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

Long Liu  ¹ , Dong-Huai Wang  ¹ , Chen-Chen Zhao  ¹ , Feng-Ming Yan  ¹ , Chao-Liang Lei  ² , Li-Juan Su  ¹ , Yuan-Chen Zhang  ³ , Qiu-Ying Huang  ² , Qing-Bo Tang  ¹

Affiliations

Affiliations

• ¹ Henan International Laboratory for Green Pest Control; Henan Engineering Laboratory of Pest Biological Control; College of Plant Protection, Henan Agricultural University, Zhengzhou 450002, China.
• ² Hubei Insect Resources Utilization and Sustainable Pest Management Key Laboratory, Huazhong Agricultural University, Wuhan 430070, China.
• ³ Taihang Mountain Forest Pests Observation and Research Station of Henan Province, Anyang 456582, China.

• PMID: 37104842
• DOI: 10.1021/acs.jafc.3c00743

Abstract

As chemical pesticides have caused serious environmental pollution, fungus-based biological control has become a developing alternative to chemical control. Here, we aimed to determine the molecular mechanism underlying how Metarhizium anisopliae facilitated invasive infection. We found that the fungus increased its virulence by downregulating glutathione S-transferase (GST) and superoxide dismutase (SOD) throughout termite bodies. Among 13 fungus-induced microRNAs throughout termite bodies, miR-7885-5p and miR-252b upregulation significantly downregulated several mRNAs in response to toxic substances to increase the fungal virulence [e.g., phosphoenolpyruvate carboxykinase (GTP) and heat shock protein homologue SSE1]. In addition, nanodelivered small interfering RNA of GST and SOD and miR-7885-5p and miR-252b mimics increased the virulence of the fungus. These findings provide new insights into the killing mechanism of entomopathogens and their utilization of the host miRNA machinery to reduce host defenses, laying the groundwork to enhance virulence of biocontrol agents for green pest management.

Keywords: entomopathogenic fungi; green pest management; nanomaterials; small RNAs; termite.