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Endophytic Fungal Entomopathogens with Activity Against Plant Pathogens: Ecology and Evolution

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Endophytic Fungal Entomopathogens with Activity Against Plant Pathogens: Ecology and Evolution BioControl (2010) 55:113–128 DOI 10.1007/s10526-009-9241-x Endophytic fungal entomopathogens with activity against plant pathogens: ecology and evolution Bonnie H. Ownley • Kimberly D. Gwinn • Fernando E. Vega Received: 17 September 2009 / Accepted: 12 October 2009 / Published online: 28 October 2009 Ó International Organization for Biological Control (IOBC) 2009 Abstract Dual biological control, of both insect resistance when endophytically colonized cotton seed- pests and plant pathogens, has been reported for the lings were challenged with a bacterial plant pathogen fungal entomopathogens, Beauveria bassiana (Bals.- on foliage. Species of Lecanicillium are known to Criv.) Vuill. (Ascomycota: Hypocreales) and Lecan- reduce disease caused by powdery mildew as well as icillium spp. (Ascomycota: Hypocreales). However, various rust fungi. Endophytic colonization has been the primary mechanisms of plant disease suppression reported for Lecanicillium spp., and it has been are different for these fungi. Beauveria spp. produce an suggested that induced systemic resistance may be array of bioactive metabolites, and have been reported active against powdery mildew. However, mycopara- to limit growth of fungal plant pathogens in vitro. In sitism is the primary mechanism employed by Lecan- plant assays, B. bassiana has been reported to reduce icillium spp. against plant pathogens. Comparisons of diseases caused by soilborne plant pathogens, such as Beauveria and Lecanicillium are made with Tricho- Pythium, Rhizoctonia, and Fusarium. Evidence has derma, a fungus used for biological control of plant accumulated that B. bassiana can endophytically pathogens and insects. For T. harzianum Rifai (Asco- colonize a wide array of plant species, both monocots mycota: Hypocreales), it has been shown that some and dicots. B. bassiana also induced systemic fungal traits that are important for insect pathogenicity are also involved in biocontrol of phytopathogens. Handling Editor: Helen Roy. Keywords Beauveria bassiana Á Fungal endophyte Á Hypocreales Á Induced systemic B. H. Ownley (&) Á K. D. Gwinn Department of Entomology and Plant Pathology, resistance Á Lecanicillium Á Mycoparasite Á The University of Tennessee, 2431 Joe Johnson Drive, Trichoderma 205 Ellington Plant Sciences Bldg, Knoxville, TN 37996-4560, USA e-mail: [email protected] Introduction K. D. Gwinn e-mail: [email protected] Resource availability can trigger shifts in functional- F. E. Vega ity within a fungal species, thereby changing the Sustainable Perennial Crops Laboratory, ecological role of the organism (Termorshuizen and United States Department of Agriculture, Jeger 2009). Shifts from one resource to another may Agricultural Research Service, Building 001, BARC-West, Beltsville, MD 20705, USA necessitate significant adaptations in metabolism, e-mail: [email protected] particularly if the resources are dissimilar (Leger 123 114 B. H. Ownley et al. et al. 1997). Among members of the Hypocreales, released by a fungal entomopathogen, carbon source animal, fungal, and plant resources are exploited. played a major role in VOC production by B. These fungi gain nutrition in a variety of ways, bassiana. When cultured on glucose-based media, including: saprotrophs that colonize the rhizosphere the VOCs identified were diisopropyl naphthalenes and phyllosphere, endophytic saprotrophs, hemibio- (\50%), ethanol (ca. 10%) and sesquiterpenes (6%), trophs and necrotrophs of plants, entomopathogens, but in media with n-octacosane (an insect-like and mycoparasites. Some of these fungi function in alkane), the primary VOCs were n-decane (84%) more than one econutritional mode. Fungi tradition- and sesquiterpenes (15%) (Crespo et al. 2008). ally known for their entomopathogenic characteris- Enzymes involved in antibiosis are distinctly tics, such as Beauveria bassiana (Bals.-Criv.) Vuill. different from those involved in mycoparasitism of (Ascomycota: Hypocreales) and Lecanicillium spp. plant pathogens. For example, the biocontrol fungus (Ascomycota: Hypocreales), have recently been Talaromyces flavus Tf1 (Klo¨cker) Stolk & Samson shown to engage in plant-fungus interactions (Vega (Ascomycota: Eurotiales) produces the enzyme glu- 2008; Vega et al. 2008), and both have been reported cose oxidase, whose reaction product, hydrogen to effectively suppress plant disease (Goettel et al. peroxide, kills microsclerotia of phytopathogenic 2008; Ownley et al. 2008). Verticillium (Fravel 1988). Fungal biocontrol organisms actively compete against plant pathogens for niche or infection site, Mechanisms of plant disease suppression carbon, nitrogen, and various microelements. The