New Insights on the Mode of Action of Fungal Pathogens of Invertebrates for Improving Their Biocontrol Performance

  • Jose G. Maciá-Vicente
  • Javier Palma-Guerrero
  • Sonia Gómez-Vidal
  • Luis V. Lopez-Llorca
Part of the Progress in Biological Control book series (PIBC, volume 11)


The main fungal pathogens of invertebrates (FPI), nematophagous fungi and entomopathogenic fungi, have an important lifestyle overlapping. This is mainly due to the characteristics in common that their host share. Both groups of biocontrol agents share pathogenic determinants because the barriers of nematodes and insects are evolutionary conserved. Recently endophytism has been found a new aspect of the mode of action of FPI which has a potential relevance in biocontrol performance. The rationale is because they can modulate plant defences and because they act where their pest targets live and act. Natural vegetation is a reservoir root endophytes and subsequently a microbe group to screen for new biocontrol agents of plant-parasitic nematodes and root dwelling insect pests. We have found that FPI are compatible with chitosan natural compounds which may enhance their biocontrol potential.


Entomopathogenic Fungus Fungal Endophyte Nematophagous Fungus Root Endophyte Insect Cuticle 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We thank Prof. H.-B. Jansson for critical reading of the manuscript. This chapter was supported with funds of the research project AGL2008-00716/AGR from the Spanish Ministry of Science and Innovation.


  1. Agrios GH (1997) Plant pathology. Academic, LondonGoogle Scholar
  2. Ahman J, Johansson T, Olsson M et al (2002) Improving the pathogenicity of a nematode-trapping fungus by genetic engineering of a subtilisin with nematotoxic activity. Appl Environ Microbiol 68:3408–3415PubMedGoogle Scholar
  3. Ait Barka E, Eullaffroy P, Clement C et al (2004) Chitosan improves development, and protects Vitis vinifera L. against Botrytis cinerea. Plant Cell Rep 22:608–614PubMedGoogle Scholar
  4. Allen MF (1992) Mycorrhizal functioning: an integrative plant-fungal process. Chapman and Hall, New YorkGoogle Scholar
  5. Andersen SO (1979) Biochemistry of insect cuticle. Annu Rev Entomol 24:29–61Google Scholar
  6. Anke H, Sterner O (2002) Insecticidal and nematicidal metabolites from fungi. In: Osiewacz K, Esser K, Bennett JW (eds) The mycota. Springer, Berlin, pp 109–128Google Scholar
  7. Artjariyasripong S, Mitchell JI, Hywel-Jones NL et al (2001) Relationship of the genus Cordyceps and related genera, based on parsimony and spectral analysis of partial 18S and 28S ribosomal gene sequences. Mycoscience 42:503–517Google Scholar
  8. Azevedo JL, Maccheroni J, Pereira JO et al (2000) Endophytic microorganisms: a review on insect control and recent advances on tropical plants. Electron J Biotechnol 3:40–65Google Scholar
  9. Bacon CW, Hill NS (1996) Symptomless grass endophytes: products of coevolutionary symbioses and their role in ecological adaptations of grasses. In: Redlin SC, Carris LM (eds) Endophytic fungi in grasses and woody plants. Systematics, ecology, and evolution. APS Press, St Paul, pp 155–178Google Scholar
  10. Bacon CW, Porter JK, Norred WP et al (1996) Production of fusaric acid by Fusarium species. Appl Environ Microbiol 62:4039–4043PubMedGoogle Scholar
  11. Barron GL (1992) Ligninolytic and cellulolytic fungi as predators and parasites. In: Carroll GC, Wicklow TD (eds) The fungal community: its organisation and role in the ecosystems. Marcel-Dekker, New York, pp 311–326Google Scholar
  12. Bautista-Banos S, Hernandez-Lauzardo AN, Velazquez-del Valle MG et al (2006) Chitosan as a potential natural compound to control pre and postharvest diseases of horticultural commodities. Crop Prot 25:108–118Google Scholar
