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Molecular Mechanism of Nematophagous Fungi Infection of Nematodes

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Part of the book series: Fungal Diversity Research Series ((FDRS,volume 23))

Abstract

Nematophagous fungi are an important group of soil microorganisms that can suppress the populations of plant-parasitic nematodes. At present, the detailed molecular pathogenic mechanisms against nematodes by nematophagous fungi have not yet been fully elucidated. However, increasing evidence show that extracellular hydrolytic enzymes including proteases, collagenase, and chitinase may be involved in nematode-cuticle penetration and host-cell digestion. Recently, the crystal structures of proteases (Ver112 and PL646) and chitinase CrChi1 from nematophagous fungi were resolved, which can help us to identify the active site residues and to elucidate the catalytic mechanism of these enzymes involved in infection against hosts. The expression and regulation of protease PrC from Clonostachys rosea by different environmental conditions has also been reported. The genome of Arthrobotrys oligospora has been sequenced, and a model of nematode trap formation in A. oligospora suggested; thus the genome data may serve as a roadmap for further investigations into the interaction between nematode-trapping fungi and their host nematodes, providing broad foundations for research on the biocontrol of pathogenic nematodes. In this chapter, we describe the characterization of extracellular enzymes from nematophagous fungi, the expression and regulation of serine protease prC in Clonostachys rosea, and the genome and proteomic analyses of the nematode-trapping fungus Arthrobotrys oligospora.

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References

  • Åhman, J., Johanson, T., Olsson, M., Punt, P. J., van den Hondel, C. A., & Tunlid, A. (2002). Improving the pathogenicity of a nematode-trapping fungus by genetic engineering of a subtilisin with nematotoxic activity. Applied and Environmental Microbiology, 68, 3408–3415.

    PubMed Central  PubMed  Google Scholar 

  • Ahrén, D., Tholander, M., Fekete, C., Rajashekar, B., Friman, E., Johansson, T., & Tunlid, A. (2005). Comparison of gene expression in trap cells and vegetative hyphae of the nematophagous fungus Monacrosporium haptotylum. Microbiology, 151, 789–803.

    PubMed  Google Scholar 

  • Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W., & Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Research, 25, 3389–3402.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Bidochka, M. J., & Khachatourians, G. G. (1987). Purification and properties of an extracellular protease produced by the entomopathogenic fungus Beauveria bassiana. Applied and Environmental Microbiology, 53, 1679–1684.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Bird, A. F., & Self, P. G. (1995). Chitin in Meloidogyne javanica. Fundamental and Applied Nematology, 18, 235–239.

    Google Scholar 

  • Blaxter, M. L., & Robertson, W. M. (1998). The cuticle. In R. N. Perry & D. J. Wright (Eds.), The physiology and biochemistry of free-living and plant-parasitic nematodes (pp. 25–48). Wallingford: CABI Publishing.

    Google Scholar 

  • Bonants, P. J. M., Fitters, P. F. L., Thijs, H., den Belder, E., Waalwijk, C., & Henfling, J. W. D. M. (1995). A basic serine protease from Paecilomyces lilacinus with biological activity against Meloidogyne hapla eggs. Microbiology, 141, 775–784.

    PubMed  CAS  Google Scholar 

  • Bordallo, J. J., Lopez-Llorca, L. V., Jansson, H. B., Salinas, J., Persmark, L., & Asensio, L. (2002). Colonization of plant roots by egg-parasitic and nematode-trapping fungi. New Phytologist, 154, 491–499.

    Google Scholar 

  • Bortone, K., Monzingo, A. F., Ernst, S., & Robertus, J. D. (2002). The structure of an allosamidin complex with the Coccidiodes immitis defines a role for second acid residue in substrate assisted mechanism. Journal of Molecular Biology, 320, 293–302.

    PubMed  CAS  Google Scholar 

  • Bose, S., Dutko, J. A., & Zitomer, R. S. (2005). Genetic factors that regulate the attenuation of the general stress response of yeast. Genetics, 169, 1215–1226.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Bradford, M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72, 248–254.

    PubMed  CAS  Google Scholar 

  • Braga, F. R., Araújo, J. V., Soares, F. E. F., Geniêr, H. L. A., & Queiroz, J. H. (2012). An extracellular serine protease of an isolate of Duddingtonia flagrans nematophagous fungus. Biocontrol Science and Technology, 22, 1131–1142.

    Google Scholar 

  • Caracuel, Z., Roncero, M. I., Espeso, E. A., Gonzalez-Verdejo, C. I., Garcia-Maceira, F. I., Di Pietro, A. (2003). The pH signalling transcription factor PacC controls virulence in the plant pathogen Fusarium oxysporum. Molecular Microbiology, 48, 765–779.

    PubMed  CAS  Google Scholar 

  • Chang, A., Scheer, M., Grote, A., Schomburg, I., & Schomburg, D. (2009). BRENDA, AMENDA and FRENDA the enzyme information system: New content and tools in 2009. Nucleic Acids Research, 37, D588–D592.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Chen, L. L., Liu, L. J., Shi, M., Song, X. Y., Zheng, C. Y., Chen, X. L., & Zhang, Y. Z. (2009). Characterization and gene cloning of a novel serine protease with nematicidal activity from Trichoderma pseudokoningii SMF2. FEMS Microbiology Letters, 299, 135–142.

    PubMed  CAS  Google Scholar 

  • Cox, G. N., Kusch, M., & Edgar, R. S. (1981). Cuticle of Caenorhabditis elegans: Its isolation and partial characterization. Journal of Cell Biology, 90, 7–17.

