Analyses of the xylem sap proteomes identified candidate Fusarium virguliforme proteinacious toxins

PLoS ONE

Volumn 9, Issue 5, 2014, Pages

  Abeysekara, Nilwala S ^a   Bhattacharyya, Madan K ^a  

^a IOWA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSYLHOMOCYSTEINASE; ASPARTATE AMINOTRANSFERASE; CALMODULIN; CALRETICULIN; CERATOPLATANIN; COPPER ZINC SUPEROXIDE DISMUTASE; CYCLOPHILIN; DIAZEPAM BINDING INHIBITOR; ENOLASE; FRUCTOKINASE; GAMMA GLUTAMYL HYDROLASE; GLYCINE HYDROXYMETHYLTRANSFERASE; GLYCOSYLTRANSFERASE; HEAT SHOCK PROTEIN 70; HISTONE H4; LACTOYLGLUTATHIONE LYASE; LECTIN; LIPOXYGENASE; MALATE DEHYDROGENASE; MYCOTOXIN; NUCLEOSIDE DIPHOSPHATE KINASE; PEROXIDASE; PLASTOCYANIN; POLLEN ANTIGEN; PROFILIN; PROTEINASE INHIBITOR; PROTEOME; SERINE CARBOXYPEPTIDASE; TRYPSIN; UNCLASSIFIED DRUG; FUNGAL PROTEIN; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CANKER; CERATOCYSTIS FIMBRIATA; CONTROLLED STUDY; ELECTROSPRAY; FUNGUS; FUNGUS IMMUNITY; FUSARIUM; FUSARIUM VIRGULIFORME; LIQUID CHROMATOGRAPHY; NONHUMAN; PLANT DEFENSE; PLANT DISEASE; PLANT IMMUNITY; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN SECRETION; SEQUENCE ANALYSIS; SOYBEAN; SUDDEN DEATH SYNDROME; TANDEM MASS SPECTROMETRY; XYLEM SAP; METABOLISM; MICROBIOLOGY; XYLEM;

FUNGAL PROTEINS; FUSARIUM; PLANT DISEASES; PLANT PROTEINS; SOYBEANS; XYLEM;

EID: 84901351555     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0093667     Document Type: Article

References (56)

