Nitrogen metabolism meets phytopathology

Journal of Experimental Botany

Volumn 65, Issue 19, 2014, Pages 5643-5656

  Fagard, Mathilde ^a   Launay, Alban ^a   Clément, Gilles ^a   Courtial, Julia ^a   Dellagi, Alia ^a   Farjad, Mahsa ^a   Krapp, Anne ^a   Soulié, Marie Christine ^a   Masclaux Daubresse, Céline ^a  

^a INSTITUT JEAN PIERRE BOURGIN   (France)

Author keywords

Disease; Metabolome; Nitrogen; Pathogen; Resistance; Transcriptome

Indexed keywords

FERTILIZER; NITRIC ACID DERIVATIVE; NITROGEN; SOIL; TRANSCRIPTOME; UREA;

CHEMISTRY; DISEASE RESISTANCE; IMMUNOLOGY; METABOLISM; METABOLOME; MICROBIOLOGY; PLANT; PLANT DISEASE; POLLUTION; SOIL;

DISEASE RESISTANCE; ENVIRONMENTAL POLLUTION; FERTILIZERS; METABOLOME; NITRATES; NITROGEN; PLANT DISEASES; PLANT PATHOLOGY; PLANTS; SOIL; TRANSCRIPTOME; UREA;

EID: 84930526480     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/eru323     Document Type: Review

References (120)

