Spatial and temporal dynamics of primary and secondary metabolism in Phaseolus vulgaris challenged by Pseudomonas syringae

Physiologia Plantarum

Volumn 153, Issue 1, 2015, Pages 161-174

  Pérez Bueno, María Luisa ^a   Pineda, Mónica ^a   Díaz Casado, Elena ^a   Barón, Matilde ^a  

^a CSIC   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

PHASEOLUS VULGARIS; PSEUDOMONAS SYRINGAE;

CHLOROPHYLL; PHENOL DERIVATIVE;

CHEMISTRY; CYTOLOGY; GENE EXPRESSION REGULATION; HOST PATHOGEN INTERACTION; METABOLISM; MICROBIOLOGY; PHASEOLUS; PHOTOSYNTHESIS; PHYSIOLOGY; PLANT DISEASE; PLANT LEAF; PLANT STOMA; PSEUDOMONAS SYRINGAE;

CHLOROPHYLL; GENE EXPRESSION REGULATION, PLANT; HOST-PATHOGEN INTERACTIONS; PHASEOLUS; PHENOLS; PHOTOSYNTHESIS; PLANT DISEASES; PLANT LEAVES; PLANT STOMATA; PSEUDOMONAS SYRINGAE;

EID: 84939419204     PISSN: 00319317     EISSN: 13993054     Source Type: Journal    
DOI: 10.1111/ppl.12237     Document Type: Article

References (78)

