Concurrent overactivation of the cytosolic glutamine synthetase and the GABA shunt in the ABA-deficient sitiens mutant of tomato leads to resistance against Botrytis cinerea
Version of Record online: 29 APR 2013
© 2013 The Authors. New Phytologist © 2013 New Phytologist Trust
Volume 199, Issue 2, pages 490–504, July 2013
How to Cite
Seifi, H. S., Curvers, K., De Vleesschauwer, D., Delaere, I., Aziz, A. and Höfte, M. (2013), Concurrent overactivation of the cytosolic glutamine synthetase and the GABA shunt in the ABA-deficient sitiens mutant of tomato leads to resistance against Botrytis cinerea. New Phytologist, 199: 490–504. doi: 10.1111/nph.12283
- Issue online: 19 JUN 2013
- Version of Record online: 29 APR 2013
- Manuscript Accepted: 14 MAR 2013
- Manuscript Received: 25 JAN 2013
- Fund for Scientific Research Flanders. Grant Numbers: 3G052607, 3G000210
- Research Foundation–Flanders
- 1977. α-aminooxy-β-phenylpropanoic acid, a potent inhibitor of L-phenylalanine ammonia-lyase in vitro and in vivo. Plant Science Letters 8: 313–317. , .
- 2007. Identification and characterization of plant genes involved in Agrobacterium-mediated plant transformation by virus-induced gene silencing. Molecular Plant-Microbe Interactions 20: 41–52. , , , , , , , .
- 2005. A novel senescence-associated gene encoding gamma-aminobutyric acid (GABA): pyruvate transaminase is upregulated during rice leaf senescence. Physiologia Plantarum 123: 1–8. , , .
- 2012. Hormonal regulation of leaf senescence in Lilium. Journal of Plant Physiology 169: 1542–1550. , .
- 2007. Resistance to Botrytis cinerea in sitiens, an abscisic acid-deficient tomato mutant, involves timely production of hydrogen peroxide and cell wall modifications in the epidermis. Plant Physiology 144: 1863–1877. , , , , , , .
- 2002. Abscisic acid determines basal susceptibility of tomato to Botrytis cinerea and suppresses salicylic acid-dependent signaling mechanisms. Plant Physiology 128: 491–501. , , .
- 2010. Riboflavin induces resistance against Botrytis cinerea in bean, but not in tomato, by priming for a hydrogen peroxide-fueled resistance response. Physiological and Molecular Plant Pathology 75: 23–29. , , , .
- 1996. Calmodulin binding to glutamate decarboxylase is required for regulation of glutamate and GABA metabolism and normal development in plants. The EMBO Journal 15: 2988–2996. , , , , , , .
- 2007. Plant physiology meets phytopathology: plant primary metabolism and plant–pathogen interactions. Journal of Experimental Botany 58: 4019–4026. , , .
- 2009. The importance of cytosolic glutamine synthetase in nitrogen assimilation and recycling. New Phytologist 182: 608–620. , .
- 2009. Primary metabolism and plant defense-fuel for the fire. Molecular Plant-Microbe Interactions 22: 487–497. .
- 2008. Lr34-mediated leaf rust resistance in wheat: transcript profiling reveals a high energetic demand supported by transient recruitment of multiple metabolic pathways. Molecular Plant-Microbe Interactions 21: 1515–1527. , , , .
- 2003. Mitochondrial succinic-semialdehyde dehydrogenase of the gamma-aminobutyrate shunt is required to restrict levels of reactive oxygen intermediates in plants. Proceedings of the National Academy of Sciences, USA 100: 6843–6848. , , , , .
- 1976. Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding. Analytical Biochemistry 72: 248–254. .
- 2011. Influence of over-expression of cytosolic aspartate aminotransferase on amino acid metabolism and defence responses against Botrytis cinerea infection in Arabidopsis thaliana. Journal of Plant Physiology 168: 1813–1819. , , , , .
- 1999. Plant succinic semialdehyde dehydrogenase. Cloning, purification, localization in mitochondria, and regulation by adenine nucleotides. Plant Physiology 121: 589–597. , .
- 2008. Tomato phenylalanine ammonia-lyase gene family, highly redundant but strongly underutilized. The Journal of Biological Chemistry 283: 33591–33601. , , , , .
- 1999. Glutamine synthetase in higher plants: regulation of gene and protein expression from the organ to the cell. Plant and Cell Physiology 40: 1187–1193. , .
- 2010. Abscisic acid deficiency causes changes in cuticle permeability and pectin composition that influence tomato resistance to Botrytis cinerea. Plant Physiology 154: 847–860. , , , , , , , , , et al.
