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This review examines the symbiotic, evolutionary, proteomic and genetic basis for a group of fungi that occupy a specialized niche as insect pathogens as well as endophytes. We focus primarily on species in the genera Metarhizium and Beauveria, traditionally recognized as insect pathogenic fungi but are also found as plant symbionts. Phylogenetic evidence suggests that these fungi are more closely related to grass endophytes and diverged from that lineage ca. 100 MYA. We explore how the dual life cycles of these fungi as insect pathogens and endophytes are coupled. We discuss the evolution of insect pathogenesis while maintaining an endophytic lifestyle and provide examples of genes that may be involved in the transition toward insect pathogenicity. That is, some genes for insect pathogenesis may have been co-opted from genes involved in endophytic colonization. Other genes may be multifunctional and serve in both lifestyle capacities. We suggest that their evolution as insect pathogens allowed them to effectively barter a specialized nitrogen source (i.e. insects) with host plants for photosynthate. These ubiquitous fungi may play an important role as plant growth promoters and have a potential reservoir of secondary metabolites.

Insecticidal fungi represent a promising alternative to chemical pesticides for disease vector control. Here, we show that the pathogenic fungus Beauveria bassiana exports a microRNA-like RNA (bba-milR1) that hijacks the host RNA-interference machinery in mosquito cells by binding to Argonaute 1 (AGO1). bba-milR1 is highly expressed during fungal penetration of the mosquito integument, and suppresses host immunity by silencing expression of the mosquito Toll receptor ligand Spätzle 4 (Spz4). Later, upon entering the hemocoel, bba-milR1 expression is decreased, which avoids induction of the host proteinase CLIPB9 that activates the melanization response. Thus, our results indicate that the pathogen deploys a cross-kingdom small-RNA effector that attenuates host immunity and facilitates infection. Fungi that infect insects can potentially be exploited for disease vector control. Here the authors show that the fungus Beauveria bassiana exports a microRNA-like RNA into mosquito cells that modulates host immunity by suppressing expression of Toll receptor ligand Spätzle 4.

Terrestrial plants can harbor endophytic fungi that may induce changes in plant physiology that in turn affect interactions with herbivorous insects. We evaluated whether the application of entomopathogenic fungi Beauveria bassiana and Metarhizium brunneum to soybean seeds could become endophytic and affect interactions with soybean aphid (Aphis glycines Matsumura). It was found that A. glycines population sizes increased on plants with M. brunneum (strain F52) seed inoculum, but no significant effects were shown with analogous treatments with B. bassiana (strain GHA). Fungi recovered from soybean plant tissues indicate that endophytism was established, and that B. bassiana was more prevalent. Metarhizium brunneum was only recovered from stems, but B. bassiana was recovered from stems and leaves. This work confirms that some entomopathogenic fungi can be endophytic in soybean, however, some of these fungi may have a negative effect on the plants by increasing susceptibility of soybean to A. glycines. We also used DNA sequence data to identify species of Metarhizium obtained from agricultural fields in Iowa. Phylogenetic analyses, based on DNA sequence data, found that all isolates were Metarhizium robertsii, which is consistent with past studies indicating a cosmopolitan distribution and wide host range for this species. These results are important for understanding the dynamics of implementing environmentally sustainable measures for the control of pest insects.

Metarhizium anisopliae (Metschnikoff) Sorokin and Beauveria bassiana (Balsamo) Vuillemin are entomopathogenic fungi commonly used in microbial control of arthropods. In this study, we evaluated the insecticidal potential of six isolates of B . bassiana (BIITAC10.3.3, BIITAC6.2.2, and BIITAC8.1.5) and M . anisopliae (MIITAC11.3.4, MIITAC6.2.2, and MIITAC6.4.2) from Cameroon, against the banana aphid Pentalonia nigronervosa Coquerel, the vector of the banana bunchy top virus (BBTV). Pathogenicity tests were initially conducted using B . bassiana and M . anisopliae isolates at a concentration of 3.2 × 10 6 conidia/ml on P . nigronervosa adults sourced from four agroecologies in Cameroon. Four isolates (BIITAC6.2.2, BIITAC10.3.3, BIITAC8.1.5, and MIITAC6.2.2) were highly pathogenic, causing greater than 75% aphid mortality in all populations. A significant decrease in aphid fecundity was observed with BIITAC6.2.2, MIITAC6.2.2, and BIITAC10.3.3. These three isolates were in a test of a series of four fungal concentrations (3.2 × 10 1 , 3.2 × 10 2 , 3.2 × 10 4 , and 3.2 × 10 6 conidia/ml). produced LC 50 of 1.31 × 10 1 and 3.12 × 10 −2 for BIITAC10.3.3 and MIITAC6.2.2, respectively. MIITAC6.2.2 had the lowest LC 90 (1.55 × 10 3 ). Our results strongly support the continued development of biopesticides based on one or more of the three fungal entomopathogens for the control of banana aphids as a component of an Integrated Pest Management (IPM) strategy for the reduction of the prevalence and transmission of BBTV under field conditions.