1. Abu Qamar S, Chen X, Dhawan R, Bluhm B, Salmeron J, Lam S, Dietrich RA, Mengiste T. 2006. Expression profling and mutant analysis reveals complex regulatory networks involved in Arabidopsis response to Botrytis infection. The Plant Journal 48, 28-44.
2. Asai S, Yoshioka H. 2009. Nitric oxide as a partner of reactive oxygen species participates in disease resistance to necrotrophic pathogen Botrytis cinerea in Nicotiana benthamiana. Molecular Plant-Microbe Interactions 22, 619-629.
3. Asselbergh B, Curvers K, Franca SC, Audenaert K, Vuylsteke M, Van Breusegem F, Hoefte M. 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.
4. Avila-Ospina L, Moison M, Yoshimoto K, Masclaux-Daubresse C. 2014. Autophagy, plant senescence, and nutrient recycling. Journal of Experimental Botany 65, 3799-3812.
5. Baker RF, Leach KA, Braun DM. 2012. SWEET as sugar: new sucrose effluxers in plants. Molecular Plant 5, 766-768.
6. Ballini E, Thuy Thu Thi N, Morel J-B. 2013. Diversity and genetics of nitrogen-induced susceptibility to the blast fungus in rice and wheat. Rice 6, 32.
7. Balmer D, Flors V, Glauser G, Mauch-Mani B. 2013. Metabolomics of cereals under biotic stress: current knowledge and techniques. Frontiers in Plant Science 4, 82.
8. Bellin D, Asai S, Delledonne M, Yoshioka H. 2013. Nitric oxide as a mediator for defense responses. Molecular Plant-Microbe Interactions 26, 271-277.
9. Bellincampi D, Cervone F, Lionetti V. 2014. Plant cell wall dynamics and wall-related susceptibility in plant-pathogen interactions. Frontiers in Plant Science 5, 228.
10. Berger S, Sinha AK, Roitsch T. 2007. Plant physiology meets phytopathology: plant primary metabolism and plant-pathogen interactions. Journal of Experimental Botany 58, 4019-4026.
11. Besson-Bard A, Pugin A, Wendehenne D. 2008. New insights into nitric oxide signaling in plants. Annual Review of Plant Biology 59, 21-39.
12. Boccara M, Mills CE, Zeier J, Anzi C, Lamb C, Poole RK, Delledonne M. 2005. Flavohaemoglobin HmpX from Erwinia chrysanthemi confers nitrosative stress tolerance and affects the plant hypersensitive reaction by intercepting nitric oxide produced by the host. The Plant Journal 43, 226-237.
13. Bolton MD. 2009. Primary metabolism and plant defense-fuel for the fre. Molecular Plant-Microbe Interactions 22, 487-497.
14. Bolton MD, Thomma B. 2008. The complexity of nitrogen metabolism and nitrogen-regulated gene expression in plant pathogenic fungi. Physiological and Molecular Plant Pathology 72, 104-110.
15. Botanga CJ, Bethke G, Chen Z, Gallie DR, Fiehn O, Glazebrook J. 2012. Metabolite profling of Arabidopsis inoculated with Alternaria brassicicola reveals that ascorbate reduces disease severity. Molecular Plant-Microbe Interactions 25, 1628-1638.
16. Bouche N, Fromm H. 2004. GABA in plants: just a metabolite? Trends in Plant Science 9, 110-115.
17. Brauc S, De Vooght E, Claeys M, Hofte M, Angenon G. 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.
18. Buchanan-Wollaston V. 1997. The molecular biology of leaf senescence. Journal of Experimental Botany 48, 181-199.
19. Camanes G, Pastor V, Cerezo M, Garcia-Agustin P, Flors Herrero V. 2012a. A deletion in the nitrate high affinity transporter NRT2.1 alters metabolomic and transcriptomic responses to Pseudomonas syringae. Plant Signaling and Behavior 7, 619-622.
20. Camanes G, Pastor V, Cerezo M, Garcia-Andrade J, Vicedo B, Garcia-Agustin P, Flors V. 2012b. A deletion in NRT2.1 attenuates pseudomonas syringae-induced hormonal perturbation, resulting in primed plant defenses. Plant Physiology 158, 1054-1066.
21. Chaffei C, Pageau K, Suzuki A, Gouia H, Ghorbel MH, Masclaux-Daubresse C. 2004. Cadmium toxicity induced changes in nitrogen management in Lycopersicon esculentum leading to a metabolic safeguard through an amino acid storage strategy. Plant and Cell Physiology 45, 1681-1693.
