Indo Asian Journal of Multidisciplinary Research (IAJMR) ISSN:

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1 Available online at Volume 3; Issue - 2; Year 2017; Page: DOI: /iajmr Indo Asian Journal of Multidisciplinary Research (IAJMR) ISSN: AGROBENEFICIAL ENTOMOPATHOGENIC FUNGI Beauveria bassiana: A REVIEW P. Saranraj* 1 and A. Jayaprakash 2, 1 Assistant Professor of Microbiology, Department of Biochemistry, Sacred Heart College (Autonomous), Tirupattur , Tamil Nadu, India. 2 Department of Biochemistry, Sacred Heart College (Autonomous), Tirupattur , Tamil Nadu, India. Abstract The use of microorganisms for the biological control of pest and disease vector insects was firstly proposed in the midst of the 19 th century, however only recently the full potential and the many advantages of this practice reached application on a commercial scale. While, only a small percentage of arthropods are classified as pest species, they nevertheless cause major devastation of crops, destroying around 18% of the world annual crop production, contributing to the loss of nearly 20% of stored food grains and causing around US$100 billion damage each year. The entomopathogenic fungus Beauveria bassiana is a globally distributed Hyphomycete, strains of which infect a range of insects. Strains of Beauveria bassiana have been used as the active agents in a number of biopesticides against a variety of agricultural pests, including whiteflies, beetles, grasshoppers and psyllids. The fungus is a facultative saprophyte and there are reports of Beauveria bassiana growing as a plant endophyte and interacting with plant roots. In this present review, we discussed about the general characteristics of Beauveria bassiana, History of Beauveria bassiana, Morphological, cultural & molecular characteristics of Beauveria bassiana, Life cycle of Beauveria bassiana, Factors responsible for germination of conidia of Beauveria bassiana, Growth characteristics of Beauveria bassiana, Pathogenicity of Beauveria bassiana, Biocontrol properties of Beauveria bassiana, Solid and diphasic production technologies, Blastospore production of Beauveria bassiana, Formulations of Beauveria bassiana and Agricultural importance of Beauveria bassiana. Key words: Entomopathogenic fungi, Beauveria bassiana, Blastospores, Formulation, Insect pests, Agricultural crops and Biocontrol. 1. Introduction Insecticides are the only tool in the pest management strategy that is reliable for emergency action when insects at the times of blooming. However, insecticidal control has led to several problems in insect management such as appearance of insecticide resistance pests, pest resurgence, undesirable toxic effects to *Corresponding author: Dr. P. Saranraj Received: ; Revised: ; Accepted: natural enemies of target pests, disruption of the ecosystem, toxic residues in crop plants and environmental problems. Consequently, the research for new environmentally safe method is being intensified. The indiscriminate use of synthetic pesticides causes some unfortunate consequences such as environmental pollution, pest resistance and toxicity to other non -target organisms including human being. At present scenario biopesticides are considered as the best alternative to chemical pesticides in the integrated pest management programmed.

2 P. Saranraj/Indo Asian Journal of Multidisciplinary Research (IAJMR), 3(2): Current estimates indicate that the global annual market for pesticides for which there may be biological alternatives. To date, however, only a relatively minor portion of this market has been captured by biological agents, most of which are the various forms of Bacillus thuringiensis. With respect to mycoinsecticides, intensive research over the past several decades has elevated most of the concerns regarding these agents, such as stability, formulation and application, mass production, and toxicity to non target pests. Field trials have proven that fungal applications can effectively reduce target insect populations, in this case grasshoppers, within a relatively short period of time. Biological control agents such as entomopathogenic fungi (EPF) can be used as a component of integrated pest management (IPM) of many insect pests. Under natural conditions, these pathogens are a frequent and often cause natural mortalities of insect populations. The main drivers behind the push for mycoinsecticides are the need for more specific agents as components of IPM programmes due to concerns over chemical residues on human health and the environment. Microbial assemblages in agricultural soils are important for ecosystem services in sustainable agricultural systems, including pest control. High populations of beneficial soil borne organisms are characteristics of healthy soils. The soil environment constitutes an important reservoir for a diversity of entomopathogenic fungi, which can contribute significantly to the regulation of insect populations. Many species belonging to Hypocreales (Ascomycota) inhabit the soil for a significant part of their life cycle at northern latitudes. Of these, Beauveria bassiana are especially common (Keller et al., 2013). Conversion from conventional to organic farming generally increases the diversity and activity of soil microorganisms over time (Mader et al., 2012). There is evidence for higher population levels of entomopathogenic fungi in soils of organically farmed fields as opposed to conventionally farmed fields (Klingen et al., 2012). Entomopathogenic fungi have played a uniquely important role in the history of microbial control of insects. Historical evidence indicated that entomopathogenic fungi were the first to be recognized as disease causing microorganisms in insects. Agostino Bassi wrote about a disease in silkworm caused by a fungus, which was later, identified as Beauveria bassiana (Kikankie, 2009). Elie Metchnikoff began with study of disease of a grain beetle Anisoplia austriaca that resulted in the discovery of the fungus Metarhizium anisopliae (Zimmermann, 2007). Beauveria bassiana, commonly known as white muscardine fungus attacks a wide range of immature and adult insects. Metarhizium anisopliae a green muscardine fungus is reported to infect 200 species of insects and arthropods. Both of these entomopathogenic fungi are soil borne and widely distributed. The entomopathogenic fungus Beauveria bassiana is well known as a potential alternative to chemical pesticides for the control of insect pests and is commercially available for such purposes in numerous countries worldwide. As a broad host range insect pathogen, strains of this fungus have been exploited for use against crop and invasive pests as well as for insects that act as human and animal disease vectors such as mosquitoes and ticks (De Faria and Wraight, 2007; Farenhorst, 2009; Kirkland et al., 2014). Aside from its interest as a pest biological control agent, Beauveria bassiana is also an emerging model organism that can be used to examine unique aspects of fungal growth and development including host pathogen interactions (Lewis, 2009; Wanchoo, 2009; Jin, 2010). Infection of insects does not require any specialized mode of entry and begins with attachment of fungal spores to the target hosts. In response to cuticle surface cues, the fungus germinates, and the emerging germ tubes produce a variety of enzymes that combined with mechanical pressure begin the process of cuticle penetration. In this regards, the surface characteristics of the infectious fungal spores as well as several genetic determinants of virulence have been characterized (Holder, 2007; Fang, 2008; Fang, 2009; Holder and Keyhani, 2015).

3 P. Saranraj/Indo Asian Journal of Multidisciplinary Research (IAJMR), 3(2): The entomopathogenic fungus, Beauveria bassiana is of commercial importance as an alternative to chemical insecticides in an agroecosystem (Khachatourians et al., 2012). The fungal pathogen Beauveria bassiana is a widely used mycoinsecticide for control of several insect pests, providing a biological alternative to synthetic chemical insecticides (Hajek et al., 2001). A key advantage for microbial control agents is their potential to replicate and persist in the environment, offering continued suppression of insect pest populations. Exploiting this advantage, however, is commensurate with the need to determine the risks to non - target organisms of mass releasing this fungus. To date, no information is available on the potential for genetic recombination between strains of Beauveria bassiana neither in agricultural fields nor on whether this recombination could result in altered virulence and host range. Beauveria species attack many insect species worldwide. Species range from the ubiquitous insect pathogen Beauveria bassiana (Balsamo) Vuillemin to rare species but the entomogenous life - style is prevalent (Glare et al., 2008; Sevim et al., 2010; Glare, 2014). Currently, six species of this genus are recognized: Beauveria bassiana, Beauveria clade, Beauveria brongniartii, Beauveria caledonica, Beauveria vermiconia and Beauveria amorpha (Rehner and Buckley, 2015; Goettel et al., 2015). Among these species, considerable effort has been spent to develop Beauveria bassiana as a biological control agent in agriculture and forestry in temperate regions and the most widely used species available commercially was Beauveria bassiana (Meyling and Eilenberg, 2007). Although, a sexual stage is now known (Li et al., 2001) most Beauveria bassiana exist as asexual organisms, reproducing mainly through the production of single cell conidia. Beauveria bassiana produce three single cell forms, aerial conidia, in vitro blastospores and submerged conidia in different conditions (Jeffs et al., 2009). Aerial conidia are produced on the surface of solid medium by a process of hyphal extension, formation of phialides (rachis) and spore production. Aerial conidia usually are used for biological control agents because they are relatively resistant to varying environmental conditions and can be formulated to prolong shelf life. Aerial conidia contain a rodlet layer that results in a hydrophobic property. Blastospores are produced in nutrient liquid medium. They are hydrophilic, and they germinate and grow at much higher rate than aerial conidia. Submerged conidia are produced in defined liquid medium. They are also hydrophilic, showing a rough surface morphology. Submerged conidia represent an important developmental stage for growth in a limited nutrient medium (Holder and Keyhani, 2015). Entomopathogens can be mass produced using the diphasic liquid solid fermentation technique developed for the LUBILOSA (Lutte Biologique contre les Locustes et Sauteriaux) project to produce Beauveria bassiana (Lomer et al., 2007). The liquid phase provides active growing mycelia and blastospores, while the solid phase provides support for development of the dry aerial conidia. The conidia produced by these fungi can be used directly as natural granules or extracted through sieving and formulated as powder, granules or oil concentrate, or any other suitable formulation depending on the target insect pest for example, Beauveria bassiana was applied as conidia or mycelia in various formulations. Control of insect pests in field after initial application is achieved through the induction of a fungal epizootic, where new spores, and vegetative cells produced in infective insects are spread, naturally, to healthy members of the insect population. 2. Beauveria bassiana The genus Beauveria contains at least 49 species of which approximately 22 are considered pathogenic (Kikankie, 2009). Beauveria bassiana, a white muscardine fungus, is the most historically important of the commonly used fungi in this genus. Originally known as Tritirachium shiotae, this fungus was renamed after the Italian lawyer and scientist Agostino Bassi who first implicated it as the causative agent of a white (later yellowish or occasionally reddish) muscardine disease in