  13. Bell AA, Hubbard JC, Liu L et al (1998) Effects of chitin and chitosan on the incidence and severity of Fusarium yellows of celery. Plant Dis 82:322–328Google Scholar
  14. Benhamou N, Lafontaine PJ, Nicole M (1994) Induction of systemic resistance to Fusarium crown and root rot in tomato plants by seed treatment with chitosan. Phytopathology 84:1432–1444Google Scholar
  15. Bidochka MJ, St Leger RJ, Stuart A et al (1999) Nuclear rDNA phylogeny in the fungal genus Verticillium and its relationship to insect and plant virulence, extracellular proteases and carbohydrases. Microbiology 145:955–963PubMedGoogle Scholar
  16. Bills GF, Peláez F, Polishook JD et al (1994) Distribution of zaragozic acids (squalestatins) among filamentous ascomycetes. Mycol Res 98:733–739Google Scholar
  17. Bing LA, Lewis LC (1993) Occurrence of the entomopathogen Beauveria bassiana (Balsamo) Vuillemin in different tillage regimes and in Zea mays L. and virulence towards Ostrinia nubilalis (Hubner). Agric Ecosys Environ 45:147–156Google Scholar
  18. Bird AF (1985) The nature of the adhesion of Corynebacterium rathayi to the cuticle of the infective larva of Anguina agrostis. Int J Parasitol 15:301–308Google Scholar
  19. Bird AF, Bird J (1991) The structure of nematodes, 2nd edn. Academic, San DiegoGoogle Scholar
  20. Bonants PJM, Fitters PFL, Thijs H et al (1995) A basic serine protease from Paecilomyces lilacinus with biological activity against Meloidogyne hapla eggs. Microbiology 141:775–784PubMedGoogle Scholar
  21. Bordallo JJ, Lopez-Llorca LV, Jansson HB et al (2002) Colonization of plant roots by egg-parasitic and nematode-trapping fungi. New Phytol 154:491–499Google Scholar
  22. Bourne JM, Kerry BR, De Leij FAAM (1996) The importance of the host plant on the interaction between root-knot nematodes (Meloidogyne spp.) and the Nematophagous fungus, Verticillium chlamydosporium Goddard. Biocontrol Sci Technol 6:539–548Google Scholar
  23. Boyle C, Gotz M, Dammann-Tugend U et al (2001) Endophyte-host interactions III. Local vs. systemic colonization. Symbiosis 31:259–281Google Scholar
  24. Butt TM (2002) Use of entomogenous fungi for the control of insect pests. In: Esser K, Bennett JW (eds) The mycota. Springer, Berlin/Heidelberg, pp 112–134Google Scholar
  25. Calhoun LA, Findlay JA, Miller JD et al (1992) Metabolites toxic to spruce budworm from balsam fir needle endophytes. Mycol Res 96:281–286Google Scholar
  26. Capellano A, Dequatre B, Valla G et al (1987) Root-nodules formation by Penicillium sp. on Alnus glutinosa and Alnus incana. Plant Soil 104:45–51Google Scholar
  27. Carroll G (1988) Fungal endophytes in stems and leaves - from latent pathogen to mutualistic symbiont. Ecology 69:2–9Google Scholar
  28. Carroll G (1995) Forest endophytes: pattern and process. Can J Bot 73:S1316–S1324Google Scholar
  29. Carvajal JA, Rodriguez-Kabana R (1998) Alginate films for assessment of parasitism of Meloidogyne incognita eggs in soils treated with organic amendments. Nematropica 28:41–48Google Scholar
  30. Charnley AK (1997) Entomopathogenic fungi and their role in pest control. In: Esser K, Lemke PA (eds) The mycota. Springer, Berlin/Heidelberg/New York, pp 185–201Google Scholar
  31. Cohen-Kupiec R, Chet I (1998) The molecular biology of chitin digestion. Curr Opin Biotechnol 9:270–279PubMedGoogle Scholar
  32. de Bary A (1866) Morphologie und physiologie der pilze, flechten und myxomyceten. Engelmann, LeipzigGoogle Scholar
  33. Deising H, Rauscher M, Haug M et al (1995) Differentiation and cell wall degrading enzymes in the obligately biotrophic rust fungus Uromyces viciae-fabae. Can J Bot 73:624–631Google Scholar