22. Choquer M, Fournier E, Kunz C, Levis C, Pradier J-M, Simon A, Viaud M. 2007. Botrytis cinerea virulence factors: new insights into a necrotrophic and polyphageous pathogen. FEMS Microbiology Letters 277, 1-10.
23. Das AK, Mitra DK. 1993. The effect of little leaf disease on nitrogen metabolism in brinjal. International Journal of Tropical Plant Diseases 11, 193-196.
24. Davidsson PR, Kariola T, Niemi O, Palva ET. 2013. Pathogenicity of and plant immunity to soft rot pectobacteria. Frontiers in Plant Science 4, 191-191.
25. Dechorgnat J, Patrit O, Krapp A, Fagard M, Daniel-Vedele F. 2012. Characterization of the Nrt2.6 gene in Arabidopsis thaliana: a link with plant response to biotic and abiotic stress. PLoS One 7, e42491.
26. Degrave A, Moreau M, Launay A, Barny M-A, Brisset M-N, Patrit O, Taconnat L, Vedel R, Fagard M. 2013. The bacterial effector DspA/E is toxic in Arabidopsis thaliana and is required for multiplication and survival of fre blight pathogen. Molecular Plant Pathology 14, 506-517.
27. Delledonne M, Xia YJ, Dixon RA, Lamb C. 1998. Nitric oxide functions as a signal in plant disease resistance. Nature 394, 585-588.
28. Delledonne M, Zeier J, Marocco A, Lamb C. 2001. Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proceedings of the National Academy of Sciences, USA 98, 13454-13459.
29. De Virgilio C, Loewith R. 2006. Cell growth control: little eukaryotes make big contributions. Oncogene 25, 6392-6415.
30. Dietrich R, Plob K, Heil M. 2004. Constitutive and induced resistance to pathogens in Arabidopsis thaliana depends on nitrogen supply. Plant, Cell and Environment 27, 896-906.
31. Dordas C. 2008. Role of nutrients in controlling plant diseases in sustainable agriculture. A review. Agronomy for Sustainable Development 28, 33-46.
32. Durner J, Wendehenne D, Klessig DF. 1998. Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose. Proceedings of the National Academy of Sciences, USA 95, 10328-10333.
33. Fernandez E, Galvan A. 2007. Inorganic nitrogen assimilation in Chlamydomonas. Journal of Experimental Botany 58, 2279-2287.
34. Fujita M, Fujita Y, Noutoshi Y, Takahashi F, Narusaka Y, Yamaguchi-Shinozaki K, Shinozaki K. 2006. Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Current Opinion in Plant Biology 9, 436-442.
35. Gagnot S, Tamby J, Martin-Magniette M, Bitton F, Taconnat L, Balzergue S, Aubourg S, Renou J, Lecharny A, Brunaud V. 2008. CATdb: a public access to Arabidopsis transcriptome data from the URGV-CATMA platform. Nucleic Acids Research 36, D986-D990.
36. Galatro A, Puntarulo S, Guiamet JJ, Simontacchi M. 2013. Chloroplast functionality has a positive effect on nitric oxide level in soybean cotyledons. Plant Physiology and Biochemistry 66, 26-33.
37. Glazebrook J. 2005. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annual Review of Phytopathology 43, 205-227.
38. Gojon A, Krouk G, Perrine-Walker F, Laugier E. 2011. Nitrate transceptor (s) in plants. Journal of Experimental Botany 62, 2299-2308.
39. Govrin EM, Levine A. 2000. The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Current Biology 10, 751-757.
40. Gupta KJ, Brotman Y, Segu S, et al. 2013. The form of nitrogen nutrition affects resistance against Pseudomonas syringae pv. phaseolicola in tobacco. Journal of Experimental Botany 64, 553-568.
41. Gupta KJ, Igamberdiev AU. 2011. The anoxic plant mitochondrion as a nitrite: NO reductase. Mitochondrion 11, 537-543.
42. Ho C-H, Lin S-H, Hu H-C, Tsay Y-F. 2009. CHL1 functions as a nitrate sensor in plants. Cell 138, 1184-1194.
43. Horst RJ, Zeh C, Saur A, Sonnewald S, Sonnewald U, Voll LM. 2012. The Ustilago maydis Nit2 homolog regulates nitrogen utilization and is required for efficient induction of filamentous growth. Eukaryotic Cell 11, 368-380.