    PubMed  CAS  Google Scholar 

  • Davis, D., Edwards, J. E., Jr Mitchell, A. P., & Ibrahim, A. S. (2000). Candida albicans RIM101 pH response pathway is required for host-pathogen interactions. Infection and Immunity, 68, 5953–5959.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Dijksterhuis, J., Veenhuis, M., Harder, W., & Nordbring-Hertz, B. (1994). Nematophagous fungi: Physiological aspects and structurefunction relationships. Advances in Microbial Physiology, 36, 111–143.

    PubMed  CAS  Google Scholar 

  • Dong, L. Q., Yang, J. K., & Zhang, K. Q. (2007). Cloning and phylogenetic analysis of the chitinase gene from the facultative pathogen Paecilomyces lilacinus. Journal of Applied Microbiology, 103, 2476–2488.

    PubMed  CAS  Google Scholar 

  • Eshel, D., Miyara, I., Ailing, T., Dinoor, A., & Prusky, D. (2002). pH regulates endoglucanase expression and virulence of Alternaria alternata in persimmon fruit. Molecular Plant-microbe Interactions 15, 774–779.

    PubMed  CAS  Google Scholar 

  • Esteves, I., Peteira, B., Atkins, S. D., Magan, N., & Kerry, B. (2009). Production of extracellular enzymes by different isolates of Pochonia chlamydosporia. Mycological Research, 113, 867–876.

    PubMed  CAS  Google Scholar 

  • Fang, W., Leng, B., Xiao, Y., Jin, K., Ma, J., Fan, Y., Feng, J., Yang, X., Zhang, Y., & Pei, Y. (2005). Cloning of Beauveria bassiana chitinase gene Bbchit1 and its application to improve fungal strain virulence. Applied and Environmental Microbiology, 71, 363–370.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Fekete, C., Tholander, M., Rajashekar, B., Ahrén, D., Friman, E., Johansson, T., & Tunlid, A. (2008). Paralysis of nematodes: Shifts in the transcriptome of the nematode-trapping fungus Monacrosporium haptotylum during infection of Caenorhabditis elegans. Environmental Microbiology, 10, 364–375.

    PubMed  CAS  Google Scholar 

  • Fernández-Acero, F. J., Jorge, I., Calvo, E., Vallejo, I., Carbú, M., Camafeita, E., Garrido, C., López, J. A., Jorrin, J., & Cantoral, J. M. (2007). Proteomic analysis of phytopathogenic fungus Botrytis cinerea as a potential tool for identifying pathogenicity factors, therapeutic targets and for basic research. Archives of Microbiology, 187, 207–215.

    PubMed  Google Scholar 

  • Fusetti, F., von Moeller, H., Houston, D., Rozeboom, H. J., Dijkstra, B. W., Boot, R. G., Aerts, J. M., & van Aalten, D. M. F. (2002). Structure of human chitotriosidase. Implications for specific inhibitor design and function of mammalian chitinase-like lectins. Journal of Biological Chemistry, 277, 25537–25544.

    PubMed  CAS  Google Scholar 

  • Galagan, J. E., Calvo, S. E., Borkovich, K. A., Selker, E. U., Read, N. D., Jaffe, D., FitzHugh, W., Ma, L. J., Smirnov, S., Purcell, S., Rehman, B., Elkins, T., Engels, R., Wang, S., Nielsen, C. B., Butler, J., Endrizzi, M., Qui, D., Ianakiev, P., Bell-Pedersen, D., Nelson, M. A., Werner-Washburne, M., Selitrennikoff, C. P., Kinsey, J. A., Braun, E. L., Zelter, A., Schulte, U., Kothe, G. O., Jedd, G., Mewes, W., Staben, C., Marcotte, E., Greenberg, D., Roy, A., Foley, K., Naylor, J., Stange-Thomann, N., Barrett, R., Gnerre, S., Kamal, M., Kamvysselis, M., Mauceli, E., Bielke, C., Rudd, S., Frishman, D., Krystofova, S., Rasmussen, C., Metzenberg, R. L., Perkins, D. D., Kroken, S., Cogoni, C., Macino, G., Catcheside, D., Li, W., Pratt, R. J., Osmani, S. A., DeSouza, C. P., Glass, L., Orbach, M. J., Berglund, J. A., Voelker, R., Yarden, O., Plamann, M., Seiler, S., Dunlap, J., Radford, A., Aramayo, R., Natvig, D. O., Alex, L. A., Mannhaupt, G., Ebbole, D. J., Freitag, M., Paulsen, I., Sachs, M. S., Lander, E. S., Nusbaum, C., & Birren, B. (2003). The genome sequence of the filamentous fungus Neurospora crassa. Nature, 422, 859–868.

    PubMed  CAS  Google Scholar 

  • Gan, Z. W., Yang, J. K., Tao, N., Liang, L. M., Mi, Q. L., Li, J., & Zhang, K. Q. (2007a). Cloning of the gene Lecanicillium psalliotae chitinase Lpchi1 and identification of its potential role in the biocontrol of root-knot nematode Meloidogyne incognita. Applied Microbiology and Biotechnology, 76, 1309–1317.

    CAS  Google Scholar 

  • Gan, Z. W., Yang, J. K., Tao, N., Yu, Z. F., & Zhang, K. Q. (2007b). Cloning and expression analysis of a chitinase gene Crchi1 from the mycoparasitic fungus Clonostachys rosea (syn. Gliocladium roseum). Journal of Microbiology, 45, 422–430.

    CAS  Google Scholar 

  • Gan, Z. W., Yang, J. K., Tao, N., Lou, Z. Y., Mi, Q. L., Meng, Z. H., & Zhang, K. Q. (2009). Crystallization and preliminary crystallographic analysis of a chitinase from Clonostachys rosea. Acta Crystallographica Section F: Structural Biology and Crystallization Communications, 65, 386–388.