  34. Dimock M, Turner J, Lampel J (1993) Endophytic microorganisms for delivery of genetically engineered microbial pesticides in plants. In: Kim L (ed) Advanced engineered pesticides. Marcel Dekker, New York/Basel/Hong Kong, pp 85–94Google Scholar
  35. Dodane V, Vilivalam VD (1998) Pharmaceutical applications of chitosan. Pharm Sci Technol Today 1:246–253Google Scholar
  36. Domsch KH, Gams W, Anderson TH (1980) Compendium of soil fungi. Academic, LondonGoogle Scholar
  37. Dong LQ, Yang JK, Zhang KQ (2007) Cloning and phylogenetic analysis of the chitinase gene from the facultative pathogen Paecilomyces lilacinus. J Appl Microbiol 103:2476–2488PubMedGoogle Scholar
  38. Dreyfuss MM, Chapela IH (1994) Potential of fungi in the discovery of novel, low-molecular weight pharmaceuticals. In: Gullo VP (ed) The discovery of natural products with therapeutic potential. Butterworth-Heinemann, Stoneham, pp 49–80Google Scholar
  39. Ernst M, Mendgen KW, Wirsel SGR (2003) Endophytic fungal mutualists: seed-borne Stagonospora spp. enhance reed biomass production in axenic microcosms. Mol Plant Microbe Interact 16:580–587PubMedGoogle Scholar
  40. Fan Y, Fang W, Guo S et al (2007) Increased insect virulence in Beauveria bassiana strains overexpressing an engineered chitinase. Appl Environ Microbiol 73:295–302PubMedGoogle Scholar
  41. Fang W, Leng B, Xiao Y et al (2005) Cloning of Beauveria bassiana chitinase gene Bbchit1 and its application to improve fungal strain virulence. Appl Environ Microbiol 71:363–370PubMedGoogle Scholar
  42. Gams W, Zare R (2001) A revision of verticillium sect. Prostrata. III. Generic classification. Nova Hedwig 72:329–337Google Scholar
  43. Gan Z, Yang J, Tao N et al (2007) Cloning of the gene Lecanicillium psalliotae chitinase Lpchi1 and identification of its potential role in the biocontrol of root-knot nematode Meloidogyne incognita. Appl Microbiol Biotechnol 76:1309–1317PubMedGoogle Scholar
  44. Gaspard JT, Mankau R (1986) Nematophagous fungi associated with Tylenchulus semipenetrans and the citrus rhizosphere. Nematologica 32:359–363Google Scholar
  45. Gloer JB (1997) Application of fungal ecology in the search for new bioactive natural products. In: Esser K, Lemke PA (eds) The mycota. Springer, Berlin/Heidelberg/New York, pp 257–283Google Scholar
  46. Gómez-Vidal S, Lopez-Llorca LV, Jansson HB et al (2006) Endophytic colonization of date palm (Phoenix dactylifera L.) leaves by entomopathogenic fungi. Micron 37:624–632PubMedGoogle Scholar
  47. Gómez-Vidal S, Salinas J, Tena M et al (2009) Proteomic analysis of date palm (Phoenix dactylifera L.) responses to endophytic colonization by entomopathogenic fungi. Electrophoresis 30:2996–3005PubMedGoogle Scholar
  48. Hajek AE, St Leger RJ (1994) Interactions between fungal pathogens and insect hosts. Annu Rev Entomol 39:293–322Google Scholar
  49. Hallmann J, Rodríguez-Kábana R, Kloepper JW (1999) Chitin-mediated changes in bacterial communities of the soil, rhizosphere and within roots of cotton in relation to nematode control. Soil Biol Biochem 31:551–560Google Scholar
  50. Jansson HB (1993) Adhesion to nematodes of conidia from the nematophagous fungus Drechmeria coniospora. J Gen Microbiol 139:1899–1906Google Scholar
  51. Jumpponen A (2001) Dark septate endophytes – are they mycorrhizal? Mycorrhiza 11:207–211Google Scholar
  52. Jumpponen A, Trappe JM (1998) Dark septate endophytes: a review of facultative biotrophic root-colonizing fungi. New Phytol 140:295–310Google Scholar
  53. Kerry BR (2000) Rhizosphere interactions and the exploitation of microbial agents for the biological control of plant-parasitic nematodes. Annu Rev Phytopathol 38:423–441PubMedGoogle Scholar
