Molecular characterization and functional analysis of a specific secreted protein from highly virulent defoliating Verticillium dahliae

Gene

Volumn 529, Issue 2, 2013, Pages 307-316

  Liu, Shao Yan ^a   Chen, Jie Yin ^a   Wang, Jin Long ^a   Li, Lei ^a   Xiao, Hong Li ^a   Adam, Sami M ^a   Dai, Xiao Feng ^a  

^a INSTITUTE OF PLANT PROTECTION   (China)

Author keywords

Pathogenicity; Plant cell wall degradation; Secreted protein; V. dahliae; VdSSP1

Indexed keywords

FUNGAL PROTEIN; UNCLASSIFIED DRUG; VDSSP1 PROTEIN;

ARTICLE; CARBON SOURCE; CARBON UTILIZATION; CONTROLLED STUDY; DEGRADATION; FUNGAL GENE; FUNGAL VIRULENCE; FUNGUS GROWTH; GENE DELETION; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PLANT CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN SECRETION; PROTEIN STRUCTURE; VERTICILLIUM DAHLIAE;

2, 3, 5-TRIPHENYLTETRAZOLIUM CHLORIDE; A RAPID AMPLIFICATION OF CDNA ENDS; CELL WALL DEGRADING ENZYME; CWDE; DI; DISEASE INDEX; HYG-E; HYGROMYCIN ELEMENT; PATHOGENICITY; PL; PLANT CELL WALL DEGRADATION; POLYSACCHARIDE LYASE; RACE; SECRETED PROTEIN; THE SPECIFIC SECRETED PROTEIN GENE 1; TTC; V. DAHLIAE; VDSSP1;

AMINO ACID SEQUENCE; CARBON; CELL WALL; FUNGAL PROTEINS; GENE DELETION; GOSSYPIUM; MOLECULAR SEQUENCE DATA; PROTEIN SORTING SIGNALS; VERTICILLIUM; VIRULENCE;

FUNGI; VERTICILLIUM DAHLIAE;

EID: 84883806015     PISSN: 03781119     EISSN: 18790038     Source Type: Journal    
DOI: 10.1016/j.gene.2013.06.089     Document Type: Article

References (82)

