A Secretory Protein of Necrotrophic Fungus Sclerotinia sclerotiorum That Suppresses Host Resistance

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Zhu, Wenjun ^a   Wei, Wei ^a   Fu, Yanping ^a   Cheng, Jiasen ^a   Xie, Jiatao ^a   Li, Guoqing ^a   Yi, Xianhong ^a   Kang, Zhensheng ^b   Dickman, Martin B ^c   Jiang, Daohong ^a  

^a HUAZHONG AGRICULTURAL UNIVERSITY   (China)

^b NORTHWEST A F UNIVERSITY   (China)

^c TEXAS A AND M UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ETHYLENE; JASMONIC ACID; PROTEIN SSITL; SECRETORY PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARABIDOPSIS; ARTICLE; BOTRYTIS CINEREA; CONTROLLED STUDY; EIN2 GENE; GENE; GENE EXPRESSION; GENE REPRESSION; GENE SILENCING; HOST PATHOGEN INTERACTION; HOST RESISTANCE; IMMUNOFLUORESCENCE TEST; IMMUNOLOCALIZATION; INOCULATION; JAR1 GENE; NAHG GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; PAD4 GENE; PDF1.2 GENE; PLANT DEFENSE; PR 1 GENE; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; SCLEROTINIA SCLEROTIORUM; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; WILD TYPE;

AMINO ACID SEQUENCE; ARABIDOPSIS; ASCOMYCOTA; CELL WALL; DISEASE RESISTANCE; EXTRACELLULAR SPACE; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; GENE SILENCING; HELA CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; INTEGRINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHENOTYPE; PLANT DISEASES; PROTEIN CONFORMATION;

ARABIDOPSIS; BOTRYOTINIA FUCKELIANA; FUNGI; SCLEROTINIA SCLEROTIORUM;

EID: 84872296026     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0053901     Document Type: Article

References (67)

