexes by inositol polyphosphates. Science, 299, 112-114.
Shi, J., Wang, H., Schellin, K., Li, B., Faller, M., Stoop, J.M., Meely, R.B., Ertl, D.S., Ranch, J.P. and Glassman, K. (2007) Embryo-specific silencing of a transporter reduces phytic acid content of maize and soybean seeds. Nat. Biotech., 25, 930-937.
Smart, C.C. and Fleming, A.J. (1993) A plant gene with homology to myo-inositol-3-phosphate synthase is rapidly and spatially up-regulated during an abscisic-acid-induced morphogenic response in Spirodela polyrrhiza. Plant J. 4, 279-293.
Stephens, L.R., Hawkins, P.T., Stanley, A.F., Moore, T., Morris, P.J., Hanley, M.R., Kay, R.R. and Irvine, R.F. (1991) myo-Inositol pentakisphosphates. Structure, biological occurrence and phosphorylation to myo-inositol hexakisphosphate. Biochem. J. 275, 485-499.
Stevenson-Paulik, J., Bastidas, R.J., Chiou, S.-T., Frye, R.A. and York, J.D. (2005) Generation of phytate-free seeds in Arabidopsis through disruption of inositol polyphosphate kinases. Proc. Natl Acad. Sci. USA, 102, 12612-12617.
Surplus, S.L., Jordan, B.R., Murphy, A.M., Carr, J.P., Thomas, B. and -Mackerness, S.A.-H. (1998) Ultraviolet-B-induced responses in Arabidopsis thaliana: role of salicylic acid and reactive oxygen species in the regulation of transcripts encoding photosynthetic and acidic pathogenesis-related proteins. Plant Cell Environ. 21, 685-694.
Sweetman, D., Johnson, S., Caddick, S.E.K., Hanke, D.E. and Brearley, C.A. (2005) Characterization of an Arabidopsis inositol 1,3,4,5,6-pentakisphosphate 2-kinase (AtIPK1). Biochem. J. 394, 95-103.
Tan, X., Calderon-Villalobos, L.I.A., Sharon, M., Zheng, C., Robinson, C.V., Estelle, M. and Zheng, N. (2007) Mechanism of auxin perception by the TIR1 ubiquitin ligase. Nature, 446, 640-645.
Thacker, P.A., Rossnagel, B.G. and Raboy, V. (2006) The effects of phytase supplementation on nutrient digestibility, plasma parameters, performance and carcass traits of pigs fed diets based on low-phytate barley without inorganic phosphorus. Can. J. Anim. Sci. 86, 245-254.
Thomma, B.P.H.J., Eggermont, K., Penninckx, I.A.M.A., Mauch-Mani, B., Vogelsang, R., Cammue, B.P.A. and Broekaert, W.F. (1998) Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc. Natl Acad. Sci. USA, 95, 15107-15111.
Ton, J. and Mauch-Mani, B. (2004) [beta]-Amino-butyric acid-induced resistance against necrotrophic pathogens is based on ABA-dependent priming for callose. Plant J. 38, 119-130.
de Torres-Zabala, M., Truman, W., Bennett, M.H., Lafforgue, G., Mansfield, J.W., Rodriguez Egea, P., Bogre, L. and Grant, M. (2007) Pseudomonas syringae pv. tomato hijacks the Arabidopsis abscisic acid signalling pathway to cause disease. EMBO J. 26, 1434-1443.
Verbsky, J. and Majerus, P.W. (2005) Increased levels of inositol hexakisphosphate (InsP6) protect HEK293 cells from tumor necrosis factor [alpha]- and Fas-induced apoptosis. J. Biol. Chem. 280, 29263-29268.
Veronese, P., Chen, X., Bluhm, B., Salmeron, J., Dietrich, R. and Mengiste, T. (2004) The BOS loci of Arabidopsis are required for resistance to Botrytis cinerea infection. Plant J. 40, 558-574.
Walsh, J.A. and Jenner, C.E. (2002) Turnip mosaic virus and the quest for durable resistance. Mol. Plant Pathol. 3, 289-300.
Whelan, M.C., Innes, R.W., Bent, A.F. and Staskawicz, B.J. (1991) Identification of Pseudomonas syringae pathogens of Arabidopsis and a bacterial locus determining avirulence on both Arabidopsis and soybean. Plant Cell, 3, 49-59.
Wildermuth, M.C., Dewdney, J., Wu, G. and Ausubel, F.M. (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature, 414, 562-565.
Xia, H.J., Brearley, C., Elge, S., Kaplan, B., Fromm, H. and Mueller-Roeber, B. (2003) Arabidopsis inositol polyphosphate 6-/3-kinase is a nuclear protein that complements a yeast mutant lacking a functional ArgR-Mcm1 transcription complex. Plant Cell, 15, 449-463.
York, J.D., Odom, A.R., Murphy, R., Ives, E.B. and Wente, S.R. (1999) A phospholipase C-dependent inositol polyphosphate kinase pathway required for efficient messenger RNA export. Science, 285, 96-99.
Yoshida, K.T., Fujiwara, T. and Naito, S. (2002) The synergistic effects of sugar and abscisic acid on myo-inositol-1-phosphate synthase expression. Physiol. Plant, 114, 581-587.
Yu, W., Murfett, J. and Schoelz, J.E. (2003) Differential induction of symptoms in Arabidopsis by P6 of Cauliflower mosaic virus. Mol. Plant Microbe Interact. 16, 35-42.
Zeier, J., Delledonne, M., Mishina, T., Severi, E., Sonoda, M. and Lamb, C. (2004) Genetic elucidation of nitric oxide signaling in incompatible plant-pathogen interactions. Plant Physiol. 136, 2875-2886.
|
Language: | English.
|
Document Type: | ORIGINAL ARTICLE.
|
Journal Subset: | Life Sciences.
|
ISSN: | 0960-7412
|
NLM Journal Code: | bru, 9207397
|
Annotation(s) | |
|
|