Differentially Expressed Proteins and Associated Histological and Disease Progression Changes in Cotyledon Tissue of a Resistant and Susceptible Genotype of Brassica napus Infected with Sclerotinia sclerotiorum

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Garg, Harsh ^a   Li, Hua ^a   Sivasithamparam, Krishnapillai ^a   Barbetti, Martin J ^a  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ETHYLENE; INITIATION FACTOR 5A; VEGETABLE PROTEIN;

ANTIOXIDANT ACTIVITY; ARTICLE; BIOSYNTHESIS; COMPARATIVE STUDY; CONTROLLED STUDY; COTYLEDON; CULTIVAR; DISEASE COURSE; FUNGAL PLANT DISEASE; FUNGUS GROWTH; FUNGUS HYPHAE; GENOTYPE; HISTOPATHOLOGY; INFECTION RESISTANCE; INFECTION SENSITIVITY; INOCULATION; NONHUMAN; PATHOGENESIS; PLANT DEFENSE; PLANT METABOLISM; PLANT RESPONSE; PLANT TISSUE; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN SYNTHESIS; PROTEOMICS; RAPESEED; SCLEROTINIA SCLEROTIORUM; TRANSLATION INITIATION; UPREGULATION; VARIETAS;

ASCOMYCOTA; BRASSICA NAPUS; COTYLEDON; GENOTYPE; PLANT DISEASES; PLANT PROTEINS;

BRASSICA NAPUS; EUKARYOTA; SCLEROTINIA; SCLEROTINIA SCLEROTIORUM;

EID: 84878950858     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0065205     Document Type: Article

References (80)

1. Bolton MD, Thomma BPHJ, Nelson BD, (2006) Sclerotinia sclerotiorum (Lib.) de Bary: biology and molecular traits of a cosmopolitan pathogen. Mol Plant Pathol 7: 1-16.
2. Boland GJ, Hall R, (1994) Index of plant hosts of Sclerotinia sclerotiorum. Can J Plant Pathol 16: 93-108.
3. Hegedus DD, Rimmer RS, (2005) Sclerotinia sclerotiorum: When ''to be or not to be'' a pathogen? FEMS Microbiol Lett 251: 177-184.
4. Hind-Lanoiselet TL (2004) Canola concepts: managing Sclerotinia. Agnote DPI-490, Department of Primary Industries, New South Wales, Wagga Wagga. Available: http://www.australianoilseeds.com/__data/assets/pdf_file/0011/4430/sclerotinia_in_canola.pdf. Accessed 2010 July 28.
5. Li CX, Liu SY, Sivasithamparam K, Barbetti MJ, (2008) New sources of resistance to Sclerotinia stem rot caused by Sclerotinia sclerotiorum in Chinese and Australian Brassica napus and Brassica juncea germplasm screened under Western Australian conditions. Australas Plant Pathol 38: 149-152.
6. Li C, Garg H, Li H, Liu S, Banga S, et al. (2009) Identifying resistance to Sclerotinia stem rot in Brassica napus and B. juncea. 14th International Sclerotinia Workshop, Wilmington, North Carolina, USA. Available: http://www.plantmanagementnetwork.org/proceedings/Sclerotinia/2009. Accessed 2010 March 4.
7. Garg H, Atri C, Sandhu PS, Kaur B, Renton M, et al. (2010) High level of resistance to Sclerotinia sclerotiorum in introgression lines derived from wild crucifers, viz. Erucastrum cardaminoides, Diplotaxis tenuisiliqua and E. abyssinicum species. Field Crops Res 117: 51-58.
8. Lumsden RD, (1979) Histology and physiology of pathogenesis in plant diseases caused by Sclerotinia species. Phytopathology 69: 890-896.
9. 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. Physiol Mol Plant Pathol 37: 179-191.
10. Li R, Rimmer R, Buchwaldt L, Sharpe AG, Seguin-Swartz G, et al. (2004) Interaction of Sclerotinia sclerotiorum with a resistant Brassica napus cultivar: expressed sequence tag analysis identifies genes associated with fungal pathogenesis. Fungal Genet Biol 41: 735-753.
