Transcriptomics Reveals the Killing Mechanism by Which Entomopathogenic Fungi Manipulate the RNA Expression Profiles of Termites and Provides Inspiration for Green Pest Management

Liu, Long; Wang, Dong-Huai; Zhao, Chenchen; Yan, Fei; Lei, Chaoliang; Su, Lihe; Zhang, Yuanchen; Huang, Qiuying; Tang, Qing-Bo

doi:10.1021/acs.jafc.3c00743

Cited by 8 publications

(5 citation statements)

References 57 publications

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“…Some fungi have been shown to actively enhance their virulence by reducing the expression of detoxification genes in their insect hosts. This manipulation could be a strategy employed by the pathogen to disrupt the insect's conventional detoxification mechanisms, making it more susceptible to infection and facilitating the success of fungal invasion [67]. A similar downregulation of detoxification genes has been observed in other insect-fungi interactions, such as in Drosophila melanogaster [22].…”

Section: Discussionmentioning

confidence: 68%

Altered Gene Expression of the Parasitoid Pteromalus puparum after Entomopathogenic Fungus Beauveria bassiana Infection

Yang,

Li,

Yang

et al. 2023

IJMS

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Both parasitoids and entomopathogenic fungi are becoming increasingly crucial for managing pest populations. Therefore, it is essential to carefully consider the potential impact of entomopathogenic fungi on parasitoids due to their widespread pathogenicity and the possible overlap between these biological control tools during field applications. However, despite their importance, little research has been conducted on the pathogenicity of entomopathogenic fungi on parasitoids. In our study, we aimed to address this knowledge gap by investigating the interaction between the well-known entomopathogenic fungus Beauveria bassiana, and the pupal endoparasitoid Pteromalus puparum. Our results demonstrated that the presence of B. bassiana significantly affected the survival rates of P. puparum under laboratory conditions. The pathogenicity of B. bassiana on P. puparum was dose- and time-dependent, as determined via through surface spraying or oral ingestion. RNA-Seq analysis revealed that the immune system plays a primary and crucial role in defending against B. bassiana. Notably, several upregulated differentially expressed genes (DEGs) involved in the Toll and IMD pathways, which are key components of the insect immune system, and antimicrobial peptides were rapidly induced during both the early and late stages of infection. In contrast, a majority of genes involved in the activation of prophenoloxidase and antioxidant mechanisms were downregulated. Additionally, we identified downregulated DEGs related to cuticle formation, olfactory mechanisms, and detoxification processes. In summary, our study provides valuable insights into the interactions between P. puparum and B. bassiana, shedding light on the changes in gene expression during fungal infection. These findings have significant implications for the development of more effective and sustainable strategies for pest management in agriculture.

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Section: Discussionmentioning

confidence: 68%

Altered Gene Expression of the Parasitoid Pteromalus puparum after Entomopathogenic Fungus Beauveria bassiana Infection

Yang,

Li,

Yang

et al. 2023

IJMS

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“…It is shown that Metarhizium anisopliae increased its virulence by downregulation of glutathione Stransferase (GST) and superoxide dismutase (SOD) throughout termite bodies. 60 Our transcriptome data reveled that some GST genes (BBA_04201, BBA_07754, BBA_03339, and BBA_07410) were significantly downregulated in the ΔBbSre1 strain; however, its virulence was significantly decreased. We speculated that downregulated GSTs could not counteract effects of reduced growth, decreased adaptations to low-oxygen and oxidative stress, as well as the decreased lipid drops with reduced TAG storage and cell membrane homeostasis on the decreased fungal virulence.…”

Section: Discussionmentioning

confidence: 82%

“…Moreover, some virulence-associated genes, e.g., Chi3 , Bly5 , Mad1 , Hyd2 , and Fre2 , ,− were dramatically downregulated in the Δ BbSre1 strain as direct targets verified with EMSA, demonstrating a virulence regulator. It is shown that Metarhizium anisopliae increased its virulence by downregulation of glutathione S-transferase (GST) and superoxide dismutase (SOD) throughout termite bodies . Our transcriptome data reveled that some GST genes (BBA_04201, BBA_07754, BBA_03339, and BBA_07410) were significantly downregulated in the Δ BbSre1 strain; however, its virulence was significantly decreased.…”