The current study aimed to isolate Beauveria brongniartii conidia from forest soils, identify the fungus, and evaluate its effectiveness on the eggs, larvae, pupae, and adults of Spodoptera litura. Insect mortality rates were recorded every 3, 6, 9, and 12 days. The identification of entomopathogenic fungi was carried out using molecular techniques, including PCR, DNA sequencing, and molecular markers, to detect species-specific 18 S rDNA genetic sequences, all performed under aseptic conditions. The results indicated that higher conidia concentrations (2.7 × 10 conidia/mL) exhibited greater virulence, with eggs showing a mortality rate of 98.66%, followed by larvae 96%, adults 90.66%, and pupae 77.33% after 12 days. Probit analysis revealed minimal LC and LC values: eggs (5.5 × 10 ; 1.0 × 10 spores/mL), larvae (8.2 × 10 ; 1.2 × 10 spores/mL), pupae (9.6 × 10 ; 7.3 × 10 spores/mL), and adults (1.0 × 10 ; 2.0 × 10 spores/mL). The total hemocyte counts and detailed observational results revealed that B. brongniartii induces cellular breakdown and cell lysis in S. litura larvae by producing enzymes that degrade the cuticle and cell membranes. Earthworm bioindicator studies showed minimal effects from B. brongniartii conidia compared to controls, while chemical treatments resulted in 96% mortality at 100 ppm. Histopathological examinations revealed no significant differences in gut tissue between earthworms treated with fungal conidia and those in the control group, unlike the substantial damage caused by chemical treatments. Biochemical analysis revealed significant alterations in enzyme activity, including reduced levels of phosphatase and catalase, as well as increased levels of lipid peroxides and superoxide dismutase. This study highlights the effectiveness of B. brongniartii in controlling S. litura, demonstrating its potential as a viable biocontrol agent and promoting eco-friendly alternatives to chemical pesticides, with no risk to non-target species or the environment.

Beauveria is a cosmopolitan anamorphic genus of arthropod pathogens that includes the agronomically important species, B. bassiana and B. brongniartii, which are used as mycoinsecticides for the biological control of pest insects. Recent phylogenetic evidence demonstrates that Beauveria is monophyletic within the Cordycipitaceae (Hypocreales), and both B. bassiana and B. brongniartii have been linked developmentally and phylogenetically to Cordyceps species. Despite recent interest in the genetic diversity and molecular ecology of Beauveria, particularly as it relates to their role as pathogens of insects in natural and agricultural environments, the genus has not received critical taxonomic review for several decades. A multilocus phylogeny of Beauveria based on partial sequences of RPB1, RPB2, TEF and the nuclear intergenic region, Bloc, is presented and used to assess diversity within the genus and to evaluate species concepts and their taxonomic status. B. bassiana and B. brongniartii, both which represent species complexes and which heretofore have lacked type specimens, are redescribed and types are proposed. In addition six new species are described including B. varroae and B. kipukae, which form a biphyletic, morphologically cryptic sister lineage to B. bassiana, B. pseudobassiana, which also is morphologically similar to but phylogenetically distant from B. bassiana, B. asiatica and B. australis, which are sister lineages to B. brongniartii, and B. sungii, an Asian species that is linked to an undetermined species of Cordyceps. The combination B. amorpha is validly published and an epitype is designated.

Beauveria bassiana (Bal.-Criv.) is an important entomopathogenic fungus being used for the management of various agricultural pests worldwide. However, all strains of B. bassiana may not be effective against whitefly, Bemisia tabaci , or other pests, and strains show diversity in their growth, sporulation, virulence features, and overall bioefficacy. Thus, to select the most effective strain, a comprehensive way needs to be devised. We studied the diversity among the 102 strains of B. bassiana isolated from 19 insect species based on their physiological features, virulence, and molecular phylogeny, to identify promising ones for the management of B. tabaci . Strains showed diversity in mycelial growth, conidial production, and their virulence against B. tabaci nymphs. The highest nymphal mortality (2nd and 3rd instar) was recorded with MTCC-4511 (95.1%), MTCC-6289 (93.8%), and MTCC-4565 (89.9%) at a concentration of 1 × 10 6 conidia ml −1 under polyhouse conditions. The highest bioefficacy index (BI) was in MTCC-4511 (78.3%), MTCC-4565 (68.2%), and MTCC-4543 (62.1%). MTCC-4511, MTCC-4565, and MTCC-4543 clustered with positive loading of eigenvalues for the first two principal components and the cluster analysis also corresponded well with PCA (principal component analysis) (nymphal mortality and BI). The molecular phylogeny could not draw any distinct relationship between physiological features, the virulence of B. bassiana strains with the host and location. The BI, PCA, and square Euclidean distance cluster were found the most useful tools for selecting potential entomopathogenic strains. The selected strains could be utilized for the management of the B. tabaci nymphal population in the field through the development of effective formulations. Key points • 102 B. bassiana strains showed diversity in growth and virulence against B. tabaci. • Bioefficacy index, PCA, and SED group are efficient tools for selecting potential strains. • MTCC-4511, 4565, and 4543 chosen as the most virulent strains to kill whitefly nymphs.