    PubMed Central  CAS  Google Scholar 

  • Gao, Q., Jin, K., Ying, S. H., Zhang, Y., Xiao, G., Shang, Y., Duan, Z., Hu, X., Xie, X. Q., Zhou, G., Peng, G., Luo, Z., Huang, W., Wang, B., Fang, W., Wang, S., Zhong, Y., Ma, L. J., St Leger, R. J., Zhao, G. P., Pei, Y., Feng, M. G., Xia, Y. X., & Wang, C. S. (2011). Genome sequencing and comparative transcriptomics of the model entomopathogenic fungi Metarhizium anisopliae and M. acridum. PLoS Genetics, 7, e100126.

    Google Scholar 

  • Gasch, A. P., Spellman, P. T., Kao, C. M., Carmel-Harel, O., Eisen, M. B., Storz, G., Botstein, D., & Brown, P. O. (2000). Genomic expression programs in the response of yeast cells to environmental changes. Molecular Biology of the Cell, 11, 4241–4257.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Gordon, D., Desmarais, C., & Green, P. (2001). Automated finishing with autofinish. Genome Research, 11, 614–625.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Haas, B. J., Salzberg, S. L., Zhu, W., Pertea, M., Allen, J. E., Orvis, J., White, O., Buell, C. R., & Wortman, J. R. (2008). Automated eukaryotic gene structure annotation using EVidenceModeler and the program to assemble spliced alignments. Genome Biology, 9, R7.

    PubMed Central  PubMed  Google Scholar 

  • Henrissat, B., & Bairoch, A. (1993). New families in the classification of glycosyl hydrolases based on amino acid sequence similarities. Biochemical Journal, 293, 781–788.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Hollis, T., Monzingo, A. F., Bortone, K., Ernst, S., Cox, R., & Robertus, J. D. (2000). The X-ray structure of a chitinase from the pathogenic fungus Coccidioides immitis. Protein Science, 9, 544–551.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Houston, D. R., Eggleston, I., Synstad, B., Eijsink, V. G., & van Aalten, D. M. F. (2002). The cyclic dipeptide C1-4[cyclo-(L-Arg-D-Pro)] inhibits family 18 chitinases by structural mimicry of a reaction intermediate. Biochemical Journal, 368, 23–27.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Hurtado-Guerrero, R., & van Aalten, D. M. F. (2007). Structure of Saccharomyces cerevisiae chitinase 1 and screening-based discovery of potent inhibitors. Chemistry & Biology, 14, 589–599.

    CAS  Google Scholar 

  • Jackson, C. W., Heale, J. B., & Hall, R. A. (1985). Traits associated with virulence to the aphid Macrosiphoniella sanbornii in eighteen isolates of Verticillium lecanii. Annals of Applied Biology, 106, 39–48.

    Google Scholar 

  • Jensen, L. J., Kuhn, M., Stark, M., Chaffron, S., Creevey, C., Muller, J., Doerks, T., Julien, P., Roth, A., Simonovic, M., Bork, P., & von Mering, C. (2009). STRING 8-a global view on proteins and their functional interactions in 630 organisms. Nucleic Acids Research, 37, D412–D416.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Joshi, L., St Leger, R. J., & Bidochka, M. J. (1995). Cloning of a cuticle-degrading protease from the entomopathogenic fungus, Beauveria bassiana. FEMS Microbiology Letters, 125, 211–217.

    PubMed  CAS  Google Scholar 

  • Kanda, S., Aimi, T., Kano, S., Ishihara, S., Kitamoto, Y., & Morinaga, T. (2008). Ambient pH signaling regulates expression of the serine protease gene (spr1) in pine wilt nematode-trapping fungus, Monacrosporium megalosporum. Microbiological Research, 163, 63–72.

    PubMed  CAS  Google Scholar 

  • Kanehisa, M., Goto, S., Kawashima, S., Okuno, Y., & Hattori, M. (2004). The KEGG resources for deciphering the genome. Nucleic Acids Research, 32, D277–D280.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Khan, A., Williams, K. L., Molloy, M. P., & Nevalainen, H. (2003). Purification and characterization of a serine protease and chitinases from Paecilomyces lilacinus and detection of chitinase activity on 2D gels. Protein Expression and Purification, 32, 210–220.

    PubMed  CAS  Google Scholar 

  • Khan, A., Williams, K. L., & Nevalainen, H. K. M. (2004). Effects of Paecilomyces lilacinus protease and chitinase on the eggshell structures and hatching of Meloidogyne javanica juveniles. Biological Control, 31, 346–352.

    CAS  Google Scholar 

  • Korf, I. (2004). Gene finding in novel genomes. BMC Bioinformatics, 5, 59.

    PubMed Central  PubMed  Google Scholar 

  • Larriba, E., Martín-Nieto, J., & Lopez-Llorca, L. V. (2012). Gene cloning, molecular modeling, and phylogenetics of serine protease P32 and serine carboxypeptidase SCP1 from nematophagous fungi Pochonia rubescens and Pochonia chlamydosporia. Canadian Journal of Microbiology, 58, 815–827.

    PubMed  CAS  Google Scholar 

  • Li, T. F., Zhang, K. Q., & Liu, X. Z. (2000). Taxonomy of nematophagous fungi (Chinese). Beijing: Science Press.

    Google Scholar 

  • Li, J., Yang, J. K., Huang, X. W., & Zhang, K. Q. (2006). Purification and characterization of an extracellular serine protease from Clonostachys rosea and its potential as a pathogenic factor. Process Biochemistry, 41, 925–929.