44. Huber DM, Watson RD. 1974. Nitrogen form and plant disease. Annual Review of Phytopathology 12, 139-165.
45. Hugouvieux-Cotte-Pattat N, Dominguez H, Robertbaudouy J. 1992. Environmental conditions affect transcription of the pectinase genes of Erwinia chrysanthemi 3937. Journal of Bacteriology 174, 7807-7818.
46. Hwang IS, An SH, Hwang BK. 2011. Pepper asparagine synthetase 1 (CaAS1) is required for plant nitrogen assimilation and defense responses to microbial pathogens. The Plant Journal 67, 749-762.
47. Jones JDG, Dangl JL. 2006. The plant immune system. Nature 444, 323-329.
48. Kale SD, Tyler BM. 2011. Entry of oomycete and fungal effectors into plant and animal host cells. Cellular Microbiology 13, 1839-1848.
49. Kim H, Woloshuk CP. 2008. Role of AREA, a regulator of nitrogen metabolism, during colonization of maize kernels and fumonisin biosynthesis in Fusarium verticillioides. Fungal Genetics and Biology 45, 947-953.
50. Kumar M, Prasad M. 1992. Organic nitrogen metabolism of crucifer seedlings in relation to their response towards Xanthomonas campestris pv. campestris. Zentralblatt für Mikobiologie 147, 92-102.
51. Lecompte F, Abro M, Nicot P. 2010. Contrasted responses of Botrytis cinerea isolates developing on tomato plants grown under different nitrogen nutrition regimes. Plant Pathology 59, 891-899.
52. Lemaître T, Gaufichon L, Boutet-Mercey S, Christ A, Masclaux-Daubresse C. 2008. Enzymatic and metabolic diagnostic of nitrogen deficiency in Arabidopsis thaliana Wassileskija accession. Plant and Cell Physiology 49, 1056-1065.
53. Li W, Wang Y, Okamoto M, Crawford NM, Siddiqi MY, Glass ADM. 2007. Dissection of the AtNRT2.1:tNRT2.2 inducible high-affinity nitrate transporter gene cluster. Plant Physiology 143, 425-433.
54. Little D, Rao H, Oliva S, Daniel-Vedele F, Krapp A, Malamy J. 2005. The putative high-affinity nitrate transporter NRT2.1 represses lateral root initiation in response to nutritional cues. Proceedings of the National Academy of Sciences, USA 102, 13693-13698.
55. Liu G, Ji Y, Bhuiyan NH, Pilot G, Selvaraj G, Zou J, Wei Y. 2010. Amino acid homeostasis modulates salicylic acid-associated redox status and defense responses in Arabidopsis. The Plant Cell 22, 3845-3863.
56. Lopez-Berges MS, Rispail N, Prados-Rosales RC, Di Pietro A. 2010. A nitrogen response pathway regulates virulence functions in Fusarium oxysporum via the protein kinase TOR and the bZIP protein MeaB. The Plant Cell 22, 2459-2475.
57. Machin F, Medina B, Navarro FJ, Perez MD, Veenhuis M, Tejera P, Lorenzo H, Lancha A, Siverio JM. 2004. The role of Ynt1 in nitrate and nitrite transport in the yeast Hansenula polymorpha. Yeast 21, 265-276.
58. Mandadi KK, Scholthof K-B G. 2013. Plant immune responses against viruses: how does a virus cause disease? The Plant Cell 25, 1489-1505.
59. Masclaux-Daubresse C, Daniel-Vedele F, Dechorgnat J, Chardon F, Gaufichon L, Suzuki A. 2010. Nitrogen uptake, assimilation and remobilization in plants: challenges for sustainable and productive agriculture. Annals of Botany 105, 1141-1157.
60. Massad TJ, Dyer LA, Vega CG. 2012. Costs of defense and a test of the carbon-nutrient balance and growth-differentiation balance hypotheses for two co-occurring classes of plant defense. PLoS One 7, e47554.
61. Matsumoto H, Jitareerat P, Baba Y, Tsuyumu S. 2003. Comparative study of regulatory mechanisms for pectinase production by Erwinia carotovora subsp carotovora and Erwinia chrysanthemi. Molecular Plant-Microbe Interactions 16, 226-237.
62. McKee MW. 1972. Some effects of Eastern X-disease on the nitrogen metabolism of peach leaves. Hortscience 7, 393-394.
63. Mengiste T. 2012. Plant immunity to necrotrophs. Annual Review of Phytopathology 50, 267-294.
64. Michaeli S, Fait A, Lagor K, et al. 2011. A mitochondrial GABA permease connects the GABA shunt and the TCA cycle, and is essential for normal carbon metabolism. The Plant Journal 67, 485-498.