  54. Kimmons CA, Gwinn KD, Bernard EC (1990) Nematode reproduction on endophyte-infected and endophyte-free tall fescue. Plant Dis 74:757–761Google Scholar
  55. Knudsen IMB, Hockenhull J, Jensen DF et al (1997) Selection of biological control agents for controlling soil and seed-borne diseases in the field. Eur J Plant Pathol 103:775–784Google Scholar
  56. Kuldau GA, Yates IE (2000) Evidence for Fusarium endophytes in cultivated and wild plants. In: Bacon W, White JF (eds) Microbial endophytes. Marcel Dekker, New York/Basel, pp 85–120Google Scholar
  57. Kumar MNVR (2000) A review of chitin and chitosan applications. React Funct Polym 46:1–27Google Scholar
  58. Laflamme P, Benhamou N, Bussieres G et al (1999) Differential effect of chitosan on root rot fungal pathogens in forest nurseries. Can J Bot 77:1460–1468Google Scholar
  59. Lafontaine PJ, Benhamou N (1996) Chitosan treatment: an emerging strategy for enhancing resistance of greenhouse tomato plants to infection by Fusarium oxysporum f.sp. radicis-lycopersici. Biocontrol Sci Technol 6:111–124Google Scholar
  60. Latch GCM (1993) Physiological interactions of endophytic fungi and their hosts. Biotic stress tolerance imparted to grasses by endophytes. Agric Ecosyst Environ 44:143–156Google Scholar
  61. Lee KY, Shibutani M, Takagi H et al (2004) Subchronic toxicity study of dietary N-acetylglucosamine in F344 rats. Food Chem Toxicol 42:687–695PubMedGoogle Scholar
  62. Leinhos GME, Buchenauer H (1992) Hyperparasitism of selected fungi on rust fungi of cereal. Z Pflanzenkrankh Pflanzenschutz 99:482–498Google Scholar
  63. Lewis LC, Bing LA (1991) Bacillus thuringiensis Berliner and Beauveria bassiana (Balsamo) vuillimen for European corn borer control: program for immediate and season-long suppression. Can Entomol 123:387–393Google Scholar
  64. Lewis LC, Cossentine JE (1986) Season long intraplant epizootics of entomopathogens, Beauveria bassiana and Nosema pyrausta, in a corn agroecosystem. Entomophaga 31:363–369Google Scholar
  65. Li J, Yang J, Huang X et al (2006) Purification and characterization of an extracellular serine protease from Clonostachys rosea and its potential as a pathogenic factor. Process Biochem 41:925–929Google Scholar
  66. Lingham RB, Silverman KC, Bills GF et al (1993) Chaetomella acutiseta produces chaetomellic acids A and B which are reversible inhibitors of farnesyl-protein transferase. Appl Microbiol Biotechnol 40:370–374PubMedGoogle Scholar
  67. Liu CH, Zou WX, Lu H et al (2001a) Antifungal activity of Artemisia annua endophyte cultures against phytopathogenic fungi. J Biotechnol 88:277–282PubMedGoogle Scholar
  68. Liu XF, Guan YL, Yang DZ et al (2001b) Antibacterial action of chitosan and carboxymethylated chitosan. J Appl Polym Sci 79:1324–1335Google Scholar
  69. Liu H, Du YM, Wang XH et al (2004) Chitosan kills bacteria through cell membrane damage. Int J Food Microbiol 95:147–155PubMedGoogle Scholar
  70. Liu SQ, Meng ZH, Yang JK et al (2007) Characterizing structural features of cuticle-degrading proteases from fungi by molecular modeling. BMC Struct Biol 7:33PubMedGoogle Scholar
  71. Lopez-Llorca LV (1990) Purification and properties of extracellular proteases produced by the nematophagous fungus Verticillium suchlasporium. Can J Microbiol 36:530–537Google Scholar
  72. Lopez-Llorca LV, Fry SC (1989) Dityrosine, trityrosine and tetratyrosine, potential cross-links in proteins of plant-parasitic nematodes. Nematologica 35:165–179Google Scholar
  73. Lopez-Llorca LV, Jansson HB (2006) Fungal parasites of invertebrates: multimodal biocontrol agents. In: Robson GD, van West P, Gadd GM (eds) Exploitation of fungi. Cambridge University Press, Cambridge, pp 310–335Google Scholar