4 P. Saranraj/Indo Asian Journal of Multidisciplinary Research (IAJMR), 3(2): domestic silkworms (Furlong and Pell, 2005; Zimmermann, 2007). All fungal phyla include species that are able to reproduce either sexually or asexually. The production of multiple spore types increases the chances of survival during adverse environmental conditions (Alexopoulos et al., 1996). These spore types can be produced in response to environmental conditions, as well as at different times in the life cycle and can have different dispersal mechanisms. Beauveria bassiana is considered to be one of the most effective entomopathogenic fungi for various reasons including: cosmopolitan distribution (Bidochka et al., 2000), ability to infect any life stage of its host, wider host range than the other Deuteromycetes, can infect almost all orders of insects (Roberts and Hajek, 2002) and can infect certain plant tissues (Bing and Lewis, 1992). Beauveria bassiana can easily be isolated from insect cadavers or from soil in forested areas by using simple media (Beilharz et al., 2002), as well as by baiting soil with insects (Zimmermann, 2006). In the laboratory it can be cultured on simple media (Goettel and Inglis 2007). Huang et al. (2002) identified Cordyceps bassiana as the ascomycote teleomorph of Beauveria bassiana. However, the organism was most frequently described and identified in the anamorph stage and assigned to the Deuteromycota. Taxonomical identification within the Deuteromycota relies heavily on physical characteristics such as shape, size and color as well as the manner in which the asexual spores, or conidia are produced. Species within the genus Beauveria are typically differentiated from other fungi by morphological characteristics. They are filamentous fungi that produce colorless (hyaline) aerial conidia from conidiogenous cells freely on the mycelia. This characteristic places them within the moniliaceous (having hyaline conidia) Hyphomycetes (De Hoog, 1972). Aerial conidia are initially produced as terminal swellings formed on the neck of the conidiophore. The next conidium grows laterally, half way up the first neck of the conidiophore, in another direction, and is pushed upwards by sympodial growth (De Hoog, 1972). The resulting denticulate rachis, with denticles equally wide as the rachis, is characteristic of Beauveria spp. Beauveria bassiana colonies grow relatively slowly and can appear powdery or wooly, with colors ranging from white to yellow and occasionally pinkish. Aerial hyphae are septate, smooth, hyaline and about 2 μm wide. Submerged hyphae are similarly structured, but larger (1.5 3 μm). Conidiogenous cells, which arise from short swollen stalk cells, are often found in dense clusters or whorls. They consist of a globose base and the characteristic denticulate rachis. The aerial conidia are hyaline, smooth, relatively thin walled and vary from being oval to spherical depending on the species and occasionally by cultural conditions (De Hoog, 1972; Huang et al., 2002). Typical entomopathogens, Beauveria bassiana invades through the host cuticle, although as with other hyphomycetes, entry through the digestive tract is also possible. The initial and crucial steps in the infection process are attachment to, and penetration of, the host cuticle. Arthropod cuticles are complex structures, which in the case of insects are composed of two main layers the epicuticle and the procuticle (Huang et al., 2002). The epicuticle, a thin layer which overlays the procuticle, lacks chitin, but was composed of sklerotinized proteins overlaid by a waxy layer containing fatty acids, sterols and lipids. The bulk of the cuticle, the procuticle, consists of chitin embedded in a protein matrix (Clarkson and Charnley, 1996; Goettel and Inglis, 2007). Fungal entomopathogens use mechanical pressure and a mixture of enzymes to penetrate and dissolve the insect cuticle. Although, several entomopathogens use swellings at the tip of the germ tube (appressoria) to generate mechanical pressure and increase attachment to the insect cuticle, such structures are rarely observed in Beauveria bassiana. However, the battery of enzymes including proteases and chitinases produced by this entomopathogen are similar in nature to those produced by other hyphomycete

5 P. Saranraj/Indo Asian Journal of Multidisciplinary Research (IAJMR), 3(2): entomopathogens such as Metharhizium ansiopliae (Clarkson and Charnley, 1996). Once the fungal hyphae reach the hemocoel, thin walled, yeast like, hyphal - bodies, or blastospores, are generated and dispersed throughout the host (Goettel and Inglis, 2007). Host death appears to result from a number of factors including production of toxins by the fungus, physical obstruction of the circulatory system, invasion of organs and nutrient depletion. Upon host death, the parasite switches from yeast like to hyphal growth invading all the tissues of the host body, while attempting to reduce or eliminate competing organisms with a variety of antimicrobial metabolites. The mummified corpse can remain in the environment unchanged for months, but under favorable conditions the hyphae emerge from within the corpse, sporulate and the resulting aerial conidia are dispersed via, air or water (Goettel and Inglis, 2007). Beauveria sp. produces a number of metabolites some of which have cytotoxic effects alexopoulos (Alexopoulos et al., 1996). These metabolites include beauvericin, bassianolide, beauveriolides, bassianin, tenellin and oosporein. Beauvericin and bassioanolide are ionophores that differ in specificity for cations. Beauvericin, a hexadepsipeptide, has antimicrobial activity against both Gram negative and Gram positive bacteria is toxic to brine shrimp with a LD 50 of 2.8 μg ml -1 water, but has no demonstrated insecticidal effects (Strasser et al., 2000). Bassianolide, a cyclooctadepsipeptide, also has antimicrobial effects and was lethal to silk worm larvae at a concentration of 13 ppm (Strasser et al., 2000). Although, beauveriolides are structurally related to beauvericin and bassioanolide, they are not as well characterized, and their antimicrobial or insecticidal potential have yet to be described. Strasser et al. (2000) have recently shown that beauveriolides have an inhibitory effect on lipid drop formation in mouse erythrocytes and as a result could be marketed as anti-cholesterol drugs. According to their data, beauveriolides have few cytotoxic effects on mouse cells at levels up to 100 mg -1 day -1. The pigments, bassianin, tenellin and oosporein are toxic to erythrocyte membrane ATPases (Jeffs and Khachatourians, 2007). Oosporein is also a denaturing agent and a potent antibiotic specific to Gram positive organisms. The toxicity of these pigments towards insect host cells has not been well defined (Strasser et al., 2000). 3. History of Entomopathogenic fungi Beauveria bassiana In the early 1800s, the silkworm farms of Italy and France were plagued with diseases that periodically decimated the European silk industry. The disease was called white muscardine after the French word for bonbons, as the disease resulted in fluffy white corpses resembling pastries. An Italian scientist named Agostino Bassi discovered that the disease was caused by a microbial infection and that it could be controlled by altering the living conditions of the silkworms to decrease the spread of the disease. One simple recommendation that he made was to remove and destroy infected and dead insects. Later the microbe, a filamentous fungus, responsible for the disease was named Beauveria bassiana in honor of Bassi s discovery. In 1835 Agostino Bassi, one of the founding fathers of insect pathology, published his findings in a paper entitled Del mal Del segno, calcinaccio o moscardino; this publication was one of the first instance of a microbe identified as the causative agent of an infectious disease (Alexopoulos, 1996). The earliest reports of a fungal entomopathogen, possibly the organism that would come to be known as Beauveria bassiana (Balsamo) Vuillemin, came from China, as far back as 2700 BC (Steinhaus, 1956). It was not until 1835 that Agostino Bassi demonstrated that Calcino, or White Muscardine, a disease that was devastating the Italian silkworm industry, was contagious and caused by a parasitic fungus (Steinhaus, 1956). Balsamo Crivelli officially named the organism Botrytis paradoxica, eventually changing the name to Botrytis bassiana to honor the man who first described it. In 1912, Vuillemin, determined that there were enough features peculiar to Botrytis bassiana to assign it to the new genus Beauveria (De Hoog, 1972). There now are multiple species in the genus Beauveria Vuill. Some of

6 P. Saranraj/Indo Asian Journal of Multidisciplinary Research (IAJMR), 3(2): the most important ones are: Beauveria bassiana, Beauveria brongniartii, Beauveria alba, Beauveria bassiana and Beauveria brogniartii well known entomopathogens with a wide host range, including arthropods other than insects, are now being used as biological control agents to control a variety of crop damaging insects. Beauveria alba is mainly isolated as an indoor contaminant and displays the lowest pathogenicity of these three Beauveria species (Alexopoulos et al., 1996). Due to the practical applications of fungal entomopathogens as biological control agents, the biology of these fungi has been the subject of much research. Agostino Bassi (1835) first described Beauveria as the causal agent of mal del segno or the mark disease, also known as calcinaccio or cannellino in Italy and white muscardino in France, which caused economically devastating epizootics of domestic larval silkworms in southern Europe during the 18 th and 19 th centuries. In his studies with Beauveria, Bassi was the first to demonstrate that microbes can act as contagious pathogens of animals, providing an important antecedent to the germ theory of disease (Ainsworth, 1973). The first taxonomic recognition of the muscardino fungus was proposed by Balsamo Crivelli (1835) who acknowledged Bassi s discoveries by naming this pathogen Botrytis bassiana. The genus Beauveria, however, was not formally described until the early 20 th century by Vuillemin (1912), who designated Botrytis bassiana as the type species. Beauveria bassiana is considered nonpathogenic to vertebrates; although there are a handful of recorded cases of human infection by this fungus (Kisla et al., 2010; Tucker et al., 2014). These cases however, involved patients with compromised immune systems increasing their susceptibility to a wide range of opportunistic infections. Based upon safety tests and considered a natural product, Beauveria bassiana has been approved by the U.S. Environmental Protection Agency for commercial use. Beauveria bassiana is non toxic to mammals, birds, or plants; and use of Beauveria is not expected to have deleterious effects on human health or the environment (EPA, 2000). Strains and various formulations of Beauveria bassiana are available commercially in various parts of the world. Major efforts have been targeted towards isolation and characterization of strains with high virulence, improved cost effectiveness and to technologies that could be applied to other economically important Ascomycetes. One of the most important steps in the host pathogen interaction is the initial attachment of the fungus to the host cuticle. Modifying the formulation of commercial products, or of the fungus itself, namely to improve targeting and attachment to the host cuticle, may lead to improvements in infection rates and host mortality, and hence the effectiveness of the biocontrol. Birth of insect pathology occurred in the nineteenth century when the Italian scientist Agostino Bassi (1835) discovered that disease in silkworm could be caused by a fungus, which was later identified as Beauveria bassiana (Gillespie and Claydon, 2009). Ignoffo and Anderson (2009) elucidated the etiology of a contagious disease for the first time, but also implied that infectious diseases identified as Beauveria bassiana could be used to control insects. The disease caused by Beauveria bassiana is known as White Muscardine. This name was derived from a type of cookies produced in Italy, which are fully covered with sugar giving a whitish appearance. The insect pests that can be controlled by Beauveria bassiana includes Rice Leaf folder, Stem borer, Homed cater pillar, Coconut rhinoceros beetle, Brinjal fruit borer, Colorado potato beetle, May beetle, Whitefly, Aphids, Thrips, Mealy bugs, Psyllids, Weevils, Caterpillars and Leafhoppers. It was being realized that this fungus was rather a generalist, with no strict host specificity (Shimuza, 2004). 4. Morphology, cultural characteristics and molecular characterization of Beauveria bassiana Beauveria bassiana is characterized morphologically by its sympodial to whorled clusters of short-globose to flask-shaped conidiogenous cells, which give rise to a succession of one-celled, hyaline, holoblastic conidia that are borne on a progressively elongating sympodial rachis. Although