65. Moche M, Stremlau S, Hecht L, Goebel C, Feussner I, Stoehr C. 2010. Effect of nitrate supply and mycorrhizal inoculation on characteristics of tobacco root plasma membrane vesicles. Planta 231, 425-436.
66. Modolo LV, Augusto O, Almeida IMG, Magalhaes JR, Salgado I. 2005. Nitrite as the major source of nitric oxide production by Arabidopsis thaliana in response to Pseudomonas syringae. FEBS Letters 579, 3814-3820.
67. Modolo LV, Augusto O, Almeida IMG, Pinto-Maglio CAF, Oliveira HC, Seligman K, Salgado I. 2006. Decreased arginine and nitrite levels in nitrate reductase-deficient Arabidopsis thaliana plants impair nitric oxide synthesis and the hypersensitive response to Pseudomonas syringae. Plant Science 171, 34-40.
68. Morcx S, Kunz C, Choquer M, Assie S, Blondet E, Simond-Cote E, Gajek K, Chapeland-Leclerc F, Expert D, Soulie M-C. 2013. Disruption of Bcchs4, Bcchs6 or Bcchs7 chitin synthase genes in Botrytis cinerea and the essential role of class VI chitin synthase (Bcchs6). Fungal Genetics and Biology 52, 1-8.
69. Moreau M, Degrave A, Vedel R, Bitton F, Patrit O, Renou JP, Barny MA, Fagard M. 2012. EDS1 contributes to nonhost resistance of Arabidopsis thaliana against Erwinia amylovora. Molecular Plant-Microbe Interactions 25, 421-430.
70. Navarova H, Bernsdorff F, Doering 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, 5123-5141.
71. Olea F, Pérez-Garcia A, Canton FR, Rivera EM, Canas R, Avila C, Cazorla FM, Canovas FM, De Vicente A. 2004. Up-regulation and localization of asparagine synthetase in tomato leaves infected by the bacterial pathogen Pseudomonas syringae. Plant and Cell Physiology 45, 770-780.
72. Oliveira HC, Justino GC, Sodek L, Salgado I. 2009. Amino acid recovery does not prevent susceptibility to Pseudomonas syringae in nitrate reductase double-deficient Arabidopsis thaliana plants. Plant Science 176, 105-111.
73. Orsel M, Eulenburg K, Krapp A, Daniel-Vedele F. 2004. Disruption of the nitrate transporter genes AtNRT2.1 and AtNRT2.2 restricts growth at low external nitrate concentration. Planta 219, 714-721.
74. Pageau K, Reisdorf-Cren M, Morot-Gaudry JF, Masclaux-Daubresse C. 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.
75. Perchepied L, Balague C, Riou C, Claudel-Renard C, Riviere N, Grezes-Besset B, Roby D. 2010. Nitric oxide participates in the complex interplay of defense-related signaling pathways controlling disease resistance to Sclerotinia sclerotiorum in Arabidopsis thaliana. Molecular Plant-Microbe Interactions 23, 846-860.
76. Pérez-Garcia A, De Vicente A, Canton FR, Cazorla FM, Codina JC, Garcia-Gutierrez A, Canovas FM. 1998a. Light-dependent changes of tomato glutamine synthetase in response to Pseudomonas syringae infection or phosphinothricin treatment. Physiologia Plantarum 102, 377-384.
77. Pérez-Garcia A, Pereira S, Pissara J, Garcia Gutiérrez A, Cazorla FM, Salema R, De Vicente A. 1998b. Cytosolic localization in tomato mesophyll cells of a novel glutamine synthetase induced in response to bacterial infection of phosphinothricin treatment. Planta 206, 426-434.
78. Pieterse CMJ, Van Der Does D, Zamioudis C, Leon-Reyes A, Van Wees SCM. 2012. Hormonal modulation of plant immunity. Annual Review of Cell and Developmental Biology 28, 489-521.
79. Pitzschke A, Schikora A, Hirt H. 2009. MAPK cascade signalling networks in plant defence. Current Opinion in Plant Biology 12, 421-426.
80. Planchet E, Gupta KJ, Sonoda M, Kaiser WM. 2005. Nitric oxide emission from tobacco leaves and cell suspensions: rate limiting factors and evidence for the involvement of mitochondrial electron transport. The Plant Journal 41, 732-743.
81. Prasch CM, Sonnewald U. 2013. Simultaneous application of heat, drought, and virus to arabidopsis plants reveals significant shifts in signaling networks. Plant Physiology 162, 1849-1866.