11. Cessna SG, Sears VE, Dickman MB, Low PS, (2000) Oxalic acid, a pathogenicity factor for Sclerotinia sclerotiorum suppresses the oxidative burst of the host plant. Plant Cell 12: 2119-2199.
12. Guimaraes RL, Stotz HU, (2004) Oxalate production by Sclerotinia sclerotiorum deregulates guard cells during infection. Plant Physiol 136: 3703-3711.
13. Li R, Rimmer R, Buchwaldt L, Sharpe AG, Seguin-Swartz G, et al. (2004) Interaction of Sclerotinia sclerotiorum with Brassica napus: cloning and characterization of endo- and exo-polygalacturonases expressed during saprophytic and parasitic modes. Fungal Genet Biol 41: 754-765.
14. Hu X, Bidney DL, Yalpani N, Duvick JP, Crasta O, et al. (2003) Overexpression of a gene encoding hydrogen peroxide-generating oxalate oxidase evokes defense responses in sunflower. Plant Physiol 133: 170-181.
15. Hegedus DD, Li R, Buchwaldt L, Parkin I, Whitwill S, et al. (2008) Brassica napus possesses an expanded set of polygalacturonase inhibitor protein genes that are differentially regulated in response to Sclerotinia sclerotiorum infection, wounding and defense hormone treatment. Planta 228: 241-253.
16. Micic Z, Hahn V, Bauer E, Melchinger AE, Knapp SJ, et al. (2005) Identification and validation of QTL for Sclerotinia midstalk rot resistance in sunflower by selective genotyping Theor Appl Genet. 111: 233-242.
17. Zhao J, Udall JA, Quijada PA, Grau CR, Meng J, et al. (2006) Quantitative trait loci for resistance to Sclerotinia sclerotiorum and its association with a homeologous non-reciprocal transposition in Brassica napus L. Theor Appl Genet. 112: 509-516.
18. Zhao J, Wang J, An L, Doerge RW, Chen ZJ, et al. (2007) Analysis of gene expression profiles in response to Sclerotinia sclerotiorum in Brassica napus. Planta 227: 13-24.
19. Calla B, Vuong T, Radwan O, Hartman GL, Clough SJ, (2009) Gene expression profiling soybean stem tissue early response to Sclerotinia sclerotiorum and in silico mapping in relation to resistance markers. Plant Genome 2: 149-166.
20. Liu R, Zhao J, Xiao Y, Meng J, (2005) Identification of prior candidate genes for Sclerotinia local resistance in Brassica napus using Arabidopsis cDNA microarray and Brassica-Arabidopsis comparative mapping. Sci China C Life Sci 48: 460-470.
21. Yang B, Srivastava S, Deyholos MK, Kav NNV, (2007) Transcriptional profiling of canola (Brassica napus L.) responses to the fungal pathogen Sclerotinia sclerotiorum. Plant Sci 173: 156-171.
22. Zhao J, Buchwaldt L, Rimmer SR, Sharpe A, McGregor L, et al. (2009) Patterns of differential gene expression in Brassica napus cultivars infected with Sclerotinia sclerotiorum. Mol Plant Pathol 10: 635-649.
23. Yang B, Rahman MH, Liang Y, Shah S, Kav NNV, (2010) Characterization of defence signaling pathways of Brassica napus and Brassica carinata in response to Sclerotinia sclerotiorum challenge. Plant Mol Biol Rep 28: 253-263.
24. Eynck C, Seguin-Swartz G, Clarke WE, Parkin IAP, (2012) Monolignol biosynthesis is associated with resistance to Sclerotinia sclerotiorum in Camelina sativa. Mol Plant Pathol 13: 887-899.
25. Liang Y, Srivastava S, Rahman MH, Strelkov SE, Kav NNV, (2008) Proteome changes in leaves of Brassica napus L. as a result of Sclerotinia sclerotiorum challenge. J Agric Food Chem 56: 1963-1976.
