Synergistic action of a metalloprotease and a serine protease from Fusarium oxysporum f. sp. lycopersici cleaves chitin-binding tomato chitinases, reduces their antifungal activity, and enhances fungal virulence

Molecular Plant-Microbe Interactions

Volumn 28, Issue 9, 2015, Pages 996-1008

  Jashni, Mansoor Karimi ^a,b   Dols, Ivo H M ^a   Iida, Yuichiro ^a,c   Boeren, Sjef ^a   Beenen, Henriek G ^a   Mehrabi, Rahim ^a,d   Collemare, Jérôme ^a,e   De Wit, Pierre J G M ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b TARBIAT MODARES UNIVERSITY   (Iran)

^c FOOD RESEARCH INSTITUTE   (Japan)

^d SEED AND PLANT IMPROVEMENT INSTITUTE   (Iran)

^e Universite d'Angers   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CHITIN; CHITINASE; FUNGAL PROTEIN; METALLOPROTEINASE; SERINE PROTEINASE;

CHEMISTRY; ENZYMOLOGY; FUSARIUM; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MICROBIOLOGY; MUTATION; PATHOGENICITY; PHYSIOLOGY; PLANT DISEASE; PLANT GENOME; TOMATO; VIRULENCE;

CHITIN; CHITINASE; FUNGAL PROTEINS; FUSARIUM; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, FUNGAL; GENE EXPRESSION REGULATION, PLANT; GENOME, PLANT; LYCOPERSICON ESCULENTUM; METALLOPROTEASES; MUTATION; PLANT DISEASES; SERINE PROTEASES; VIRULENCE;

EID: 84942543899     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-04-15-0074-R     Document Type: Article

References (76)