7 P. Saranraj/Indo Asian Journal of Multidisciplinary Research (IAJMR), 3(2): morphologically distinctive as a genus, species identification in Beauveria is difficult because of its structural simplicity and the lack of distinctive phenotypic variation. Conidia are the principal morphological feature used for species identification in Beauveria. In shape conidia may be globose, ellipsoidal, reniform to cylindrical, or comma shaped and range in size from 1.7 to 5.5 mm. Species identification in Beauveria has been complicated by the proliferation of new species described between the late 19 th to mid-20 th centuries, few of which are morphologically distinct from previously described species (Petch, 2006). Several revisionary studies of Beauveria have been conducted to evaluate morphological species concepts. Petch (2006) recognized two species, Beauveria bassiana and Beauveria densa (Link) F. Picard and concluded that cultural data were uninformative for delimiting species. Macleod (2014) monographed Beauveria and, like Petch, recognized only two species, which he classified in Beauveria bassiana and Beauveria brongniartii (Sacc.) Petch (5 Beauveria densa). Macleod (2014) concurred recognized an additional species, Beauveria alba (Limber) Saccas, which was later transferred to Engyodontium (Limber) (Hoog, 2008). Hoog and Rao (2015) described several new species. In all, forty nine species have been placed in Beauveria and 22 epithets are currently valid. Today, researchers generally follow Macleod (2014) and Hoog (2012) and classify most environmental isolates of Beauveria in either Beauveria bassiana or Beauveria brongniartii, a practice reflected in contemporary texts and keys to species identification (Humber, 2007; Tanada and Kaya, 2013). Ongoing difficulties in applying morphological approaches to species recognition in Beauveria have spurred the search for additional sources of taxonomic characters. Alternative character systems that have been investigated include isozymes (Maurer et al., 2007), chemotaxonomic characters (Mugnai et al., 2009), mitochondrial RFLP (Hegedus and Khachatourians, 2006), immunological approaches (Tan and Ekramoddoullah, 2011), rrna sequencing (Rakotonirainy et al., 2011), RFLP (Kosir et al., 2011), introns in the large subunit rdna (Neuveglise et al., 2006; Neuveglise and Brygoo, 2014), RFLP and nucleotide sequences of ITS (Neuveglise et al., 2014), SSCP analysis of taxon specific markers (Hegedus and Khachatourians, 2006), RAPD markers (Cravanzola et al., 2007; Maurer et al., 2007), and the combined use of morphology and RAPD markers (Glare and Inwood, 2008). Although, all character systems investigated in these studies were effective in detecting genetic variation within Beauveria, none have been applied directly to taxonomic investigations in this genus. Although, biologically relevant species concepts and explicit species recognition criteria have yet to be defined for Beauveria, recent molecular and cultural studies have provided insight regarding the phylogenetic position and reproductive biology of several species. An rdna phylogeny by Sung et al. (2001) supports a single evolutionary origin of Beauveria within the sub-family Cordycipitoideae of the Clavicipitaceae, and that the teleomorph Cordyceps scarabaeicola is nested within Beauveria and is the sister to Beauveria caledonica Bissett and Widden. Second, strains isolated from stromata of several Cordyceps species produce Beauveria anamorphs, clearly demonstrating that some Beauveria species are sexual. These Cordyceps species include Cordyceps bassiana (Li et al., 2001), Cordyceps brongniartii (Shimazu et al., 2008), Cordyceps staphylinidaecola (Kobayasi and Shimazu, 2002) and Cordyceps sobolifera (Li et al., 2001). Beauveria is ubiquitous in plant debris and soil and may be isolated from foodstuffs, infected insects and indoor air environment. It has a wide host range of insects and is common in nature. Beauveria densa isolated from cadavers was able to attack Coleoptera and Lepidoptera but not Orthoptera. Beauveria bassiana is the most common parasite of insects that has been isolated from soil and litter and from dead and moribund insects in nature. Over 200 species of insects in nine orders, mainly Lepidoptera and Coleoptera, have been recorded as hosts of Beauveria bassiana. Other Beauveria species, like Beauveria brongniarti, have been used in France for control of insect pests (Feng

8 P. Saranraj/Indo Asian Journal of Multidisciplinary Research (IAJMR), 3(2): et al., 2004). Beauveria was isolated from insects belonging to the Scarabaeidae family (Humber, 2007). Beauveria amorpha was recorded in South America from Lepidoptera and Coleoptera insects (Boucias and Pendland, 2008). In culture, Beauveria bassiana grows as a white mold. On most common cultural media, it produces many dry, powdery conidia in distinctive white spore balls. Each spore ball was composed of a cluster of conidiogenous cells. The conidiogenous cells of Beauveria bassiana are short and ovoid, and terminate in a narrow apical extension called a rachis. The rachis elongates after each conidium was produced, resulting in a long zig - zag extension. The conidia are single -celled, haploid and hydrophobic. Beauveria bassiana was usually found growing densely through the exoskeleton of insect cadavers killed by the fungus. Beauveria bassiana has also been reported to be endophytic. It was also observed penetration of developing hyphae on the leaf surface of Zea mays that reached the xylem and provided insecticidal protection against damage by the European corn borer, Osirinia nubilalis. The conidiogenous cells are usually clustered, colorless, with a globose base and a denticulate apical extension (Humber, 2007). Conidia are 2-6 µm in diameter and are borne out of zig - zag phialides or apical extensions (rachis) (Humber, 2007; Boucias and Pendland, 2008). 5. Life cycle of Beauveria bassiana Beauveria bassiana is considered to be the anamorph of Cordyceps bassiana, an ascomycete in the order Clavicipitales. The genus Cordyceps and its anamorph Beauveria are endoparasitic pathogens of insects and other arthropods (Nikoh and Fukatsu, 2000). Beauveria bassiana is a polymorphic fungus whose life cycle includes both single and multicellular stages. Beauveria bassiana is an ubiquitous saprobe and can be found in soil or decaying plant material, where it grows as multicellar mycelia by absorbing nutrients from the decaying matter (St Germain, 2006). Reproduction and dispersion of progeny is accomplished by the production of asexual spores called conidia. Conidia of Beauveria bassiana are smaller than most other fungal spores measuring only 2-4 μm wide (Akbar et al., 2004; Bounechada and Doumandji, 2004). Conidia are produced from conidiogenic cells that protrude in a zig-zag structure from mycelia hyphae. Conidia released into the environment remain dormant or in a non - vegetative state until appropriate conditions activate germination. Humidity is a major factor in activation of conidia independent of a host (Boucias et al., 2008). Attachment of the conidia to the exoskeleton of a host insect also stimulates germination. The initial attachment of Beauveria bassiana conidia to the host exoskeleton is thought to be a function of hydrophobicity which creates a strong interaction between the conidia surface and the waxy layer/chitonous surface of the host (Holder and Keyhani, 2015). Germination involves the development of a hyphal structure called a germ tube; the germ tube grows along the surface of the cuticle and can penetrate into the cuticle by enzymatic digestion and mechanical rupture of exoskeletal components. Once through the exoskeleton, the fungus reaches the hemolymph and there in produces single celled morpho-types known as in vivo blastospores. These cells replicate by budding and proliferate within the hemolymph, evading any innate immune responses (Lord et al., 2012). When nutrients in the hemolymph are consumed the blastospores produce elongating hyphae. These hyphae grow until they exit the cadaver and begin producing conidia one the insect surface. The result is a fuzzy white mummified insect corpse. 6. Factors responsible for germination of conidia of Beauveria bassiana Germination of conidia depends largely on environmental conditions including temperature, light and especially relative humidity. Ferron (2007) found that insects can be infected with Beauveria bassiana at ambient relative humidities and less than 92 per cent are required for germination and inycelial growth in vitro. He suggests that the initial infective phase (germination on the cuticle of the insect) may be less dependent on ambient humidity, because the microclimate of the insect cuticle is similar to

9 P. Saranraj/Indo Asian Journal of Multidisciplinary Research (IAJMR), 3(2): that of their host plants. The ranges of temperature and humidity for germination are broader. Entomopathogenic fungi of Deuteromycotina infect their host via, conidia which produce hyphae that grow directly through insect integument. In the case of Beauveria bassiana, the most common route of infection is through the cuticle (Ferron, 2008; Pekrul and Grula, 2009). Temperature required for germination of Beauveria bassiana conidia ranges from 0 to 40 C with an optimum temperature of C (Schaerffenberg, 2007; Hall, 2011; Benz, 2015). Most fungal entomopathogens require temperatures between C and relative humidity above 97 per cent for germination. The conidia of many entomopathogenic fungi will survive in the environment until they contact a nutritional source that will trigger germination (Smith and Grula, 2011; Ignoffo et al., 2012; Hunt et al., 2014; Gillespie and Crawford, 2015). Beauveria bassiana germination depends on sources of carbon such as glucose, glucosamine, chitin and starch. Nitrogen is also necessary for hyphal growth (Tanada and Kaya, 2013). Rapid germination is desired in field situations to avoid the ill effects of ultraviolet light on the germination and survival of the fungus (Moore and Prior, 2006; Inglis et al., 2009). The conidia penetrate Heliothis zea (Boddie) through the spiracles and causes infection (Pekrul and Grula, 2009). Beauveria bassiana has been reported to infect several mosquito species through the posterior siphon and through the respiratory system (Clark et al., 2012). Hyphae penetrate the cuticle through a series of mechanical and enzymatic processes (Ferron, 2015). Infection of conidia through the integument depends primarily on the nature of the cuticle, its thickness, sclerotization and the presence of antifungal and nutritional substances (Charnley, 2009). The entomopathogenic species of Deuteromycotina require, a relative humidity above 90 per cent for conidial germination in vitro. Beauveria bassiana conidia germinate in a range of temperatures between 8 C and 35 C, with an optimum between 25 C and 30 C (Tanada and Kaya, 2013). The amount of Beauveria bassiana inoculum needs to be increased with the older instars of larvae to achieve the same level of mortality (Fargues and Robert, 1983). Feng et al. (2004) found first instar of Qstrinia nubilalis (Hubner) to be more susceptible to Beauveria bassiana than later instars. It is also suggested that ingestion after penetration of hyphae reach the homeocoel and produce hyphal bodies (blastospores) that circulate through the hemolymph (Tanada and Kaya, 2013) and multiply by budding. Vandenberg et al. (1998) found Diamond back moth early stages to be less susceptible to Beauveria bassiana. Budding continues for a period of 3 to 7 days before the fungus reverts to a hyphal form, which infects other tissues and organs. Development of hyphal bodies in the hemolymph of Beauveria bassiana infected Spodotera exigua (Hubner) are known to disrupt the cellular defense response of hemocytes (Hung and Boucias, 1992; Hung et al., 1993). Sieglaff et al. (1997) observed less susceptibility to Metarrhizium flavoviride of the sixth instar Schistocerca americana (Drury) than of the fourth instar. The lack of structural components (e.g. chitin) of the hyphal bodies in the hemolymph of Spodotera exigua larvae is an important factor for evasion of host cellular defense mechanisms. Deuteromycotinia also produce cyclic peptides that are found to inhibit phagocytic activity of insect plasmocytes in a dose - dependent. Other factors influencing host susceptibility to fungal infections are the age and stage of the insect at the time of infection, host nutrition and exposure to chemical insecticides (Mazet et al., 1994; De Jonghe et al., 2007; Arti Prasad et al., 2010). In order to overcome insect defenses, the fungus can also produce newer mycotoxins. These toxins also function as antimicrobials that prevent infected silkworms from subsequently acquiring bacterial infections. Some of these toxins are proteases that damage the principal functions of the hemolymph or produce toxic by-products in the insect. Other toxins are low molecular weight compounds such as beauvericin, oosporein and bassianolide that have been demonstrated to be insecticidal (Tanada and Kaya, 2013; Gupta et al., 1995).