1. Agrios G. Plant Pathology 2005, Elsevier Academic Press, Burlington.
2. Altschul S.F., et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997, 25:3389-3402.
3. An Z.Q., Wang C.S., Liu X.Z., Bennett J.W. China's fungal genomics initiative: a whitepaper. Mycology 2010, 1:1-8.
4. Appel R.D., Bairoch A., Hochstrasser D.F. A new generation of information retrieval tools for biologists: the example of the ExPASy WWW server. Trends Biochem. Sci. 1994, 19:258-260.
5. Bejarano-Alcázar J., Melero-Vara J.M., Blanco-López M.A., Jiménez-Díaz R.M. Influence of inoculum density of defoliating and nondefoliating pathotypes of Verticillium dahliae on epidemics of Verticillium wilt in southern Spain. Phytopathology 1995, 85:1474-1481.
6. Bejarano-Alcázar J., Blanco-López M.A., Melero-Vara J.M., Jiménez-Díaz R.M. The influence of Verticillium wilt epidemics on cotton in southern Spain. Plant Pathol. 1997, 46:168-178.
7. Bhat R.G., Subbarao K.V. Host range specificity in Verticillium dahliae. Phytopathology 1999, 8912:1218-1225.
8. Briesemeister S., Rahnenführer J., Kohlbacher O. YLoc - an interpretable web server for predicting subcellular localization. Nucleic Acids Res. 2010, 38 (Web Server issue):W497-W502.
9. Buchner V., Nachmias A., Burstein Y. Isolation and partial characterization of a phytotoxic glycopeptide from a protein-lipopolysaccharide complex produced by a potato isolate of Verticillium dahliae. FEBS Lett. 1982, 138:261-264.
10. Carder J.H., Hignett R.C., Swinburne T.R. Relationship between the virulence of hop isolates of Verticillium albo-atrum and their in vitro secretion of cell-wall degrading enzymes. Physiol. Mol. Plant Pathol. 1987, 31:441-452.
11. Catanzariti A.M., Dodds P.N., Lawrence G.J., Ayliffe M.A., Ellis J.G. Haustorially expressed secreted proteins from flax rust are highly enriched for avirulence elicitors. Plant Cell 2006, 18:243-256.
12. Chenna R., et al. Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res. 2003, 31:3497-3500.
13. Cooper R.M., Wood R.K.S. Cell wall degrading enzymes of vascular wilt fungi. III. Possible involvement of endo-pectin lyase in Verticillium wilt of tomato. Physiol. Plant Pathol. 1980, 16:285-300.
14. Davis D.A., Low P.S., Heinstein P. Purification of a glycoprotein elicitor of phytotoxin formation from Verticillium dahliae. Physiol. Mol. Plant Pathol. 1998, 52:259-273.
15. de Jonge R., Bolton M.D., Thomma B.P.H.J. How filamentous pathogens co-opt plants: The ins and outs of fungal effectors. Curr. Opin. Plant Biol. 2011, 14:400-406.
16. de Jonge R., et al. Tomato immune receptor Ve1 recognizes effector of multiple fungal pathogens uncovered by genome and RNA sequencing. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:5110-5115.
17. Dean R.A., et al. The genome sequence of the rice blast fungus Magnaporthe grisea. Nature 2005, 434:980-986.
18. Durrands P.K., Cooper R.M. The role of pectinases in vascular wilt disease as determined by defined mutants of Verticillium albo-atrum. Physiol. Mol. Plant Pathol. 1988, 32:363-371.
19. Durrands P.K., Cooper R.M. Selection and characterization of pectinase-deficient mutants of the vascular wilt pathogen Verticillium albo-atrum. Physiol. Mol. Plant Pathol. 1988, 32:343-362.
20. Fradin E.F., Thomma B.P.H.J. Physiology and molecular aspects of Verticillium wilt diseases caused by V. dahliae and V. albo-atrum. Mol. Plant Pathol. 2006, 7:71-86.
21. Gao F., et al. A glutamic acid-rich protein identified in Verticillium dahliae from an insertional mutagenesis affects microsclerotial formation and pathogenicity. PLoS One 2010, 5:e15319.
22. Garcia O., et al. Characterization of necrosis and ethylene-inducing proteins (NEP) in the basidiomycete Moniliophthora perniciosa, the causal agent of witches' broom in Theobroma cacao. Mycol. Res. 2007, 111:443-455.
23. Gietz R.D., Schiestl R.H., Willems A.R., Woods R.A. Studies on the transformation of intact yeast cells by the LiAc/SSDNA/PEG procedure. Yeast 1995, 11:355-360.
24. Haas B.J., et al. Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 2009, 461:393-398.
25. Howell C.R. Use of enzyme deficient mutants of Verticillium dahliae to assess the importance of pectolytic enzyme in symptom expression of Verticillium wilt of cotton. Physiol. Plant Pathol. 1976, 9:279-283.
26. Huang L.K., Mahoney R.R. Purification and characterization of an endopolygalacturonase from Verticillium albo-atrum. J. Appl. Microbiol. 1999, 86:145-156.
27. Jacobs K.A., et al. A genetic selection for isolating cDNAs encoding secreted proteins. Gene 1997, 198:289-296.
28. James C. Global review of commercialized transgenic Crops: 2001 Feature: Bt Cotton. ISAAA Briefs 2002, 26.
29. Käll L., Krogh A., Sonnhammer E.L.A. A combined transmembrane topology and signal peptide prediction method. J. Mol. Biol. 2004, 338:1027-1036.
