Modulation of cellular redox status by thiamine-activated NADPH oxidase confers Arabidopsis resistance to Sclerotinia sclerotiorum

Journal of Experimental Botany

Volumn 64, Issue 11, 2013, Pages 3261-3272

  Zhou, Jun ^a   Sun, Aizhen ^a   Xing, Da ^a  

^a Institute of Laser Life Science   (China)

Author keywords

Callose; NADPH oxidase; oxalate; redox status; Sclerotinia; thiamine.

Indexed keywords

CALLOSE; OXALIC ACID; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; THIAMINE;

ARABIDOPSIS; ARTICLE; ASCOMYCETES; DISEASE RESISTANCE; DRUG EFFECT; ENZYMOLOGY; METABOLISM; MICROBIOLOGY; OXIDATION REDUCTION REACTION; PATHOGENICITY; REDOX STATUS; SCLEROTINIA; THIAMINE.;

CALLOSE; NADPH OXIDASE; OXALATE; REDOX STATUS; SCLEROTINIA; THIAMINE.;

ARABIDOPSIS; ASCOMYCOTA; DISEASE RESISTANCE; NADPH OXIDASE; OXIDATION-REDUCTION; THIAMINE;

EID: 84882358513     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/ert166     Document Type: Article

References (47)

1. Ahn IP, Kim S, Lee YH, Suh SC. 2007. Vitamin B1-induced priming is dependent on hydrogen peroxide and the NPR1 gene in Arabidopsis. Plant Physiology 143, 838-848.
2. Ahn IP, Kim S. Lee YH. 2005. Vitamin B1 functions as an activator of plant disease resistance. Plant Physiology 138, 1505-1515.
3. Asensi-Fabado MA, Munné-Bosch S. 2010. Vitamins in plants: occurrence, biosynthesis and antioxidant function. Trends in Plant Science 15, 582-592.
4. Azami-Sardooei Z, França SC, Vleesschauwer DD, Höfte M. 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.
5. Bateman DF, Beer SV. 1965. Simultaneous production and synergistic action of oxalic acid and polygalacturonase during pathogenesis by Sclerotiorum rolfsii. Phytopathology 55, 204-211.
6. Bolton MD, Thomma BPHJ, Nelson BD. 2006. Pathogen profile Sclerotinia sclerotiorum Lib.de Bary: biology and molecular traits of a cosmopolitan pathogen. Molecular Plant Pathology 7, 1-16.
7. Cessna SG, Sears VE, Dickman MB, Low PS. 2000. Oxalic acid, a pathogenicity factor for Sclerotinia sclerotiorum, supresses the oxidative burst of the host plant. Plant Cell 12, 2191-2199.
8. Dong X, Ji R, Guo X, Foster S, et al. 2008. Expressing a gene encoding wheat oxalate oxidase enhances resistance to Sclerotinia sclerotiorum in oilseed rape. Planta 228, 331-340.
9. Errakhi R, Meimoun P, Lehner A, Vidal G, Briand J, Corbineau F, Rona JP, Bouteau F. 2008. Anion channel activity is necessary to induce ethylene synthesis and programmed cell death in response to oxalic acid. Journal of Experimental Botany 59, 3121-3129.
10. Foyer CH, Noctor G. 2005. Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17, 1866-1875.
11. Foyer CH, Noctor G. 2011. Ascorbate and glutathione: the heart of the redox hub. Plant Physiology 155, 2-18.
12. Godoy G, Steadman JR, Dickman MB, Dam R. 1990. Use of mutants to demonstrate the role of oxalic acid in pathogenicity of Sclerotinia sclerotiorum on Phaseolus vulgaris. Physiological and Molecular Plant Pathology 37, 179-191.
13. Goyer A. 2010. Thiamine in plants: aspects of its metabolism and functions. Phytochemistry 71, 1615-1624.
14. Guimarães RL, Stotz HU. 2004. Oxalate production by Sclerotinia sclerotiorum deregulates guard cells during infection. Plant Physiology 136, 3703-3711.
15. Guo XM, Stotz HU. 2010. ABA signaling inhibits oxalate-induced production of reactive oxygen species and protects against Sclerotinia sclerotiorum in Arabidopsis thaliana. European Journal of Plant Pathology 128, 7-19.
16. Hardham AR, Jones DA, Takemoto D. 2007. Cytoskeleton and cell wall function in penetration resistance. Current Opinion in Plant Biology 10, 342-348.
17. Hegedus DD, Rimmer SR. 2005. Sclerotinia sclerotiorum: When "to be or not to be" a pathogen FEMS Microbiology Letters 251, 177-184.
18. Hu X, Bidney DL, Yalpani N, et al. 2003. Overexpression of a gene encoding hydrogen peroxide-generating oxalate oxidase evokes defense responses in sunflower. Plant Physiology 133, 170-181.
19. Huang YB, Xie XL, Yang L, Zhang J, Li GQ, Jiang DH. 2011. Susceptibility of Sclerotinia sclerotiorum strains different in oxalate production to infection by the mycoparasite Coniothyrium minitans. World Journal of Microbiology and Biotechnology 27, 2799-2805.
20. Jabs T, Dietrich RA, Dangl JL. 1996. Initiation of runaway cell death in an Arabidopsis mutant by extracellular superoxide. Science 273, 1853-1856.
21. Jiang F, Zhang Y, Dusting GJ. 2011. NADPH Oxidase-mediated redox signaling: roles in cellular stress response, stress tolerance, and tissue repair. Pharmacological Reviews 63, 218-242.
22. Jiang MY, Zhang JH. 2002. Water stress-induced abscisic acid accumulation triggers the increased generation of reactive oxygen species and up-regulates the activities of antioxidant enzymes in maize leaves. Journal of Experimental Botany 53, 2401-2410.
