Molecular characterization and functional analysis of cytochrome P450-mediated detoxification CYP302A1 gene involved in host plant adaptation in Spodoptera frugieprda

Muhammad Hafeez; Xiaowei Li; Limin Chen; Farman Ullah; Jun Huang; Zhijun Zhang; Jinming Zhang; Junaid Ali Siddiqui; Shu-Xing Zhou; Xiao-Yun Ren; Muhammad Imran; Mohammed A Assiri; Yonggen Lou; Yaobin Lu

doi:10.3389/fpls.2022.1079442

Molecular characterization and functional analysis of cytochrome P450-mediated detoxification CYP302A1 gene involved in host plant adaptation in Spodoptera frugieprda

Front Plant Sci. 2023 Jan 25:13:1079442. doi: 10.3389/fpls.2022.1079442. eCollection 2022.

Authors

Muhammad Hafeez^{1

2}, Xiaowei Li², Limin Chen^{2

3}, Farman Ullah⁴, Jun Huang¹, Zhijun Zhang², Jinming Zhang², Junaid Ali Siddiqui⁵, Shu-Xing Zhou², Xiao-Yun Ren², Muhammad Imran⁶, Mohammed A Assiri⁶, Yonggen Lou¹, Yaobin Lu²

Affiliations

¹ State Key Laboratory of Rice Biology and Ministry of Agriculture Key Lab of Molecular Biology of Crop Pathogens and Insects, Institute of Insect Sciences, Zhejiang University, Hangzhou, China.
² State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural Sciences, Hangzhou, China.
³ Integrated Plant Protection Center, Lishui Academy of Agricultural and Forestry Sciences, Lishui, China.
⁴ Department of Plant Biosecurity, College of Plant Protection, China Agricultural University, Beijing, China.
⁵ College of Agriculture, College of Tobacco Science, Guizhou University, Guiyang, China.
⁶ Department of Chemistry, Faculty of Science, King Khalid University, Abha, Saudi Arabia.

Abstract

The fall armyworm (FAW) Spodoptera frugiperda is a destructive and polyphagous pest of many essential food crops including maize and rice. The FAW is hard to manage, control, or eradicate, due to its polyphagous nature and voracity of feeding. Here, we report the characterization and functional analysis of the detoxification gene CYP302A1 and how S. frugieprda larvae use a detoxification mechanism to adapt host plants. Results demonstrated that CYP302A1 expression levels were much higher in midgut tissue and the older S. frugiperda larvae. Our current studies revealed the enhanced P450 activity in the midguts of S. frugiperda larvae after exposure to rice plants as compared to corn plants and an artificial diet. Furthermore, higher mortality was observed in PBO treated larvae followed by the exposure of rice plants as compared to the corn plant. The dsRNA-fed larvae showed downregulation of CYP302A1 gene in the midgut. At the same time, higher mortality, reduced larval weight and shorter developmental time was observed in the dsRNA-fed larvae followed by the exposure of rice plant as compared to the corn plant and DEPC-water treated plants as a control. These results concluded that the inducible P450 enzyme system and related genes could provide herbivores with an ecological opportunity to adapt to diverse host plants by utilizing secondary compounds present in their host plants.

Keywords: CYP302a1; P450 detoxification enzyme; RNAi; host adaptation; spodoptera frugiperda.

Grants and funding

This work was supported by the National Natural Science Foundation of China (32272524, the Key R&D Program of Zhejiang Province (2020C02003), the Shanghai Innovation Project for Agricultural Promotion (2019N3- 9), and the Joint Agricultural Project between Pinghu County and Zhejiang Academy of Agricultural Sciences (PH20190002). M.A.A. expresses appreciation to the Deanship of Scientific Research at KKU SA for funding through the research groups program under grant number R.G.P.2/170/43. Project funded by China National Postdoctoral Science foundation (2020M681921) and the Primary Research & Development Plan of Lishui (No. 2021ZDYF10).