    CAS  Google Scholar 

  • Li, J., Yu, L., Yang, J. K., Dong, L. Q., Tian, B. Y., Yu, Z. F., Liang, L. M., Zhang, Y., Wang, X., & Zhang, K. Q. (2010). New insights into the evolution of subtilisin-like serine protease genes in Pezizomycotina. BMC Evolutionary Biology, 10, 68.

    PubMed Central  PubMed  Google Scholar 

  • Liang, L. M., Meng, Z. H., Ye, F. P., Yang, J. K., Liu, S. Q., Sun, Y., Guo, Y., Mi, Q. L., Huang, X. W., Zou, C. G., Rao, Z. H., Lou, Z. Y., & Zhang, K. Q. (2010). The crystal structures of two cuticle-degrading proteases from nematophagous fungi and their contribution to infection against nematodes. FASEB Journal, 24, 1391–1400.

    PubMed  CAS  Google Scholar 

  • Liang, L. M., Liu, S. Q., Yang, J. K., Meng, Z. H., Lei, L. P., & Zhang, K. Q. (2011a). Comparison of homology models and crystal structures of cuticle-degrading proteases from nematophagous fungi: Structural basis of nematicidal activity. FASEB Journal, 25, 1894–1902.

    CAS  Google Scholar 

  • Liang, L. M., Yang, J. K., Li, J., Mo, Y. Y., Li, L., Zhao, X. Y., & Zhang, K. Q. (2011b). Cloning and homology modeling of a serine protease gene (PrC) from the nematophagous fungus Clonostachys rosea. Annals of Microbiology, 61, 511–516.

    CAS  Google Scholar 

  • Limon, M. C., Pintor-Toro, J. A., & Benitez, T. (1999). Increased anti-fungal activity of Trichoderma harzianum transformants that overexpress a 33-kDa chitinase. Phytopathology, 89, 254–261.

    PubMed  CAS  Google Scholar 

  • Liu, S. Q., Tao, Y., Meng, Z. H., Fu, Y. X., & Zhang, K. Q. (2011). The effect of calciums on the molecular motions of proteinase K. Journal of Molecular Modeling, 17, 289–300.

    PubMed  CAS  Google Scholar 

  • Lorito, M. S., Woo, L., Garcia, I., Colucci, G., Harman, G. E., Pintor-Toro, J. A., Filippone, E., Muccifora, S., Lawrence, C. B., Zoina, A., Tuzun, S., & Scala, F. (1998). Genes from mycoparasitic fungi as a source for improving plant resistance to fungi pathogens. Proceedings of the National academy of Sciences of the United States of America, 95, 7860–7865.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Lopez-Llorca, L. V. (1990). Purification and properties of extracellular proteases produced by the nematophagous fungus Verticillium suchlasporium. Canadian Journal of Microbiology, 36, 530–537.

    CAS  Google Scholar 

  • Lopez-Llorca, L. V., & Robertson, W. M. (1992). Immumocytochemical locolization of a 32-kDa protease from the nematophagous fungus Verticillium suchlasporium in infected nematode eggs. Experimental Mycology, 16, 261–267.

    CAS  Google Scholar 

  • Lýsek, H., & Krajcí, D. (1987). Penetration of ovicidal fungus Verticillium chlamydosporium through the Ascaris lumbricoides egg-shells. Folia Parasitologica, 34, 57–60.

    PubMed  Google Scholar 

  • Maclennan, J. D., Mandl, I., & Howes, E. L. (1953). Bacterial digestion of collagen. Journal of Clinical Investigation, 32, 1317–1322.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Majoros, W. H., Pertea, M., & Salzberg, S. L. (2004). TigrScan and GlimmerHMM: Two open source ab initio eukaryotic gene-finders. Bioinformatics, 20, 2878–2879.

    PubMed  CAS  Google Scholar 

  • Margulies, M., Egholm, M., Altman, W. E., Attiya, S., Bader, J. S., Bemben, L. A., Berka, J., Braverman, M. S., Chen, Y. J., Chen, Z., Dewell, S. B., Du, L., Fierro, J. M., Gomes, X. V., Godwin, B. C., He, W., Helgesen, S., Ho, C. H., Irzyk, G. P., Jando, S. C., Alenquer, M. L., Jarvie, T. P., Jirage, K. B., Kim, J. B., Knight, J. R., Lanza, J. R., Leamon, J. H., Lefkowitz, S. M., Lei, M., Li, J., Lohman, K. L., Lu, H., Makhijani, V. B., McDade, K. E., McKenna, M. P., Myers, E. W., Nickerson, E., Nobile, J. R., Plant, R., Puc, B. P., Ronan, M. T., Roth, G. T., Sarkis, G. J., Simons, J. F., Simpson, J. W., Srinivasan, M., Tartaro, K. R., Tomasz, A., Vogt, K. A., Volkmer, G. A., Wang, S. H., Wang, Y., Weiner, M. P., Yu, P., Begley, R. F., & Rothberg, J. M. (2005). Genome sequencing in microfabricated high-density picolitre reactors. Nature, 437, 376–380.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Mi, Q. L., Yang, J. K., Ye, F. P., Gan, Z. W., Wu, C. W., Niu, X. M., Zou, C. G., & Zhang, K. Q. (2010). Cloning and overexpression of Pochonia chlamydosporia chitinase gene pcchi44, a potential virulence factor in infection against nematodes. Process Biochemistry, 45, 810–814.

    CAS  Google Scholar 

  • Mileweski, S., O’Donnell, R. W., & Gooday, G. W. (1992). Chemical modification studies of the active center of Candida albicans chitinase and its inhibition by allosamidin. Journal of General Microbiology, 138, 2545–5501.

    Google Scholar 

  • Mo, M. H., Chen, W. M., Su, H. Y., Zhang, K. Q., Duan, C. Q., & He, D. M. (2006). Heavy metal tolerance of nematode-trapping fungi in lead-polluted soils. Applied Soil Ecology, 31, 11–19.