23. Jung IL, Kim IG. 2003. Thiamin protects against paraquatinduced damage: scavenging activity of reactive oxygen species. Environmental Toxicology and Pharmacology 15, 19-26.
24. Kim KS, Min JY, Dickman MB. 2008. Oxalic acid is an elicitor of plant programmed cell death during Sclerotinia sclerotiorum disease development. Molecular Plant-Microbe Interactions 21, 605-612.
25. Liu J, Zhou J, Xing D. 2012. Phosphatidylinositol 3-kinase plays a vital role in regulation of rice seed vigor via altering NADPH oxidase activity. PLoS ONE 7, e33817.
26. Marino D, Dunand C, Puppo A, Pauly N. 2012. A burst of plant NADPH oxidases. Trends in Plant Science 17, 9-15.
27. Maxwell DP, Lumsden RD. 1970. Oxalic acid production by Sclerotinia sclerotiorum in infected bean and in culture. Phytopathology 60, 1395-1398.
28. Parisy V, Poinssot B, Owsianowski L, Buchala A, Glazebrook J, Mauch F. 2007. Identification of PAD2 as a -glutamylcysteine synthetase highlights the importance of glutathione in disease resistance of Arabidopsis. The Plant Journal 49, 159-172.
29. Pastori GM, Kiddle G, Antoniw J, Bernard S, Veljovic-Jovanovic S, Verrier PJ, Noctor G, Foyer CH. 2003. Leaf vitamin C contents modulate plant defense transcripts and regulate genes that control development through hormone signaling. Plant Cell 15, 939-951.
30. Penfield S, Li Y, Gilday AD, Graham S, Graham IA. 2006. Arabidopsis ABA INSENSITIVE4 regulates lipid mobilization in the embryo and reveals repression of seed germination by the endosperm. Plant Cell 18, 1887-1899.
31. Perchepied L, Balagué C, Riou C, Claudel-Renard C, Rivière 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.
32. Purdy LH. 1979. Sclerotinia sclerotiorum: history, disease and symptomatology, host range, geographic distribution and impact. Phytopathology 69, 875-880.
33. Quagliaro L, Piconi L, Assaloni R, Martinelli L, Motz E, Ceriello A. 2003. Intermittent high glucose enhances apoptosis related to oxidative stress in human umbilical vein endothelial cells: the role of protein kinase C and NADPH-oxidase activation. Diabetes 52, 2795-2804.
34. Queval G, Noctor G. 2007. A plate reader method for the measurement of NAD, NADP, glutathione, and ascorbate in tissue extracts: application to redox profiling during Arabidopsis rosette development. Analytical Biochemistry 363, 58-69.
35. Rao MV, Paliyath G, Ormrod DP. 1996. Ultraviolet-B-and ozoneinduced biochemical changes in antioxidant enzymes of Arabidopsis thaliana. Plant Physiology 110, 125-136.
36. Rapala-Kozik M, Kowalska E, Ostrowska K. 2008. Modulation of thiamine metabolism in Zea mays seedlings under conditions of abiotic stress. Journal of Experimental Botany 59, 4133-4143.
37. Rapala-Kozik M, Wolak N, Kujda M, Banas AK. 2012. The upregulation of thiamine vitamin B1 biosynthesis in Arabidopsis thaliana seedlings under salt and osmotic stress conditions is mediated by abscisic acid at the early stages of this stress response. BMC Plant Biology 12, 2.
38. Sagi M, Fluhr R. 2001. Superoxide production by plant homologues of the gp91phox NADPH oxidase. Modulation of activity by calcium and by tobacco mosaic virus infection. Plant Physiology 126, 1281-1290.
39. Sun AZ, Nie SJ, Xing D. 2012. Nitric oxide-mediated maintenance of redox homeostasis contributes to NPR1-dependent plant innate immunity triggered by lipopolysaccharides. Plant Physiology 160, 1081-1096.
40. Thulke O, Conrath U. 1998. Salicylic acid has a dual role in the activation of defence related genes in parsley. The Plant Journal 14, 35-42.
41. Ton J, Mauch-Mani B. 2004. -Aminobutyric acid induced resistance against necrotrophic pathogens is based on ABAdependent priming of callose. The Plant Journal 38, 119-130.
42. Tu JC. 1985. Tolerance of white bean (Phaseolus vulgaris) to white mold (Sclerotinia sclerotiorum) associated with tolerance to oxalic acid. Physiological Plant Pathology 26, 111-117.
43. Tunc-Ozdemir M, Miller G, Song L, et al. 2009. Thiamin confers enhanced tolerance to oxidative stress in Arabidopsis. Plant Physiology 151, 421-432.
44. Vallet C, Chabbert B, Czaninski Y, Monties B. 1996. Histochemistry of lignin deposition during sclerenchyma differentiation in alfalfa stems. Annals of Botany 78, 625-632.
45. Wang H, Liu G, Zheng Y, Wang X, Yang Q. 2004. Breeding of the Brassica napus cultivar Zhongshuang 9 with high-resistance to Sclerotinia sclerotiorum and dynamics of its important defense enzyme activity. Scientia Agricultura Sinica 2004, 23-28.
46. Williams B, Kabbage M, Kim HJ, Britt R, Dickman MB. 2011. Tipping the balance: Sclerotinia sclerotiorum secreted oxalic acid suppresses host defenses by manipulating the host redox environment. PLoS Pathogens 7, e1002107.
47. Yue HY, Nie SJ, Xing D. 2012. Over-expression of Arabidopsis Bax inhibitor-1 delays methyl jasmonate-induced leaf senescence by suppressing the activation of MAP kinase 6. Journal of Experimental Botany 63, 4463-4474.