1. Ploper D (1993). Síndrome de la muerte súbita: nueva enfermedad de la soja en el noroeste argentino. Avance Agroindustrial Año 13: 5-9.
2. Anderson TR, Tenuta AU (1998) First report of Fusarium solani f. sp. glycines causing sudden death syndrome of soybean in Canada. Plant Dis 82: 448.
3. Nakajima T, Mitsueda T, Charchar MJD (1996) First occurrence of sudden death syndrome of soybean in Brazil. Jpn Agric Res Q 30: 31-34.
4. Wrather JA, Koenning SR (2006) Estimates of disease effects on soybean yields in the United States 2003 to 2005. J Nematol 38: 137-180.
5. Butzen S (2010) Sudden death syndrome of soybean. Crop Insights, 19: 1-4.
6. Babadoost M (1997) Sudden death syndrome of soybeans. RPD No. 512. http://ipm.illinois.edu/diseases/series500/rpd512/.
7. Wrather JA (2011) Soybean disease loss estimates for the United States, 1996-2010. http://aes.missouri.edu/delta/research/soyloss.stm.
8. Aoki T, O'Donnell K, Homma Y, Lattanzi AR (2003) Sudden death syndrome of soybean is caused by two morphologically and phylogenetically distinct species within the Fusarium solani species complex-F. virguliforme in North America and F. tucumaniae in South America. Mycologia 95: 660-684. (Pubitemid 37231936)
9. Aoki T, O'Donnell K, Scandiani MM (2005) Sudden death syndrome of soybean in South America is caused by four species of Fusarium: Fusarium brasiliense sp nov, F. cuneirostrum sp nov, F. tucumaniae and F. virguliforme. Mycoscience 46: 162-168.
10. Li S, Hartman GL, Widholm JM (1999) Viability staining of soybean suspension-cultured cells and a seedling stem cutting assay to evaluate phytotoxicity of Fusarium solani f. sp glycines culture filtrates. Plant Cell Rep 18: 375-380.
11. Roy KW, Lawrence GW, Hodges HH, McLean KS, Killebrew JF (1989) Sudden death syndrome of soybean: Fusarium solani as incident and relation of Heterodera glycines to disease severity. Phytopathology 79: 191-197.
12. Rupe JC (1989) Frequency and pathogenecity of Fusarium solani recovered from soybean with sudden death syndrome. Plant Dis 73: 581-584.
13. Brar HK, Swarminathan S, Bhattacharyya MK (2011) The Fusarium virguliforme toxin FvTox1 causes foliar sudden death syndrome-like symptoms in soybean. Mol Plant Microbe Interact 24: 1179-1188.
14. Ji J, Scott MP, Bhattacharyya MK (2006) Light is essential for degradation of ribulose-15-bisphosphate carboxylase-oxygenase large subunit during sudden death syndrome development in soybean. Plant Biol 8: 597-605. (Pubitemid 44510524)
15. Jin H, Hartman GL, Nickell CD, Widholm JM (1996) Characterization and purification of a phytotoxin produced by Fusarium solani the causal agent of soybean sudden death syndrome. Phytopathology 86: 277-282. (Pubitemid 126609599)
16. Brar HK, Bhattacharyya MK (2012) Expression of a single-chain variable-fragment antibody against a Fusarium virguliforme toxin peptide enhances tolerance to sudden death syndrome in transgenic soybean plants. Mol Plant Microbe Interact 25: 817-824.
17. Pudake RN, Swaminathan S, Sahu BB, Leandro LF, Bhattacharyya MK (2013) Investigation of the Fusarium virguliforme fvtox1 mutants revealed that the FvTox1 toxin is involved in foliar sudden death syndrome development in soybean. Curr Genet: DOI:10-1007/s00294-013-0392-z.
18. Kav NNV, Srivastava S, Yajima W, Sharma N (2007) Application of proteomics to investigate plant-microbe interactions. Curr proteomics 4: 28-43.
19. Mehta A, Brasileiro ACM, Souza DSL, Romano E, Campos MA, et al (2008) Plant-pathogen interactions: what is proteomics telling us? FEBS J 275: 3731-46. (Pubitemid 351990947)
20. Dafoe NJ, Constabel CP (2009) Proteomic analysis of hybrid poplar xylem sap. Phytochem 70: 856-63.
21. Aki T, Shigyo M, Nakano R, Yoneyama T, Yanagisawa S (2008) Nano scale proteomics revealed the presence of regulatory proteins including three FT-like proteins in phloem and xylem saps from rice. Plant Cell Physiol 49: 767-90. (Pubitemid 351769880)
22. Kehr J, Buhtz A, Giavalisco P (2005) Analysis of xylem sap proteins from Brassica napus. BMC Plant Biol 5: 11.
23. Zhou W, Eudes F, Laroche A (2006) Identification of differentially regulated proteins in response to a compatible interaction between the pathogen Fusarium graminearum and its host Triticum aestivum. Proteomics 6: 4599-4609. (Pubitemid 44336974)
24. Houterman PM, Speijer D, Dekker HL, De Koster CG, Cornelissen BJC, et al. (2007) The mixed xylem sap proteome of Fusarium oxysporum-infected tomato plants. Mol Plant Pathol 8: 215-221.
25. Lee J, Bricker TM, Lefevre M, Pinson SRM, Oard JH (2006) Proteomic and genetic approaches to identifying defence-related proteins in rice challenged with the fungal pathogen Rhizoctonia solani. Mol Plant Pathol 7: 405-416. (Pubitemid 44337799)
26. Rep M, Dekker HL, Vossen JH, de Boer AD, Houterman PM, et al. (2002) Mass spectrometric identification of isoforms of PR proteins in xylem sap of fungus-infected tomato. Plant Physiol 130: 904-917. (Pubitemid 35224791)
27. Kim ST, Kim SG, Hwang DH, Kang SY, Kim HJ, et al. (2004) Proteomic analysis of pathogen-responsive proteins from rice leaves induced by rice blast fungus Magnaporthe grisea. Proteomics 4: 3569-3578.
28. Pos V, Halasz K, Mesterhazi A, Csosz L, Manninger K, et al. (2005) Proteomic investigation of wheat intercellular washing fluid. Proceedings of the 8th Hungarian congress on plant physiology and the 6th Hungarian conference on photosynthesis. Acta Biol Szegediensis 49: 31-32.