1. Aldea M, Frank TD, DeLucia EH (2006a) A method for quantitative analysis of spatially variable physiological processes across leaf surfaces. Photosynth Res 90: 161-172
2. Aldea M, Hamilton JG, Resti JP, Zangerl AR, Berenbaum MR, Frank TD, Delucia EH (2006b) Comparison of photosynthetic damage from arthropod herbivory and pathogen infection in understory hardwood saplings. Oecologia 149: 221-232
3. Arnold DL, Lovell HC, Jackson RW, Mansfield JW (2011) Pseudomonas syringae pv. phaseolicola: from 'has bean' to supermodel. Mol Plant Pathol 12: 617-627
4. Barón M, Flexas J, DeLucia E (2012) Photosynthesis responses to biotic stress. In: Flexas J, Loreto F, Medrano H (eds) Terrestrial Photosynthesis in a Changing Environment: A Molecular, Physiological and Ecological Approach. Cambridge Press, Cambridge, pp 331-350
5. Bender CL, Alarcon-Chaidez F, Gross DC (1999) Pseudomonas syringae phytotoxins: mode of action, regulation, and biosynthesis by peptide and polyketide synthetases. Microbiol Mol Biol Rev 63: 266-292
6. Berger S, Sinha AK, Roitsch T (2007) Plant physiology meets phytopathology: plant primary metabolism and plant pathogen interactions. J Exp Bot 58: 4019-4026
7. Bolton MD (2009) Primary metabolism and plant defense - fuel for the fire. Mol Plant Microbe Interact 22: 487-497
8. Bonfig KB, Schreiber U, Gabler A, Roitsch T, Berger S (2006) Infection with virulent and avirulent P. syringae strains differentially affects photosynthesis and sink metabolism in Arabidopsis leaves. Planta 225: 1-12
9. Buschmann C, Lichtenthaler HK (1998) Principles and characteristics of multi-colour fluorescence imaging of plants. J Plant Physiol 152: 297-314
10. Buschmann C, Langsdorf G, Lichtenthaler HK (2000) Imaging of the blue, green, and red fluorescence emission of plants: an overview. Photosynthetica 38: 483-491
11. Chaerle L, Van der Straeten D (2000) Imaging techniques and the early detection of plant stress. Trends Plant Sci 5: 495-501
12. Chaerle L, Van der Straeten D (2001) Seeing is believing: imaging techniques to monitor plant health. Biochim Biophys Acta 1519: 153-166
13. Chaerle L, Van Caeneghem W, Messens E, Lambers H, Van Montagu M, Van der Straeten D (1999) Presymptomatic visualization of plant-virus interactions by thermography. Nat Biotechnol 17: 813-816
14. Chaerle L, Hagenbeek D, De Bruyne E, Valcke R, Van der Straeten D (2004) Thermal and chlorophyll-fluorescence imaging distinguish plant-pathogen interactions at an early stage. Plant Cell Physiol 45: 887-896
15. Chaerle L, Pineda M, Romero-Aranda R, Van der Straeten D, Barón M (2006) Robotized thermal and chlorophyll fluorescence imaging of pepper mild mottle virus infection in Nicotiana benthamiana. Plant Cell Physiol 47: 1323-1336
16. Chaerle L, Leinonen I, Jones HG, Van der Straeten D (2007a) Monitoring and screening plant populations with combined thermal and chlorophyll fluorescence imaging. J Exp Bot 58: 773-784
17. Chaerle L, Lenk S, Hagenbeek D, Buschmann C, Van Der Straeten D (2007b) Multicolour fluorescence imaging for early detection of the hypersensitive reaction to tobacco mosaic virus. J Plant Physiol 164: 253-262
18. Chen JY, Wen PF, Kong WF, Pan QH, Zhan JC, Li JM, Wan SB, Huang WD (2006) Effect of salicylic acid on phenylpropanoids and phenylalanine ammonia-lyase in harvested grape berries. Postharvest Biol Technol 40: 64-72
19. Cheynier V, Comte G, Davies KM, Lattanzio V, Martens S (2013) Plant phenolics: recent advances on their biosynthesis, genetics, and ecophysiology. Plant Physiol Biochem 72: 1-20
20. Chun OK, Kim DO (2004) Consideration on equivalent chemicals in total phenolic assay of chlorogenic acid-rich plums. Food Res Int 37: 337-342
21. Cuppels D (1986) Generation and characterization of Tn5 insertion mutations in Pseudomonas syringae pv. tomato. Appl Environ Microbiol 51: 323-327
22. Denancé N, Sánchez-Vallet A, Goffner D, Molina A (2013) Disease resistance or growth: the role of plant hormones in balancing immune responses and fitness costs. Front Plant Sci 4
23. Dixon RA, Achnine L, Kota P, Liu CJ, Srinivasa Reddy MS, Wang L (2002) The phenylpropanoid pathway and plant defence - a genomics perspective. Mol Plant Pathol 3: 371-390
24. Dong J, Wan G, Liang Z (2010) Accumulation of salicylic acid-induced phenolic compounds and raised activities of secondary metabolic and antioxidative enzymes in Salvia miltiorrhiza cell culture. J Biotechnol 148: 99-104
25. Dorey S, Kopp M, Geoffroy P, Fritig B, Kauffmann S (1999) Hydrogen peroxide from the oxidative burst is neither necessary nor sufficient for hypersensitive cell death induction, phenylalanine ammonia lyase stimulation, salicylic acid accumulation, or scopoletin consumption in cultured tobacco cells treated with elicitin. Plant Physiol 121: 163-172
26. Fillingham AJ, Wood J, Bevan JR, Crute IR, Mansfield JW, Taylor JD, Vivian A (1992) Avirulence genes from Pseudomonas syringae pathovars phaseolicola and pisi confer specificity towards both host and non-host species. Physiol Mol Plant Pathol 40: 1-15