  74. Lopez-Llorca LV, Robertson WM (1992) Immunocytochemical localization of a 32-kDa protease from the nematophagous fungus Verticillium suchlasporium in infected nematode eggs. Exp Mycol 16:261–267Google Scholar
  75. Lopez-Llorca LV, Bordallo JJ, Salinas J et al (2002) Use of light and scanning electron microscopy to examine colonisation of barley rhizosphere by the nematophagous fungus Verticillium chlamydosporium. Micron 33:61–67PubMedGoogle Scholar
  76. Lopez-Llorca LV, Jansson HB, Maciá-Vicente JG et al (2006) Nematophagous fungi as root endophytes. In: Schulz B, Boyle C, Sieber TN (eds) Microbial root endophytes. Springer, Heidelberg, pp 191–206Google Scholar
  77. Lopez-Llorca LV, Maciá-Vicente JG, Jansson HB (2008) Mode of action and interactions of nematophagous fungi. In: Ciancio A, Mukerji KG (eds) Integrated management and biocontrol of vegetable and grain crops nematodes. Springer, Dordrecht, pp 51–76Google Scholar
  78. Maciá-Vicente JG, Jansson HB, Abdullah SK et al (2008a) Fungal root endophytes from natural vegetation in Mediterranean environments with special reference to Fusarium spp. FEMS Microbiol Ecol 64:90–105PubMedGoogle Scholar
  79. Maciá-Vicente JG, Jansson HB, Mendgen K et al (2008b) Colonization of barley roots by endophytic fungi and their reduction of take-all caused by Gaeumannomyces graminis var. tritici. Can J Microbiol 54:600–609PubMedGoogle Scholar
  80. Maciá-Vicente JG, Jansson HB, Talbot NJ et al (2009a) Real time-PCR quantification and live cell imaging of endophytic colonisation of barley (Hordeum vulgare) roots by Fusarium equiseti and Pochonia chlamydosporia. New Phytol 182:213–228PubMedGoogle Scholar
  81. Maciá-Vicente JG, Rosso LC, Ciancio A et al (2009b) Colonisation of barley roots by endophytic Fusarium equiseti and Pochonia chlamydosporia: effects on plant growth and disease. Ann Appl Biol 155:391–401Google Scholar
  82. Monfort E, Lopez-Llorca LV, Jansson HB et al (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 Biol Biochem 37:1229–1235Google Scholar
  83. Morton CO, Hirsch PR, Peberdy JP et al (2003) Cloning of and genetic variation in protease VCP1 from the nematophagous fungus Pochonia chlamydosporia. Mycol Res 107:38–46PubMedGoogle Scholar
  84. Nitao JK, Meyer SLF, Schmidt WF et al (2001) Nematode-antagonistic trichothecenes from Fusarium equiseti. J Chem Ecol 27:859–869PubMedGoogle Scholar
  85. Noble HM, Langley D, Sidebottom PJ et al (1991) An echinocandin from an endophytic Cryptosporiopsis sp. and Pezicula sp. in Pinus sylvestris and Fagus sylvatica. Mycol Res 95:1439–1440Google Scholar
  86. Nogawa M, Takahashi H, Kashiwagi A et al (1998) Purification and characterization of exo-beta-d-glucosaminidase from a cellulolytic fungus, Trichoderma reesei PC-3-7. Appl Environ Microbiol 64:890–895PubMedGoogle Scholar
  87. Obledo EN, Barragan-Barragan LB, Gutierrez-Gonzalez P et al (2003) Increased photosyntethic efficiency generated by fungal symbiosis in Agave victoria-reginae. Plant Cell Tissue Organ Cult 74:237–241Google Scholar
  88. Olivares-Bernabeu CM, Lopez-Llorca LV (2002) Fungal egg-parasites of plant-parasitic nematodes from Spanish soils. Rev Iberoam Micol 19:104–110Google Scholar
  89. Palma-Guerrero J, Jansson HB, Salinas J et al (2008) Effect of chitosan on hyphal growth and spore germination of plant pathogenic and biocontrol fungi. J Appl Microbiol 104:541–553PubMedGoogle Scholar
  90. Palma-Guerrero J, Lopez-Jimenez JA, Pérez-Berná AJ et al (2010) Membrane fluidity determines sensitivity of filamentous fungi to chitosan. Mol Microbiol 75:1021–1032PubMedGoogle Scholar
  91. Park RD, Jo KJ, Jo YY et al (2002) Variation of antifungal activities of chitosans on plant pathogens. J Microbiol Biotechnol 12:84–88Google Scholar