1. Boland GJ, Hall R, (1994) Index of plant hosts of Sclerotinia sclerotiorum. Can J Plant Pathol 16: 93-108.
2. Bolton MD, Thomma BPHJ, Nelson BD, (2006) Sclerotinia sclerotiorum (Lib.) de Bary: biology and molecular traits of a cosmopolitan pathogen. Mol Plant Path 7: 1-16.
3. Oirdi ME, Rahman TAE, Rigano L, Hadrami AE, Rodriguez MC, et al. (2011) Botrytis cinerea manipulates the antagonistic effects between immune pathways to promote disease development in tomato. The Plant Cell, Vol. 23: 2405-2421.
4. Lai ZB, Wang F, Zheng ZY, Fan BF, Chen ZX, (2011) A critical role of autophagy in plant resistance to necrotrophic fungal pathogens. The Plant J 66: 953-968.
5. Shlezinger N, Minz A, Gur Y, Hatam I, Dagdas YF, et al. (2011) Anti-apoptotic machinery protects the necrotrophic fungus Botrytis cinerea from host-induced apoptotic-like cell death during plant infection. PLoS Pathog 7(8): e1002185.
6. Miya A, Albert P, Shinya T, Desaki Y, Ichimura K, et al. (2007) CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc Natl Acad Sci U S A 104: 19613-19618.
7. Wan J, Zhang XC, Neece D, Ramonell KM, Clough S, et al. (2008) A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis. Plant Cell 20: 471-481.
8. Yamaguchi Y, Huffaker A, Bryan AC, Tax FE, Ryan CA, (2010) PEPR2 is a second receptor for the Pep1 and Pep2 peptides and contributes to defense responses in Arabidopsis. Plant Cell 22: 508-522.
9. Yamaguchi Y, Pearce G, Ryan CA, (2006) The cell surface leucine-rich repeat receptor for AtPep1, an endogenous peptide elicitor in Arabidopsis, is functional in transgenic tobacco cells. PNAS 103: 10104-10109.
10. Brutus A, Sicilia F, Macone A, Cervone F, De Lorenzo G, (2010) A domain swap approach reveals a role of the plant wall-associated kinase 1 (WAK1) as a receptor of oligogalacturonides. Proc Natl Acad Sci U S A107: 9452-9457.
11. 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 Pathog 7(6): e1002107.
12. Durrant WE, Dong X, (2004) Systemic acquired resistance. Annu Rev Phytopathol 42: 185-209.
13. Glazebrook J, (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43: 205-227.
14. Grant M, Lamb C, (2006) Systemic immunity. Curr Opin Plant Biol 9: 414-420.
15. Guo XM, Stotz HU, (2007) Defense against Sclerotinia sclerotiorum in Arabidopsis is dependent on jasmonic acid, salicylic acid, and ethylene signaling. Mol Plant Microbe Interact 20: 1384-1395.
16. Ferrari S, Plotnikova JM, Loren GD, Ausubel FM, (2003) Arabidopsis local resistance to Botrytis cinerea involves salicylic acid and camalexin and requires EDS4 and PAD2, but not SID2, EDS5 or PAD4. The Plant J 35: 193-205.
17. Mur LAJ, Kenton P, Atzorn R, Miersch O, Wasternack C, (2006) The outcomes of concentration-specific interactions between salicylate and jasmonate signaling include synergy, antagonism, and oxidative stress leading to cell death. Plant Physiol 140: 249-262.
18. Koornneef A, Pieterse CMJ, (2008) Cross talk in defense signaling. Plant Physiol 146: 839-844.
19. Spoel SH, Johnson JS, Dong X, (2007) Regulation of tradeoffs between plant defenses against pathogens with different lifestyles. Proc Natl Acad Sci U S A 104: 18842-18847.
20. Riou C, Freyssinet G, Fevre M, (1992) Purification and characterization of extracellular pectinolytic enzymes produced by Sclerotinia sclerotiorum. Appl Environ Microbiol 58: 578-583.
21. 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: 2191-2200.
22. Kim KS, Min JY, Dickman MB, (2008) Oxalic acid is an elicitor of plant programmed cell death during Sclerotinia sclerotiorum disease development. Mol Plant Microbe Interact 21: 605-612.
23. Li H, Fu YP, Jiang DH, Li GQ, Ghabrial SA, et al. (2008) Down-regulation of Sclerotinia sclerotiorum gene expression in response to infection with Sclerotinia sclerotiorum debilitation-associated RNA virus. Virus Res 135: 95-106.