Section: Discussionmentioning

confidence: 86%

Sterol Regulatory Element-Binding Protein, BbSre1, Controls Oxidative Stress Response, Peroxisome Division, and Lipid Homeostasis in an Insect Fungal Pathogen

Zhao

Gao

et al. 2023

J. Agric. Food Chem.

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Sterol regulatory element-binding protein, Sre1, regulates sterol biosynthesis, lipid metabolism, hypoxia adaptation, and virulence in some fungi, even though its roles are varied in fungal species. However, few studies report its other functions in fungi. Here, we report novel roles of Sre1 homolog, BbSre1, in the insect fungal pathogen, Beauveria bassiana, that regulates oxidative stress response, peroxisome division, and redox homeostasis. The gene disruption stain showed increased sensitivity to oxidative stress, which was in line with oxidative stress-induced-BbSre1 nuclear import and control of antioxidant and detoxification-involved genes. The gene mutation also inhibited peroxisome division, affected redox homeostasis, and impaired lipid/fatty acid metabolism and sterol biosynthesis, which was verified by downregulation of their associated genes. These data broaden our understanding of role of Sre1, which regulates peroxisome division, antioxidant, and detoxification-involved genes for control of redox homeostasis and oxidative stress response that links to lipid/fatty acid metabolism and sterol biosynthesis.

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“…Insect detoxification and antioxidant systems often function in conjunction with the immune system, which effectively reduces the risk of toxins and reactive oxygen species (ROS) during host–pathogen interactions (Syazwan et al, 2021). It has been verified that the fungus Metarhizium anisopliae increased its virulence by downregulating glutathione S‐transferase ( GST ) and superoxide dismutase ( SOD ) throughout termite bodies (Liu, Wang, et al, 2023).…”

Section: Introductionmentioning

confidence: 99%

Different strategies between queens and workers against fungal pathogens in the termite Reticulitermes chinensis

Dong,

Niu,

Bai

et al. 2024

Ecosphere

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Social insects are prone to pathogen infection because of high exposure rates from social interactions. However, it remains unclear whether queens have enhanced pathogen resistance, because reproduction is largely confined to queens. Here, we used a natural host–pathogen system, the subterranean termite Reticulitermes chinensis and the entomopathogenic fungus Metarhizium anisopliae, to investigate the differences in allogrooming, locomotion, and immune gene expression between queens and workers against pathogen infection. We found that fungal infection significantly reduced survival in both queens and workers. Infected queens received significantly more grooming time from sanitary nestmates than infected workers, but they returned much less grooming time to sanitary nestmates than infected workers. Infection resulted in a reduction in the average locomotion speed and distance of queens but had no effect on worker locomotion. Infection resulted in upregulated expression of two immune genes (termicin and transferrin), two antioxidant genes (CAT and SOD), and phosphate genes CYP450 in queens but not in workers. Our results indicated that eusocial termites evolved strategies that prioritize the reproductive castes' welfare in defending against the pathogen infection to ensure continued reproduction and colony persistence.

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Transcriptomics Reveals the Killing Mechanism by Which Entomopathogenic Fungi Manipulate the RNA Expression Profiles of Termites and Provides Inspiration for Green Pest Management

Cited by 8 publications

References 57 publications

Altered Gene Expression of the Parasitoid Pteromalus puparum after Entomopathogenic Fungus Beauveria bassiana Infection

Altered Gene Expression of the Parasitoid Pteromalus puparum after Entomopathogenic Fungus Beauveria bassiana Infection

Sterol Regulatory Element-Binding Protein, BbSre1, Controls Oxidative Stress Response, Peroxisome Division, and Lipid Homeostasis in an Insect Fungal Pathogen

Different strategies between queens and workers against fungal pathogens in the termite Reticulitermes chinensis

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