27. Freeman BC, Beattie GA (2009) Bacterial growth restriction during host resistance to Pseudomonas syringae is associated with leaf water loss and localized cessation of vascular activity in Arabidopsis thaliana. Mol Plant Microbe Interact 22: 857-867
28. Gálvez M, Martín-Cordero C, Houghton PJ, Ayuso MJ (2005) Antioxidant activity of methanol extracts obtained from Plantago species. J Agric Food Chem 53: 1927-1933
29. Glenn DM (2012) Infrared and chlorophyll fluorescence imaging methods for stress evaluation. HortScience 47: 697-698
30. Göhre V, Jones AME, Sklenář J, Robatzek S, Weber APM (2012) Molecular crosstalk between PAMP-triggered immunity and photosynthesis. Mol Plant Microbe Interact 25: 1083-1092
31. Gómez-Gómez L, Boller T (2002) Flagellin perception: a paradigm for innate immunity. Trends Plant Sci 7: 251-256
32. Jones HG (1999) Use of thermography for quantitative studies of spatial and temporal variation of stomatal conductance over leaf surfaces. Plant Cell Environ 22: 1043-1055
33. Jones JDG, Dangl JL (2006) The plant immune system. Nature 444: 323-329
34. Jones AME, Thomas V, Bennett MH, Mansfield J, Grant M (2006) Modifications to the Arabidopsis defense proteome occur prior to significant transcriptional change in response to inoculation with Pseudomonas syringae. Plant Physiol 142: 1603-1620
35. Kabiri R, Nasibi F, Farahbakhsh H (2014) Effect of exogenous salicylic acid on some physiological parameters and alleviation of drought stress in Nigella sativa plant under hydroponic culture. Plant Protect Sci 50: 41-51
36. Kangasjärvi S, Neukermans J, Li S, Aro EM, Noctor G (2012) Photosynthesis, photorespiration, and light signalling in defence responses. J Exp Bot 63: 1619-1636
37. Kliebenstein DJ (2014) Orchestration of plant defense systems: genes to populations. Trends Plant Sci 19: 250-255
38. Koes RE, Quattrocchio F, Mol JNM (1994) The flavonoid biosynthetic pathway in plants: function and evolution. Bioessays 16: 123-132
39. Kumar AS, Lakshmanan V, Caplan JL, Powell D, Czymmek KJ, Levia DF, Bais HP (2012) Rhizobacteria Bacillus subtilis restricts foliar pathogen entry through stomata. Plant J 72: 694-706
40. Lee S, Ishiga Y, Clermont K, Mysore KS (2013a) Coronatine inhibits stomatal closure and delays hypersensitive response cell death induced by nonhost bacterial pathogens. PeerJ 1: e34
41. Lee S, Yang DS, Uppalapati SR, Sumner LW, Mysore KS (2013b) Suppression of plant defense responses by extracellular metabolites from Pseudomonas syringae pv. tabaci in Nicotiana benthamiana. BMC Plant Biol 13: 65
42. Li XZ, Starratt AN, Cuppels DA (1998) Identification of tomato leaf factors that activate toxin gene expression in Pseudomonas syringae pv. tomato DC3000. Phytopathology 88: 1094-1100
43. López-Gresa MP, Maltese F, Bellés JM, Conejero V, Kim HK, Choi YH, Verpoorte R (2010) Metabolic response of tomato leaves upon different plant-pathogen interactions. Phytochem Anal 21: 89-94
44. Maestro-Durán R, Borja Padilla R, Martín Martín A, Fiestas de Ursinos JA, Alba Mendoza J (1991) Biodegradación de los compuestos fenólicos presentes en el alpechín. Grasas Aceites 42: 271-276
45. Mansfield J, Genin S, Magori S, Citovsky V, Sriariyanum M, Ronald P, Dow M, Verdier V, Beer SV, Machado MA, Toth I, Salmond G, Foster GD (2012) Top 10 plant pathogenic bacteria in molecular plant pathology. Mol Plant Pathol 13: 614-629
46. Melotto M, Underwood W, Koczan J, Nomura K, He SY (2006) Plant stomata function in innate immunity against bacterial invasion. Cell 126: 969-980
47. Melotto M, Underwood W, He SY (2008) Role of stomata in plant innate immunity and foliar bacterial diseases. Annu Rev Phytopathol 46: 101-122
48. Milosevic N, Slusarenko AJ (1996) Active oxygen metabolism and lignification in the hypersensitive response in bean. Physiol Mol Plant Pathol 49: 143-158
49. Montillet JL, Leonhardt N, Mondy S, Tranchimand S, Rumeau D, Boudsocq M, Garcia AV, Douki T, Bigeard J, Lauriere C, Chevalier A, Castresana C, Hirt H (2013) An abscisic acid-independent oxylipin pathway controls stomatal closure and immune defense in Arabidopsis. PLoS Biol 11: e1001513
50. Murchie EH, Lawson T (2013) Chlorophyll fluorescence analysis: a guide to good practice and understanding some new applications. J Exp Bot 64: 3983-3998
51. Nicholson RL, Hammerschmidt R (1992) Phenolic compounds and their role in disease resistance. Annu Rev Phytopathol 30: 369-389
52. Parker D, Beckmann M, Zubair H, Enot DP, Caracuel-Rios Z, Overy DP, Snowdon S, Talbot NJ, Draper J (2009) Metabolomic analysis reveals a common pattern of metabolic re-programming during invasion of three host plant species by Magnaporthe grisea. Plant J 59: 723-737
53. Pastor V, Luna E, Mauch-Mani B, Ton J, Flors V (2013) Primed plants do not forget. Environ Exp Bot 94: 46-56