24. Marcantonio EE, Hynes RO, (1988) Antibodies to the conserved cytoplasmic domain of the integrin β1 subunit react with proteins in vertebrates, invertebrates and fungi. J Cell Biol 106: 1765-1772.
25. Giancotti FG, Ruoslahti E, (1999) Integrin signaling. Science 285: 1028-1032.
26. Hynes RO, (1992) Integrins: versatility, modulation and signaling in cell adhesion. Cell 69: 11-25.
27. Hynes RO, (2002) Integrins: Bidirectional, allosteric signaling machines. Cell 110: 673-687.
28. Schindler M, Meiners S, Cheresh DA, (1989) RGD-dependent link age between plant cell wall and plasma membrane: consequences for growth. J Cell Biol 108: 1955-1965.
29. Nagpal P, Quatrano RS, (1999) Isolation and characterization of a cDNA clone from Arabidopsis thaliana with partial sequence similarity to integrins. Gene 230: 33-40.
30. Knepper C, Savory EA, Day B, (2011) Arabidopsis NDR1 is an integrin-like protein with a role in fluid loss and plasma membrane-cell wall adhesion. Plant Physiol 156: 286-300.
31. Edwards JE, Gaither TA, O'Shea JJ, Rotrosen D, Lawley TJ, et al. (1986) Expression of specific binding sites on Candida with functional and antigenic characteristics of human complement receptors. J Immunol 137: 3577-3583.
32. Corrêa Jr, A, Staples RC, Hoch HC, (1996) Inhibition of thigmostimulated cell differentiation with RGD-peptides in Uromyces germlings. Protoplasma 194: 91-102.
33. Hostetter MK, Tao NJ, Gale C, Herman DJ, McClellan M, et al. (1995) Antigenic and functional conservation of an integrin I-domain in Saccharomyces cerevisiae. Biochem Mol Med. 55: 122-130.
34. Gale CA, Finkel D, Tao N, Meinke M, McClellan M, et al. (1996) Cloning and expression of a gene encoding an integrin-like protein in Candida albicans. Proc Natl Acad Sci U S A 93: 357-361.
35. Gale CA, Bendel CM, McClellan M, Hauser M, Becker JM, et al. (1998) Linkage of adhesion, filamentous growth, and virulence in Candida albicans to a single gene, INT1. Science 279: 1355-1358.
36. Tucker SL, Talbot NJ, (2001) Surface attachment and pre-penetration stage development by plant pathogenic fungi. Annu Rev Phytopathol 39: 385-417.
37. Zhang L, Wu MD, Li GQ, Jiang DH, Huang HC, (2010) Effect of Mitovirus infection on formation of infection cushions and virulence of Botrytis cinerea. Physiol Mol Plant Pathol 75: 71-80.
38. Rollins JA, (2003) The Sclerotinia sclerotiorum pac1 gene is required for sclerotial development and virulence. Mol Plant Microbe Interact 16: 785-795.
39. Yu Y, Jiang D, Xie J, Cheng J, Li G, et al. (2012) Ss-Sl2, a novel cell wall protein with PAN modules, is essential for sclerotial development and cellular integrity of Sclerotinia sclerotiorum. PLoS ONE 7(4): e34962.
40. Harel A, Bercovich S, Yarden O, (2006) Calcineurin is required for sclerotial development and pathogenicity of Sclerotinia sclerotiorum in an oxalic acid-independent manner. Mol Plant Microbe Interact 19: 682-693.
41. Xu ZY, Hong N, Xiang B, Wang GP, (2006) Partial molecular characterization of a Chinese isolate of grapevine leafroll-associated virus2 and production antisera to recombinant viral proteins. J Plant Pathol 88: 87-92.
42. Kang ZS, Huang LL, Han QM, Zhang HC, (2007) Cytochemistry of cell wall component alterations in wheat spikes infected by Fusarium graminearun. Acta Phytopathologica Sinica 37: 623-628.
43. Li J, Wen R, Andersen P, Liang YP, Li Q, et al. (2010) Zebrafish Ubc13 is required for Lys63-linked polyubiquitination and DNA damage tolerance. Mol Cell Biochem 343: 173-182.
44. Krasileva KV, Dahlbeck D, Staskawicz BJ, (2010) Activation of an Arabidopsis resistance protein is specified by the in planta association of its Leucine-rich repeat domain with the cognate Oomycete effector. The Plant Cell 22: 1-15.
45. Zhang XR, Henriques R, Lin SS, Niu QW, Chua NH, (2006) Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method. Nature Protocols 1: 1-6.
46. Springer TA, (1997) Folding of the N-terminal, ligand-binding region of integrin alpha- subunits into a beta-propeller domain. Proc Natl Acad Sci U S A 94: 65-72.