82. Rasmussen S, Barah P, Suarez-Rodriguez MC, Bressendorff S, Friis P, Costantino P, Bones AM, Nielsen HB, Mundy J. 2013. Transcriptome responses to combinations of stresses in Arabidopsis. Plant Physiology 161, 1783-1794.
83. Reverchon S, Expert D, Robert Baudouy J, Nasser W. 1997. The cyclic AMP receptor protein is the main activator of pectinolysis genes in Erwinia chrysanthemi. Journal of Bacteriology 179, 3500-3508.
84. Robert-Seilaniantz A, Grant M, Jones JDG. 2011. Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annual Review of Phytopathology 49, 317-343.
85. Rockel P, Strube F, Rockel A, Wildt J, Kaiser WM. 2002. Regulation of nitric oxide (NO) production by plant nitrate reductase in vivo and in vitro. Journal of Experimental Botany 53, 103-110.
86. Rohde JR, Bastidas R, Puria R, Cardenas ME. 2008. Nutritional control via Tor signaling in Saccharomyces cerevisiae. Current Opinion in Microbiology 11, 153-160.
87. Rojas CM, Senthil-Kumar M, Tzin V, Mysore KS. 2014. Regulation of primary plant metabolism during plant-pathogen interactions and its contribution to plant defense. Frontiers in Plant Science 5, 17.
88. Ruemer S, Gupta KJ, Kaiser WM. 2009. Plant cells oxidize hydroxylamines to NO. Journal of Experimental Botany 60, 2065-2072.
89. Schober BM, Vermeulen T. 1999. Enzymatic maceration of witloof chicory by the soft rot bacteria Erwinia carotovora subsp carotovora: the effect of nitrogen and calcium treatments of the plant on pectic enzyme production and disease development. European Journal of Plant Pathology 105, 341-349.
90. Seifi HS, Curvers K, De Vleesschauwer D, Delaere I, Aziz A, Hofte M. 2013a. 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.
91. Seifi H, De Vleesschauwer D, Aziz A, Höfte M. 2014. Modulating plant primary amino acid metabolism as a necrotrophic virulence strategy: the immune-regulatory role of asparagine synthetase in Botrytis cinerea-tomato interaction. Plant Signaling and Behavior 9, e27995.
92. Seifi HS, Van Bockhaven J, Angenon G, Hofte M. 2013b. Glutamate metabolism in plant disease and defense: friend or foe? Molecular Plant-Microbe Interactions 26, 475-485.
93. Sharma SS, Dietz KJ. 2006. The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress. Journal of Experimental Botany 57, 711-726.
94. Snedden WA, Fromm H. 1999. Regulation of the gamma-aminobutyratesynthesizing enzyme, glutamate decarboxylase, by calcium-calmodulin: a mechanism for rapid activation in response to stress. In: Lerner HR, ed. Plant responses to environmental stresses: from phytohormones to genome reorganization. New York: Marcel Dekker, 549-574.
95. Snoeijers SS, Pérez-Garcia A, Joosten M, De Wit P. 2000. The effect of nitrogen on disease development and gene expression in bacterial and fungal plant pathogens. European Journal of Plant Pathology 106, 493-506.
96. Solomon PS, Oliver R P. 2001. The nitrogen content of the tomato leaf apoplast increases during infection by Cladosporium fulvum. Planta 213, 241-249.
97. Solomon PS, Oliver RP. 2002. Evidence that gamma-aminobutyric acid is a major nitrogen source during Cladosporium fulvum infection of tomato. Planta 214, 414-420.
98. Stohr C, Strube F, Marx G, Ullrich WR, Rockel P. 2001. A plasma membrane-bound enzyme of tobacco roots catalyses the formation of nitric oxide from nitrite. Planta 212, 835-841.
99. Stuehr DJ, Santolini J, Wang ZQ, Wei CC, Adak S. 2004. Update on mechanism and catalytic regulation in the NO synthases. Journal of Biological Chemistry 279, 36167-36170.
100. Svennerstam H, Ganeteg U, Bellini C, Nasholm T. 2007. Comprehensive screening of Arabidopsis mutants suggests the lysine histidine transporter 1 to be involved in plant uptake of amino acids. Plant Physiology 143, 1853-1860.
