Redox activities and ROS, NO and phenylpropanoids production by axenically cultured intact olive seedling roots after interaction with a mycorrhizal or a pathogenic fungus

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  Espinosa, Francisco ^a   Garrido, Inmaculada ^a   Ortega, Alfonso ^a   Casimiro, Ilda ^a   Álvarez Tinaut, Ma Carmen ^a  

^a UNIVERSITY OF EXTREMADURA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

FLAVONOID; JASMONIC ACID METHYL ESTER; NITRIC OXIDE; PEROXIDASE; PHENOL DERIVATIVE; PHENYLPROPANOID GLYCOSIDE; PLANT GLYCOSIDE; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; SUPEROXIDE; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG; ACETIC ACID DERIVATIVE; ANTIOXIDANT; CYCLOPENTANE DERIVATIVE; OXYLIPIN;

APOPLAST; ARTICLE; AXENIC CULTURE; BIOSYNTHESIS; CONTROLLED STUDY; CYTOSOL; MYCORRHIZA; NONHUMAN; OLIVE; OXIDATION REDUCTION REACTION; PLANT DEFENSE; PLANT FUNGUS INTERACTION; PLANT ROOT; RESPIRATORY BURST; RHIZOPHAGUS IRREGULARIS; SEEDLING; VERTICILLIUM DAHLIAE; CHEMISTRY; CULTURE TECHNIQUE; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; HOST PATHOGEN INTERACTION; METABOLISM; MICROBIOLOGY; OLIVE TREE; PHYSIOLOGY; SYMBIOSIS;

ACETATES; ANTIOXIDANTS; CULTURE TECHNIQUES; CYCLOPENTANES; HOST-PATHOGEN INTERACTIONS; MYCORRHIZAE; NITRIC OXIDE; OLEA; OXIDATION-REDUCTION; OXYLIPINS; PHENOLS; REACTIVE OXYGEN SPECIES; SEEDLING; SYMBIOSIS;

EID: 84903398931     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0100132     Document Type: Article

References (66)

