Genomic and transcriptomic analysis unveils population evolution and development of pesticide resistance in fall armyworm Spodoptera frugiperda
Furong Gui1,12, Tianming Lan2,9, Yue Zhao1, Wei Guo3,15, Yang Dong1,12, Dongming Fang2, Huan Liu2,9, Haimeng Li2, Hongli Wang2, Ruoshi Hao12, Xiaofang Cheng5, Yahong Li16, Pengcheng Yang4, Sunil Kumar Sahu2, Yaping Chen1, Le Cheng7, Shuqi He1, Ping Liu5, Guangyi Fan6, Haorong Lu8,10, Guohai Hu8,10, Wei Dong2, Bin Chen1, Yuan Jiang18, Yongwei Zhang18, Hanhong Xu17, Fei Lin17, Bernard Slipper19, Alisa Postma19, Matthew Jackson19, Birhan Addisie Abate20, Kassahun Tesfaye20,21, Aschalew Lemma Demie20, Meseret Destaw Bayeleygne20, Dawit Tesfaye Degefu22, Feng Chen5, Paul K. Kuria23, Zachary M. Kinyua23, Tong-Xian Liu13, Huanming Yang10,11, Fangneng Huang1,4(), Xin Liu2,10(), Jun Sheng1,12(), Le Kang3,4,15()
1. State Key Laboratory for Conservation and Utilization of Bioresources in Yunnan, Yunnan Agricultural University, Kunming 650201, China 2. State Key Laboratory of Agricultural Genomics, BGI-Shenzhen, Shenzhen 518083, China 3. State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China 4. Beijing Institutes of Life Science, Chinese Academy of Sciences, Beijing 100101, China 5. MGI, BGI-Shenzhen, Shenzhen 518083, China 6. BGI-Qingdao, BGI-Shenzhen, Qingdao 266555, China 7. BGI-Yunnan, No. 389 Haiyuan Road, High-tech Development Zone, Kunming 650106, China 8. China National GeneBank, Jinsha Road, Dapeng New District, Shenzhen 518120, China 9. Department of Biology, University of Copenhagen, 2100 Copenhagen, Denmark 10. Guangdong Provincial Key Laboratory of Genome Read and Write, BGI-Shenzhen, Shenzhen 518120, China 11. Guangdong Provincial Academician Workstation of BGI Synthetic Genomics, BGI-Shenzhen, Shenzhen 518120, China 12. Yunnan Plateau Characteristic Agriculture Industry Research Institute, Kunming 650201, China 13. College of Plant Health and Medicine, Qingdao Agricultural University, Qingdao 266109, China 14. Department of Entomology, Louisiana State University Agricultural Center, Baton Rouge, LA 70803, USA 15. CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, Beijing 100101, China 16. Yunnan Plant Protection and Quarantine Station, Kunming 650034, China 17. State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, South China Agricultural University, Guangzhou 510642, China 18. BGI-Americas, One Broadway, 14th Floor, Cambridge, MA 02142, USA 19. Department of Biochemistry, Genetics and Microbiology, Forestry and Agricultural Biotechnology Institute, University of Pretoria, Pretoria, South Africa 20. Ethiopian Biotechnology Institute, Addis Ababa, Ethiopia 21. College of Natural Science, Addis Ababa University, Addis Ababa, Ethiopia 22. Melkassa Agricultural Research Center, Ethiopian Institute of Agricultural Research, Melkassa, Addis Ababa, Ethiopia 23. Kenya Agricultural and Livestock Research Organization, P.O. Box 57811, Nairobi 00800, Kenya
The fall armyworm (FAW), Spodoptera frugiperda, is a destructive pest native to America and has recently become an invasive insect pest in China. Because of its rapid spread and great risks in China, understanding of FAW genetic background and pesticide resistance is urgent and essential to develop effective management strategies. Here, we assembled a chromosome-level genome of a male FAW (SFynMstLFR) and compared resequencing results of the populations from America, Africa, and China. Strain identification of 163 individuals collected from America, Africa and China showed that both C and R strains were found in the American populations, while only C strain was found in the Chinese and African populations. Moreover, population genomics analysis showed that populations from Africa and China have close relationship with significantly genetic differentiation from American populations. Taken together, FAWs invaded into China were most likely originated from Africa. Comparative genomics analysis displayed that the cytochrome p450 gene family is extremely expanded to 425 members in FAW, of which 283 genes are specific to FAW. Treatments of Chinese populations with twenty-three pesticides showed the variant patterns of transcriptome profiles, and several detoxification genes such as AOX, UGT and GST specially responded to the pesticides. These findings will be useful in developing effective strategies for management of FAW in China and other invaded areas.
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