- 2010. Abscisic acid-induced resistance against the brown spot pathogen Cochliobolus miyabeanus in rice involves MAP kinase-mediated repression of ethylene signaling. Plant Physiology 152: 2036–2052. , , , .
- 2012. The top 10 fungal pathogens in molecular plant pathology. Molecular Plant Pathology 13: 414–430. , , , , , , , , , et al.
- 1995. The regulation of carbon partitioning in plants. Current Topics in Plant Physiology 13: 258–267. , .
- 2002. The phenylpropanoid pathway and plant defence – a genomics perspective. Molecular Plant Pathology 3: 371–390. , , , , , .
- 2009. Amino acid changes during sunflower infection by the necrotrophic fungus B. cinerea. Plant Signaling & Behavior 4: 859–861. , , , .
- 2008. Highway or byway: the metabolic role of the GABA shunt in plants. Trends in Plant Science 13: 14–19. , , , , .
- 2005. GABA shunt deficiencies and accumulation of reactive oxygen intermediates: insight from Arabidopsis mutants. FEBS Letters 579: 415–420. , , .
- 1991. Genetic-basis of resistance to benzimidazole and dicarboximide fungicides in Botryotinia fuckeliana (Botrytis cinerea). Mycological Research 95: 943–951. , .
- 1971. Inactivation in-vivo of glutamine synthetase and NAD-specific glutamate dehydrogenase – its role in regulation of glutamine synthesis in yeasts. Journal of General Microbiology 69: 423–427. , .
- 2001. Lysine catabolism: a stress and development super-regulated metabolic pathway. Current Opinion in Plant Biology 4: 261–266. , , , .
- 2000. The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Current Biology 10: 751–757. , .
- 2006. An elicitor from Botrytis cinerea induces the hypersensitive response in Arabidopsis thaliana and other plants and promotes the gray mold disease. Phytopathology 96: 299–307. , , , , .
- 1989. Phenolic constituents of plant-cell walls and wall biodegradability. ACS Symposium Series 399: 137–145. , .
- 2002. Induced systemic resistance (ISR) against pathogens in the context of induced plant defences. Annals of Botany 89: 503–512. , .
- 2008. Differential regulation of root arginine catabolism and polyamine metabolism in clubroot-susceptible and partially resistant Arabidopsis genotypes. Plant Physiology 146: 2008–2019. , , , , , , .
- 2005. A duplicated pair of Arabidopsis RING-finger E3 ligases contribute to the RPM1-and RPS2-mediated hypersensitive response. Plant Journal 44: 258–270. , , , , , , .
- 2000. Gamma aminobutyric acid (GABA) and plant responses to stress. Critical Reviews in Plant Sciences 19: 479–509. , .
- 1965. Anaplerotic sequences in microbial metabolism. Angewandte Chemie International Edition 4: 558–565. .
- 1996. The molecular-genetics of nitrogen assimilation into amino acids in higher plants. Annual Review of Plant Physiology and Plant Molecular Biology 47: 569–593. , , , , .
- 2011. Living colors in the gray mold pathogen Botrytis cinerea: codon-optimized genes encoding green fluorescent protein and mCherry, which exhibit bright fluorescence. Applied and Environmental Microbiology 77: 2887–2897. , , , , , , .
- 2010. Amino acid homeostasis modulates salicylic acid-associated redox status and defense responses in Arabidopsis. Plant Cell 22: 3845–3863. , , , , , , .
- 2002a. Virus-induced gene silencing in tomato. Plant Journal 31: 777–786. , , .
- 2002b. Tobacco Rar1, EDS1 and NPR1/NIM1 like genes are required for N-mediated resistance to tobacco mosaic virus. Plant Journal 30: 415–429. , , , .
- 2009. Reference gene selection for quantitative real-time PCR normalization in tomato subjected to nitrogen, cold, and light stress. Analytical Biochemistry 387: 238–242. , .
- 2003. Structural and physiological changes in the roots of tomato plants over-expressing a basic peroxidase. Physiologia Plantarum 118: 422–429. , , , , , .
- 2008. Mutants of GABA transaminase (POP2) suppress the severe phenotype of succinic semialdehyde dehydrogenase (SSADH) mutants in Arabidopsis. PLoS ONE 3: e3383. , , , , .
- 2001. N-partitioning, nitrate reductase and glutamine synthetase activities in two contrasting varieties of maize. Pesquisa Agropecuária Brasileira 36: 249–256. , , .
- 2002. Diurnal changes in the expression of glutamate dehydrogenase and nitrate reductase are involved in the C/N balance of tobacco source leaves. Plant, Cell & Environment 25: 1451–1462. , , , , .