1. Apel K, Hirt H (2004) Reactive oxygen species: Metabolism, oxidative stress and signal transduction. Ann Rev Plant Biol 109: 1247-1257.
2. Wrzaczek M, Brosché M, Kangasjärvi J (2013) ROS signaling loops-production, perception, regulation. Curr Opin Plant Biol 16: 1-8.
3. Bolwell GP, Page A, Pislewska M, Wojtaszek P (2001) Phatogenic infection and the oxidative defences in plant apoplast. Protoplasma 217: 20-32. (Pubitemid 32657042)
4. O'Brien JA, Daudi A, Butt AS, Bolwell GP (2012) Reactive oxygen species and their role in plant defence and cell wall metabolism. Planta 236: 765-779.
5. Garrido I, Espinosa F, Córdoba-Pedregosa MC, González-Reyes JA, Alvarez-Tinaut MC (2003) Redox related peroxidative responses evoked by Methyl-Jasmonate in axenically cultured aeroponic sunflower (Helianthus annuus, L.) seedling roots. Protoplasma 221(1-2): 79-91. (Pubitemid 36658587)
6. Garrido I, Espinosa F, Álvarez-Tinaut MC (2009) Oxidative defence reactions in sunflower roots induced by methyl-jasmonate and methyl-salicylate and their relations with calcium signaling. Protoplasma 237: 27-39.
7. Nanda K, Emilie A, Daniel M, Pauly N, Dunand C (2010) Reactive oxygen species during plant-microorganism early interactions. J Integ Plant Biol 52(2): 195-204.
8. Torres MA, Dangl JL, Jones JDG (2006) Reactive oxygen species signalling in response to pathogens. Plant Physiol 141: 373-378. (Pubitemid 43974530)
9. Bolwell GP, Bindschedler LV, Blee KA, Butt VS, Davies DR, et al. (2002) The apoplastic oxidative burst in response to biotic stress in plants: a three-component systems. J Exp Bot 53: 1367-1376. (Pubitemid 34544056)
10. O'Connell RJ, Panstruga R (2006) Tête à tête inside a plant cell: establishing compatibility between plants and biotrophic fungi and oomycetes. New Phytol 171: 699-718. (Pubitemid 44175192)
11. Catanzariti AM, Dodds PN, Lawrence GJ, Ayliffe MA, Ellis JG (2005) Haustorially expressed secreted proteins from flax rust are highly enriched for avirulence elicitos. Plant Cell 18: 243-256. (Pubitemid 43951327)
12. Chisholm ST, Coaker G, Day B, Staskaeicz BJ (2006) Host-microbe interactions: shapping the evolution of the plant immune response. Cell 124: 803-814. (Pubitemid 43261453)
13. Heller J, Tudzynski P (2011) Reactive oxygen species in phytopathogenic fungi: signaling, development, and disease. Annu Rev Phytopathol 49: 369-390.
14. Garrido I, Caraballo-Sánchez AM, Llerena JL, Espinosa F (2012) Oxidative reactions in axenically seedling roots of olive (Olea europaea, L.) Plant Growth Regul 68: 203-210.
15. Dixon RY, Achnine L, Kota P, Liu CHJ, Reddy MSS, et al. (2002) The phenylpropanoid pathway and plant defence - a genomics perspective. Mol Plant Pathol 3: 371-390.
16. 2, peroxidase and lignins and drives PAL gene expresión. BMC Plant Biol 10: 232.
17. Harborne JB, Williams CA (2000) Advances in flavonoid research since 1992. Phytochemistry 55: 481-504.
18. Shi FM, Li YZ (2008) Verticillium dahliae toxins-induced nitric oxide production in Arabidopsis is major dependent on nitrate reductase. BMB Rep 41: 79-85.
19. Gupta KJ, Fernier AR, Kaiser WM, van Dongen JT (2011) On the origin of nitric oxid. Trends Plant Sci 16: 160-168.
20. Neill SJ, Desikan R, Clarke A, Hurst RD, Hancock JT (2002) Hydrogen peroxide and nitric oxide as signaling molecules in plants. J Exp Bot 53: 1237-1247. (Pubitemid 34544046)
21. Wendehenne D, Durner J, Klessing DF (2004) Nitric oxide: a new player in plant signaling and defence responses. Curr Opin Plant Biol 7: 449-455. (Pubitemid 38871620)
22. van Baarlen P, Woltering EJ, Staats M, van Kan JAL (2004) Histochemical and genetic analysis of host and non-host interactions of Arabidopsis with three Botrytis species: an important role for cell death control. Mol Plant Pathol 8: 41-54. (Pubitemid 46066636)
23. Gianinazzi-Pearson V, Séjalon-Delmas N, Genre A, Jeandroz S, Bonfante P (2008) Plants and Arbuscular Mycorrhizal Fungi: Cues and Communication in the Early Steps of Symbiotic Interactions. Adv Bot 46: 181-219.