30. Kämper J., et al. Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 2006, 444:97-101.
31. Keen N.T. Endopolygalacturonase: evidence against involvement in Verticillium wilt of cotton. Phytopathology 1971, 61:198-203.
32. Khang C.H., Park S.Y., Lee Y.H., Kang S.A. Dual selection based, targeted gene replacement tool for Magnaporthe grisea and Fusarium oxysporum. Fungal Genet. Biol. 2005, 42:483-492.
33. Klein R.D., Gu Q., Goddard A., Rosenthal A. Selection for genes encoding secreted proteins and receptors. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:7108-7113.
34. Klimes A., Dobinson K.F. A hydrophobin gene, VDH1, is involved in microsclerotial development and spore viability in the plant pathogen Verticillium dahliae. Fungal Genet. Biol. 2006, 43:283-294.
35. Klosterman S.J., et al. Comparative genomics yields insights into niche adaptation of plant vascular wilt pathogens. PLoS Pathog. 2011, 7:e1002137.
36. Korolev N., et al. Vegetative compatibility of cotton-defoliating Verticillium dahliae in Israel and its pathogenicity to various crop plants. Eur. J. Plant Pathol. 2008, 122:603-617.
37. Lee S.J., et al. A functional screen to characterize thesecretomes of eukaryotic pathogens and their hosts in planta. Mol. Plant Microbe Interact. 2006, 19:1368-1377.
38. Lévesque C.A., et al. Genome sequence of the necrotrophic plant pathogen Pythiumultimum reveals original pathogenicity mechanisms and effector repertoire. Genome Biol. 2010, 11:R73.
39. Ma L.J., et al. Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 2010, 464:367-373.
40. Mansoori B., Milton J.M., Smith C.J. Isolation and partial purification of a phytotoxin related to pathogenic Verticillium species. J. Phytopathol. 1995, 143:33-36.
41. Martin R., et al. The Candida albicans-specific gene EED1 encodes a key regulator of hyphal extension. PLoS One 2011, 6:e18394.
42. Maruthachalam K., Klosterman S.J., Kang S., Hayes R.J., Subbarao K.V. Identification of pathogenicity-related genes in the vascular wilt fungus Verticillium dahliae by Agrobacterium tumefaciens-mediated T-DNA insertional mutagenesis. Mol. Biotechnol. 2011, 49:209-221.
43. Mercado-Blanco J., Rodríguez-Jurado M.D., Pérez-Artés E., Jiménez-Díaz R.M. Detection of the nondefoliating pathotype of Verticillium dahliae in infected olive plants by nested PCR. Plant Pathol. 2001, 50:609-619.
44. Mercado-Blanco J., Rodríguez-Jurado M.D., Pérez-Artés E., Jiménez-Díaz R.M. Detection of the defoliating pathotype of Verticillium dahliae in infected olive plants by nested PCR. Eur. J. Plant Pathol. 2002, 108:1-13.
45. Meyer R., Slater V., Dubery I.A. A phytotoxic protein-lipopolysaccharide complex produced by Verticillium dahliae. Phytochemistry 1994, 35:1449-1453.
46. Mullins E.D., Kang S. Transformation: a tool for studying fungal pathogens of plants. Cell Mol. Life Sci. 2001, 58:2043-2052.
47. Mussel H.W., Strause B. Characterization of two polygalacturonases produced by Verticillium albo-atrum. Can. J. Biochem. 1972, 50:625-632.
48. Nachmias A., Buchner V., Tsror L., Burstein Y., Keen N. Differential phytotoxicity of peptides from culture fluids of Verticillium dahliae races 1 and 2 and their relationship to pathogenecity of the fungi on tomato. Phytopathology 1987, 77:506-510.
49. Nadal M., Garcia-Pedrajas M.D., Gold S.E. The snf1 gene of Ustilago maydis acts as a dual regulator of cell wall degrading enzymes. Phytopathology 2010, 100:1364-1372.
50. Nielsen H., Engelbrecht J., Brunak S., von Heijne G. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng. 1997, 10:1-6.
51. Parlange F., et al. Leptosphaeria maculans avirulence gene AvrLm4-7 confers a dual recognition specificity by the Rlm4 and Rlm7 resistance genes of oilseed rape, and circumvents Rlm4-mediated recognition through a single amino acid change. Mol. Microbiol. 2009, 71:851-863.
52. Pegg G.F. Biochemistry and physiology of pathogenesis. Fungal Wilt Diseases of Plants 1981, 193-253. Academic Press, New York. M.E. Mace, A.A. Bell, C.H. Beckman (Eds.).
53. Pegg G.F., Brady B.L. Verticillium Wilts 2002, CABI Publishing, Wallingford, UK.
54. Powell N.T., Melendez P.L., Batten C.K. Disease complexes in tobacco involving Meloidogyne incognita and certain soil-borne fungi. Phytopathology 1971, 61:1332-1337.
55. Puhalla J.E., Bell A.A. Genetics and biochemistry of wilt pathogens. Fungal Wilt Diseases of Plants 1981, 146-192. Academic Press, New York. M.E. Mace, A.A. Bell, C.H. Beckman (Eds.).
56. Puhalla J.E., Howell C.R. Significance of endopolygalacturonase activity to symptom expression of Verticillium wilt in cotton, assessed by use of mutants of Verticillium dahliae Kleb. Physiol. Plant Pathol. 1975, 7:147-152.