29. Rep M, Dekker HL, Vossen JH, de Boer AD, Houterman PM, et al. (2003) A tomato xylem sap protein represents a new family of small cysteine-rich proteins with structural similarity to lipid transfer proteins. FEBS Lett 534: 82-86. (Pubitemid 36084521)
30. Alvarez S, Goodger JQD, Marsh EL, Chen MS, Asirvatham VS, et al. (2006) Characterization of the maize xylem sap proteome. J Prot Res 5: 963-972.
31. Djordjevic MA, Oakes M, Li DX, Hwang CH, Hocart CH, et al. (2007) The Glycine max xylem sap and apoplast proteome. J Prot Res 6: 3771-3779. (Pubitemid 47522765)
32. Subramanian S, Cho U, Keyes C, Yu O (2009) Distinct changes in soybean xylem sap proteome in response to pathogenic and symbiotic microbe interactions. BMC Plant Biol 9: 119.
33. Krishnan HB, Natarajan SS, Bennett JO, Sicher RC (2011) Protein and metabolic composition of xylem sap from field-grown soybeans (Glycine max). Planta 233: 921-931.
34. Li S, Hartman GL, Lee B-S, Widholm JW (2000) Identification of a stress-induced protein in stem exudates of soybean seedlings root-infected with Fusarium solani f. sp. glycines. Plant Physiol Biochem 38: 803-809.
35. Hartman GL, Huang YH, Nelson RL, Noel GR (1997) Germplasm evaluation of Glycine max for resistance to Fusarium solani, the causal organism of sudden death syndrome. Plant Dis 81: 515-518.
36. Lightfoot DA, Gibson PT, Meksem K (2007) Method of determining soybean sudden death syndrome resistance in a soybean plant. U.S. Patent 7,288,386.
37. Ishihama Y, Yoda Y, Tabuta T, Sato T, Nagasu T, et al (2005) Exponentially modified protein abundance index (emPAI) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein. Mol Cell Proteomics 4: 1265-1272. (Pubitemid 41448714)
38. Petersen TN, Brunak S, von Heijne G, Nielsen H (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nature Methods 8: 785-786.
39. Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, et al. (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21: 3674-3676. (Pubitemid 41264107)
40. Conesa A, Gotz S (2009) Blast2Go tutorial. www.blast2go.com/data/ blast2go/b2g-tutorial- 23062009.pdf.
41. Pazzagli L, Cappugi G, Manao G, Camici G, Santini A, et al. (1999) Purification of cerato-platanin a new phytotoxic protein from Ceratocystis fimbriata f. sp platani. J Biol Chem 274: 24959-24964.
42. Pazzagli L, Pantera B, Carresi L, Zoppi C, Pertinhez TA, et al. (2006) Ceratoplatanin the first member of a new fungal protein family: cloning expression and characterization. Cell Biochem Biophys 44: 512-521. (Pubitemid 43780407)
43. de Oliveira AL, Gallo M, Pazzagli L, Benedetti CE, Cappugi G, et al. (2011) The structure of the elicitor Cerato-platanin (CP), the first member of the CP fungal protein family, reveals a double-barrel fold and carbohydrate binding. J Biol Chem 286: 17560-17568.
44. Scala A, Pazzagli L, Comparini C, Santini A, Tegli S, et al. (2004) Ceratoplatanin, an early-produced protein by Ceratocystis fimbriata f. sp. platani, elicits phytoalexin synthesis in host and non-host plants. J Plant Pathol 86: 23-29.
45. Fontana F, Santini A, Salvini M, Pazzagli L, Cappugi G,et al. (2008) Ceratoplatanin treated plane leaves restrict Ceratocystis platani growth and overexpress defense-related genes. J Plant pathol 90: 295-306.
46. Bernardi R, Baccelli I, Carresi L, Comparini C, Pazzagli L, et al. (2011) Ceratoplatanin elicits transcription of defence-related genes earlier than Ceratocystis platani on Platanus acerifolia. Forest Pathol 41: 255-261.
47. Stintzi A, Heitz T, Prasad V, Wiedemann-Merdinoglu S, Kauffmann S, et al. (1993) Plant pathogenesis related proteins and their role in defense against pathogens. Biochimie 75: 687-706. (Pubitemid 23305236)
48. Simmons CR (1994) The physiology and molecular biology of plant 1,3-beta-d-glucanases and 1,3;1,4-beta-d-glucanases. Crit Rev Plant Sci 13: 325-87.
49. Sela-Buurlage MB, Ponstein AS, Bres-Vloemans SA, Melchers LS, van den Elzen PJM, et al. (1993) Only specific tobacco (Nicotiana tabacum) chitinases and β-1,3-glucanases exhibit antifungal activity. Plant Physiol 101: 857-863.
50. Woloshuk CP, Meulenhoff JS, Sela-Buurlage M, van den Elzen PJM, Cornelissen BJC (1991) Pathogen induced proteins with inhibitory activity towards Phytophthora infestans. The Plant cell 3: 619-628. (Pubitemid 21913726)
51. Schaaf J, Walter MH, Hess D (1995) Primary metabolism in plant defense (regulation of a bean malic enzyme gene promoter in transgenic tobacco by developmental and environmental cues). Plant Physiol 108: 949-960.
52. Biles CL, Abeles FB (1991) Xylem sap proteins. Plant Physiol 96: 597-601. (Pubitemid 21914055)
53. Ligat L, Lauber E, Albenne C, Clemente HS, Valot B, et al.(2011) Analysis of the xylem sap proteome of Brassica oleracea reveals a high content in secreted proteins. Proteomics 11: 1798-1813.
54. Sakuta C, Satoh S (2000) Vascular tissue-specific gene expression of xylem sap glycine rich proteins in root and their localization in the walls of metaxylem vessels in cucumber. Plant Cell Physiol 41: 627-638. (Pubitemid 30388065)
55. Vizcaino JA, Cote RG, Csordas A, Dianes JA, Fabregat A, Foster JM, Griss J, Alpi E, Birim M, Contell J, O'Kelly G, Schoenegger A, Ovelleiro D, Perez-Riverol Y, Reisinger F, Rios D, Wang R, Hermjakob H (2013) The Proteomics Identifications (PRIDE) database and associated tools: status in 2013. Nucleic Acids Res. 41(D1):D1063-9. doi:10.1093/nar/gks1262. PubMed PMID: 23203882.
56. Srivastava SK, Huang X, Brar HK, Fakhoury AM, Bluhm BH, Bhattacharyya MK (2014) The genome sequence of the fungal pathogen Fusarium virguliforme that causes sudden death syndrome in soybean. PLoS One 9: e81832.