24. Calcagno C, Novero M, Genre A, Bonfante P, Lanfranco L (2012) The exudate from an arbuscular mycorrhizal fungus induces nitric oxide accumulation in Medicago truncata roots. Mycorrhiza 22: 259-269.
25. Zeidler D, Zahringer U, Gerber I, Dubery I, Hartung T, et al. (2004). Innate immunity in Arabidopsis thaliana: lipopolysaccharides activate nitric oxide synthase (NOS) and induce defense genes. Proc Natl Acad Sci USA 101: 15811-15816. (Pubitemid 39473570)
26. Scheler C, Durner J, Astier J (2013) Nitric oxid and reactive oxygen species in plant biotic interactions. Curr Op Biol 16: 534-539.
27. Salzer P, Corbière H, Boller T (1999) Hydrogen peroxide accumulation in Medicago truncata roots colonized by the arbuscular mycorrhiza-forming fungus Glomus intraradices. Planta 208: 319-325.
28. Fester T, Hause G (2005) Accumulation of reactive oxygen species in arbuscular mycorrhizal roots. Mycorrhiza 15: 373-379. (Pubitemid 40968300)
29. Lambais MR, Rios-Ruiz WF, Andrade RM (2003) Antioxidant responses in bean (Phaseolus vulgaris) roots colonized by arbuscular mycorrhizal fungi. New Phytol 160: 421-428. (Pubitemid 37298619)
30. Baptista P, Martins A, Pais MS, Tavares RM, Lino-Neto T (2007) Involvement of reactive oxygen species during early stages of ectomycorrhiza establishment between Castanea sativa and Pisolithus tinctorius. Mycorrhiza 17: 188-193.
31. Dotan Y, Lichtenberg D, Pinchuk I (2004) Lipid peroxidation cannot be used as a universal criterion of oxidative stress. Prog Lipid Res 43: 200-227. (Pubitemid 38299193)
32. Dumas-Gaudot E, Gollotte A, Cordier C, Gianinazzi S, Gianinazzi-Pearson V (2000) Modulation of the host defence systems. In: Kapulnik Y, Douds DD (eds) Arbuscular mycorrhizas: physiology and function. Kluwer, Dordrecht, 173-200.
33. García-Garrido JM, Ocampo J (2002) Regulation of the plant defence response in arbuscular mycorrhizal symbiosis. J Exp Bot 53: 1377-1386. (Pubitemid 34589552)
34. Liu J, Blaylock LA, Endre G, Choc J, Town CD, et al. (2003) Transcript profiling coupled with spatial expression analyses reveals genes involved in distinct developmental stages of an arbuscular mycorrhizal symbiosis. Plant Cell 15: 2106-2123. (Pubitemid 37144064)
35. Kapulnik Y, Volpin H, Itzhaki H, Ganon D, Galili S, et al. (1996) Supression of defence responses in mycorrhizal alfalfa tobacco roots. New Phytol 133: 59-64. (Pubitemid 126558382)
36. Spanu P, Boller T, Ludwig A, Wiemken A, Faccio A, et al. (1989) Chitinase in roots of mycorrhizal Allium porrum: regulation and localization. Planta 177(4): 447-455.
37. Hause B, Fester T (2005) Molecular and cell biology of arbuscular mycorrhizal symbiosis. Planta 221: 184-196. (Pubitemid 40660380)
38. Peipp H, Maier W, Schmidt J, Wray V, Strack D (1997) Arbuscular mycorrhizal fungus-induced changes in the accumulation of secondary compounds in barley roots. Phytochemistry 44: 581-587. (Pubitemid 27073853)
39. Blilou I, Ocampo JA, García-Garrido JM (2000) Induction of Ltp (lipid transfer protein) and Pal (phenylalanine ammonia-lyase) gene expresión in rice roots colonized by the arbuscular mycorrhizal fungus Glomus mosseae. J Exp Bot 51: 1969-1977. (Pubitemid 32100624)
40. Seo HS, Song JT, Cheong JJ, Lee YH, Lee YW, et al. (2001) Jasmonic acid carboxylmethyltransferase: a key enzyme for jasmonate-regulated plant responses. Proc Natl Acad Sci USA 98: 4788-4793. (Pubitemid 32295054)
41. Staswick PE (1992) Jsmonate, genes and fragante signals. Plant Physiol 99: 804-807.
42. Jiménez-Díaz RM, Tjamos EC, Cirulli M (1998) Verticillium wilt of major tree hosts: olive. Hiemstra JA, Harris DC (Eds.), A Compendium of Verticillium Wilt in Tree Species, Pousen and Looijen, Wageningen, The Netherlands, 13-16.
43. Estaún V, Camprubí A, Clavet C, Pinochet J (2003) Nursery and field response of olive trees inoculated with arbuscular mycorrhizal fungi, Glomus intraradices and Glomus mossea. J Amer Soc Hort Sci 128(5): 767-775. (Pubitemid 36941414)