10 P. Saranraj/Indo Asian Journal of Multidisciplinary Research (IAJMR), 3(2): Wagner and Lewis (2000) have shown that following conidia germination and germ tube development, Beauveria bassiana enters maize tissues directly through the plant cuticle. Subsequent hyphal growth occurs within the apoplast, but only occasionally extending into the xylem elements. The introduction of endophytic Beauveria bassiana in maize is compatible with other pest management strategies. It has been shown that endophytic Beauveria bassiana is compatible with both Bacillus thuringiensis and carbofuran applications used to suppress insect pests. Loc et al. (2002) also reported that Metarhizium anisopliae and Beauveria bassiana used at the dose of conidia/ha in the rice fields had no adverse effect on predatory wolf spider as Lycosa peudoannulata, Araneus inustus, Tetragnatha maxillosa, Cyrtohinus lividipennis and Polytoxus fuscovittatus. 7. Growth characteristics of Beauveria bassiana Some studies made with Beauveria bassiana reveal that, the carbon sources used for production are closely related with the spore production (Thomas, 1987) and also with the spore - type produced (Hegedus et al., 1990), whereas Jackson et al. (1997) demonstrated that, the adequate sources of carbon and nitrogen in the culture media, would produce tolerant - desiccation blastospores of Isaria fumosorosea after air - dried conditions; in a similar way, Sandoval Coronado et al. (2001) found that, different supports used for formulation, such as talc, lime, gypsum or clay maintained the viability of Isaria fumosorosea propagules to levels around 50 to 70 % for cultures obtained in liquid media after different storage times. Radial growth Kula et al. (2002) observed that the highest radial growth (4.07 cm) Metarhizium anisopliae cultured on Sabouraud's dextrose agar with yeast (SDAY) medium for 10 days of incubation. The growth parameters viz., radial growth, biomass and spore production of some isolates of entomopathogenic fungi Beauveria, Verticillium and Metarrhizium were assessed and they observed that the spore production and radial growth of Beauveria was highest in Potato Dextrose Broth (Nirmala et al., 2005). Spore production Samsinakova et al. (1981), who obtained 10 8 conidia of Beauveria bassiana in the medium composed of peptone 0.8 per cent and sorbitol one per cent. Rombach (1988) recorded blastospores ml -1 in Beauveria bassiana using the media containing sucrose (2.5 %) and yeast extract (2.5 %). Cherry et al. (1999) harvested dry conidial power with an average of 31.1 mg g -1 of Beauveria bassiana. Kula et al. (2002) observed highest spore count of spores ml -1 with Metarhizium anisopliae in Earner's medium. Uma Maheswara Rao et al. (2006) studied the impact of Beauveria bassiana on Spodoptera litura in relation to different temperatures and ph and the initial ph of 6-8 to be the most suitable for spore formation. Senthamizhselvan et al. (2010) observed that growth, sporulation and biomass production of Beauveria bassiana was influenced by the medium used. Growth and sporulation of Beauveria bassiana on different commodities Basal medium containing various carbohydrate sources on growth and sporulation of Beauveria bassiana also showed that the fungus grow best on melezitose but sporulated best on sucrose, trehalose and D - glucose. However, least growth and sporulation were observed on L - rhamnose and D - sorbose (Campbell et al., 1983). Bidochka et al. (1997) reported production of blastospores of Beauveria bassiana on liquid media containing peptone, peptone -glucose, peptone - yeast extract. Results showed four - fold higher production of blastospores in peptone - glucose as compared to glucose - peptone yeast extract. Growth and sporulation of an isolate of Beauveria bassiana recorded from Nilaparvata lugens obtained from China revealed that maximum mycelial growth of this fungus was possible in liquid culture containing sucrose and yeast extract at 3.5 per cent each. However, production of maximum conidia ( conidia mg -1 ) was recorded in the medium containing 2 per cent maltose along with 0.75 per cent yeast extract. It was concluded that production of dry mycelia is the practical

11 P. Saranraj/Indo Asian Journal of Multidisciplinary Research (IAJMR), 3(2): approach for mass production of Beauveria bassiana (Rombach et al., 1988). 8. Pathogenicity of Beauveria bassiana The insect infection by fungal pathogens occurs through four successive steps. They are contacts between the host and fungal propagules, attachment and germination of propagules, penetration of cuticle or gut wall with subsequent invasion of host tissue and organ and finally death of host by physical blockage of the gut, trachea, circulatory systems, histolysis and toxin production. After the death of the host, saprophytic development of fungus is necessary for the completion of pathogenic cycle. A fungus, unlike other microbials does not require ingestion for infection in the host- Infection through mouth parts, and orifice, digestive and genital tracts have also been reported (Ferron, 2008). The fungal pathogenesis begins with adhesion of conidia to the cuticle of host followed by germination of conidia which penetrates the cuticle through germ tube. The germ tube passes through the integument of insect. Finally, the fungus develops inside the body of host which results in death of the host insect. Under suitable environmental conditions, death was followed by external sporulation of fungus (Moore and Prior, 2006). The infection of insects by entomopathogenic fungi occurs following germination of conidia/spores on the cuticle and it penetrates through the integument (Clarkson et al., 1998). Clark et al. (2012) reported that the formation of germ tube on the integument of host, penetration of cuticle by penetration peg is usually followed by formation of appresorium that finally attach the fungus to the epicuticle and provides basic support for mechanical and enzymatic process through epicuticle, penetrant hyphae and penetrant plates develop in the procuticle which produce hyphae that give rise to both irregular and smooth walled hyphal bodies. The two primary infection sites were the head and the anal region and the most preferred site for fungal development was the larval gut (Miranpuri and Khachatourians, 2007). The hyphal bodies of Beauveria bassiana produce hyphae, which ultimately penetrate the procuticle and move to haemocoel (Hajek et al., 2001). The hyphal bodies which are single or multinucleated structures without cell wall but contain a thin fibrillar layer with plasma membrane (Referred as blastospores) that produce new hyphae that ultimately fill the body cavity and remain as resting spores in the dead host. Ferron et al. (1991) observed that selection of fungal pathogens tolerant to the temperature range in the ecosystem in which they are to be used is imperative for their use as mycopesticides. Doberski (1981) selected fungal strains with pathogenic activity below 15 C for insect pests in temperate regions; McClatchie et al. (1994) chose strains active at temperatures >30 C for use against desert locusts in West Africa. Similarly, Mohammed et al. (1977) sought isolates adapted to temperatures >25 C for control of noctuid insects in the southeastern USA. 9. Beauveria bassiana as a Biocontrol agent As agricultural pests present an economic and resource production problem to human society, other arthropod pests are a direct human health concern. In this regards, a number of parasitic arthropods act as vectors for the transmission of infectious diseases. Because of their ability to access the human circulatory system, blood feeding arthropods, are important vectors by which microbial parasites can be transmitted between various hosts. Beauveria bassiana shows potential for controlling arthropod disease vectors, and hence has the potential to decrease the spread of diseases carried by these insects. Ticks are an example of an arthropod that can carry and transmit a wide variety of disease causing agents. Ticks, obligate blood feeders, are potential carriers of the bacteria Borrelia burgdorferi, the causative agent of Lyme disease in humans and domestic animals (Stricker et al., 2006). Other tick born diseases include; Rickettsia rickettsii, causative agent of Rocky Mountains spotted fever in both humans and some domestic animals; Babesia canis and Babesia gibsoni, a protozoan parasite of domestic animals; and several species of the

12 P. Saranraj/Indo Asian Journal of Multidisciplinary Research (IAJMR), 3(2): genus Ehrlichia, an obligate intracellular cocci responsible for a variety of blood cell diseases in domestic animals (Ettinger, 2000; Waner, 2001). Research studies have shown that the prominent tick species including those known to transmit Lyme disease are susceptible to infection by Beauveria bassiana (Kirkland et al., 2014). Chaga s disease is a parasite infection that is transmitted by an insect vector, primarily the South American kissing bug (Triatoma infestans) (Lazzarini et al., 2006). Chaga s disease is a serious health problem in South America where approximately 20 million people are infected. The health costs associated with treating an infection is often too high for the majority of those inflicted with the disease. For this reason, research into the control and prevention of the disease, is focused on vector control and involving the use of Beauveria bassiana and other entomopathogenic fungi. Brazil and Argentina are two countries with research facilities studying the pathogenicity of Beauveria toward these insect disease vectors (Luz and Fargues, 1998; Luz et al., 1998; Marti et al., 2005). Beauveria bassiana occurs worldwide and it is the most frequent species isolated from insects and soil samples, where it can survive for long periods in saprogenesis. Under laboratory conditions, it can colonize the majority of insects, occurring enzootically and epizootically in the field. The infection occurs naturally via, tegument, where the fungi germinate within 12 to 18 hrs, depending on the presence of nutrients, such as glucose, chitin, and nitrogen among others (Alves, 1998). Beauveria bassiana may also be a valuable tool in the fight against malaria. Between 300 and 500 million people are infected with malaria, and this disease is responsible for as many 1.5 million deaths annually (Geetha and Balaraman, 1999; O'Hollaren, 2006). Currently, there are no vaccines against malaria; however, studies have shown the potential for fungal entomopathogens to reduce the spread of this disease (Blanford et al., 2005; Scholte et al., 2005). In this regard, the use of entomopathogenic fungi resulting in the infection of as little as 23 % of the indoor mosquitoes reduced the yearly number of bites received by residents by as much as 75 %. Indoor treatment combined with outdoor applications to control mosquito populations at hot spots it is projected that bites by mosquitoes could be lowered by as much as 96 % (Scholte et al., 2004; Scholte et al., 2005). Bittencourt et al. (1997) have evaluated the action of different isolates of Beauveria bassiana and Metarhizium anisopliae fungi on distinct stages of Beauveria microplus, proving their in vitro pathogenicity to this tick species. The entomopathogenic action of Beauveria bassiana has also been demonstrated for other tick species such as Rhipicephalus sanguineus (Monteiro, 1997), Amblyomma cajennense and Boophilus decoloratus (Kaaya and Hassan, 2000). According to Kaaya and Hassan (2000), the use of entomopathogenic fungi to control ticks may reduce the frequency of chemical acaricide use and the need for treatment for tickborne diseases. These authors also conclude that mycopesticides are safer for the environment than conventional acaricides. 10. Solid & Diphasic production technologies The genus Beauveria is a parasite of a great number of arthropods, occurring in more than 200 species of insects and acaridae. These entomopathogenic fungi may occur in enzootic and epizootic forms in field or produced in vitro through fermentative processes (Alves, 1998). Solid State fermentation (SSF) may be defined as the growth of microorganisms in solid substrates in the absence of free water. The free water is found in the complexes form in the interior of a solid matrix (Lonsane et al., 1985; Pandey et al., 2001; Soccol and Vandenberghe, 2003). Solid State fermentation may be classified by the function of the solid phase; it can serve only as a support for the growth of microorganisms and be inert for nutritional purposes and in such case the nutritive sources necessary for the growth of microorganisms are adsorbed by the support. The solid phase may be the support and at the same time the substrate for fermentation. In this case, the support gives also the nutrients required for the growth of microorganisms (Brand et al., 2000). Solid State