26. Yajima W, Kav NNV, (2006) The proteome of the phytopathogenic fungus Sclerotinia sclerotiorum. Proteomics 6: 5995-6007.
27. Colditz F, Krajinski F, Niehaus K (2007) Plant proteomics upon fungal attack. In: Šamaj J, Thelen J, eds. Plant Proteomics, Heidelberg: Springer. 283-309.
28. Sharma N, Hotte N, Rahman MH, Mohammadi M, Deyholos MK, et al. (2008) Towards identifying Brassica proteins involved in mediating resistance to Leptosphaeria maculans: A proteomics-based approach. Proteomics 8: 3516-3535.
29. Mehta A, Brasileiro ACM, Souza DSL, Romano E, Campos MA, et al. (2008) Plant-pathogen interaction: what is proteomics telling us? FEBS J 275: 3731-3746.
30. Gygi SP, Rochon Y, Franza BR, Aebersold BR, (1999) Correlation between protein and mRNA abundance in yeast. Mol Cell Biol 19: 1720-1730.
31. Carpentier SC, Coemans B, Podevin N, Laukens K, Wittes E, et al. (2008) Functional genomics in a non-model crop: transcriptomics or proteomics? Physiol Plant 133: 117-130.
32. Garg H, Sivasithamparam K, Banga SS, Barbetti MJ, (2008) Cotyledon assay as a rapid and reliable method of screening for resistance against Sclerotinia sclerotiorum in Brassica napus genotypes. Australas Plant Pathol 37: 106-111.
33. Garg H, Kohn LM, Andrew M, Hua Li, Sivasithamparam K, et al. (2010) Pathogenicity of morphologically different isolates of Sclerotinia sclerotiorum with Brassica napus and B. juncea genotypes. Eur J Plant Pathol 126: 305-315.
34. Ge X, Li YP, Wan ZJ, You MP, Finnegan PM, et al. (2012) Delineation of Sclerotinia sclerotiorum pathotypes using differential resistance responses on Brassica napus and B. juncea genotypes enables identification of resistance to prevailing pathotypes. Field Crops Res 127: 248-258.
35. Garg H, Hua Li, Kuo J, Sivasithamparam K, Barbetti MJ, (2010) The infection processes of Sclerotinia sclerotiorum in cotyledon tissue of Brassica napus is affected in a tolerant genotype. Ann Bot 106: 897-908.
36. Hua Li, Stone V, Dean N, Sivasithamparam K, Barbetti MJ, (2007) Breaching by a new strain of Leptosphaeria maculans of anatomical barriers in cotyledons of Brassica napus cultivar Surpass 400 with resistance based on a single dominant gene. J Gen Plant Pathol 73: 297-303.
37. Marra R, Ambrosino P, Carbone V, Vinale F, Woo SL, et al. (2006) Study of the three-way interaction between Trichoderma atroviride, plant and fungal pathogens by using a proteomic approach. Curr Genet 50: 307-321.
38. Bringans S, Eriksen S, Kendrick T, Gopalakrishnakone P, Livk A, et al. (2008) Proteomic analyses of the venom of Heterometrus longimanus (Asian black scorpion). Proteomics 8: 1081-1096.
39. Sharma N, Rahman MH, Strelkov S, Thiagarajah M, Bansal VK, et al. (2007) Proteome-level changes in two Brassica napus varieties exhibiting differential responses to the fungal pathogen Alternaria brassicae. Plant Sci 172: 95-110.
40. Berger S, Sinha AK, Roitsch T, (2007) Plant physiology meets phytopathology: plant primary metabolism and plant-pathogen interactions. J Exp Bot 58: 4019-4026.
41. Slaymaker DH, Navarre DA, Clark D, del Pozo O, Martin GB, et al. (2002) The tobacco salicylic acid-binding protein 3 (SABP3) is the chloroplast carbonic anhydrase, which exhibits antioxidant activity and plays a role in the hypersensitive defense response. Proc Natl Acad Sci U S A 99: 11640-11645.