57. Rauyaree P., et al. Mutations in VMK1, a mitogen-activated protein kinase gene, affect microsclerotia formation and pathogenicity in Verticillium dahliae. Curr. Genet. 2005, 48:109-116.
58. Roncero M.I., et al. Role of cell wall-degrading enzymes in pathogenicity of Fusarium oxysporum. Rev. Iberoam. Micol. 2000, 17:S47-S53.
59. Sambrook J., Russell D.W. Molecular Cloning: a Laboratory Manual 2001.
60. Santhanam P., Thomma B.P.H.J. Verticillium dahliae Sge1 differentially regulates expression of candidate effector genes. Mol. Plant Microbe Interact. 2013, 26:249-256.
61. Santhanam P., van Esse H.P., Albert I., Faino L., Nürnberger T., Thomma B.P.H.J. Evidence for functional diversification within a fungal NEP1-like protein family. Mol. Plant Microbe Interact. 2013, 26:278-286.
62. Schouten A., van Baarlen P., van Kan J.A. Phytotoxic Nep1-like proteins from the necrotrophic fungus Botrytis cinerea associate with membranes and the nucleus of plant cells. New Phytol. 2008, 177:493-505.
63. Sesma A., Osbourn E.A. The rice leaf blast pathogen undergoes developmental processes typical of root-infecting fungi. Nature 2004, 431:582-586.
64. Sonnhammer E.L., von Heijne G., Krogh A. A hidden Markov model for predicting transmembrane helices in protein sequences. Proc. Int. Conf. Intell. Syst. Mol. Biol. 1998, 6:175-182.
65. Staats M., van Baarlen P., Schouten A., van Kan J.A. Functional analysis of NLP genes from Botrytis elliptica. Mol. Plant Pathol. 2007, 8:209-214.
66. Stergiopoulos I., de Wit P.J. Fungal effector proteins. Annu. Rev. Phytopathol. 2009, 47:233-263.
67. Tjamos E.C. Problems and prospects in controlling Verticillium wilt. Vascular wilt Diseases of Plants 1989, 440-456. Springer-Verlag, Berlin. E.C. Tjamos, C.H. Beckman (Eds.).
68. Tzima A., Paplomatas E.J., Rauyaree P., Kang S. Roles of the catalytic subunit of cAMP-dependent protein kinase A in virulence and development of the soilborne plant pathogen Verticillium dahliae. Fungal Genet. Biol. 2010, 47:406-415.
69. Tzima A.K., Paplomatas E.J., Rauyaree P., Ospina-Giraldo M.D., Kang S. VdSNF1, the sucrose nonfermenting protein kinase gene of Verticillium dahliae, is required for virulence and expression of genes involved in cell-wall degradation. Mol. Plant Microbe Interact. 2011, 24:129-142.
70. Tzima A.K., Paplomatas E.J., Tsitsigiannis D.I., Kang S. The G protein β subunit controls virulence and multiple growth- and development-related traits in Verticillium dahliae. Fungal Genet. Biol. 2012, 49:271-283.
71. van der Does H.C., Rep M. Virulence genes and the evolution of host specificity in plant-pathogenic fungi. Mol. Plant Microbe Interact. 2007, 20:1175-1182.
72. Wang J.Y., et al. VdNEP, an elicitor from Verticillium dahliae, induces cotton plant wilting. Appl. Environ. Microbiol. 2004, 70:4989-4995.
73. Wang J.L., Chen J.Y., Liu S.Y., Li L., Dai X.F. Construction and pathogenicity tests of a mutated specific fragment SCF73 in Verticillium dahliae. Wei Sheng Wu Xue Bao 2012, 52:1335-1343.
74. Westerink N., Brandwagt B.F., De Wit P.J.G.M., Joosten M.H.A.J. Cladosporium fulvum circumvents the second functional resistance gene homologue at the Cf-4 locus (Hcr9-4E) by secretion of a stable avr4E isoform. Mol. Microbiol. 2004, 54:533-545.
75. Xu Z., Ali Z., Hou X., Li H., Yi J.X., Abbasi P.A. Characterization of Chinese eggplant isolates of the fungal pathogen Verticillium dahliae from different geographic origins. Genet. Mol. Res. 2013, 12:183-195.
76. Yajima W., Kav N.N. The proteome of the phytopathogenic fungus. Proteomics 2006, 6:5995-6007.
77. Yao L.L., Zhou Q., Pei B.L., Li Y.Z. Hydrogen peroxide modulates the dynamic microtubule cytoskeleton during the defence responses to Verticillium dahliae toxins in Arabidopsis. Plant Cell Environ. 2011, 34:1586-1598.
78. Yi M., et al. The ER chaperone LHS1 is involved in asexual development and rice infection by the blast fungus Magnaporthe oryzae. Plant Cell 2009, 21:681-695.
79. Yoshida K., et al. Association genetics reveals three novel avirulence genes from the rice blast fungal pathogen Magnaporthe oryzae. Plant Cell 2009, 21:1573-1591.
80. Yu J.H., Hamari Z., Han K.H., Seo J.A., Reyes-Dominguez Y., Scazzocchio C. Double-joint PCR: a PCR-based molecular tool for gene manipulations in filamentous fungi. Fungal Genet. Biol. 2004, 41:973-981.
81. Yuan H.Y., Yao L.L., Jia Z.Q., Li Y., Li Y.Z. Verticillium dahliae toxin induced alterations of cytoskeletons and nucleoli in Arabidopsis thaliana suspension cells. Protoplasma 2006, 229:75-82.
82. Zhou B.J., Jia P.S., Gao F., Guo H.S. Molecular characterization and functional analysis of a necrosis- and ethylene-inducing, protein-encoding gene family from Verticillium dahliae. Mol. Plant Microbe Interact. 2012, 25:964-975.