    Google Scholar 

  • Monfort, E., Lopez-Llorca, L. V., & Jansson, H.-B. (2005). Colonisation of seminal roots of wheat and barley by egg-parasitic nematophagous fungi and their effects on Gaeumannomyces graminis var. tritici and development of root-rot. Soil Biology and Biochemistry, 37, 1229–1235.

    CAS  Google Scholar 

  • Nordbring-Hertz, B. (2004). Morphogenesis in the nematode-trapping fungus Arthrobotrys oligospora-an extensive plasticity of infection structures. Mycologist, 18, 125–133.

    Google Scholar 

  • Nordbring-Hertz, B., Neumeister, H., Sjollema, K., & Veenhuis, M. (1995). A conidial trap - forming mutant of Arthrobotrys oligospora. Mycological Research, 99, 1395–1398.

    Google Scholar 

  • Nordbring-Hertz, B., Jansson, H. B., & Tunlid, A. (2006). Nematophagous fungi. Encyclopedia of Life Sciences. doi:10.1002/9780470015902.a0000374.pub3. (John Wiley & Sons, Ltd: Chichester).

    Google Scholar 

  • Olsson, S., & Persson, Y. (1994). Transfer of phosphorus from Rhizoctonia solani to the mycoparasite Arthrobotrys oligospora. Mycological Research, 98, 1065–1068.

    Google Scholar 

  • Orikoshi, H., Nakayama, S., Miyamoto, K., Hanato, C., Yasuda, M., Inamori, Y., & Tsujibo, H. (2005). Roles of four chitinases (chia, chib, chic, and chid) in the chitin degradation system of marine bacterium Alteromonas sp. strain O-7. Applied and Environmental Microbiology, 71, 1811–1815.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Overbeek, R., Fonstein, M., D’Souza, M., Pusch, G. D., & Maltsev, N. (1999). The use of gene clusters to infer functional coupling. Proceedings of the National academy of Sciences of the United States of America, 96, 2896–2901.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Papanikolau, Y., Tavlas, G., Vorgias, C. E., & Petratos, K. (2003). De novo purification scheme and crystallization conditions yield highresolution structures of chitinase A and its complex with the inhibitor allosamidin. Acta Crystallographica Section D: Biological Crystallography, 59, 400–403.

    Google Scholar 

  • Peñalva, M. A., Tilburn, J., Bignell, E., & Arst, H. N. Jr. (2008). Ambient pH gene regulation in fungi: Making connections. Trends in Microbiology, 16, 291–300.

    PubMed  Google Scholar 

  • Perry, R. N., & Trett, M. W. (1986). Ultrastructure of the egg shell of Heterodera schachtii and H. glycines (Nematoda: Tylenchida). Revue de Nématologie, 9, 399–403.

    Google Scholar 

  • Persmark, L., & Nordbring-Hertz, B. (1997). Conidial trap formation of nematode-trapping fungi in soil and soil extracts. FEMS Microbiology Ecology, 22, 313–323.

    CAS  Google Scholar 

  • Pfister, D. H., & Liftik, M. E. (1995). Two Arthrobotrys anamorphs from Orbilia auricolor. Mycologia, 87, 684–688.

    Google Scholar 

  • Phillips, D. C. (1967). The hen-egg-white lysozyme molecule. Proceedings of the National academy of Sciences of the United States of America, 57, 484–495.

    CAS  Google Scholar 

  • Quackenbush, J., Cho, J., Lee, D., Liang, F., Holt, I., Karamycheva, S., Parvizi, B., Pertea, G., Sultana, R., & White, J. (2001). The TIGR Gene Indices: Analysis of gene transcript sequences in highly sampled eukaryotic species. Nucleic Acids Research, 29, 159–164.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Quevillon, E., Silventoinen, V., Pillai, S., Harte, N., Mulder, N., Apweiler, R., & Lopez, R. (2005). InterProScan: Protein domains identifier. Nucleic Acids Research, 33, W116–W120.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Rao, F. V., Andersen, O. A., Vora, K. A., Demartino, J. A., & van Aalten, D. M. (2005a). Methylxanthine drugs are chitinase inhibitors: Investigation of inhibition and binding modes. Chemistry & Biology, 12, 973–980.

    CAS  Google Scholar 

  • Rao, F. V., Houston, D. R., Boot, R. G., Aerts, J. M., Hodkinson, M., Adams, D. J., Shiomi, K., Omura, S., & van Aalten, D. M. (2005b). Specificity and affinity of natural product cyclopentapeptide inhibitors against A. fumigatus, human, and bacterial chitinases. Chemistry & Biology, 12, 65–76.

    CAS  Google Scholar 

  • Rollins, J. A., & Dickman, M. B. (2001). pH signaling in Sclerotinia sclerotiorum: Identification of a pacC/RIM1 homolog. Applied and Environmental Microbiology, 67, 75–81.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Rost, B. (1999). Twilight zone of protein sequence alignments. Protein Engineering, 12, 85–94.

    PubMed  CAS  Google Scholar 

  • Schenck, S., Chase, T. J., Rosenzweig, W. D., & Pramer, D. (1980). Collagenase production by nematode-trapping fungi. Applied and Environmental Microbiology, 40, 567–570.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Schmidt, A. R., Dörfelt, H., & Perrichot, V. (2007). Carnivorous fungi from Cretaceous Amber. Science, 318, 1743.

    PubMed  CAS  Google Scholar 

  • Schultz, R. M., & Liebman, M. N. (1997). Structure-function relationship in protein families. In T. M. Devlin (Ed.), Textbook of biochemistry with clinical correlations (4th ed., pp. 1–2). New York: Wiley-Liss.