  92. Pascencia-Jatomea M, Viniegra G, Olayo R et al (2003) Effect of chitosan and temperature on spore germination of Aspergillus niger. Macromol Biosci 3:582–586Google Scholar
  93. Peláez F, Collado J, Arenal F et al (1998) Endophytic fungi from plants living on gypsum soils as a source of secondary metabolites with antimicrobial activity. Mycol Res 102:755–761Google Scholar
  94. Persmark L, Jansson HB (1997) Nematophagous fungi in the rhizosphere of agricultural crops. FEMS Microbiol Ecol 22:303–312Google Scholar
  95. Persmark L, Nordbring-Hertz B (1997) Conidial trap formation of nematode-trapping fungi in soil and soil extracts. FEMS Microbiol Ecol 22:313–323Google Scholar
  96. Persson C, Jansson HB (1999) Rhizosphere colonization and control of Meloidogyne spp. by nematode-trapping fungi. J Nematol 31:164–171PubMedGoogle Scholar
  97. Peterson EA, Katznelson H (1964) Occurrence of nematode-trapping fungi in the rhizosphere. Nature 204:1111–1112Google Scholar
  98. Petrini O (1991) Fungal endophytes of tree leaves. In: Andrews JH, Hirano S (eds) Microbial ecology of leaves. Springer, New York, pp 179–197Google Scholar
  99. Rabea EI, Badawy ME, Stevens CV et al (2003) Chitosan as antimicrobial agent: applications and mode of action. Biomacromolecules 4:1457–1465PubMedGoogle Scholar
  100. Read DJ (1999) Mycorrhiza – the state of the art. In: Varma A, Hock B (eds) Mycorrhiza. Springer, Berlin, pp 3–34Google Scholar
  101. Read JC, Camp BJ (1986) The effect of the fungal endophyte Acremonium coenophialum in tall fescue on animal performance, toxicity, and stand maintenance. Agron J 80:811–814Google Scholar
  102. Redman RS, Ranson JC, Rodriguez RJ (1999) Conversion of the pathogenic fungus Colletotrichum magna to a nonpathogenic, endophytic mutualist by gene disruption. Mol Plant Microbe Int 12:969–975Google Scholar
  103. Redman RS, Dunigan DD, Rodriguez RJ (2001) Fungal symbiosis from mutualism to parasitism: who controls the outcome, host or invader? New Phytol 151:705–716Google Scholar
  104. Redman RS, Sheehan KB, Stout RG et al (2002) Thermotolerance generated by plant/fungal symbiosis. Science 298:1581PubMedGoogle Scholar
  105. Riekert HF, Tiedt LR (1994) Scanning electron microscopy of Meloidogyne incognita juveniles entrapped in maize roots by a nematode-trapping fungus Arthrobotrys dactyloides. S Afr J Zool 29:189–190Google Scholar
  106. Rodriguez R, Redman R (2008) More than 400 million years of evolution and some plants still can’t make it on their own: plant stress tolerance via fungal symbiosis. J Exp Bot 59:1109–1114PubMedGoogle Scholar
  107. Rodriguez-Kabana R, Morgan-Jones G, Chet I (1987) Biological control of nematodes: soil amendments and microbial antagonists. Plant Soil 100:237–247Google Scholar
  108. Schulz B, Boyle C (2005) The endophytic continuum. Mycol Res 109:661–686PubMedGoogle Scholar
  109. Schulz B, Boyle C (2006) What are endophytes? In: Schulz B, Boyle C, Sieber TN (eds) Microbial root endophytes. Springer, Heidelberg, pp 1–14Google Scholar
  110. Schulz B, Sucker J, Aust HJ et al (1995) Biologically active secondary metabolites of endophytic Pezicula species. Mycol Res 99:1007–1015Google Scholar
  111. Schulz B, Guske S, Dammann U et al (1998) Endophyte-host interactions. II. Defining symbiosis of the endophyte-host interaction. Symbiosis 25:213–227Google Scholar
  112. Schulz B, Rommert AK, Dammann U et al (1999) The endophyte-host interaction: a balanced antagonism? Mycol Res 103:1275–1283Google Scholar
  113. Schulz B, Boyle C, Draeger S et al (2002) Endophytic fungi: a source of novel biologically active secondary metabolites. Mycol Res 106:996–1004Google Scholar
  114. Segers R, Butt TM, Kerry BR et al (1994) The Nematophagous fungus Verticillium chlamydosporium produces a chymoelastase-like protease which hydrolyzes host nematode proteins in situ. Microbiology 140:2715–2723PubMedGoogle Scholar