1. Aimé, S., Alabouvette, C., Steinberg, C., and Olivain, C. 2013. The endophytic strain Fusarium oxysporum Fo47: A good candidate for priming the defense responses in tomato roots. Mol. Plant-Microbe Interact. 26:918-926.
2. Arlorio, M., Ludwig, A., Boller, T., and Bonfante, P. 1992. Inhibition of fungal growth by plant chitinases and b-1, 3-glucanases. Protoplasma 171:34-43.
3. Balasubramanian, V., Vashisht, D., Cletus, J., and Sakthivel, N. 2012. Plant b-1, 3-glucanases: Their biological functions and transgenic expression against phytopathogenic fungi. Biotechnol. Lett. 34:1983-1990.
4. Ball, A. M., Ashby, A. M., Daniels, M. J., Ingram, D. S., and Johnstone, K. 1991. Evidence for the requirement of extracellular protease in the pathogenic interaction of Pyrenopeziza brassicae with oilseed rape. Physiol. Mol. Plant Pathol. 38:147-161.
5. Benhamou, N., Joosten, M. H. A. J., and de Wit, P. J. G. M. 1990. Subcellular localization of chitinase and of its potential substrate in tomato root tissues infected by Fusarium oxysporum f. sp. radicislycopersici. Plant Physiol. 92:1108-1120.
6. Bindschedler, L. V., Sanchez, P., Dunn, S., Mikan, J., Thangavelu, M., Clarkson, J. M., and Cooper, R. M. 2003. Deletion of the SNP1 trypsin protease from Stagonospora nodorum reveals another major protease expressed during infection. Fungal Genet. Biol. 38:43-53.
7. Cletus, J., Balasubramanian, V., Vashisht, D., and Sakthivel, N. 2013. Transgenic expression of plant chitinases to enhance disease resistance. Biotechnol. Lett. 35:1719-1732.
8. Cota, I. E., Troncoso-Rojas, R., Sotelo-Mundo, R., Sánchez-Estrada, A., and Tiznado-Hernández, M. E. 2007. Chitinase and b-1, 3-glucanase enzymatic activities in response to infection by Alternaria alternata evaluated in two stages of development in different tomato fruit varieties. Sci. Hortic. (Amsterdam) 112:42-50.
9. Cox, J., and Mann, M. 2008. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26:1367-1372.
10. Cox, J., Neuhauser, N., Michalski, A., Scheltema, R. A., Olsen, J. V., and Mann, M. 2011. Andromeda: A peptide search engine integrated into the MaxQuant environment. J. Proteome Res. 10:1794-1805.
11. Danhash, N., Wagemakers, C. A., van Kan, J. A., and de Wit, P. J. 1993. Molecular characterization of four chitinase cDNAs obtained from Cladosporium fulvum-infected tomato. Plant Mol. Biol. 22:1017-1029.
12. Dana, M. de lasM., Pintor-Toro, J. A., and Cubero, B. 2006. Transgenic tobacco plants overexpressing chitinases of fungal origin show enhanced resistance to biotic and abiotic stress agents. Plant Physiol. 142:722-730.
13. deWit, P. G. M., and Spikman, G. 1982. Evidence for the occurence of race and cultivar-specific elicitors of necrosis in intercellular fluids of compatible interactions of Cladosporium fulvum and tomato. Physiol. Plant Pathol. 21:1-8.
14. de Wit, P. J. G. M., van der Burgt, A., Ökmen, B., Stergiopoulos, I., Abd- Elsalam, K.A., Aerts, A. L., Bahkali, A.H., Beenen, H. G., Chettri, P., Cox, M. P., Datema, E., de Vries, R. P., Dhillon, B., Ganley, A. R., Griffiths, S. A., Guo, Y., Hamelin, R. C., Henrissat, B., Kabir, M. S., Jashni, M. K., Kema, G., Klaubauf, S., Lapidus, A., Levasseur, A., Lindquist, E., Mehrabi, R., Ohm, R. A., Owen, T. J., Salamov, A., Schwelm, A., Schijlen, E., Sun, H., van den Burg, H. A., van Ham, R. C. H. J., Zhang, S., Goodwin, S. B., Grigoriev, I. V., Collemare, J., and Bradshaw, R. E. 2012. The genomes of the fungal plant pathogens Cladosporium fulvum and Dothistroma septosporum reveal adaptation to different hosts and lifestyles but also signatures of common ancestry. PLoS Genet. 8:e1003088.
15. Di Pietro, A., Huertas-González, M. D., Gutierrez-Corona, J. F., Martínez- Cadena, G., Méglecz, E., and Roncero, M. I. G. 2001. Molecular characterization of a subtilase from the vascular wilt fungus Fusarium oxysporum. Mol. Plant-Microbe Interact. 14:653-662.
16. Edgar, R. C. 2004. MUSCLE: A multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5:113.
17. Finn, R. D., Bateman, A., Clements, J., Coggill, P., Eberhardt, R. Y., Eddy, S. R., Heger, A., Hetherington, K., Holm, L., Mistry, J., Sonnhammer, E. L. L., Tate, J., and Punta, M. 2014. Pfam: The protein families database. Nucleic Acids Res. 42:D222-D230.