    Google Scholar 

  • Schüttelkopf, A. W., Andersen, O. A., Rao, F. V., Allwood, M., Lloyd, C., Eggleston, I. M., & van Aalten, D. M. (2006). Screening-based discovery and structural dissection of a novel family 18 chitinase inhibitor. Journal of Biological Chemistry, 281, 27278–27285.

    PubMed  Google Scholar 

  • Segers, R., Butt, T. M., Kerry, B. R., & Peberdy, J. F. (1994). The nematophagous fungus Verticillium chlamydosporium produces a chymoelastase-like protease which hydrolyses host nematode proteins in situ. Microbiology, 140, 2715–2723.

    PubMed  CAS  Google Scholar 

  • Seidl, V., Huemer, B., Seiboth, B., & Kubicek, C. P. (2005). A complete survey of Trichoderma chitinases reveals three distinct subgroups of family 18 chitinases. FEBS Journal, 272, 5923–5939.

    PubMed  CAS  Google Scholar 

  • Siddiqui, Z. A., & Mahmood, I. (1996). Biological control of plant parasitic nematodes by fungi: A review. Bioresource Technology, 58, 229–239.

    CAS  Google Scholar 

  • Siezen, R. J., & Leunissen, J. A. M. (1997). Subtilases: The superfamily of subtilisin like serine protease. Protein Science, 6, 501–523.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Slater, G. S. C., & Birney, E. (2005). Automated generation of heuristics for biological sequence comparison. BMC Bioinformatics, 6, 31.

    PubMed Central  PubMed  Google Scholar 

  • Soares, F. E., Braga, F. R., Araújo, J. V., dos Santos Lima, W., Mozer, L. R., & Queiróz, J. H. (2012). In vitro activity of a serine protease from Monacrosporium thaumasium fungus against first-stage larvae of Angiostrongylus vasorum. Parasitology Research, 110, 2423–2427.

    PubMed  Google Scholar 

  • Stanke, M., & Waack, S. (2003). Gene prediction with a hidden Markov model and a new intron submodel. Bioinformatics, 19, ii215–ii225.

    PubMed  Google Scholar 

  • St Leger, R. J., & Wang, C. (2011). Genetic engineering of fungal biocontrol agents to achieve greater efficacy against insect pests. Applied Microbiology and Biotechnology, 85, 901–907.

    Google Scholar 

  • St Leger, R. J., Charnley, A. K., & Cooper, R. M. (1986). Cuticle-degrading enzymes of entomopathogenic fungi: Synthesis in culture on cuticle. Journal of Invertebrate Pathology, 48, 85–95.

    CAS  Google Scholar 

  • St Leger, R. J., Frank, D. C., Roberts, D. W., & Staples, R. C. (1992). Molecular cloning and regulatory analysis of the cuticle-degrading protease structural gene from the entomopathogenic fungus Metarhizium anisopliae. European Journal of Biochemistry, 204, 991–1001.

    PubMed  CAS  Google Scholar 

  • St Leger, R. J., Staples, R. C., & Roberts, D. W. (1993). Entomopathogenic isolates of Metarhizium anisopliae, Beauvaria bassiana, and Aspergillus flavus produce multiple extracellular chitinase isozymes. Journal of Invertebrate Pathology, 61, 81–84.

    CAS  Google Scholar 

  • St Leger, R. J., Nelson, J. O., & Screen, S. E. (1999). The entomopathogenic fungus Metarhizium anisopliae alters ambient pH, allowing extracellular protease production and activity. Microbiology, 145, 2691–2699.

    PubMed  CAS  Google Scholar 

  • Sutton, J. C., Li, D. W., Peng, G., Yu, H., Zhang, P., & Valdebenito-Sanhueza, R. M. (1997). Gliocladium roseum a versatile adversary of a Botrytis cinerea in crops. Plant Disease, 81, 316–328.

    Google Scholar 

  • Tamura, K., Dudley, J., Nei, M., & Kumar, S. (2007). MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution, 24, 1596–1599.

    PubMed  CAS  Google Scholar 

  • Tao, Y., Rao, Z. H., & Liu, S. Q. (2010). Insight derived from molecular dynamics simulation into substrate-induced changes in protein motions of proteinase K. Journal of Biomolecular Structure and Dynamics, 28, 143–157.

    PubMed  CAS  Google Scholar 

  • Tatusov, R. L., Fedorova, N. D., Jackson, J. D., Jacobs, A. R., Kiryutin, B., Koonin, E. V., Krylov, D. M., Mazumder, R., Mekhedov, S. L., Nikolskaya, A. N., Rao, B. S., Smirnov, S., Sverdlov, A. V., Vasudevan, S., Wolf, Y. I., Yin, J. J., & Natale, D. A. (2003). The COG database: An updated version includes eukaryotes. BMC Bioinformatics, 4, 41.

    PubMed Central  PubMed  Google Scholar 

  • Ter-Hovhannisyan, V., Lomsadze, A., Chernoff, Y. O., & Borodovsky, M. (2008). Gene prediction in novel fungal genomes using an ab initio algorithm with unsupervised training. Genome Research, 18, 1979–1990.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Terwisscha van Scheltinga, A. C., Armand, S., Kalk, K. H., Isogai, A., Henrissat, B., & Dijkstra, B. W. (1995). Stereochemistry of chitin hydrolysis by a plant chitinase/lysozyme and X-ray structure of a complex with allosamidin: Evidence for substract assisted catalysis. Biochemistry, 34, 15619–15623.

    PubMed  CAS  Google Scholar 

  • Tikhonov, V. E., Lopez-Llorca, L. V., Salinas, J., & Jansson, H. B. (2002). Purification and characterization of chitinases from the nematophagous fungi Verticillium chlamydosporium and V. suchlasporium. Fungal Genetics and Biology, 35, 67–78.