site by biocontrol fungi of competition is often the rhizosphere, phyllosphere, or intercellularly within the plant. Successful com- Biological control of plant pathogens usually refers to petition is often a matter of timing as resources are the use of microorganisms that reduce the disease- likely to go to the initial colonizer. causing activity or survival of plant pathogens. Mycoparasitism is the parasitism of one fungus by Several different biological control mechanisms another. Varying degrees of host specificity are against plant pathogens have been identified. With displayed by mycoparasites. Within a given species some mechanisms, such as antibiosis, competition, of mycoparasite, some isolates may infect a large and parasitism, the biocontrol organism is directly number of taxonomically diverse fungi, while others involved. With other modes of biological control, demonstrate a high level of specificity (Askary et al. such as induced systemic resistance and increased 1998). As reviewed in Harmon et al. (2004), parasit- growth response, endophytic colonization by the ism by the biocontrol fungus Trichoderma (Ascomy- biocontrol organism triggers responses in the plant cota: Hypocreales) begins with detection of the that reduce or alleviate plant disease. fungal host before contact is made. Trichoderma produces low levels of an extracellular exochitinase, which diffuse and catalyze the release of cell-wall Antibiosis, competition, and mycoparasitism oligomers from the target host fungus. This activity induces Trichoderma to release fungitoxic endoch- The mechanism of antibiosis includes production of itinases, which also degrade the fungal host cell wall. antibiotics, bioactive volatile organic compounds Attachment of the mycoparasite to the host fungus is (VOCs), and enzymes. Volatile bioactive compounds mediated by binding of carbohydrates in the Trich- include acids, alcohols, alkyl pyrones, ammonia, oderma cell wall to lectins in the cell wall of the esters, hydrogen cyanide, ketones, and lipids (Ownley fungal host. Upon contact, hyphae of Trichoderma and Windham 2007). The fungal endophyte Muscodor coil around the host fungus and form appressoria. albus Worapong, Strobel & W.M. Hess (Ascomycota: Several lytic enzymes are involved in degradation of Xylariales) produces a mixture of VOCs that are lethal the cell walls of fungal and oomycetous plant to a variety of microorganisms (Strobel et al. 2001; pathogens, including chitinases, ß-1,3 gluconases, Mercier and Jime´nez 2004; Mercier and Smilanick proteases, and lipases. 2005; Strobel 2006), as well as to insects (Riga et al. In many cases, mechanisms of biocontrol are not 2008; Lacey et al. 2009). In the first report of VOCs mutually exclusive, i.e. multiple mechanisms may be 123 Endophytic fungal entomopathogens 115 operating against a specific plant pathogen, or a given 2009). Induction of systemic resistance via the JA/ biocontrol fungus may employ different mechanisms ethylene signaling pathway has been reported pri- against different phytopathogens. For example, con- marily for plant growth-promoting bacteria, however, trol of Botrytis cinerea Pers. (Ascomycota: Heloti- it is also operative for many mycorrhizal fungi ales) on grapes (Vitis) with Trichoderma involves (Gutjahr and Paszkowski 2009) and biocontrol fungi competition for nutrients and mycoparasitism of (Harmon et al. 2004; Vinale et al. 2008). sclerotia, the overwintering, long-term survival struc- ture of Botrytis. Both mechanisms contribute to suppression of the pathogen’s capability to cause Endophytism by fungal entomopathogens and perpetuate disease (Dubos 1987). Following application to leaves as a preventative, Trichoderma Even though the term ‘‘endophyte’’ has several induced resistance to downy mildew, Plasmopara definitions (Hyde and Soytong 2008), it is widely viticola (Berk. & M.A. Curtis) Berl. & De Toni accepted that endophytes are microorganisms present (Oomycota: Peronosporales), in grape (Perazzolli in plant tissues without causing any apparent symp- et al. 2008). Therefore, it is possible that induced toms. Fungal endophytes are widespread and quite systemic resistance may also play a role in biocontrol diverse in nature (Arnold et al. 2000; Arnold 2007). of Botrytis. Induced resistance to Botrytis, following For example, Vega et al. (2009b) reported 257 unique application of T. harzianum T39 Rifai (Ascomycota: ITS genotypes for fungal endophytes isolated from Hypocreales) to roots and leaves of several ecotypes coffee plants in Hawaii, Mexico, Colombia, and of Arabidopsis thaliana (L.) Heynh. has been Puerto Rico. Infection by fungal endophytes can be reported (Korolev et al. 2008). localized (i.e., not systemic; see Saikkonen et al. 1998 and references therein), and establishing a long- term systemic infection with endophytic fungal Induced systemic resistance entomopathogens that can
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