42. Gross GG, Janse C, Elstner EF, (1977) Involvement of malate, monophenols, and the superoxide radical in hydrogen peroxide formation by isolated cell walls from horseradish (Armoracia lapathijolia Gilib.). Planta 136: 271-276.
43. Ishida A, Ookubo K, Ono K, (1987) Formation of hydrogen peroxide by NAD(P)H oxidation with isolated cell wall-associated peroxidase from cultured liverwort cells, Marchantia polymorpha L. Plant Cell Physiol. 28: 723-726.
44. Cushman JC, (1993) Molecular cloning and expression of chloroplast NADP-malate dehydrogenase during Crassulacean acid metabolism induction by salt stress. Photosynth Res 35: 15-27.
45. Subramanian B, Bansal VK, Kav NN, (2005) Proteome-level investigation of Brassica carinata-derived resistance to Leptosphaeria maculans. J Agric Food Chem 53: 313-324.
46. Alwine JC, Russell FM, Murray KN, (1973) Characterization of an Escherichia coli mutant deficient in dihydrolipoyl dehydrogenase activity. J Bacteriol 115: 1-8.
47. Gazaryan IG, Krasnikov BF, Ashby GA, Thorneley RN, Kristal BS, et al. (2002) Zinc is a potent inhibitor of thiol oxidoreductase activity and stimulates reactive oxygen species production by lipoamide dehydrogenase. J Biol Chem 277: 10064-10072.
48. Tahara EB, Barros MH, Oliveira GA, Netto LES, Kowaltowski AJ, (2007) Dihydrolipoyl dehydrogenase as a source of reactive oxygen species inhibited by caloric restriction and involved in Saccharomyces cerevisiae aging. FASEB J 21: 274-283.
49. Lamb C, Dixon RA, (1997) The oxidative burst in plant disease resistance. Annu Rev Plant Biol 48: 251-275.
50. Neill SJ, Desikan R, Clarke A, Hurst RD, Hancock JT, (2002) Hydrogen peroxide and nitric oxide as signalling molecules in plants. J Exp Bot 53: 1237-1242.
51. Halliwell B, Gutteridge JMC (1989) Free Radicals in Biology and Medicine (2nd ed.). Oxford, UK: Clarendon.
52. Gara LD, de Pinto MC, Tommasi F, (2003) The antioxidant systems vis-à-vis reactive oxygen species during plant-pathogen interaction. Plant Physiol Biochem 41: 863-870.
53. Marrs KA, (1996) The function and regulation of glutathione S-transferases in plants. Annu Rev Plant Physiol Plant Mol Biol 47: 127-158.
54. Noji M, Saito M, Nakamura M, Aono M, Saji H, et al. (2001) Cysteine synthase overexpression in tobacco confers tolerance to sulfur-containing environmental pollutants. Plant Physiol 126: 973-980.
55. Wirtz M, Berkowitz O, Droux M, Hell R (2001) The cysteine synthase complex from plants. Eur J Biochem 268, 686-693.
56. Noctor G, Foyer CH, (1998) Ascorbate and glutathione: Keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49: 249-279.
57. Mauch F, Dudler R, (1993) Differential induction of distinct glutathione-S-transferases of wheat by xenobiotics and by pathogen attack. Plant Physiol 102: 1193-1201.
58. Edwards R, Blount JW, Dixon RA, (1991) Glutathione and elicitation of the phytoalexin response in legume cell cultures. Planta 184: 403-409.
59. Loyall L, Uchida K, Braun S, Furuya M, Frohnmeyer H, (2000) Glutathione and a UV light-induced glutathione S-transferase are involved in signaling to chalcone synthase in cell cultures. Plant Cell 12: 1939-1950.
60. Wingate VPM, Lawton MA, Lamb CJ, (1988) Glutathione causes a massive and selective induction of plant defence genes.Plant Physiol. 87: 206-210.