101. Swarbrick PJ, Schulze-Lefert P, Scholes JD. 2006. Metabolic consequences of susceptibility and resistance (race-specific and broadspectrum) in barley leaves challenged with powdery mildew. Plant, Cell and Environment 29, 1061-1076.
102. Szabados L, Savoure A. 2010. Proline: a multifunctional amino acid. Trends in Plant Science 15, 89-97.
103. Tao Y, Xie ZY, Chen WQ, Glazebrook J, Chang HS, Han B, Zhu T, Zou GZ, Katagiri F. 2003. Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae. The Plant Cell 15, 317-330.
104. Tavernier V, Cadiou S, Pageau K, Laugé R, Reisdorf-Cren M, Langin T, Masclaux-Daubresse C. 2007. The plant nitrogen mobilization promoted by Colletotrichum lindemuthianum in Phaseolus leaves depends on fungus pathogenicity. Journal of Experimental Botany 58, 3351-3360.
105. Thomma B, Nurnberger T, Joosten M. 2011. Of PAMPs and effectors: the blurred PTI-ETI dichotomy. The Plant Cell 23, 4-15.
106. Tun NN, Santa-Catarina C, Begum T, Silveira V, Handro W, Floh EIS, Scherer GFE. 2006. Polyamines induce rapid biosynthesis of nitric oxide (NO) in Arabidopsis thaliana seedlings. Plant and Cell Physiology 47, 346-354.
107. Van Heeswijk WC, Westerhoff HV, Boogerd FC. 2013. Nitrogen assimilation in Escherichia coli: putting molecular data into a systems perspective. Microbiology and Molecular Biology Reviews 77, 628-695.
108. Verslues PE, Juenger TE. 2011. Drought, metabolites, and Arabidopsis natural variation: a promising combination for understanding adaptation to water-limited environments. Current Opinion in Plant Biology 14, 240-245.
109. Walters D, Heil M. 2007. Costs and trade-offs associated with induced resistance. Physiological and Molecular Plant Pathology 71, 3-17.
110. Walters DR, Bingham IJ. 2007. Influence of nutrition on disease development caused by fungal pathogens: implications for plant disease control. Annals of Applied Biology 151, 307-324.
111. Wang K, Senthil-Kumar M, Ryu C-M, Kang L, Mysore KS. 2012. Phytosterols play a key role in plant innate immunity against bacterial pathogens by regulating nutrient efflux into the apoplast. Plant Physiology 158, 1789-1802.
112. Wang P, Du Y, Li Y, Ren D, Song C-P. 2010. Hydrogen peroxidemediated activation of MAP kinase 6 modulates nitric oxide biosynthesis and signal transduction in Arabidopsis. The Plant Cell 22, 2981-2998.
113. Ward J, Forcat S, Beckmann M, et al. 2010. The metabolic transition during disease following infection of Arabidopsis thaliana by Pseudomonas syringae pv. tomato. The Plant Journal 63, 443-457.
114. Wei ZM, Sneath BJ, Beer SV. 1992. Expression of Erwinia amylovora Hrp genes in response to environmental stimuli. Journal of Bacteriology 174, 1875-1882.
115. Weiss V, Kramer G, Dunnebier T, Flotho A. 2002. Mechanism of regulation of the bifunctional histidine kinase NtrB in Escherichia coli. Journal of Molecular Microbiology and Biotechnology 4, 229-233.
116. Wimalasekera R, Villar C, Begum T, Scherer GFE. 2011. COPPER AMINE OXIDASE1 (CuAO1) of Arabidopsis thaliana contributes to abscisic acid- and polyamine-induced nitric oxide biosynthesis and abscisic acid signal transduction. Molecular Plant 4, 663-678.
117. Wong KH, Hynes MJ, Davis MA. 2008. Recent advances in nitrogen regulation: a comparison between Saccharomyces cerevisiae and filamentous fungi. Eukaryotic Cell 7, 917-925.
118. Yaeno T, Iba K. 2008. BAH1/NLA, a RING-type ubiquitin E3 ligase, regulates the accumulation of salicylic acid and immune responses to Pseudomonas syringae DC3000. Plant Physiology 148, 1032-1041.
119. Yamamoto-Katou A, Katou S, Yoshioka H, Doke N, Kawakita K. 2006. Nitrate reductase is responsible for elicitin-induced nitric oxide production in Nicotiana benthamiana. Plant and Cell Physiology 47, 726-735.
120. Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W. 2004. GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiology 136, 2621-2632.