Entomopathogenic fungi and their insect hosts represent a model system for examining invertebrate-pathogen coevolutionary selection processes. Here we report the characterization of competing components of an arms race consisting of insect protective antimicrobial compounds and evolving fungal mechanisms of detoxification. The insect pathogenic fungus Beauveria bassiana has a remarkably wide host range; however, some insects are resistant to fungal infection. Among resistant insects is the tenebrionid beetle Tribolium castaneum that produces benzoquinone-containing defensive secretions. Reduced fungal germination and growth was seen in media containing T. castaneum dichloromethane extracts or synthetic benzoquinone. In response to benzoquinone exposure, the fungus expresses a 1,4-benzoquinone oxidoreductase, BbbqrA , induced >40-fold. Gene knockout mutants ( ΔBbbqrA ) showed increased growth inhibition, whereas B. bassiana overexpressing BbbqrA ( Bb::BbbqrA ᴼ) displayed increased resistance to benzoquinone compared with wild type. Increased benzoquinone reductase activity was detected in wild-type cells exposed to benzoquinone and in the overexpression strain. Heterologous expression and purification of BbBqrA in Escherichia coli confirmed NAD(P)H-dependent benzoquinone reductase activity. The ΔBbbqrA strain showed decreased virulence toward T. castaneum , whereas overexpression of BbbqrA increased mortality versus T. castaneum . No change in virulence was seen for the ΔBbbqrA or Bb::BbbqrA ᴼ strains when tested against the greater wax moth Galleria mellonella or the beetle Sitophilus oryzae , neither of which produce significant amounts of cuticular quinones. The observation that artificial overexpression of BbbqrA results in increased virulence only toward quinone-secreting insects implies the lack of strong selection or current failure of B. bassiana to counteradapt to this particular host defense throughout evolution. Although entomopathogenic fungi and their invertebrate hosts share a >300 million year co-evolutionary history, little is known concerning the biochemical and genetic basis of insect defensive tactics and the countermeasures evolved and evolving by the pathogen to thwart these defenses. Our results provide a molecular mechanism to help explain why some insects are more resistant to broad host-range entomopathogenic fungi. We identify beetle cuticular secretions and a fungal detoxifying enzyme as components of an arms race between insects and the fungal pathogen, suggesting an evolving role for the quinone reductase enzyme as a specific virulence factor for host quinone detoxification. As races have winners and losers, this paper captures a snapshot where the host is leading the race.

Siderophores are essential for iron uptake under iron-limiting conditions and are involved in fungal niche competition and pathogenicity via siderophore-iron transporters (SITs)-mediated uptake of specific substrates. However, the details of many SIT-mediated substrates in fungal colonization of hosts remain limited. Here, we identify two SITs, BbMirA and BbMirB, in the entomopathogenic fungus Beauveria bassiana , which are highly expressed during colonization of insect hemocoel. The two SITs have complementary functions in siderophore-iron uptake in vitro , but only BbMirB dominantly mediates the uptake of a derivative of dimerumic acid in vivo and plays a critical role in the pathogenic process via disturbing insect immune defense responses. These findings provide insights into the mechanisms of SITs mediating the interaction of fungal pathogens with their hosts.

Inoculating plants with entomopathogenic fungi may influence plant nutrient uptake and growth, and herbivore performance. Knowledge is limited concerning the effects of this symbiosis on higher trophic levels. We examined how fungal treatment of faba bean seeds with the entomopathogenic fungus Beauveria bassiana influenced the choice-behavior and development of the aphid parasitoid Aphidius colemani. We also sampled plant material for analysis of changes in expression of genes related to plant defense pathways. While parasitoids were compatible with plants inoculated with B. bassiana initially (66 vs. 65% parasitization on inoculated and control plants, respectively; similar development times of parasitoids: 9.2 days), the emergence of adult parasitoids originating from aphids on fungus treated plants was significantly lower (67 vs. 76%, respectively). We also found that the defense response changed, similar to induced systemic resistance, when plants were treated with B. bassiana, similarly to what has been found for other plant symbiotic microorganisms. These novel findings show that although the application of entomopathogenic fungi to plants can alter the plants' defense against herbivores, it may also have an impact on beneficial insects, so their function and use should be evaluated on a case-by-case basis.