61. Shinshi H, Neuhaus JM, Ryals J, Meins F, (1990) Structure of a tobacco endochitinase gene: evidence that different chitinase genes can arise by transposition of sequences encoding a cysteine-rich domain. Plant Mol Biol 14: 357-368.
62. Upadhyay RS, Jayaswal RK, (1992) Pseudomonas cepacia causes mycelial deformities and inhibition of conidiation in phytopathogenic fungi. Curr Microbiol 24: 181-187.
63. Mittler R, (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7: 405-410.
64. Sakihama Y, Mano J, Sano S, Asada K, Yamasaki H, (2000) Reduction of phenoxyl radicals mediated by monodehydroascorbate reductase. Biochem Biophys Res Commun 279: 949-954.
65. Bowler C, Montagu MV, Inze D, (1992) Superoxide dismutase and stress tolerance. Annu Rev Plant Physiol Plant Mol Biol 43: 83-116.
66. Govrin EM, Levine A, (2000) The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Curr Biol 10: 751-757.
67. Dickman MB, Park YK, Oltersdorf T, Li W, Clemente T, et al. (2001) Abrogation of disease development in plants expressing animal antiapoptotic genes. Proc Natl Acad Sci U S A 98: 6957-6962.
68. Liang Y, Strelkov SE, Kav NNV, (2009) Oxalic acid-mediated responses in Brassica napus L. Proteomics. 9: 3156-3173.
69. Feng H, Chen Q, Feng J, Zhang J, Yang X, et al. (2007) Functional characterization of the Arabidopsis eukaryotic translation initiation factor 5A-2 that plays a crucial role in plant growth and development by regulating cell division, cell growth, and cell death. Plant Physiol 144: 1531-1545.
70. Hopkins MT, Lampi Y, Wang TW, Liu Z, Thompson JE, (2008) Eukaryotic translation initiation factor 5A is involved in pathogen-induced cell death and development of disease symptoms in Arabidopsis. Plant Physiol 148: 479-489.
71. Liu X, Huang B, Lin J, Fei J, Chen Z, et al. (2006) A novel pathogenesis-related protein (SsPR10) from Solanum surattense with ribonucleolytic and antimicrobial activity is stress- and pathogen-inducible. J Plant Physiol 163: 546-556.
72. Osmark P, Boyle B, Brisson N, (1998) Sequential and structural homology between intracellular pathogenesis-related proteins and a group of latex proteins. Plant Mol Biol 38: 1243-1246.
73. Liu JJ, Ekramoddoullah AKM, (2006) The family 10 of plant pathogenesis related proteins: their structure, regulation, and function in response to biotic and abiotic stresses. Physiol Mol Plant Pathol 68: 3-13.
74. Yang SF, Hoffman NE, (1984) Ethylene biosynthesis and its regulation in higher plants. Annu Rev Phytopathol 35: 155-189.
75. Peleman J, Boerjan W, Engler G, Seurinck J, Botterman J, et al. (1989) Strong cellular preference in the expression of a housekeeping gene of Arabidopsis thaliana encoding S-Adenosylmethionine synthetase. Plant Cell 1: 81-93.
76. Bouchereau A, Aziz A, Larher F, Martin-Tanguy J, (1999) Polyamines and environmental challenges: recent development. Plant Sci 140: 103-125.
77. Broekaert WF, Delaure SL, De Bolle MFC, Cammue BPA, (2006) The role of ethylene in host-pathogen interactions. Annu Rev Phytopathol 44: 393-416.
78. Ravanel S, Gakiere B, Job D, Douce R, (1998) The specific features of methionine biosynthesis and metabolism in plants. Proc Natl Acad Sci U S A 95: 7805-7812.
79. Hartl FU, (1996) Molecular chaperones in cellular protein folding. Nature 381: 571-580.
80. Wang W, Vinocur B, Shoseyov O, Altman A, (2004) Role of plant heat-shock proteins and molecular chaprones in the abiotic stress response. Trends Plant Sci 9: 245-252.