    PubMed  CAS  Google Scholar 

  • Tilburn, J., Sarkar, S., Widdick, D. A., Espeso, E. A., Orejas, M., Mungroo, J., Peñalva, M. A., & Arst, H. N. Jr. (1995). The Aspergillus PacC zinc finger transcription factor mediates regulation of both acidand alkaline-expressed genes by ambient pH. EMBO Journal, 14, 779–790.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Tosi, S., Annovazzi, L., Tosi, I., Iadrola, P., & Caretta, G. (2001). Collagenase production in an antarctic strain of Arthrobotrys tortor Jarowaja. Mycopathologia, 153, 157–162.

    Google Scholar 

  • Tunlid, A., & Jansson, S. (1991). Proteases and their involvement in the infection and immobilization of nematodes by the nematophagous fungus Arthrobotrys oligospora. Applied and Environmental Microbiology, 57, 2868–2872.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Tunlid, A., Rosen, S., Ek, B., & Rask, L. (1994). Purification and characterization of an extracellular serine protease from the nematode-trapping fungus Arthrobotrys oligospora. Microbiology, 140, 1687–1695.

    PubMed  Google Scholar 

  • van Aalten, D. M., Komander, D., Synstad, B., Gåseidnes, S., Peter, M. G., & Eijsink, V. G. (2001). Structural insights into the catalytic mechanism of a family 18 exo-chitinase. Proceedings of the National academy of Sciences of the United States of America, 98, 8979–8984.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Wang, B., Wu, W. P., & Liu, X. Z. (2007). Purification and characterization of a neutral serine protease with nematicidal activity from Hirsutella rhossiliensis. Mycopathologia, 163, 169–176.

    PubMed  CAS  Google Scholar 

  • Wang, M., Yang, J. K., & Zhang, K. Q. (2006a). Characterization of an extracellular protease and its cDNA from the nematode-trapping fungus Monacrosporium microscaphoides. Canadian Journal of Microbiology, 52, 130–139.

    CAS  Google Scholar 

  • Wang, R. B., Yang, J. K., Lin, C., & Zhang, K. Q. (2006b). Purification and characterization of an extracellular serine protease from the nematode-trapping fungus Dactylella shizishanna. Letters in Applied Microbiology, 42, 589–594.

    CAS  Google Scholar 

  • Wang, B., Liu, X., Wu, W. P., Liu, X., & Li, S. (2009). Purification, characterization, and gene cloning of an alkaline serine protease from a highly virulent strain of the nematode-endoparasitic fungus Hirsutella rhossiliensis. Microbiological Research, 164, 665–673.

    PubMed  CAS  Google Scholar 

  • Ward, E., Kerry, B. R., Manzanilla-López, R. H., Mutua, G., Devonshire, J., Kimenju, J., & Hirsch, P. R. (2012). The Pochonia chlamydosporia serine protease gene vcp1 is subject to regulation by carbon, nitrogen and pH: Implications for nematode biocontrol. PLoS One, 7, e35657.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Watanabe, T., Kobori, K., Miyashita, K., Fujii, T., Sakai, H., Uchida, M., & Tanaka, H. (1993). Identification of glutamic acid 204 and aspartic acid 200 in chitinase A1 of Bacillus circulans WL212 as essential residues for chitinase activity. Journal of Biological Chemistry, 268, 18567–18572.

    PubMed  CAS  Google Scholar 

  • Wharton, D. A. (1980). Nematode egg-shells. Parasitology, 81, 447–463.

    PubMed  CAS  Google Scholar 

  • Winnenburg, R., Baldwin, T. K., Urban, M., Rawlings, C., Köhler, J., & Hammond-Kosack, K. E. (2006). PHI-base: A new database for pathogen host interactions. Nucleic Acids Research, 34, D459–D464.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Xue, A. G. (2003). Biological control of pathogens causing root rot complex in field pea using Clonostachys rosea strain ACM941. Phytopathology, 93, 329–335.

    PubMed  Google Scholar 

  • Yakoby, N., Kobiler, I., Dinoor, A., & Prusky, D. (2000). pH regulation of pectate lyase secretion modulates the attack of Colletotrichum gloeosporioides on avocado fruits. Applied and Environmental Microbiology, 66, 1026–1030.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Yang, J. K., Huang, X. W., Tian, B. Y., Wang, M., Niu, Q. H., & Zhang, K. Q. (2005a). Isolation and characterization of a serine protease from the nematophagous fungus, Lecanicillium psalliotae, displaying nematicidal activity. Biotechnology Letters, 27, 1123–1128.

    CAS  Google Scholar 

  • Yang, J. K., Huang, X. W., Tian, B. Y., Sun, H., Duan, J. X., Wu, W. P., & Zhang, K. Q. (2005b). Characterization of an extracellular serine protease gene from the nematophagous fungus Lecanicillium psalliotae. Biotechnology Letters, 27, 1329–1334.

    CAS  Google Scholar 

  • Yang, J. K., Tian, B. Y., Liang, L. M., & Zhang, K. Q. (2007a). Extracellular enzymes and the pathogenesis of nematophagous fungi. Applied Microbiology and Biotechnology, 75, 21–31.

    CAS  Google Scholar 

  • Yang, J. K., Li, J., Liang, L. M., Tian, B. Y., Zhang, Y., Chen, C. M., & Zhang, K. Q. (2007b). Cloning and characterization of an extracellular serine protease from the nematode-trapping fungus Arthrobotrys conoides. Archives of Microbiology, 188, 167–174.