18. Godoy, A. V., Olivieri, F. P., and Casalongue, C. A. 1996. Induction of hydrolytic enzymes and antifungal in vitro activity in S. tuberosum subsp. andigena after infection with Fusarium solani f. sp. eumartii. Potato Res. 39:259-266.
19. Grover, A. 2012. Plant chitinases: Genetic diversity and physiological roles. Crit. Rev. Plant Sci. 31:57-73.
20. Ham, K. S., Wu, S. C., Darvill, A. G., and Albersheim, P. 1997. Fungal pathogens secrete an inhibitor protein that distinguishes isoforms of plant pathogenesis-related endo-b-1, 3-glucanases. Plant J. 11: 169-179.
21. Hamid, R., Khan, M. A., Ahmad, M., Ahmad, M. M., Abdin, M. Z., Musarrat, J., and Javed, S. 2013. Chitinases: An update. J. Pharm. Bioallied Sci. 5:21-29.
22. Houterman, P. M., Speijer, D., Dekker, H. L., DE Koster, C. G., Cornelissen, B. J. C., and Rep, M. 2007. The mixed xylem sap proteome of Fusarium oxysporum-infected tomato plants. Mol. Plant Pathol. 8:215-221.
23. Iqbal, M. M., Nazir, F., Ali, S., Asif, M. A., Zafar, Y., Iqbal, J., and Ali, G. M. 2012. Over expression of rice chitinase gene in transgenic peanut (Arachis hypogaea L.) improves resistance against leaf spot. Mol. Biotechnol. 50:129-136.
24. Iseli, B., Boller, T., and Neuhaus, J. M. 1993. The N-terminal cysteine-rich domain of tobacco class I chitinase is essential for chitin binding but not for catalytic or antifungal activity. Plant Physiol. 103:221-226.
25. Jongedijk, E., Tigelaar, H., Van Roekel, J. S., Bres-Vloemans, S. A., Dekker, I., van den Elzen, P. J., Cornelissen, B. J., and Melchers, L. S. 1995. Synergistic activity of chitinases and b-1, 3-glucanases enhances fungal resistance in transgenic tomato plants. Euphytica 85:173-180.
26. Joosten, M. H. A. J., and De Wit, P. J. G. M. 1989. Identification of several pathogenesis-related proteins in tomato leaves inoculated with Cladosporium fulvum (syn. Fulvia fulva) as 1, 3-b-glucanases and chitinases. Plant Physiol. 89:945-951.
27. Joosten, M. H. A. J., Verbakel, H., Nettekoven, M., Van Leeuwen, J., Van der Vossen, R., and de Wit, P. J. G. M. 1995. The phytopathogenic fungus Cladosporium fulvum is not sensitive to the chitinase and b-1, 3-glucanase defence proteins of its host, tomato. Physiol. Mol. Plant Pathol. 46:45-59.
28. Kolosova, N., Breuil, C., and Bohlmann, J. 2014. Cloning and characterization of chitinases from interior spruce and lodgepole pine. Phytochemistry 101:32-39.
29. Kombrink, A. 2012. Heterologous production of fungal effectors in Pichia pastoris. Methods Mol. Biol. 835:209-217.
30. Lange, J., Mohr, U., Wiemken, A., Boller, T., and Vögeli-Lange, R. 1996. Proteolytic processing of class IV chitinase in the compatible interaction of bean roots with Fusarium solani. Plant Physiol. 111:1135-1144.
31. Li, H., and Greene, L. H. 2010. Sequence and structural analysis of the chitinase insertion domain reveals two conserved motifs involved in chitin-binding. PLoS ONE 5:e8654.
32. Livak, K. J., and Schmittgen, T. D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2 -D D C(T) method. Methods 25:402-408.
33. Lu, J., Boeren, S., de Vries, S. C., van Valenberg, H. J. F., Vervoort, J., and Hettinga, K. 2011. Filter-aided sample preparation with dimethyl labeling to identify and quantify milk fat globule membrane proteins. J. Proteomics 75:34-43.
34. Lu, S.-W., Kroken, S., Lee, B.-N., Robbertse, B., Churchill, A. C. L., Yoder, O. C., and Turgeon, B. G. 2003. A novel class of gene controlling virulence in plant pathogenic ascomycete fungi. Proc. Natl. Acad. Sci. U.S.A. 100:5980-5985.
35. Mauch, F., Mauch-Mani, B., and Boller, T. 1988. Antifungal hydrolases in pea tissue. II. Inhibition of fungal growth by combinations of chitinase and b-1, 3-glucanase. Plant Physiol. 88:936-942.
36. Maximova, S. N., Marelli, J.-P., Young, A., Pishak, S., Verica, J. A., and Guiltinan, M. J. 2006. Over-expression of a cacao class I chitinase gene in Theobroma cacao L. enhances resistance against the pathogen, Colletotrichum gloeosporioides. Planta 224:740-749.
37. McGowan, S. 2013.Working in concert: The metalloaminopeptidases from Plasmodium falciparum. Curr. Opin. Struct. Biol. 23:828-835.
