Entomopathogenic fungi are the key regulators of insect populations and some of them are important biological agents used in integrated pest management strategies. Compared with their ability to become resistant to insecticides, insect pests do not easily become resistant to the infection by entomopathogenic fungi. In this study, we evaluated the mortality and immune response of the serious crop pest Locusta migratoria manilensis after exposure to a new entomopathogenic fungus strain, Metarhizium anisopliae CQMa421. M. anisopliae CQMa421 could effectively infect and kill the L. migratoria adults and nymphs. The locust LT50 under 1 × 108 conidia/mL concentration of M. anisopliae was much lower than that under conidial concentration 1 × 105 conidia/mL (i.e., 6.0 vs. 11.2 and 5.0 vs. 13.8 for adults and nymphs, respectively). The LC50 (log10) of M. anisopliae against locust adults and nymphs after 10 days was 5.2 and 5.6, respectively. Although the number of hemocytes in L. migratoria after exposure to M. anisopliae did not differ with that in the controls, the enzymatic activity of superoxide dismutase (SOD) and prophenoloxidase (ProPO) did differ between the two treatments. The activities of both SOD and ProPO under the M. anisopliae treatment were lower than that in the controls, except for the ProPO activity at 72 h and the SOD activity at 96 h. Further, the expression of the L. migratoria immune-related genes defensin, spaetzle, and attacin differed after exposure to M. anisopliae for 24 h to 96 h. Taken together, this study indicated that infection with M. anisopliae CQMa421 could cause the death of L. migratoria by interacting with the immune responses of the host, demonstrating that this fungal strain of M. anisopliae can be an efficient biocontrol agent against L. migratoria.

Nilaparvata lugens is one of the major pests of rice and results in substantial yield loss every year. Our previous study found that the entomopathogenic fungus Metarhizium anisopliae showed effective potential for controlling this pest. However, the mechanisms underlying M. anisopliae infection of N. lugens are not well known. In the present study, we further examined the transcriptome of N. lugens at 4 h, 8 h, 16 h, and 24 h after M. anisopliae infection by Illumina deep sequencing. In total, 174.17 Gb of data was collected after sequencing, from which 23,398 unigenes were annotated by various databases, including 3694 newly annotated genes. The results showed that there were 246 vs 75, 275 vs 586, 378 vs 1055, and 638 vs 182 up- and downregulated differentially expressed genes (DEGs) at 4 h, 8 h, 16 h, and 24 h after M. anisopliae infection, respectively. The biological functions and associated metabolic processes of these genes were determined with the Clusters of Orthologous Groups (COG), Gene Ontology (GO), and Kyoto Encyclopedia of Genes and Genomes (KEGG) databases. The DEGs data were verified using RT-qPCR. These results indicated that the DEGs during the initial fungal infection appropriately reflected the time course of the response to the fungal infection. Taken together, the results of this study provide new insights into the molecular mechanisms underlying the insect host response to fungal infection, especially during the initial stage of infection, and may improve the potential control strategies for N. lugens.

Entomopathogenic fungi can regulate insect populations and function as crucial biological control agents against insect pests, but their impacts on nontarget microorganisms are poorly understood. In this study, we investigated the potential of the fungal strain Metarhizium anisopliae CQMa421 to control rice planthoppers under field conditions and its effects on rice microbiota. This fungus suppressed rice planthoppers during this period, and its control efficiency was more than 60% 7 days post application and did not significantly differ from that of the chemical treatment except in 2019. Both treatments showed a lower population of rice planthoppers than the controls. After application, M. anisopliae was maintained on rice plants for approximately 14 days, showing a decreasing trend over time. Furthermore, the results showed that the bacterial and fungal richness (operational taxonomic units) and diversity (Shannon index) did not significantly differ between the fungal treatment and the controls after application. The major bacterial taxa of Proteobacteria (including Alphaproteobacteria, Betaproteobacteria, Gammaproteobacteria, and Deltaproteobacteria), Actinobacteria, Bacteroidetes and Cyanobacteria accounted for more than 80% of the bacterial community after fungal application, and the major fungal taxa of Ascomycota (including Eurotiomycetes, Dothideomycetes and Sordariomycetes), and Basidiomycota (including Ustilaginomycetes) represented more than 90% of fungal community. However, the microbial communities of the rice phyllosphere did not significantly change after entomopathogenic agent application, indicating that the indigenous microbial communities may adapt to fungal insecticide application. Taken together, the results suggest that this fungal agent has good potential for rice planthopper control with no substantial effects on rice microbial communities. IMPORTANCE Entomopathogenic fungi may be used as crucial biocontrol agents for the control of insect pests, but few effective fungal strains have been reported for the control of the rice planthopper, a major pest of rice. More importantly, the impacts of fungal insecticide application on nontarget microorganisms have not been well evaluated, especially under field conditions. Therefore, in this study, we investigated the effects of the fungal strain M. anisopliae CQMa421 on rice planthopper populations from 2017 to 2019 and evaluated its potential impacts on the microbiota of rice plants after application. The results suggested that this fungal agent has good potential for use in the control of rice planthoppers with no significant effects on rice microbial communities, representing an alternative strategy for the control of rice pests.