  115. Shimosaka M, Nogawa M, Ohno Y et al (1993) Chitosanase from the plant-pathogenic fungus, Fusarium solani f.sp. phaseoli - purification and some properties. Biosci Biotechnol Biochem 57:231–235Google Scholar
  116. Siddiqui ZA, Akhtar MS (2008) Synergistic effects of antagonistic fungi and a plant growth promoting rhizobacterium, an arbuscular mycorrhizal fungus, or composted cow manure on populations of Meloidogyne incognita and growth of tomato. Biocontrol Sci Technol 18:279–290Google Scholar
  117. Sieber TN (2002) Fungal root endophytes. In: Waisel Y, Eshel A, Kafkafy U (eds) Plant roots: the hidden half. Marcel-Dekker, Basel/New York, pp 887–917Google Scholar
  118. Sikora RA, Pocasangre L, zum Felde A et al (2008) Mutualistic endophytic fungi and in-planta suppressiveness to plant-parasitic nematodes. Biol Control 46:15–23Google Scholar
  119. Spiegel Y, Cohn E, Chet I (1986) Use of chitin for controlling plant-parasitic nematodes - I. Direct effects on nematode reproduction and plant performance. Plant Soil 95:87–95Google Scholar
  120. Spiegel Y, Chet I, Cohn E (1987) Use of chitin for controlling plant plant-parasitic nematodes - II. Mode of action. Plant Soil 98:337–345Google Scholar
  121. Spiegel Y, Chet I, Cohn E et al (1988) Use of chitin for controlling plant-parasitic nematodes - III. Influence of temperature on nematicidal effect, mineralization and microbial population buildup. Plant Soil 109:251–256Google Scholar
  122. St Leger RJ, Staples RC, Roberts DW (1993) Entomopathogenic isolates of Metarhizium anisopliae, Beauveria bassiana, and Aspergillus flavus produce multiple extracellular chitinase isozymes. J Invert Pathol 61:81–84Google Scholar
  123. St Leger RJ, Joshi L, Bidochka MJ et al (1996a) Characterization and ultrastructural localization of chitinases from Metarhizium anisopliae, M. flavoviride, and Beauveria bassiana during fungal invasion of host (Manduca sexta) cuticle. Appl Environ Microbiol 62:907–912Google Scholar
  124. St Leger RJ, Joshi L, Bidochka MJ et al (1996b) Biochemical characterization and ultrastructural localization of two extracellular trypsins produced by Metarhizium anisopliae in infected insect cuticles. Appl Environ Microbiol 62:1257–1264PubMedGoogle Scholar
  125. Stirling GR (1991) Biological control of plant-parasitic nematodes. Progress, problems and prospects. CAB International, WallingfordGoogle Scholar
  126. Stone J, Viret O, Petrini O et al (1994) Histological studies of host penetration and colonization by endophytic fungi. In: Petrini O, Oullette GB (eds) Host wall alterations by parasitic fungi. Phytopathological Society Press, St Paul, pp 115–128Google Scholar
  127. Summerell BA, Leslie JF (2004) Genetic diversity and population structure of plant-pathogenic species in the genus Fusarium. In: Gillins M, Holmes A (eds) Plant microbiology. Bios, Oxford, pp 207–223Google Scholar
  128. Tikhonov VE, Lopez-Llorca LV, Salinas J et al (2002) Purification and characterization of chitinases from the nematophagous fungi Verticillium chlamydosporium and V. suchlasporium. Fungal Genet Biol 35:67–78PubMedGoogle Scholar
  129. Tikhonov VE, Stepnova EA, Babak VG et al (2006) Bactericidal and antifungal activities of a low molecular weight chitosan and its N-/2(3)-(dodec-2-enyl)succinoyl/-derivatives. Carbohydr Polym 64:66–72Google Scholar
  130. Trillas I, Aviles M, Ordovas J et al (2002) Using compost as a methyl bromide alternative. BioCycle 43:64Google Scholar
  131. Trillas MI, Casanova E, Cotxarrera L et al (2006) Composts from agricultural waste and the Trichoderma asperellum strain T-34 suppress Rhizoctonia solani in cucumber seedlings. Biol Control 39:32–38Google Scholar
