Disruption of the odorant receptor co-receptor (Orco) reveals its critical role in multiple olfactory behaviors of a cosmopolitan pest

Xuanhao Chen; Shuyuan Yao; Liangqian Xie; Jinyang Li; Lei Xiong; Xiaozhen Yang; Yi Chen; Fang Cao; Qing Hou; Minsheng You; Yuanyuan Liu; Geoff M Gurr; Shijun You

doi:10.1016/j.ibmb.2024.104248

Disruption of the odorant receptor co-receptor (Orco) reveals its critical role in multiple olfactory behaviors of a cosmopolitan pest

Insect Biochem Mol Biol. 2024 Dec 12:177:104248. doi: 10.1016/j.ibmb.2024.104248. Online ahead of print.

Authors

Xuanhao Chen¹, Shuyuan Yao², Liangqian Xie³, Jinyang Li⁴, Lei Xiong⁵, Xiaozhen Yang⁶, Yi Chen⁷, Fang Cao⁸, Qing Hou⁹, Minsheng You¹⁰, Yuanyuan Liu¹¹, Geoff M Gurr¹², Shijun You¹³

Affiliations

¹ State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, College of Life Science, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fuzhou, 350002, China; Ministerial and Provincial Joint Innovation Centre for Safety Production of Cross-Strait Crops, Fujian Agriculture and Forestry University, Fuzhou, 350002, China; Joint International Research Laboratory of Ecological Pest Control, Ministry of Education, Fuzhou, 350002, China. Electronic address: [email protected].
² State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, College of Life Science, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fuzhou, 350002, China; Ministerial and Provincial Joint Innovation Centre for Safety Production of Cross-Strait Crops, Fujian Agriculture and Forestry University, Fuzhou, 350002, China; Joint International Research Laboratory of Ecological Pest Control, Ministry of Education, Fuzhou, 350002, China. Electronic address: [email protected].
³ State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, College of Life Science, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fuzhou, 350002, China; Ministerial and Provincial Joint Innovation Centre for Safety Production of Cross-Strait Crops, Fujian Agriculture and Forestry University, Fuzhou, 350002, China; Joint International Research Laboratory of Ecological Pest Control, Ministry of Education, Fuzhou, 350002, China. Electronic address: [email protected].
⁴ State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, College of Life Science, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fuzhou, 350002, China; Ministerial and Provincial Joint Innovation Centre for Safety Production of Cross-Strait Crops, Fujian Agriculture and Forestry University, Fuzhou, 350002, China; Joint International Research Laboratory of Ecological Pest Control, Ministry of Education, Fuzhou, 350002, China. Electronic address: [email protected].
⁵ Institute of Plant Protection, Jiangxi Academy of Agricultural Sciences, Nanchang, 330200, China. Electronic address: [email protected].
⁶ State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, College of Life Science, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fuzhou, 350002, China; Ministerial and Provincial Joint Innovation Centre for Safety Production of Cross-Strait Crops, Fujian Agriculture and Forestry University, Fuzhou, 350002, China; Joint International Research Laboratory of Ecological Pest Control, Ministry of Education, Fuzhou, 350002, China. Electronic address: [email protected].
⁷ State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, College of Life Science, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fuzhou, 350002, China; Ministerial and Provincial Joint Innovation Centre for Safety Production of Cross-Strait Crops, Fujian Agriculture and Forestry University, Fuzhou, 350002, China; Joint International Research Laboratory of Ecological Pest Control, Ministry of Education, Fuzhou, 350002, China. Electronic address: [email protected].
⁸ State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, College of Life Science, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fuzhou, 350002, China; Ministerial and Provincial Joint Innovation Centre for Safety Production of Cross-Strait Crops, Fujian Agriculture and Forestry University, Fuzhou, 350002, China; Joint International Research Laboratory of Ecological Pest Control, Ministry of Education, Fuzhou, 350002, China. Electronic address: [email protected].
⁹ State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, College of Life Science, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fuzhou, 350002, China; Ministerial and Provincial Joint Innovation Centre for Safety Production of Cross-Strait Crops, Fujian Agriculture and Forestry University, Fuzhou, 350002, China; Joint International Research Laboratory of Ecological Pest Control, Ministry of Education, Fuzhou, 350002, China. Electronic address: [email protected].
¹⁰ State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, College of Life Science, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fuzhou, 350002, China; Ministerial and Provincial Joint Innovation Centre for Safety Production of Cross-Strait Crops, Fujian Agriculture and Forestry University, Fuzhou, 350002, China; Joint International Research Laboratory of Ecological Pest Control, Ministry of Education, Fuzhou, 350002, China. Electronic address: [email protected].
¹¹ State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, College of Life Science, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fuzhou, 350002, China. Electronic address: [email protected].
¹² State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, College of Life Science, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fuzhou, 350002, China; Joint International Research Laboratory of Ecological Pest Control, Ministry of Education, Fuzhou, 350002, China; Gulbali Institute, Charles Sturt University, Orange, NSW, 2800, Australia. Electronic address: [email protected].
¹³ State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, College of Life Science, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fuzhou, 350002, China; Ministerial and Provincial Joint Innovation Centre for Safety Production of Cross-Strait Crops, Fujian Agriculture and Forestry University, Fuzhou, 350002, China; Joint International Research Laboratory of Ecological Pest Control, Ministry of Education, Fuzhou, 350002, China. Electronic address: [email protected].

PMID: 39674517
DOI: 10.1016/j.ibmb.2024.104248

Abstract

The olfactory system of insects plays a pivotal role in multiple, essential activities including feeding, mating, egg laying, and host localization. The capacity of odorant receptors to recognize odor molecules relies on odorant receptor co-receptors forming heterodimers. Here we report the successful engineering a homozygous mutant strain of diamondback moth (Plutella xylostella) in which the odorant receptor co-receptor PxOrco was silenced using CRISPR/Cas9. This insect is a globally important crop pest for which novel control methods are urgently required. Behavioral assays demonstrated that PxOrco knockout males exhibited abolished courtship behaviors, inability to mate, and loss of selective preference for P. xylostella's key sex pheromone components. Whilst female mating behavior and fecundity remained unaffected by PxOrco knockout, oviposition response to leaf alcohol, a key cue for normal oviposition behavior, was lost. Electroantennography revealed drastically reduced responses to sex pheromones and plant volatiles in PxOrco-deficient adults but food location by larvae was unaffected. Moreover, expression analysis of PxOrco-deficient pheromone receptors (PRs) indicated varied regulation patterns, with down-regulation observed in several PRs in both sexes. These findings underscore the critical role of PxOrco in regulating multiple olfactory aspects in P. xylostella, including feeding, mating, and host location. Our study identifies the potential of disrupting the Orco gene in this and other pest species to provide novel avenues for future pest control.

Keywords: Electroantennography; Mating disruption; Odorant receptor co-receptors (orco); Oviposition behavior; Pheromone.