38. Mehrabi, R., Mirzadi-Gohari, A., Ferreira da Silva, G., Steinberg, G., and Kema, G. H. J., and deWit, P. J. G. M. 2015. Flexible gateway constructs for functional analyses of genes in plant pathogenic fungi. Fungal Genet. Biol. 79:186-192.
39. Michielse, C. B., van Wijk, R., Reijnen, L., Cornelissen, B. J., and Rep, M. 2009. Insight into the molecular requirements for pathogenicity of Fusarium oxysporum f. sp. lycopersici through large-scale insertional mutagenesis. Genome Biol. 10:R4.
40. Murphy, J. M., and Walton, J. D. 1996. Three extracellular proteases from Cochliobolus carbonum: Cloning and targeted disruption of ALP1. Mol. Plant-Microbe Interact. 9:290-297.
41. Nagy, N. E., and Fossdal, C. G. 2013. Host responses in Norway spruce roots induced to the pathogen Ceratocystis polonica are evaded or suppressed by the ectomycorrhizal fungus Laccaria bicolor. Plant Biol Stuttg 15:99-110.
42. Naumann, T. A. 2011. Modification of recombinant maize ChitA chitinase by fungal chitinase-modifying proteins. Mol. Plant Pathol. 12:365-372.
43. Naumann, T. A., andWicklow, D. T. 2010. Allozyme-specific modification of a maize seed chitinase by a protein secreted by the fungal pathogen Stenocarpella maydis. Phytopathology 100:645-654.
44. Naumann, T. A., and Wicklow, D. T. 2013. Chitinase modifying proteins from phylogenetically distinct lineages of Brassica pathogens. Physiol. Mol. Plant Pathol. 82:1-9.
45. Naumann, T. A., Wicklow, D. T., and Kendra, D. F. 2009. Maize seed chitinase is modified by a protein secreted by Bipolaris zeicola. Physiol. Mol. Plant Pathol. 74:134-141.
46. Naumann, T. A., Wicklow, D. T., and Price, N. P. J. 2011. Identification of a chitinase-modifying protein from Fusarium verticillioides: Truncation of a host resistance protein by a fungalysin metalloprotease. J. Biol. Chem. 286:35358-35366.
47. Neuhaus, J. M., Sticher, L., Meins, F., Jr., and Boller, T. 1991. A short C-terminal sequence is necessary and sufficient for the targeting of chitinases to the plant vacuole. Proc. Natl. Acad. Sci. U.S.A. 88: 10362-10366.
48. Ohnuma, T., Numata, T., Osawa, T., Inanaga, H., Okazaki, Y., Shinya, S., Kondo, K., Fukuda, T., and Fukamizo, T. 2012. Crystal structure and chitin oligosaccharide-binding mode of a 'loopful' family GH19 chitinase from rye, Secale cereale, seeds. FEBS (Fed. Eur. Biochem. Soc.) J. 279:3639-3651.
49. Ohnuma, T., Numata, T., Osawa, T., Mizuhara, M., Lampela, O., Juffer, A. H., Skriver, K., and Fukamizo, T. 2011. A class V chitinase from Arabidopsis thaliana: Gene responses, enzymatic properties, and crystallographic analysis. Planta 234:123-137.
50. Ökmen, B., Etalo, D. W., Joosten, M. H. A. J., Bouwmeester, H. J., de Vos, R. C. H., Collemare, J., and de Wit, P. J. G. M. 2013. Detoxification of a-tomatine by Cladosporium fulvum is required for full virulence on tomato. New Phytol. 198:1203-1214.
51. Olivieri, F., Eugenia Zanetti, M., Oliva, C. R., Covarrubias, A. A., and Casalongué, C. A. 2002. Characterization of an extracellular serine protease of Fusarium eumartii and its action on pathogenesis related proteins. Eur. J. Plant Pathol. 108:63-72.
52. Petersen, T. N., Brunak, S., von Heijne, G., and Nielsen, H. 2011. SignalP 4.0: Discriminating signal peptides from transmembrane regions. Nat. Methods 8:785-786.
53. Rep, M., Dekker, H. L., Vossen, J. H., de Boer, A. D., Houterman, P. M., Speijer, D., Back, J.W., de Koster, C. G., and Cornelissen, B. J. C. 2002. Mass spectrometric identification of isoforms of PR proteins in xylem sap of fungus-infected tomato. Plant Physiol. 130:904-917.
54. Rooney, H. C. E., Van't Klooster, J. W., van der Hoorn, R. A. L., Joosten, M. H. A. J., Jones, J. D. G., and de Wit, P. J. G. M. 2005. Cladosporium Avr2 inhibits tomato Rcr3 protease required for Cf-2-dependent disease resistance. Science 308:1783-1786.
55. Rose, J. K. C., Ham, K.-S., Darvill, A. G., and Albersheim, P. 2002. Molecular cloning and characterization of glucanase inhibitor proteins: Coevolution of a counterdefense mechanism by plant pathogens. Plant Cell 14:1329-1345.
56. Schickler, H., and Chet, I. 1997. Heterologous chitinase gene expression to improve plant defence against phytopathogenic fungi. J. Ind. Microbiol. Biotechnol. 19:196-201.