44. Cañas LA, Carramolino L, Vicente M (1987) Vegetative propagation of the olive tree from in vitro cultured embryos. Plant Sci 50: 85-90.
45. St-Arnaud M, Hamel C, Vimard B, Caron M, Fortin JA (1996) Enhanced hyphal growth and spore production of the arbuscular mycorrhizal fungus G. intraradices in an in vitro system in the absence of host roots. Mycol Res 100: 328-332.
46. Krüger M, Krüger C, Walker C, Stockinger H, Schübler A (2012) Phylogenetic reference data for systematics and phylotaxonomy of arbuscular mycorrhizal fungi from phylum to species level. New Phytol 193: 970-984.
47. Bécard GA, Fortin JA (1988) Early events of vesicular-arbuscular mycorrhiza formation on Ri T-DNA transformed roots. New Phytol 108(2): 211-218.
48. Misra HR, Fridovich I (1972) The univalent reduction of oxygen by reduced flavins and quinones. J Biol Chem 24: 188-192.
49. Ngo TT, Lenhoff HM (1980) A sensitive and versatile chromogenic assay for peroxidase-coupled reactions. Anal Biochem 105: 389-397.
50. McCord JM, Fridovich JM (1996) Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). J Biol Chem 244(22): 6049-55.
51. Singleton VL, Rossi JA (1965) Colorimetry of total phenolics with phosphomo-lybdic-phosphotungstic acid reagents. Amer J Enol Vitic 16: 144-158.
52. Kim D, Jeong SW, Leo CY (2003) Antioxidant capacity of phenolic phytochemicals from various cultivars of plums, Food Chem 81: 321-326. (Pubitemid 36349460)
53. Gálvez M, Martín-Cordero C, Houghton PJ, Ayuso MJ (2008) Antioxidant activity of methanol extracts obtained from Plantago species. J Agric Food Chem 53(6): 1927-1933.
54. Rodríguez-Serrano M, Romero-Puertas MC, Zabalza A, Corpas FJ, Gómez M, et al. (2006) Cadmium effect on oxidative metabolism of pea (Pisum sativum L.) roots: imaging of reactive oxygen species and nitric oxide accumulation in vivo. Plant Cell Environ 29: 1532.
55. Egan MJ, Wang ZY, Jones MA, Smirnoff N, Talbot NJ (2007) Generation of reactive oxygen species by fungal NADPH oxidases is required for rice blast disease. Proc Natl Acad Sci USA 104: 11772-11777. (Pubitemid 47175088)
56. Samalova M, Johnson J, Illes M, Kelly S, Fricker M, et al. (2013) Nitric oxide generated by the rice blast fungus Magnaporthe oryzae drives plant infection. New Phytol 197: 207-222.
57. Ruiz-Lozano JM, Cllados C, Barea JM, Azcón R (2001) Cloning of cDNAs encoding SODs from lettuce plants which show differential regulation by arbuscular mycorrhizal symbiosis and by drought stress. J Exp Bot 52: 2241-2242. (Pubitemid 33045005)
58. Passardi F, Cosio C, Penel C, Dunand C (2005) Peroxidases have more functions than a Swiss army knife. Plant Cell Rep 24: 255-265. (Pubitemid 41116471)
59. Tsai SM, Phillips DA (1991) Flavonoids released naturally from alfalfa promote development of symbiotic Glomus spores in vitro. Appl Environ Microbiol. 57: 1485-8.
60. Vierheilig H, Piche Y (2002) Signalling in arbuscular mycorrhiza, facts and hypotheses. In: Buslig B, Manthey J, (eds). Flavonoids in cell functions. New York: Kluwer Academic/Plenum Publishers, 23-39. (Pubitemid 34526421)
61. Abdel-Lateif K, Bogusz D, Hocher V (2012) The role of flavonoids in the establishment of plant roots endosymbioses with arbuscular mycorrhiza fungi, rhizobia and Frankia bacteria. Plant Signal Behav 7 (6): 636-641.
62. 2 andOH) by maize roots and their role in wall loosening and elongation growth. Plant Physiol 136: 3114-3123.
63. Foissner I, Wendehenne D, Langebartels C, Durner J (2000) In vivo imaging of an elicitor-induced nitric oxide burst in tobacco. Plant J 23(6): 817-824.
64. Correa-Aragunde N, Lombardo C, Lamattina L (2008) Nitric oxide: an active molecule that modulages cellulose synthesis in tomato roots. New Phytol 179: 247-249.
65. Siciliano V, Genre A, Balestrini R, Cappellazzo G, DeWitt P, et al. (2007) Transcriptome analysis of arbuscular mycorrhizal roots during development of the prepenetration apparatus. Plant Physiol 144: 1455-1466. (Pubitemid 47037464)
66. Wojtaszek P (1997) Oxidative burst: an early plant response to pathogen infection. Biochem j 322: 681-692.