- 2012. Plant immunity to necrotrophs. Annual Review of Phytopathology 50: 267–294. .
- 2011. A mitochondrial GABA permease connects the GABA shunt and the TCA cycle, and is essential for normal carbon metabolism. Plant Journal 67: 485–498. , , , , , , , , , et al.
- 2006. The two senescence-related markers, GS1 (cytosolic glutamine synthetase) and GDH (glutamate dehydrogenase), involved in nitrogen mobilization, are differentially regulated during pathogen attack and by stress hormones and reactive oxygen species in Nicotiana tabacum L. leaves. Journal of Experimental Botany 57: 547–557. , , , .
- 2010. Mutations in gamma-aminobutyric acid (GABA) transaminase genes in plants or Pseudomonas syringae reduce bacterial virulence. Plant Journal 64: 318–330. , , , , , , , .
- 1998. Cytosolic localization in tomato mesophyll cells of a novel glutamine synthetase induced in response to bacterial infection or phosphinothricin treatment. Planta 206: 426–434. , , , , , , , .
- 2009. Networking by small-molecule hormones in plant immunity. Nature Chemical Biology 5: 308–316. , , , .
- 2000. Molecular aspects of leaf senescence. Trends in Plant Science 5: 278–282. , , , .
- 2007. Does GABA act as a signal in plants? Hints from molecular studies. Plant Signaling & Behavior 2: 408–409. .
- 2007. Pathological hormone imbalances. Current Opinion in Plant Biology 10: 372–379. , , , .
- 2001. Overlapping expression of cytosolic glutamine synthetase and phenylalanine ammonia-lyase in immature leaf blades of rice. Physiologia Plantarum 113: 400–408. , , .
- 2013. Glutamate metabolism in plant disease and defense: friend or foe? Molecular Plant-Microbe Interactions 26: 475–485. , , , .
- 2012. Compartmentation of GABA metabolism raises intriguing questions. Trends in Plant Science 17: 57–59. , , .
- 2002. Evidence that gamma-aminobutyric acid is a major nitrogen source during Cladosporium fulvum infection of tomato. Planta 214: 414–420. , .
- 2008. Differential regulation of phenylalanine ammonia lyase activity and protein level by light in tomato seedlings. Plant Physiology and Biochemistry 46: 444–451. , .
- 2008. Botrytis cinerea induces senescence and is inhibited by autoregulated expression of the IPT gene. European Journal of Plant Pathology 120: 289–297. , , , , .
- 2002. The impact of oxidative stress on Arabidopsis mitochondria. Plant Journal 32: 891–904. , , , , , , .
- 1984. Inhibition of photosensitive lettuce-seed germination by methionine sulfoximine, a specific inhibitor of glutamine-synthetase. Plant and Cell Physiology 25: 49–54. .
- 2006. Inhibition of GABA shunt enzymes' activity by 4-hydroxybenzaldehyde derivatives. Bioorganic & Medicinal Chemistry Letters 16: 592–595. , , , , .
- 2007. The plant nitrogen mobilization promoted by Colletotrichum lindemuthianum in Phaseolus leaves depends on fungus pathogenicity. Journal of Experimental Botany 58: 3351–3360. , , , , , , .
- 2000. Control of abscisic acid synthesis. Journal of Experimental Botany 51: 1563–1574. , , .
- 1988. The wilty tomato mutants flacca and sitiens are impaired in the oxidation of ABA-aldehyde to ABA. Plant, Cell & Environment 11: 739–745. , , , , .
- 1997. Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant Journal 11: 1187–1194. , , , .
- 2004. Induction of programmed cell death in lily by the fungal pathogen Botrytis elliptica. Molecular Plant Pathology 5: 559–574. , , .
- 2007. Histochemical and genetic analysis of host and non-host interactions of Arabidopsis with three Botrytis species: an important role for cell death control. Molecular Plant Pathology 8: 41–54. , , , .
- 2006. Licensed to kill: the lifestyle of a necrotrophic plant pathogen. Trends in Plant Science 11: 247–253. .
- 2009. Virus-induced gene silencing (VIGS) in Nicotiana benthamiana and tomato. Journal of Visualized Experiments 28: e1292. , , .
- 2008. Are green islands red herrings? Significance of green islands in plant interactions with pathogens and pests. Biological Reviews 83: 79–102. , , .
- 2006. Molecular cloning and differential expression of a gamma-aminobutyrate transaminase gene, OsGABA-T, in rice (Oryza sativa) leaves infected with blast fungus. Journal of Plant Research 6: 663–669. , , , , .
- 2005. Gene-expression analysis and network discovery using Genevestigator. Trends in Plant Science 10: 407–409. , , .