13 P. Saranraj/Indo Asian Journal of Multidisciplinary Research (IAJMR), 3(2): fermentation shows advantages for the production of spores in short period of time, due to its simplicity in comparison with submerged cultivation. To make the production of fungal spores process at semi-industrial scale viable, it is necessary to obtain an ideal, cheap and highly productive culture media, which maintain morphological, pathogenically and virulogically characteristics. These are several studies on the efficient utilization of agro-industrial residues with value addition (Soccol and Vandenberghe, 2003; Soccol, 1994; Pandey et al., 2001). The residues could be utilized as substrates and support for the production of citric acid (Vandenberghe, 1999); biological detoxification of coffee husk for the production of animal feed (Brand et al., 2000), edible mushrooms (Leifa et al., 2000), enzymes and ethanol; reducing in this way environmental pollution problem that the disposal of this residues may cause (Pandey et al., 2001). Diverse raw materials have been tested for the production of entomopathogenic fungi, such as caupi, sorgo, broad bean, beans, cassava bagasse, rye flour, cassava flour, different types of rice and residues such as sugar - cane bagasse enriched with cane syrup and torula residues, or still refused potatoes are utilized (Burtet et al., 1997; Soccol et al., 2003; Vilas Boas et al., 1996; Calderon et al., 1995). With high carbohydrates, proteins and significant amounts of salts and vitamins, potato has a high nutritional value (Trindade, 1994). Production of adequate quantities of a good quality inoculum is an essential component of the biocontrol programme. The production of entomopathogens may be taken up by the following methods based on the quantity of the product desired: 1) relatively small quantities of the inoculum for laboratory experimentation and field testing during the development of mycopesticide and 2) development of a basic production system for large - scale production by following the labour intensive and economically viable methods for relatively small size markets. China (Feng et al., 2004) and America (Alves and Pereira, 1989) is supplier of fungal pathogens by this method in sufficient quantities for niche markets in their immediate area. Development of simple and reliable production system follows the basic multiplication procedures of submerged liquid fermentation for the production of blastospores, which are short lived and hydrophilic (Romback, 1989) or solid state fermentation (Rousson et al., 1983) for the production of aerial conidia. However, the most viable mass production technologies include making use of a diphasic strategy in which the fungal inoculum is produced in liquid culture, which is further utilized for inoculating the solid substrates for conidia production (Burges and Hussey, 1981). The insect infection by fungal pathogens occurs through four successive steps. They are contacts between the host and fungal propagules, attachment and germination of propagules, penetration of cuticle or gut wall with subsequent invasion of host tissue and organ and finally death of host by physical blockage of the gut, trachea, circulatory systems, histolysis and toxin production. After the death of the host, saprophytic development of fungus is necessary for the completion of pathogenic cycle. A fungus, unlike other microbials does not require ingestion for infection in the host- Infection through mouth parts, and orifice, digestive and genital tracts have also been reported (Ferron, 2008). The fungal pathogenesis begins with adhesion of conidia to the cuticle of host followed by germination of conidia which penetrates the cuticle through germ tube. The germ tube passes through the integument of insect. Finally, the fungus develops inside the body of host which results in death of the host insect. Under suitable environmental conditions, death is followed by external sporulation of fungus (Moore and Prior, 2006). According to Moore et al. (2000), fungal spores are living organisms and their viability diminishes with time depending on environmental conditions. It is therefore essential to determine the best substrate for spore production and their viability. Previous studies by Kutywayo et al. (2005) revealed that the three

14 P. Saranraj/Indo Asian Journal of Multidisciplinary Research (IAJMR), 3(2): isolates were unique and had potential as biocontrol agents. The author also determined the suitable temperature for spore production as 28 C. 11. Blastospore production of Beauveria bassiana Blastospores are produced during the fermentation process in commercial production of spores where as aerial spores are produced on conidiogenous cells on the infected insects. However the pathogenicity of blastospores and aerial spores is same. The death of insect may result due to non - availability of nutrients, invasion of organs by fungus and toxicosis due to toxins produced by Beauveria bassiana. After the death of the insect, fungus grows saprophytically inside the body of the insects and produces metabolites that may not allow other competing microbes to grow in the cadaver. It reproduces sexually in soils throughout the world and asexually in a variety of insect hosts. In its asexual form it produces spores known as conidia which are wind dispersed. Once they are released they may land upon another insect host, or once again return to the soil where they reproduce sexually retaining the properties which make it an effective pest control, and preventing the qualities which cause it to be harmful to beneficial insects (Boucias and Pendland, 2008). Blastospore production using liquid culture fermentation is vegetative fungal propagules that are the preferred mode of growth for many entomopathogens in the haemocoel of infected insects (Shimuzu et al., 1993; Sieglaff et al., 1997; Vestergaard et al., 1999; Askary et al., 1999). Yeast - like growth allows the fungus better access to the nutrients within the insect. Numerous entomopathogens of the genera Beanveria can be induced to grow in a 'yeast - like' fashion in submerged liquid culture. Blastospore based mycoinsecticides are currently produced commercially by Beauveria bassiana. The impact of nutrition on conidial yields for various fungal entomopathogens in liquid culture was found to be significant (Vega et al., 2003). Poly Ethylene Glycol incorporation in the media increased the blastospores and curtailed the mycelial pellet development (Sree Ramakumar et al., 2005). The optimization of glycerol and erithritol in the conidia increases germination and increase spore longevity of blastospore, in addition to conferring greater osmotic tolerance. The Beauveria bassiana should be included in the list of versatile deuteromycetes that store carbohydrates, including glycogen and the polyols mannitol, erythritol, glycerol and arabitol (Bidochka et al., 1990; Hallsworth and Magan, 1995; Faria and Wraight, 2007). Glycerol, erythritol, arabitol and manniiol accumulate in fungal cells at low level. Intracellular accumulation of these polyols reduces cytoplasrnic activity and yet does not disrupt enzyme structure and function, thus allowing metabolic activity to continue during periods of low water availability (Beever and Laracy, 1986; Van Eck et al., 1993). Humphreys et al. (1989) grew the entomopathogenic fungus in submerged liquid culture on glucose and polyethylene glycol - adjusted media of differential water activities. They recorded increase in yield of blastospores of fed batch liquid culture of Beauveria bassiana when water activity of the nutrient feed was reduced by the addition of 2.4 MPEG. According to Vega et al. (2009), the highest spore yields of Beauveria bassiana in liquid concentration of 36 g L -1 and a C: N ratio of 10: 1 using sucrose and casamino acid. CSL contains water (46 %), proteins (47 %), amino acids, minerals, vitamins, reducing sugars, organic acids, enzymes, fat and elemental nutrients (White and Johnson, 2003). These constituents can be readily assimilated into normal cell metabolism. The blastospore production of Metarhizium flavoviride Mfl89 was based on sucrose and brewer's yeast, with a C: N ratio of 1: 6 (Issaly et al., 2005). 12. Formulations of Beauveria bassiana The development of a suitable formulation was essential to the successful utilization of commercial mycoinsecticides (Daoust et al., 1983). For example, many formulations can affect the conidial viability resulting in a short shelf life (Moore and Prior, 1993). There is a need for careful assessment of

15 P. Saranraj/Indo Asian Journal of Multidisciplinary Research (IAJMR), 3(2): the compatibility of formulation components with conidia prior to their use in formulations (Daoust et al., 1983). Therefore, one of the first steps in developing a mycoinsecticide formulation was to evaluate the effects of its components on conidial viability to select products compatible with fungal conidia. The development of fungal pathogen formulation depends on fungal strains, mass production ability and appropriate climate region (Butt et al., 2001). The most important factors limiting the use of fungi as an insecticide were solar ultraviolet radiation, temperature, humidity and their ability on spreading on the surface (Stathers et al., 1993). Formulating pathogens in oil enhances their infectivity compared to conventional water - based formulations (Agudelo and Falcon, 1983; Prior et al., 1988; Bateman et al., 1993). Knudsen et al. (1990) formulated the Beauveria bassiana mycelium in granules of sodium alginate with and without the addition of ground wheat. After five months of storage at room temperature, the fungi with most spore production came from the granules with wheat, with conidia per granule. These, once placed on seedlings of wheat infested with Schizaphis graminum Rondani, caused the death of three to forty - four percent of aphis, against zero percent in the control. In general, temperature and moisture content, or the humidity of the storage atmosphere is the major factors which influence conidial longevity (Hong et al., 1997). Hedgecock et al. (1995) studied the influence of moisture content on temperature tolerance and storage of Metarhizium anisopliae var. acridum in oil formulation and the results demonstrated that viability declined due to high temperatures and high moisture contents. Drying the conidia with silica gel greatly improved high temperature tolerance (McClatchie et al., 1994). The optimal moisture content for dried conidia storage was found to be 4 to 5 % and a range of mineral oils proved satisfactory for dried conidia storage (Moore et al., 1996). Less moisture content than 4 to 5 % may give better results but it is difficult to achieve. Suspo - emulsions can be defined as heterogeneous formulations consisting of a stable dispersion of active ingredients in the form of solid particles and of fine globules in a continuous water phase combinations (GCPF, 1994). They are relatively new to the agricultural market and have a great potential for formulation and application of mycoinsecticides for pest control. They can be sprayed by very low volume/controlled droplet application techniques still allow the use of conventional hydraulic sprayers and nozzles and water - the cheapest and most readily available carrier liquid for pesticides (Alves et al., 1998). In the field, efficiency of entomopathogens depends up on virulency towards target insect, coverage and persistence on target site. However, major constraints for successful use of such bioagents are their short shelf - life and dependability on the prevailing environmental conditions (Kaur et al., 1999). The foregoing problem can largely be overcome by developing suitable formulation technology. The performance and shelf - life can be improved by adding suitable ingredients that may act as nutrient, adhesive or wettable agents. Xutrilite products Inc., Buena parts. California., U.S.A were the first company in U.S.A to develop both dust and wettable powder formulations of Beauveria bassiana for research purpose (Dunn and Mechalas, 1963). Scientists of USSR also developed dust formulation of this fungus as boverin using inert materials like talc or perlite, kaolin, bentonite, starch etc., (Ignoffo et al., 2009). Pereira and Roberts (1991) reported that corn starch with oil formulation produced more conidia from each gram of incorporated mycelia while alginate formulation could protect the fungus better from artificial solar radiation as compared to corn starch oil. The liquid formulations were prepared by supplementing polymers which increased the spore longevity, viability thereby the shelf - life of the organism is increased. The studies on liquid formulation are detailed hereunder. Addition of certain polymers in growth media is one of the various techniques through which mycelia pellet formation can be decreased by encouraging diffuse mycelia growth or formation of tiny hyphal fragments or blastospores for liquid formulation (Bidochka et al., 1990). Kleepspies and Zimmermann (1992) have also obtained increased blastospore