57. Sela-Buurlage, M. B. (1996) In vitro sensitivity and tolerance of Fusarium solani towards chitinases and b-1, 3-glucanases. Ph.D. thesis, Wageningen University, The Netherlands.
58. Sela-Buurlage, M. B., Ponstein, A. S., Bres-Vloemans, S. A., Melchers, L. S., Van Den Elzen, P., and Cornelissen, B. 1993. Only specific tobacco (Nicotiana tabacum) chitinases and b-1, 3-glucanases exhibit antifungal activity. Plant Physiol. 101:857-863.
59. Sels, J., Mathys, J., De Coninck, B. M. A., Cammue, B. P. A., and De Bolle, M. F. C. 2008. Plant pathogenesis-related (PR) proteins: A focus on PR peptides. Plant Physiol. Biochem. 46:941-950.
60. Sinha, M., Singh, R. P., Kushwaha, G. S., Iqbal, N., Singh, A., Kaushik, S., Kaur, P., Sharma, S., and Singh, T. P. 2014. Current overview of allergens of plant pathogenesis related protein families. Scientific World Journal 2014:543195.
61. Sreedhar, L., Kobayashi, D. Y., Bunting, T. E., Hillman, B. I., and Belanger, F. C. 1999. Fungal proteinase expression in the interaction of the plant pathogen Magnaporthe poae with its host. Gene 235:121-129.
62. Stergiopoulos, I., van den Burg, H. A., Ökmen, B., Beenen, H. G., van Liere, S., Kema, G. H. J., and de Wit, P. J. G. M. 2010. Tomato Cf resistance proteins mediate recognition of cognate homologous effectors from fungi pathogenic on dicots and monocots. Proc. Natl. Acad. Sci. U.S.A. 107:7610-7615.
63. Suarez, V., Staehelin, C., Arango, R., Holtorf, H., Hofsteenge, J., and Meins, F., Jr. 2001. Substrate specificity and antifungal activity of recombinant tobacco class I chitinases. Plant Mol. Biol. 45:609-618.
64. Talavera, G., and Castresana, J. 2007. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst. Biol. 56:564-577.
65. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. 2011. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28:2731-2739.
66. ten Have, A., Espino, J. J., Dekkers, E., Van Sluyter, S. C., Brito, N., Kay, J., González, C., and van Kan, J. A. L. 2010. The Botrytis cinerea aspartic proteinase family. Fungal Genet. Biol. 47:53-65.
67. Tian, M., Benedetti, B., and Kamoun, S. 2005. A second Kazal-like protease inhibitor from Phytophthora infestans inhibits and interacts with the apoplastic pathogenesis-related protease P69B of tomato. Plant Physiol. 138:1785-1793.
68. Tian, M., Huitema, E., Da Cunha, L., Torto-Alalibo, T., and Kamoun, S. 2004. A Kazal-like extracellular serine protease inhibitor from Phytophthora infestans targets the tomato pathogenesis-related protease P69B. J. Biol. Chem. 279:26370-26377.
69. Truong, N.-H., Park, S.-M., Nishizawa, Y., Watanabe, T., Sasaki, T., and Itoh, Y. 2003. Structure, heterologous expression, and properties of rice (Oryza sativa L.) family 19 chitinases. Biosci. Biotechnol. Biochem. 67: 1063-1070.
70. Untergasser, A., Nijveen, H., Rao, X., Bisseling, T., Geurts, R., and Leunissen, J. A. M. 2007. Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Res. 35:W71-W74.
71. van den Burg, H. A., Harrison, S. J., Joosten, M. H. A. J., Vervoort, J., and de Wit, P. J. G. M. 2006. Cladosporium fulvum Avr4 protects fungal cell walls against hydrolysis by plant chitinases accumulating during infection. Mol. Plant-Microbe Interact. 19:1420-1430.
72. Van Esse, H. P., Bolton, M. D., Stergiopoulos, I., deWit, P. J.G.M., andThomma, B. P. H. J. 2007 The chitin-binding Cladosporium fulvum effector protein Avr4 is a virulence factor. Mol. Plant-Microbe Interact. 20 1092-1101.
73. van Loon, L. C., Rep, M., and Pieterse, C.M. J. 2006. Significance of inducible defense-related proteins in infected plants. Annu. Rev. Phytopathol. 44: 135-162.
74. Wu, S. W., Wang, H. W., Yang, Z. D., and Kong, L. R. 2014. Expression comparisons of pathogenesis-related (PR) genes in wheat in response to infection/infestation by Fusarium, Yellow dwarf virus (YDV) aphidtransmitted and hessian fly. J. Integr. Agr. 13:926-936.
75. Wubben, J. P., Joosten, M. H. A. J. M., Vankan, J. A. L., and de Wit, P. J. G. M. 1992. Subcellular localization of plant chitinases and 1, 3- beta-glucanases in Cladosporium fulvum (syn. Fulvia fulva)-infected tomato leaves. Physiol. Mol. Plant Pathol. 41:23-32.
76. Yamagami, T., and Ishiguro, M. 1998. Complete amino acid sequences of chitinase-1 and -2 from bulbs of genus Tulipa. Biosci. Biotechnol. Biochem. 62:1253-1257.