47. Cioci G, Mitchell EP, Chazalet V, Debray H, Oscarson S, et al. (2006) β-Propeller crystal structure of Psathyrella velutina Lectin: An integrin-like fungal protein interacting with monosaccharides and calcium. J Mol Biol 357: 1575-1591.
48. Mentlak TA, Kombrink A, Shinya T, Ryder LS, Otomo I, et al. (2012) Effector-mediated suppression of chitin-triggered immunity by Magnaporthe oryzae is necessary for rice blast disease. The Plant Cell 24: 322-335.
49. Khang CH, Berruyer R, Giraldo MC, Kankanala P, Park SY, et al. (2010) Translocation of Magnaporthe oryzae effectors into rice cells and their subsequent cell-to-cell movement. The Plant Cell 22: 1388-1403.
50. Rafiqi M, Gan PHP, Ravensdale M, Lawrence GJ, Ellis JG, et al. (2010) Internalization of flax rust avirulence proteins into flax and tobacco cells can occur in the absence of the pathogen. The Plant Cell 22: 2017-2032.
51. Dai FM, Xu T, Wolf GA, He ZH, (2006) Physiological and molecular features of the pathosystem Arabidopsis thaliana L.-Sclerotinia sclerotiorum Libert. J Integr Plant Biol 48: 44-52.
52. Tan KC, Oliver RP, Solomon PS, Moffat CS, (2010) Proteinaceous necrotrophic effectors in fungal virulence. Funct Plant Biol 37: 907-912.
53. Marciano P, Lenna PD, Magro P, (1983) Oxalic acid, cell wall-degrading enzymes and pH in pathogenesis and their significance in the virulence of two Sclerotinia sclerotiorum isolates on sunflower. Physiol Plant Pathol 22: 339-345.
54. Movahedi S, Heale JB, (1990) The roles of aspartic proteinase and endopectin lyase enzymes in the primary stages of infection and pathogenesis of various host tissues by different isolates of Botrytis cinerea Pers Ex Pers. Physiol Mol Plant Pathol 36: 303-324.
55. Kikot GE, Hours RA, Alconada TM, (2009) Contribution of cell wall degrading enzymes to pathogenesis of Fusarium graminearum: a review. J Basic Microb 49: 231-241.
56. Oliver RP, Solomon PS, (2010) New developments in pathogenicity and virulence of necrotrophs. Curr Opin Plant Biol 13: 415-419.
57. 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.
58. Guimarães RL, Stotz HU, (2004) Oxalate production by Sclerotinia sclerotiorum deregulates guard cells during infection. Plant Physiol 136: 3703-3711.
59. Li GQ, Jiang DH, Zhou B, Wang D, Rimmer R (2001) Oxlic acid production in hypovirulent and virulent strains of Sclerotinia sclerotiorum. In: Proceedings of International Symposium on Rapeseed Science. Ed by Liu Houli and Fu Tingdong, Science Press, New York. 261-270.
60. Xu LS, Xiang M, White D, Chen WD, (2011) Oxalate-minus mutants of Sclerotinia sclerotiorum via random mutagenesis retain pathogenicity. Phytopathology 101: S104.
61. Hostetter MK, (1999) Integrin-like proteins in Candida spp. and other microorganisms. Fungal Genet Biol 28: 135-145.
62. Kaku H, Nishizawa Y, Ishii-Minami N, Akimoto-Tomiyama C, Dohmae N, et al. (2006) Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proc Natl Acad Sci U S A 103: 11086-11091.
63. Shimizu T, Nakano T, Takamizawa D, Desaki Y, Ishii-Minami N, et al. (2010) Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice. Plant J 64: 204-214.
64. Century KS, Shapiro AD, Repetti PP, Dahlbeck D, Holub E, et al. (1997) NDR1, a Pathogen-induced component required for Arabidopsis disease resistance. Science 278: 1963-1965.
65. Coppinger P, Repetti PP, Day B, Dahlbeck D, Mehlert A, et al. (2004) Overexpression of the plasma membrane-localized NDR1 protein results in enhanced bacterial disease resistance in Arabidopsis thaliana. The Plant J 40: 225-237.
66. Day B, Dahlbeck D, Staskawicz BJ, (2006) NDR1 interaction with RIN4 mediates the differential activation of multiple disease resistance pathways in Arabidopsis. The Plant Cell 18: 2782-2791.
67. Kaminskyj SG, Heath IB, (1995) Integrin and spectrin homologues and cytoplasm-cell wall adhesion in tip growth. J Cell Sci 108: 849-856.