    CAS  Google Scholar 

  • Yang, J. K., Liang, L. M., Zhang, Y., Li, J., Zhang, L., Ye, F. P., Gan, Z. W., & Zhang, K. Q. (2007c). Purification and cloning of a novel serine protease from the nematode-trapping fungus Dactylellina varietas and its potential roles in infection against nematodes. Applied Microbiology and Biotechnology, 75, 557–565.

    CAS  Google Scholar 

  • Yang, Y., Yang, E. C., An, Z. Q., & Liu, X. Z. (2007d). Evolution of nematode-trapping cells of predatory fungi of the Orbiliaceae based on evidence from rRNA-encoding DNA and multiprotein sequences. Proceedings of the National academy of Sciences of the United States of America, 104, 8379–8384.

    CAS  Google Scholar 

  • Yang, J. K., Ye, F. P., Mi, Q. L., Tang, S. Q., Li, J., & Zhang, K. Q. (2008). Purification and cloning of an extracellular serine protease from the nematode-trapping fungus Monacrosporium cystosporium. Journal of Microbiology and Biotechnology, 18, 852–858.

    PubMed  CAS  Google Scholar 

  • Yang, J. K., Gan, Z. W., Lou, Z. Y., Tao, N., Mi, Q. L., Liang, L. M., Sun, Y., Guo, Y., Huang, X. W., Zou, C. G., Rao, Z. H., Meng, Z. H., & Zhang, K. Q. (2010). Crystal structure and mutagenesis analysis of chitinase CrChi1 from the nematophagous fungus Clonostachys rosea in complex with the inhibitor caffeine. Microbiology, 156, 3566–3574.

    PubMed  CAS  Google Scholar 

  • Yang, J. K., Wang, L., Ji, X. L., Feng, Y., Li, X. M., Zou, C. G., Xu, J. P., Ren, Y., Mi, Q. L., Wu, J. L., Liu, S. Q., Liu, Y., Huang, X. W., Wang, H. Y., Niu, X. M., Li, J., Liang, L. M., Luo, Y. L., Ji, K. F., Zhou, W., Yu, Z. F., Li, G. H., Liu, Y. J., Li, L., Qiao, M., Feng, L., & Zhang, K. Q. (2011a). Genomic and proteomic analyses of the fungus Arthrobotrys oligospora provide insights into nematode-trap formation. PLoS Pathogens, 7, e1002179.

    CAS  Google Scholar 

  • Yang, J. K., Zhao, X. N., Liang, L. M., Xia, Z. Y., Lei, L. P., Niu, X. M., Zou, C. G., & Zhang, K. Q. (2011b). Overexpression of a cuticle-degrading protease Ver112 increases the nematicidal activity of Paecilomyces lilacinus. Applied Microbiology and Biotechnology, 89, 1895–1903.

    CAS  Google Scholar 

  • Yang, J. K., Liang, L. M., Li, J., & Zhang, K. Q. (2013). Nematicidal enzymes from microorganisms and their applications. Applied Microbiology and Biotechnology, 97, 7081–7095.

    PubMed  CAS  Google Scholar 

  • Ye, F. P., Liang, L. M., Mi, Q. L., Yang, J. K., Lou, Z. Y., Sun, Y. N., Guo, Y., Meng, Z. H., & Zhang, K. Q. (2009). Preliminary crystallographic study of two cuticle-degrading proteases from the nematophagous fungi Lecanicillium psalliotae and Paecilomyces lilacinus. Acta Crystallographica Section F: Structural Biology and Crystallization Communications, 65, 271–274.

    PubMed Central  CAS  Google Scholar 

  • Yousef, G. M., Kopolovic, A. D., Elliott, M. B., & Diamandis, E. P. (2003). Genomic overview of serine proteases. Biochemical and Biophysical Research Communications, 305, 28–36.

    PubMed  CAS  Google Scholar 

  • Zhang, Y. J., Liu, X. Z., & Wang, M. (2008). Cloning, expression, and characterization of two novel cuticle-degrading serine proteases from the entomopathogenic fungus Cordyceps sinensis. Research in Microbiology, 159, 462–469.

    PubMed  CAS  Google Scholar 

  • Zhao, M. L., Mo, M. H., & Zhang, K. Q. (2004). Characterization of a neutral serine protease and its full-length cDNA from the nematode-trapping fungus Arthrobotrys oligospora. Mycologia, 96, 16–22.

    CAS  Google Scholar 

  • Zou, C. G., Tu, H. H., Liu, X. Y., Tao, N., & Zhang, K. Q. (2010a). PacC in the nematophagous fungus Clonostachys rosea controls virulence to nematodes. Environmental Microbiology, 12, 1868–1877.

    CAS  Google Scholar 

  • Zou, C. G., Tao, N., Liu, W. J., Yang, J. K., Huang, X. W., Liu, X. Y., Tu, H. H., Gan, Z. W., & Zhang, K. Q. (2010b). Regulation of subtilisin-like protease prC expression by nematode cuticle in the nematophagous fungus Clonostachys rosea. Environmental Microbiology, 12, 3243–3252.

    CAS  Google Scholar 

  • Zou, C. G., Xu, Y. F., Liu, W. J., Zhou, W., Tao, N., Tu, H. H., Huang, X. W., Yang, J. K., & Zhang, K. Q. (2010c). Expression of a serine protease gene prC is up-regulated by oxidative stress in the fungus Clonostachys rosea: Implications for fungal survival. PLoS One, 5, e13386.

    Google Scholar 

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Yang, J., Liang, L., Zou, C., Zhang, KQ. (2014). Molecular Mechanism of Nematophagous Fungi Infection of Nematodes. In: Zhang, KQ., Hyde, K. (eds) Nematode-Trapping Fungi. Fungal Diversity Research Series, vol 23. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-8730-7_6

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