54. Pineda M, Gaspar L, Morales F, Szigeti Z, Barón M (2008) Multicolor fluorescence imaging of leaves - a useful tool for visualizing systemic viral infections in plants. Photochem Photobiol 84: 1048-1060
55. Poiatti VAD, Dalmas FR, Astarita LV (2009) Defense mechanisms of Solanum tuberosum L. in response to attack by plant-pathogenic bacteria. Biol Res 42: 205-215
56. Preston GM (2000) Pseudomonas syringae pv. tomato: the right pathogen, of the right plant, at the right time. Mol Plant Pathol 1: 263-275
57. Rico A, McCraw SL, Preston GM (2011) The metabolic interface between Pseudomonas syringae and plant cells. Curr Opin Microbiol 14: 31-38
58. Robbins MP, Bolwell GP, Dixon RA (1985) Metabolic changes in elicitor-treated bean cells. Eur J Biochem 148: 563-569
59. Robert-Seilaniantz A, Grant M, Jones JD (2011) Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annu Rev Phytopathol 49: 317-343
60. Rodríguez-Moreno L, Pineda M, Soukupova J, Macho AP, Beuzon CR, Barón M, Ramos C (2008) Early detection of bean infection by Pseudomonas syringae in asymptomatic leaf areas using chlorophyll fluorescence imaging. Photosynth Res 96: 27-35
61. Rojas CM, Senthil-Kumar M, Tzin V, Mysore K (2014) Regulation of primary plant metabolism during plant-pathogen interactions and its contribution to plant defense. Front Plant Sci 5
62. Rolfe SA, Scholes JD (2010) Chlorophyll fluorescence imaging of plant-pathogen interactions. Protoplasma 247: 163-175
63. Sawinski K, Mersmann S, Robatzek S, Bohmer M (2013) Guarding the green: pathways to stomatal immunity. Mol Plant Microbe Interact 26: 626-632
64. Scharte J, Schon H, Weiss E (2005) Photosynthesis and carbohydrate metabolism in tobacco leaves during an incompatible interaction with Phytophtohora nicotianae. Plant Cell Environ 28: 1421-1435
65. Simon C, Langlois-Meurinne M, Bellvert F, Garmier M, Didierlaurent L, Massoud K, Chaouch S, Marie A, Bodo B, Kauffmann S, Noctor G, Saindrenan P (2010) The differential spatial distribution of secondary metabolites in Arabidopsis leaves reacting hypersensitively to Pseudomonas syringae pv. tomato is dependent on the oxidative burst. J Exp Bot 61: 3355-3370
66. Sørhagen K, Laxa M, Peterhansel C, Reumann S (2013) The emerging role of photorespiration and non-photorespiratory peroxisomal metabolism in pathogen defence. Plant Biol (Stuttg) 15: 723-736
67. Swarbrick PJ, Schulze-Lefert P, Scholes JD (2006) Metabolic consequences of susceptibility and resistance (race-specific and broad-spectrum) in barley leaves challenged with powdery mildew. Plant Cell Environ 29: 1061-1076
68. Takács Z, Lichtenthaler HK, Tuba Z (2000) Fluorescence emission spectra of desiccation-tolerant cryptogamic plants during a rehydration-desiccation cycle. J Plant Physiol 156: 375-379
69. Tao Y, Xie Z, Chen W, Glazebrook J, Chang HS, Han B, Zhu T, Zou G, Katagiri F (2003) Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae. Plant Cell 15: 317-330
70. Thilmony R, Underwood W, He SY (2006) Genome-wide transcriptional analysis of the Arabidopsis thaliana interaction with the plant pathogen Pseudomonas syringae pv. tomato DC3000 and the human pathogen Escherichia coli O157:H7. Plant J 46: 34-53
71. Truman W, de Zabala MT, Grant M (2006) Type III effectors orchestrate a complex interplay between transcriptional networks to modify basal defence responses during pathogenesis and resistance. Plant J 46: 14-33
72. Vargas P, Felipe A, Michán C, Gallegos MT (2011) Induction of Pseudomonas syringae pv. tomato DC3000 MexAB-OprM multidrug efflux pump by flavonoids is mediated by the repressor PmeR. Mol Plant Microbe Interact 24: 1207-1219
73. Ward JL, Forcat S, Beckmann M, Bennett M, Miller SJ, Baker JM, Hawkins ND, Vermeer CP, Lu C, Lin W, Truman WM, Beale MH, Draper J, Mansfield JW, Grant M (2010) The metabolic transition during disease following infection of Arabidopsis thaliana by Pseudomonas syringae pv. tomato. Plant J 63: 443-457
74. Yang S, Peng Q, San Francisco M, Wang Y, Zeng Q, Yang CH (2008) Type III secretion system genes of Dickeya dadantii 3937 are induced by plant phenolic acids. PLoS One 3: e2973
75. Zeng W, Melotto M, He SY (2010) Plant stomata: a checkpoint of host immunity and pathogen virulence. Curr Opin Biotechnol 21: 599-603
76. Zheng XY, Spivey NW, Zeng W, Liu PP, Fu ZQ, Klessig DF, He SY, Dong X (2012) Coronatine promotes Pseudomonas syringae virulence in plants by activating a signaling cascade that inhibits salicylic acid accumulation. Cell Host Microbe 11: 587-596
77. Zhishen J, Mengcheng T, Jianming W (1999) The determination of flavonoid contents in mulberry and their scavenging effects on superoxide radicals. Food Chem 64: 555-559
78. Zou J, Rodriguez-Zas S, Aldea M, Li M, Zhu J, Gonzalez DO, Vodkin LO, DeLucia E, Clough SJ (2005) Expression profiling soybean response to Pseudomonas syringae reveals new defense-related genes and rapid HR-specific downregulation of photosynthesis. Mol Plant Microbe Interact 18: 1161-1174