Research Article

Entomopathogenic Fungi as Microbial Biocontrol Agent  

Sehroon Khan , Lihua Guo , Yushanjiang Maimaiti , Mahmut Mijit , Dewen Qiu
Key Laboratory of Integrated Pest Management in Crops, Ministry of Agriculture, Institute of Plant Protection, Chinese Academy of Agricultural Sciences (CAAS), Beijing, P.R. China
Author    Correspondence author
Molecular Plant Breeding, 2012, Vol. 3, No. 7   doi: 10.5376/mpb.2012.03.0007
Received: 25 Apr., 2012    Accepted: 11 May, 2012    Published: 20 May, 2012
© 2012 BioPublisher Publishing Platform
This is an open access article published under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Preferred citation for this article:

Khan et al., 2012, Entomopathogenic Fungi as Microbial Biocontrol Agent, Molecular Plant Breeding, Vol.3, No.7 63-79 (doi: 10.5376/mpb.2012.03.0007)

Abstract

An attractive alternative method to chemical pesticides is the microbial biocontrol (MBCAs) agents. They are the natural enemies devastating the pest population with no hazard effects on human health and the environment. Entomopathogenic fungi has an important position among all the biocontrol agents because of its route of pathogenicity, broad host rang and its ability to control  both sap sucking pests such as mosquitoes and aphids as well as pests with chewing mouthparts, yet they only cover a small percentage of the total insecticide market. Improvements are needed to fulfill the requirements for high market share. Entomopathogenic fungi differ from other microorganisms in their infection process: they directly breach the cuticle to enter the insect hemocoel, while other microorganisms enter by ingestion through mouth and then cause disease. Insect cuticle is mainly composed of chitin and protein surrounded by wax, lipid layer or fatty acids. Fungal pathogenesis mainly starts with the secretion of cuticle degrading enzymes. Some important and well known cuticle degrading enzymes are chitinase, protease and lipase which can degrade chitin, protein and lipid of the cuticle, respectively.  In this review we collected literatures from different sources and we arranged them in a such a way to better to understand the process of insect pathogenicity of entomopathogenic fungi and to find ways to improve the virulence of wild strain fungi to shorten the killing time of the pest and to commercialize the entomopathogenic fungi. In this way, the market share of the fungal entomopathogenic fungi will increase and a decrease in the usage of synthetic chemical pesticides will automatically follow.

Keywords
Entomopathogenic fungi; Beauveria bassiana; Biocontrol agents; Enzymes; Pathogenesis

 Integrated Pest Management (IPM) involves inspection, identification and treatment of pests. The treatment (when required) is carried out after inspection and identification with an environmentally safe and pest specific pesticide with limited persistence. Therefore biological pest management is considered as an important part of IPM. Biological control is an important part of integrated pest management (IPM). According to Oerke and Dehne (2004), insect pests are responsible for an estimated 42% of all losses in crop production. Extensive use of synthetic chemical pesticides, insecticide resistance to chemical pesticides (Ffrench-Constant et al., 2004), the resulting environmental pollution, adverse effects on human health and other organisms and the demand for reduced chemical inputs in agriculture have provided an impetus to the development of alternative forms of pest control (Wilson and Tisdall, 2001). An attractive alternative method to chemical pesticides is biocontrol (Nicholson, 2007) and the microbial biocontrol (MBCAs) agents as the natural enemies of the pest population devastate pests with no hazard effects on human health and environment. As the microbial biocontrol agents have complex mode of action, it’s very difficult for a pest to develop resistance against MBCAs. The present MBCAs are viruses, bacteria, nematodes, and fungi and they are used throughout the world with great advantage and success. But fungal biocontrol agents are the most important among all the MBCAs due to easy delivery, improving formulation, vast number of pathogenic strains known, easy engineering techniques and over-expression of endogenous proteins or exogenous toxins (St. Leger et al., 1996; Butt et al., 2001; Wang and St. Leger, 2007; Federici et al., 2008; St. Leger and Wang, 2010). Similarly, the entomopathogenic fungi are important among all the biological control agents due to its broad host range, route of pathogenicity and its ability to control sap sucking pests such as mosquitoes and aphids (Butt, 2002; Qazi and Khachatourians, 2005; Thomas and Read, 2007; Fan et al., 2007) as well as pests with chewing mouthparts (Hajek and St. Leger, 1994; de Faria and Wraight, 2007).

This review will help us understand entomopathogenic fungal virulence and present the most recent improvements and achievements in the relevant field. This will help us determine how to improve the virulence of entomopathogenic fungi to shorten the killing time of pest.