  132. Trotel-Aziz P, Couderchet M, Vernet G et al (2006) Chitosan stimulates defense reactions in grapevine leaves and inhibits development of Botrytis cinerea. Eur J Plant Pathol 114(4):405–413Google Scholar
  133. Tsai GJ, Su WH, Chen HC et al (2002) Antimicrobial activity of shrimp chitin and chitosan from different treatments and applications of fish preservation. Fish Sci 68:170–177Google Scholar
  134. Tunlid A, Rosen S, Ek B et al (1994) Purification and characterization of an extracellular serine protease from the nematode-trapping fungus Arthrobotrys oligospora. Microbiology 140:1687–1695PubMedGoogle Scholar
  135. Varma A, Verma S, Sudha et al (1999) Piriformospora indica, a cultivable plant-growth-promoting root endophyte. Appl Environ Microbiol 65:2741–2744PubMedGoogle Scholar
  136. Varma A, Singh A, Sahay NS et al (2000) Piriformospora indica: an axenically culturable mycorrhiza-like endosymbiotic fungus. In: Hock B (ed) Mycota. Springer, Heidelberg/New York, pp 101–106Google Scholar
  137. Vega FE (2008) Insect pathology and fungal endophytes. J Invert Pathol 98:277–279Google Scholar
  138. Vega FE, Posada F, Catherine Aime M et al (2008) Entomopathogenic fungal endophytes. Biol Control 46:72–82Google Scholar
  139. Vilich V, Dolfen M, Sikora RA (1998) Chaetomium spp. colonization of barley following seed treatment and its effect on plant growth and Erysiphe graminis f. sp. hordei disease severity. Z Pflanzenkrankh Pflanzenschutz 105:130–139Google Scholar
  140. Wang M, Yang J, Zhang KQ (2006a) Characterization of an extracellular protease and its cDNA from the nematode-trapping fungus Monacrosporium microscaphoides. Can J Microbiol 52:130–139PubMedGoogle Scholar
  141. Wang RB, Yang JK, Lin C et al (2006b) Purification and characterization of an extracellular serine protease from the nematode-trapping fungus Dactylella shizishanna. Lett Appl Microbiol 42:589–594PubMedGoogle Scholar
  142. West CP, Izekor E, Oosterhuis DM et al (1988) The effect of Acremonium coenophialum on the growth and nematode infestation of tall fescue. Plant Soil 112:3–6Google Scholar
  143. Wharton D (1980) Nematode egg-shells. Parasitology 81:447–463PubMedGoogle Scholar
  144. Wilson D (1995) Endophyte - the evolution of a term, and clarification of its use and definition. Oikos 73:274–276Google Scholar
  145. Yang J, Huang X, Tian B et al (2005) Characterization of an extracellular serine protease gene from the nematophagous fungus Lecanicillium psalliotae. Biotechnol Lett 27:1329–1334PubMedGoogle Scholar
  146. Yang J, Tian B, Liang L et al (2007) Extracellular enzymes and the pathogenesis of nematophagous fungi. Appl Microbiol Biotechnol 75:21–31PubMedGoogle Scholar
  147. Zhang Y, Liu X, Wang M (2008a) Cloning, expression, and characterization of two novel cuticle-degrading serine proteases from the entomopathogenic fungus Cordyceps sinensis. Res Microbiol 159:462–469PubMedGoogle Scholar
  148. Zhang YJ, Feng MG, Fan YH et al (2008b) A cuticle-degrading protease (CDEP-1) of Beauveria bassiana enhances virulence. Biocontrol Sci Technol 18:551–563Google Scholar
  149. Zhao ML, Mo MH, Zhang KQ (2004) Characterization of a neutral serine protease and its full-length cDNA from the nematode-trapping fungus Arthrobotrys oligospora. Mycologia 96:16–22Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Jose G. Maciá-Vicente
    • 1
  • Javier Palma-Guerrero
    • 1
  • Sonia Gómez-Vidal
    • 1
  • Luis V. Lopez-Llorca
    • 1
  1. 1.Laboratory of Plant Pathology, Department of Marine Sciences and Applied Biology, Multidisciplinary Institute for Environmental Studies (MIES) Ramón MargalefUniversity of AlicanteAlicanteSpain

Personalised recommendations