16 P. Saranraj/Indo Asian Journal of Multidisciplinary Research (IAJMR), 3(2): production and reduced pellet formation of Metarhizium anisopliae (Metschn.) Sorokin using PEG 200. Tween 80 and high or low ph. Inch and Trinci (1987) and Humphreys et al. (1989) reported that the addition of PEG 200 suppressed the formation of pellets in liquid cultures of certain entomopathogenic fungi having commercial value. Knudsen et al. (1991) reported that conidia production of Beauveria bassiana was very fast in alginate pellets with polyethylene glycol 8000 coated wheat bran as compared to uncoated pellets. Geetha and Balaraman (2001) reported that PEG (2 %) favoured both higher biomass and blastospores in the case of Beauveria bassiana. Poly Ethylene Glycol at 6 per cent concentration in Sabouraud's Dextrose Agar influenced both quality and quantity of the biomass of Hirsutella thompsonii (non - synnematous) and Hirsutella thompsonii var. Synnematosa (synnematous) fungi in submerged culture (Sreeramakumar et al., 2005). Efficacy of Beauveria bassiana combined with various stickers or spreaders revealed very high percentage of mortality of Dicladispa armigera using Tween - 80 (Puzari and Hazarika, 1991). Use of two formulations of mineral oil (Emulsiflable concentrate and emulsion concentrate) containing Beauveria bassiana in the laboratory at 26 C and 70 per cent relative humidity resulted in 77.5 and 100 per cent mortality, respectively as compared to 38 per cent caused by fungus alone at 16 days after treatment (Batista et al., 1994). Inglish et al. (1996) investigated the efficacy of two formulations (oil and water) and two bait substrates (Lettuce and bran containing Beauveria bassiana) against the nymphs of Metarhizium sanguinipes. Based on their experiment they reported superiority of oil formulations over water formulations; while no differences in mortality was observed between lettuce and bran substrates. Formulation of conidia of the Beauveria bassiana in paraffin oil or dried powder showed greater percentage of germination of the sample stored in dry conditions as compared to oil formulation of different temperature viz., 10 C, 20 C, 30 C, 40 C and 50 C. Smith et al. (1999) also tested aggregation phremone in the vegetable fat pellets (hydrogenated rapeseed oil) containing Beauveria bassiana as formulation against Prostephenus truncates under laboratory. The investigation on stability of the formulation sodium alginate and pregelatinized corn starch at different temperatures for 120 days revealed the suitability of pregelatinized corn starch for the formulation with mycelia of Beauveria bassiana (Marques et al., 1999). The use of formulations containing Beauveria bassiana is an eco-friendly approach, especially due to proper understanding of problems due to indiscriminate use of insecticides in many countries in the last environmental hazards, insect resistance to insecticides, sustainability in crop productive, pesticide free organic food and maintenance of biodiversity. 13. Agricultural importance of Beauveria bassiana Agricultural pests continue to be a major problem, responsible for tremendous losses in productivity. Traditionally, chemical pesticides such as DDT and endosulfan have been used to kill unwanted insects. The use of chemical pesticides, however, has resulted in numerous problems. Many insects develop resistance to chemical poisons making these compounds less effective and therefore required in higher concentrations. Extensive application of chemicals into the environment often has deleterious effects on non - target organisms including beneficial insects such as pollinators and natural predators of the target pest. Finally, chemical pesticides display significant health risks to workers who are exposed to the chemicals in the fields as well as to consumers who purchase food products with residual pesticides. Thus, there is great interest in alternatives to chemical pesticides. The use of biological pesticides such as entomopathogenic fungi is growing in popularity because it is able to alleviate many of the concerns associated with chemical poisons. First, entomopathogenic fungi are found ubiquitously in the soil throughout the world, therefore they

17 P. Saranraj/Indo Asian Journal of Multidisciplinary Research (IAJMR), 3(2): would not be considered as introduced organisms into the environment. Second, although Beauveria bassiana is considered a broad - spectrum insect pathogen, strains can be developed that are more hosts specific. With research into pathogenicity and strain specificity, it is anticipated that fungal biological control agents can be selected to target specific insect pest. Entomopathogenic fungi are effective and environmentally safe biological control agents that can be used against many important pest species in both agriculture and forestry because they are safe for animals, plants and environment (Chandler et al., 2000; Shah and Pell, 2003; Goettel et al., 2015; Gokce and Er, 2005). Entomopathogenic fungi differ from other insect pathogens since they are able to infect through the host s integument, therefore ingestion is unnecessary and infection is not limited to chewing insects. Therefore, they are unique to control insect pests which feed by sucking plant or animal fluid (St Leger and Roberts, 1997). Entomopathogenic fungal species belong to Beauveria genus attack many insect pests worldwide and species within the genus range from the ubiquitous insect pathogen such as Beauveria bassiana to rare species. However, the entomopathogenic life - style is dominant (Glare, 2014; Glare et al., 2008; Sevim et al., 2010). A total of six species were described within this genus and they were designated as Beauveria bassiana, Beauveria bassiana cf. Clade C, Beauveria brongniartii, Beauveria caledonica, Beauveria vermiconia and Beauveria amorpha (Glare and Inwood, 2008; Glare and Inwood, 2004; Glare, 2014; Rehner and Buckley, 2015; Sevim et al., 2010). Among these species, Beauveria bassiana is the most studied one and remarkable effort were spent to develop microbial control agent using this species. Moreover, the most widely used species available commercially is Beauveria bassiana (Meyling and Eilenberg, 2007; Goettel et al., 2015). The entomopathogenic fungus Beauveria bassiana is extensively used for the control of many important pests of various crops around the world and it was tested on different target insects (Campbell et al., 1985; Leathers and Gupta, 1993; Padmaja and Kaur, 2001; Todorova et al., 2002; Tafoya et al., 2004; Sevim et al., 2010). There are extensive efforts to develop Beauveria as a biological agent. Beauveria has been examined as a potential biological control agent of Ocneridia volxemi. A species of grasshopper, Ocneridia volxemi is one of the most destructive pests of cereals crops in Algeria (Bounechada and Doumandji, 2004). Beauveria is also being examined as method to control the citrus rust mite, Phyllocoptruta oleivora, a citrus crop pest of South America (Alves et al., 2005). One of the most destructive pests being targeted by application of Beauveria control is the coffee berry borer (Hypothenemus hampei), which is endemic to most coffee growing regions and results in upto 40 % losses of the crop. Hypothenemus hampei is an agricultural pest responsible for hundreds of millions of dollars in losses by coffee growers each year (Posada et al., 2004). Beauveria was studied around the world as an effective control agent of coffee berry borer including research facilities found in Honduras, Brazil, Mexico and India (Fernandez, 1985; Haraprasad, 2001). Due to the illegalization of some pesticides including enosulfan; Columbia is an example of a country that utilizes Beauveria against this pest (Cruz et al., 2005). Beauveria bassiana as well as Metarhizium anisopliae are under investigation and show promise for the control of the tobacco spider mite. The tobacco spider mite is one of several species of mites belonging to the genus Tetranychus. Found throughout the United States Tetranychus mites are responsible for the destruction of crops ranging from fruits and vegetables to cotton and decorative plants. Studies showed that the treatment of miteinfected tomato plants with conidia of these entomopathogens greatly reduced the number of mites on the treated plants as compared to untreated plants (Wekesa et al., 2005). Dirlbek et al. (1989) observed slightly better results when Boverol (Beauveria bassiana) 0.3 per cent in combination with delta methrin 2.5

18 P. Saranraj/Indo Asian Journal of Multidisciplinary Research (IAJMR), 3(2): per cent against Trialeurodes vaporarionim while good reduction in pest population resulted when methidathion 40 wp was added. The fungus Beauveria bassiana was effective against Ostrinia nubilalis and the damage caused by the larvae to plant and ears reduced by 50 per cent as compared to the control (Yashugina, 1970). Soil application of Beauveria bassiana and Paecilomyces farinosus, resulted in significant reduction in population of Leptinotarsa decemlineata (Bajan et al., 1973). Beauveria 1.32 to 1.8 kg ha -1 mixed with sevin 0.14 kg ha -1 or kg ha -1 provided 58.1 to 75.5 and 73.3 to 86.3 per cent: control Carpocapsa pomonella and Hoplocampa testudinea, respectively (Prieditis and Rituma, 1974). Use of parasitoid Trichogramma sp., the microbial pathogen Bacillus thuringiensis and Beauveria bassiana along with insecticides trichlorophon (Chlorofos) against Mamestra brassicae, Pieris brassicae and Plutella xylostella resulted in increase in yield of cabbage by 6 to 7 per cent (Garnaga, 1975). Three application of low doses of both Boverin (Beauveria bassiana) and trichlorophon (Chlorofos) on egg plants produced excellent control of Leptinotarsa decemlineata throughout the season, which resulted in substantial increase in yield. The Beauveria. bassiana was effective against Nilapawata 4 10 to 5 10 conidia ml -1. The fungus produced per cent mortality 3 weeks after application (Rombach, 1989). The dry mycelium of Beauveria 200 and 2000 g ha -1 and the ha -1 had significant control over Nilaparvata lugens (Aguda et al., 1987; Pham et al., 1994). Purwar and Sachan (2005) studied the impact of different isolate such as Pantnagar isolates and IMTECH strains of Beauveria bassiana and Metarhizium anisopliae on Spilarctia iitura and Spilarctia obliqua. Uma Maheswara Rao et al. (2006) also studied the impact of Beauveria bassiana on Spilarctia litura in relation to different temperatures. 14. Conclusion From the present review, it was concluded that the various formulation of entomopathogenic fungi Beauveria bassiana was highly effective against various insect pests which causes heavy economic loss to the agricultural crops when compared to the commercial synthetic insecticides. The entomopathogenic fungi Beauveria bassiana also reduces the larval population and crop damage caused by target pests and increases the yield of agricultural crops particularly vegetable crops. Application of entomopathogenic fungi Beauveria bassiana in agricultural fields for the control of insect larvae and pests was cost effective, increases the yield of agricultural products, minimizes the usage of chemical pesticides and prevent the environment from the pesticide pollution. 15. References 1) Agastino Bassi Beauveria bassiana and its effect on agricultural crops. Part I, Teoria. Orcesi, Lodi, pg: ) Aguda, R.M., M. C. Rombach and B. M. Shepard Suppression of populations of the Brown Plant Hopper, Nilaparvata lugens (Stal) (Horn: Delphacidae) in field cages by entomogenous fungi (Deuteromycotina) on rice in Korea. Journal of Applied Entomology, 104: ) Agudelo, F and L. A. Falcon Mass production, infectivity and field application studies with the entomogenous fungus Paecilomyces farinosus. Journal of Invertebrate Pathology, 42: ) Ainsworth, G. C Agostino Bassi, Nature, 177: ) Akbar, W., J. C. Lord, J. R. Nechols and R. W. Howard Diatomaceous earth increases the efficacy of Beauveria bassiana against Tribolium castaneum larvae and increases conidia attachment. Journal of Economical Entomology,97:

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20 P. Saranraj/Indo Asian Journal of Multidisciplinary Research (IAJMR), 3(2): ) Bateman, R. P., M. Carey, D. Moore and C. Prior The enhanced infectivity of Metarhizium flavoviride in oil formulations to desert locusts at low humidities. Annals of Applied Biology, 122: ) Batista, F. A, A. E.F. Leitao, M. E. Sato and L. G. Leite Effect of association of Beauveria bassiana with mineral oil on the mortality of Cosmopolites sordidus Gennar (Coleoptera: Curculionidae). Bioscience Research, 23: ) Beever, R. E and E.P. Laracy Osmotic adjustment in the filamentous fungus Aspergillus nidulans. Journal of Bacteriology, 168: ) Beilharz, V. C., D. G. Parberry and H. J. Swart Dodine: A selective agent for certain soil fungi. Transactions of the British MycologicalSociety,79: ) Beisher, L Microbiology in practice: Self instructional laboratory course. Harper Collins Pub. Inc., New York, pp ) Benz, G Environment, In: J. R. Fuuxa and Y. Tanada. (Eds.). Epizootiology of Insect Diseases. Wiley and Sons, New York, pp ) Bergvinson, D and S. Garcia Lara Genetic approaches to reducing losses of stored grain to insects and diseases. Current Opinions in Plant Biology, 7: ) Bidochka, M. J, M. A. Mc Donald, R. J. Leger and D. W. Roberts Differentiation of species and strains of entomopathogenic fungi by random amplification of polymorphic DNA (RAPD). Current Genetics, 25: ) Bidochka, M. J., A. M. Kamp and W. Gam Insect pathologic fungi: from genes to populations. In: Fungal pathology. Ed, Kronstad J. W.: Kluwer Academic Publishers, Dordrecht. 35) Bidochka, M. J., N. H. Low and G. G. Khachatourians Carbohydrate storage in the entomopathogenic fungus Beauveria bassiana. Applied Environmental Microbiology, 56: ) Bidochka, M. J., R. J. St. Leger and D. W. Roberts Mechanisms of Deuteromycete fungal infections in grasshoppers and locusts: An overview. In: Microbial Control of Grasshoppers and Locusts. Memois of the Entomological Society of Canada. (Eds.) M.S. Goettel and D.L. Johnson. 171: ) Bing, L. A and L. C. Lewis Endophytic Beauveria bassiana (Balsamo) Vuillemin in corn: the influence of the plant stage and Ostrrinia nubilalis (Hubner). Biocontrol Science and Technology, 2: ) Bittencourt, V. R. E. P., S. L. F. S. Peralva, E. C. Viegas and S. B. Alves Avaliação dos efeitos do contato de Beauveria bassiana (Bals.) Vuill. com ovos e larvas de Boophilus microplus (Canestrini, 1887) (Acari: Ixodidae). Reviews of Parasitology and Veterinary, 5: ) Bittencourt, V.R.E.P., E. J. Souza, S.L.F.S. Peralva, A. G. Mascarenhas and S. B. Alves Avaliação da eficácia in vitro de dois isolados do fungo entomopatogênico Beauveria bassiana em fêmeas ingurgitadas de Boophilus microplus. Rev Bras Parasitol Vet., 6: ) Blanford, S., B. H. Chan, N. Jenkins, D. Sim, R. J. Turner, A. F. Read and M. B. Thomas Fungal pathogen reduces potential for malaria transmission. Science, 308: ) Boucias, D. G., J. C. Pendland and J. P. Latge Non - specific factors involved in attachment of entomopathogenic Deuteromycetes to Host Insect Cuticle. Applied Environmental Microbiology,54: ) Boucias, D. G and J. C. Pendland Principles of Insect Pathology. Kluwer Academic Publisher, Boston, Massachusetts. 43) Bounechada, M and S. E. Doumandji Effect of Ocneridia volxemi Bolivar (Pamphaginae, Orthoptera) hoppers and adults by Beauveria

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23 P. Saranraj/Indo Asian Journal of Multidisciplinary Research (IAJMR), 3(2): Applied Microbiology and Biotechnology, 33: ) Dunn, P. H and B. J. Mechalas The potential of Beauveria bassiana (Balsamo) vuillemin as a microbial insecticide. Journal of Insect Pathology, 5: ) Ekesi, S., R. S. Adamu and N. K. Maniania Ovicidal activity of entomopathogenic hyphomycetes to the legume pod borer, Maruca vitrata and the pod sucking bug, Clavigralla tomentosicollis. Crop Protection, 21: ) El Damir, M Effect of growing media and water volume on conidial production of Beauveria bassiana and Metarhizium anisopliae. Journal of Biological Sciences, 6 (2): ) EPA Biopesticide Fact Sheet: Beauveria bassiana strain ATCC (128818). 83) Ettinger, S. J and E. C. Feldman Diseases of the Dog and Cat. In Textbook of Veterinary Internal Medicine, Vol. 1, p W.B. Saunders Co, Philadelphia. 84) Fang, W. G Implication of a regulator of G protein signalling (BbRGS1) in conidiation and conidial thermotolerance of the insect pathogenic fungus Beauveria bassiana. Fems Microbiology Letters, 279: ) Fang, W. G Expressing a fusion protein with protease and chitinase activities increases the virulence of the insect pathogen Beauveria bassiana. Journal of Invertebrate Pathology, 102: ) Farenhorst, M Fungal infection counters insecticide resistance in African malaria mosquitoes. Proceedings of the National Academy of Sciences of the United States of America, 106: ) Fargues, I. F and P. H. Robert Effects of passaging through scarabid hosts on virulence and host specificity of two strains of the entomopathogenic hyphomycete Metarhizium anisopliae. Canadian Journal of Microbiology, 29: ) Fargues, J., A. Ouedraogo, M. Goettel and C. Lomer Effects of temperature, humidity and inoculation method on susceptibility of Schistocerca gregaria to Metarhizium flavoviride. Biocontrol in Science and Technology, 7: ) Faria, M. R and S. P. Wraight Mycoinsecticides and mycoacaricides: a comprehensive list with worldwide coverage and international classification of formulation types. Biological Control, 43: ) Feng, M. G., X. Y. Pu, S. H. Ying and Y. G. Wang Field trials of an oil based emulsifiable formulation of Beauveria bassiana conidia and low application rates of imidacloprid for control of false - eyed leafhopper Empoasca vitis in Southern China. Journal of Crop Protection, 23 (6): ) Feng, M. G., T. J. Paponsk and G. G. Khachatourians Production, formulation and application of the entomopathogenic fungus Beauveria bassiana for insect control. Biocontrol in Science and Technology, 4: ) Feng, M. G., I. B. Johnson and L.P. Kish Virulence of Verticillium lecanii and aphid derived isolate of Beauveria bassiana for six species of cereal infesting aphids. Environmental Entomology, 19: ) Fernandez, P. M. L. R and S. Alves Patogenicidade de Beauveria bassiana (Bals) Vuill a broca do cafe Hypothenemus hampei (Coleoptera), Scolytidae. Ecossistema,10: ) Ferron, P Influence of relative humidity on the development of fungal infection caused by Beauveria bassiana in imagines of Acanthoscelides obtectus (Coleoptera: Bruchidae). Entomophaga, 2: ) Ferron, P Biological control of insect pests by entomogenous fungi. Reviews in Entomology, 23:

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26 P. Saranraj/Indo Asian Journal of Multidisciplinary Research (IAJMR), 3(2): ) Humber, R. A Fungi: identification. In: Lacey L, ed. Manual of techniques in insect pathology. San Diego: Academic Press. Pg: ) Humphreys, A. M., P. Matewele, A. P. J. Trinci and A. T. Gillespie Effects of water activity on morphology, growth and blastospore production of Metarhizium anisopliae, Beauveria bassiana and Paecilomyces farinoscus in batch and fedbatch culture. Mycology Research, 92: ) Hung, C. Y and D. G. Boucias Influence of Beauveria bassiana on the cellular defense response of the beet, Spodoptera exigua. Journal Invertebrate Pathology, 60: ) Hung, S. Y, D. G. Boucias and A. J. Vey Effect of Beauveria bassiana and Candida albicans on the cellular defense response of Spodoptera exigua. Journal Invertebrate Pathology, 61: ) Hunt, D. W. A., J. H. Borden, J. E. Rahe and H. S. Whitney Nutrient mediated germination of Beauveria bassiana conidia on the integument of bark beetle Dendroctonus ponderosae (Coleoptera: Scolytidae). Journal Invertebrate Pathology, 44: ) Ibrahim, Y. B and W. Low Potential of mass production and field efficacy of Isolates of the entomopathogenic fungi Beauveria bassiana & Paecilomyces fumosoroseus on Plutella xylostella. Journal Invertebrate Pathology, 39: ) Ignoffo, C. M and R. F. Anderson Bioinsecticides In: Microbial Technology, Vol. 1: Microbial Processes, 2 nd ed., (Eds.) H. J. Peppler and D. Perlman. Academic Press, New York. pp ) Ignoffo, C. M., C. Garcia, A. Alyoshina and N. V. Lappa Laboratory and field studies with Boverin: A mycoinsecticidal preparation of Beauveria bassiana produced in the Soviet Union. Journal of Economic Entomology, 72: ) Ignoffo, C. M., C. Garcia, M. Kroha and T. L. Couch Use of larvae of Trichoplusia sp. to bioassay conidia of Beauveria bassiana. Journal of Economic Entomology, 75: ) Inch, J. M. M and A. P. J. Trinci Effects of water activity on growth and sporulation of Paecilomyces farinoscus in liquid and solid media. Journal of General Microbiology, 133: ) Inglis, G. D., D. L. Johnson and M. S. Goettel Effect of bait substrate and formulation on infection of grasshopper nymphs by Beauveria bassiana. Biocontrol in Science and Technology, 6: ) Inglis, G. D., G. M. Duke, L. M. Kanchuk and M. S. Goettel nf1uence of oscillating temperatures on the comparative infection and colonization of the migratory grasshopper by Beauveria bassiana and Metarhizium flavoviride. Biological Control, 14: ) Issaly, N., H. Chauveau, F. Aglevor, L. Fergues and A. Durand Influence of nutrient, ph and dissolved oxygen on the production of blastospores in submerged batch culture. Process Biochemistry, 40: ) Jackson, M., M. McGuire, L. Lacey and S. Wraight Liquid culture production of desiccation tolerant blastospores of the bioinsecticidal fungus Paecilomyces fumosoroseus. Mycology Research, 101: ) Jackson, M. A The biotechnology of producing and stabilizing living, microbial biological control agents for insect and weed control. In: Hou, C.T., Shaw, F.J. (Eds.) Biocatalysis and biotechnology: functional foods and industrial products. CRC Press, Boca Raton, pp ) Jackson, M. A and R.J. Bothast Carbon concentration and carbon to nitrogen ratio influence submergedculture conidiation by the potential bioherbicide Colletotrichum truncatum. Applied Environmental Microbiology, 56:

27 P. Saranraj/Indo Asian Journal of Multidisciplinary Research (IAJMR), 3(2): ) James, B., I. Godonou, C. Atcha - Ahowe, I. Glitho, S. Vodouhe, A. Ahanchede, C. Kooyman and G. Goergen Extending integrated pest management to indigenous vegetables. Acta Horticulturae, 752: ) Jeffs, L. B and G. G. Khachatourians Toxic properties of Beauveria pigments on erythrocyte membranes. Toxicon, 35: ) Jeffs, L. B., I. J. Xavier, R. E. Matai and G. G. Khachatourians Relationships between fungal spore morphologies and surface properties for entomopathogenic members of the genera Beauveria, Matarhizium, Paecilomyces, Tolypocladium and Verticillium. Canadian Journal of Microbiology, 45: ) Jenkins, N. E. and C. Prior Growth and formation of true conidia by Metarhizium flavoviride in a simple liquid medium. Mycological Research, 97: ) Jin, K Carboxylate transporter gene JEN1 from the entomopathogenic fungus Beauveria bassiana was involved in conidiation and virulence. Applied and Environmental Microbiology, 76: ) Jin, X., G. E. Harman and A. G. Taylor Conidial biomass and dessication tolerance of Trichoderma harzianum produced at different medium water potentials. Biological Control, 3: ) Joseph C. Gilman A Manual of Soil Fungi. 2 nd Edition, Published by Oxford and IBH Publishing Company, India. p ) Kaaya, G. P and S. Hassan Entomogenous fungi as promising biopesticides for tick control. Experimental and Applied Biology, 24: ) Karr, A., L. Joher and P. Albersheim Polysaccharide - degrading enzymes are unable to attack plant cell walls without prior action by a cell wall modifying enzyme. Plant Physiology, 46: ) Kaur, G., V. Padmaja and V. Sasikala Control of insect pests on cotton through mycopesticide formulations. Indian Journal of Microbiology, 39: ) Keller, S., P. Kessler and C. Schweizer Distribution of insect pathogenic soil fungi in Switzerland with special reference to Beauveria brongniartii and Metarhizium anisopliae. Biocontrol, 48: ) Khachatourians, G. G., E. Valencia and G. S. Miranpuri Beauveria bassiana and other entomopathogenic fungi in the management of insect pests. In: Koul, O., Dhaliwal, G. S. (Eds.), Microbial Biopesticides, Vol. 2. Harwood Academic Publishers, Reading, UK: pp ) Kikankie, K Susceptibility of laboratory colonies of members of the Anopheles gambiae complex to entomopathogenic fungi. M.Sc Thesis, University of the Witwatersrand, Johannesburg. 162) Kirkland, B. H., G. S. Westwood and N. O. Keyhani Pathogenicity of entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae to Ixodidae tick species Dermacentor variabilis, Rhipicephalus sanguineus and Ixodes scapularis. Journal of Medical Entomology, 41: ) Kisla T. A., A. Unjieng, L. Sigler and J. Sugar Medical management of Beauveria bassiana. Cornea,19: ) Kleepspies, R. G and G. Zimmermann Production of blastospores by three strains of Metarhizium anisopliae (Metch.) Sork. In submerged culture. Biocontrol Science and Technology, 2: ) Klingen, I., J. Eilenberg and R. Meadow Effects of farming system, field margins and bait insect on the occurrence of insect pathogenic fungi in soils. Agricultural Ecosystem and Environment, 91:

28 P. Saranraj/Indo Asian Journal of Multidisciplinary Research (IAJMR), 3(2): ) Knudsen, G., R. J. B. Johnson and D. J. Eschen Alginate pellet formulation of a Beauveria bassiana (Fungi: Hypomycetes) isolate pathogenic to cereal aphids. Journal of Economical Entomology, 83: ) Knudsen, G. R., D. J. Eschen, L. M. Dandurand and Z. G. Wang Method to enhance growth and sporulation of palletized biocontrol fungi. Applied Environmental Microbiology, 57: ) Kobayasi, Y and D. Shimizu Cordyceps species from Japan: 4. Bulletin Natural Science, Tokyo, 8: ) Kosir, J. M., J. M. MacPherson and G. G. Khachatourians Genomic analysis of a virulent and a less virulent strain of the entomopathogenic fungus Beauveria bassiana using restriction fragment length polymorphisms. Canadian Journal of Microbiology, 37: ) Ku1a, S. S., N. N. Zade, L. N. Peshkar and S. Yarhade Influence of different culture media on growth and sporulation of Metarhizium anisopliae (Metchiniikoff) Sorokin. Journal of Biological Control, 16: ) Kucera, M and A. Samsinakova Toxins of the entomophagous fungus Beauveria bassiana. Journal of Invertebrate Pathology, 12: ) Kunitz, M Crystalline soya bean trypsin inhibitor. II. General Properties. Journal of Genetics and Physiology, 30: ) Kutywayo V., L. Karanja and G. Oduor Effect of temperature and photoperiod on radial growth of Metarhizium anisopliae and Beauveria bassiana isolate with potential for control of Coffee stem borer. African Crop Science Conference Proceedings, Printed in Uganda, 7: ) Lane, B. S., A. P. J. Trinci and A. T. Gillespie Influence of cultural conditions on the virulence of conidia and blastospores of Beauveria bassiana to the green leafhopper, Nephotettix virescens. Mycological Research, 95: ) Latch, G. C and R. F. Fallon Studies on the use of Metarhizium anisopliae to control Oryctes rhinoceros. Entomophaga, 21: ) Lazzarini G. M., L. H. Rocha and C. Luz Impact of moisture on in vitro germination of Metarhizium anisopliae and Beauveria bassiana and their activity on Triatoma infestans. Mycology Research,110: ) Leathers, T. D and S. C. Gupta Susceptibility of the eastern tent caterpillar (Malacosoma americanum) to the entomogenous fungus Beauveria bassiana. Journal of Invertebrate Pathology, 61: ) Leifa, F., A. Pandey and C. R. Soccol Use of various coffee industry residues for the production of Pleurotus ostreatus in Solid state fermentation. Acta Biotechnology, 20: ) Lewis, L. C., D. J. Bruch, R. D. Gunarson and K. G. Bidne Assessment of plant pathogenicity of endophytic Beauveria bassiana in Bt transgenic and non - transgenic corn. Crop Science, 41: ) Lewis, M. W Uptake of the fluorescent probe FM4-64 by hyphae and haemolymph - derived in vivo hyphal bodies of the entomopathogenic fungus Beauveria bassiana. Microbiology Sgm, 155: ) Li, Z., C. Li, B. Huang and N. Nan Discovery and demonstration of the teleomorph of Beauveria bassiana (Bals) Vuill., an important entomogenous fungus. Chinese Science Bulletin, 46: ) Liu, Z. Y., Z. Q. Liang, A. J. S. Whalley, A. Y. Liu and Y. J. Yao A new species of Beauveria, the anamorph of Cordyceps sobolifera. Fungal Diversity, 7: ) Loc, N. T, V. T. B. Chi, P. Q. Hung, N. T. Nhan and N. D. Thanh Effect of Beauveria bassiana and Metarhizium anisopliae on some natural enemies of rice insect pests. Science and Technology

29 P. Saranraj/Indo Asian Journal of Multidisciplinary Research (IAJMR), 3(2): Journal of Agriculture & Rural Development, 2 (6): ) Lomer, C. J., A. Cherry and D. Denis Systemic Beauveria isolates for control of maize stem borers in Africa. In: Proceedings of the 30 th Annual Meeting of the Society for Invertebrate Pathology, Banff, Canada, p ) Lonsane, B. K., N. P. Ghildyal and S. Budiatman Engineering aspects of Solid state fermentation. Enzyme Microbial Technology, 7: ) Lord J. C., S. Anderson and D. W. Stanley Eicosanoids mediate Manduca sexta cellular response to the fungal pathogen Beauveria bassiana: a role for the lipoxygenase pathway. Arch Insect Biochemistry and Physiology,51: ) Lowry, O. H., N. J. Rosebrough, A. L. Farr and R. J. Randall Protein measurement with Folin phenol reagent. Journal of Biological Chemistry, 193: ) Luz, C and J. Fargues Factors affecting conidial production of Beauveria bassiana from fungus - killed cadavers of Rhodnius prolixus. Journal of Invertebrate Pathology,72: ) Luz, C., I. G. Silva, C. M. Cordeiro and M. S. Tigano Beauveria bassiana (Hyphomycetes) as a possible agent for biological control of Chagas disease vectors. Journal of Medical Entomology, 35: ) Macleod, D. M Investigations on the genera Beauveria Vuill. and Tritirachium Limber. Canadian Journal of Botany, 32: ) Mader, P., A. Fliessbach, D. Dubois, L. Gunst, P. Fried and U. Niggli Soil fertility and biodiversity in organic farming. Science, 296: ) Magdoff, F Concept, components and strategies of soil health in agroecosystems. Journal of Nematology, 33: ) Marques, E. J., S. B. Alves and L. M. R. Marques Effects of the temperature and storage on formulations with mycelia of Beauveria bassiana (Bals.) Yuill and Metarhizium anisopliae (Metschn.). Archives in Biotechnology, 42: ) Marti, G. A., A. Scorsetti, A. C. Siri and C. C. Lastra Isolation of Beauveria bassiana (Bals.) Vuill. (Deuteromycotina: Hyphomycetes) from the Chagas disease vector, Triatoma infestans (Hemiptera: Reduviidae) in Argentina. Mycopathologia,159: ) Maurer, P., Y. Couteaudier, P. A. Girard, P. D. Bridge and G. Riba Genetic diversity of Beauveria bassiana and relatedness to host insect range. Mycology Research, 101: ) Mazet, L., S.Y. Hung and D.G. Boucias Detection of toxic metabolites in the haemolymorph of Beauveria bassiana infected Spodoptra exigua larvae. Experientia, 50: ) McClatchie, G., D. Moore, R. P. Bateman and C. Prior Effect of temperature on the viability of the conidia of Metarhizium xavoviride in oil formulations. Mycology Research, 98: ) Meyling, N. V and J. Eilenberg Ecology of the entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae in temperate agroecosystems: Potential for conservation biological control. Biological Control, 43: ) Mietkiewski, R. T., J. K. Pell and S. K. Clark Influence of pesticide use on the natural occurrence of entomopathogenic fungi in arable soils in the UK; field and laboratory comparisons. Biocontrol Science Technology, 7: ) Miranpuri, O. S and J. P. Khachatourians Infection sites of the entomopathogenic fungus Beauveria bassiana in the larvae of Aedes aegpti. Entomologia Experimentalis Applicata, 59 (1): ) Mohammed, A. K. A., P. P. Sikorowski and J. V. Bell The susceptibility of Heliothis zea larvae to Nomuraea rileyi

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