1 Entomopathogenic Fungi (EPF)
Entomopathogenic fungi (EPF) are widely distributed with both restricted and wide host ranges which have different biocontrol potentials against arthropods insects and plant pathogenic fungi. Entomopathogenic fungi were among the first organisms to be used for the biological control of pests. More than 700 species of fungi from around 90 genera are pathogenic to insects (Khachatourians and Sohail, 2008). Most EPF species are from the fungal divisions Ascomycota and Zygomycota. The ascomycete fungi were previously divided into two groups, the Ascomycota and the Deuteromycota (Table 1). The Fungi Imperfecti of Deuteromycota was known for having no sexual stage was known called as. But later on, cultural and molecular studies have demonstrated that some of these “imperfect fungi” (formally class Hyphomycetes in the Deuteromycota) were in fact anamorphs (asexual forms) of the Ascomycota within the order Hypocreales, and Clavicipitaceae family (Fukatzu, 1997; Hodge, 2003; Krasnoff, 1995; Shimazu, 1998). Within the Zygomycota, the most entomopathogenic species are in the order Entomophthorales (Roy et al., 2006).


Table 1 Classification of entomopathogenic fungi (Roy et al., 2006)

 


These fungi nutritionally may be saprotrophs that colonize the rhizosphere and phyllosphere, endophytic saprotrophs, hemibiotrophic, necrotrophic of plants, entomopathogenic or mycoparasitic and some of them have adopted more than one econutritional mode.

2 Life cycle of entomopathogenic fungi
The life cycle of EPF is composed of the spore which geminates into mycelia and the mycelia in turnproduce spores (spore–mycelia–spore phases). The life cycle of most entomopathogenic fungi consist of two phases: a normal mycelia growth phase mostly outside the host body and a yeast like budding phase mostly in the hemocoel of host. The yeast-like, dimorphic mode of growth in Beauveria bassiana was described by Alves et al (2002); and the production of oblong blastospore-like propagules in M. flavoviride was described by Fargues et al (2002). The life cycle of M. anisopliae under liquid culture conditions has also been described (Uribe and Khachatourians, 2008).

Beauveria bassiana in the absence of a specific insect host grows through an asexual vegetative life cycle consists of germination, filamentous growth and formation of sympoduloconidia (Figure 1B). In the presence of its host insect, Beauveria conidiospores germinate on the surface of the cuticle of host and penetrate the insects integument through the germinated hyphal tubes where the fungus alters its growth morphology to a yeast-like phase and produces hyphal bodies by budding like growth, which circulate in the haemolymph (Figure 1A) resulting in the host death. The fungal growth then reverts back to the typical hyphal form (the saprotrophic stage). The ability to convert to the yeast-like phase may be a prerequisite for pathogenicity.


Figure 1 Entomopathogenic dimorphic mode of growth

 


Entomopathogenic fungi, Verticillium lecanii, Beauveria bassiana and Metarhizium anisopliae are intensively studied as common natural enemies and important epizootics of aphids and other agricultural pests (Roberts and St. Leger, 2004; Thomas and Read, 2007; Wang et al., 2004; Milner, 1997; Li and Sheng, 2007). Beauveria bassiana (Balsamo) Vuilemin is one of the major fungal entomopathogens infecting nearly 95% of migratory alate aphids, especially M. persicae (Chen et al., 2008). Beauveria bassiana and Verticillium lecanii have dual biological control properties, i.e. they are natural enemies of pests and also plant pathogens (Bonnie et al., 2010; Goettel et al., 2008). Koppert Biological Systems currently use Verticillium lecanii (Zimm. Viegas) as an insect pathogen which has been commercialized for controlling aphids (Faria and Wraight, 2007) and it is effective in controlling plant pathogenic fungi like powdery mildews (Askary et al., 1998; Dik et al., 1998; Miller et al., 2004), rusts (Spencer and Atkey, 1981), green molds (Benhamou and Brodeur, 2000), Fusarium (Koike et al., 2007), Verticillium dahliae (Kusunoki et al., 2006) and Pythium ultimum (Benhamou and Brodeur, 2001). Beauveria bassiana is reported to limit the growth of plant pathogenic fungi in vitro, colonize endophytically in numerous plants and induce systemic resistance when pathogen infect the plant as well as reducing the diseases caused by soil born plant pathogens like Pythium, Rhizoctonia, and Fusarium (Ownley et al., 2010). Mitosporic fungi are generally environmentally friendly with negligible or low mammalian toxicity, have no residual toxicity (Copping, 2004) and are successful as mycoinsecticides against aphids (Faria and Wraight, 2007; Milner, 1997; Shah and Pell, 2003).

To date, several mycopesticides have been developed and used in several countries including the United Kingdom and the United States (Table 2) (Goettel et al., 2005; Kiss

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