[en] Odorant receptors (ORs) are essential for plant-insect interactions. However, despite the global impacts of Lepidoptera (moths and butterflies) as major herbivores and pollinators, little functional data are available about Lepidoptera ORs involved in plant-volatile detection. Here, we initially characterized the plant-volatile-sensing function(s) of 44 ORs from the cotton bollworm Helicoverpa armigera, and subsequently conducted a large-scale comparative analysis that establishes how most orthologous ORs have functionally diverged among closely related species whereas some rare ORs are functionally conserved. Specifically, our systematic analysis of H. armigera ORs cataloged the wide functional scope of the H. armigera OR repertoire, and also showed that HarmOR42 and its Spodoptera littoralis ortholog are functionally conserved. Pursuing this, we characterized the HarmOR42-orthologous ORs from 11 species across the Glossata suborder and confirmed the HarmOR42 orthologs form a unique OR lineage that has undergone strong purifying selection in Glossata species and whose members are tuned with strong specificity to phenylacetaldehyde, a floral scent component common to most angiosperms. In vivo studies via HarmOR42 knockout support that HarmOR42-related ORs are essential for host-detection by sensing phenylacetaldehyde. Our work also supports that these ORs coevolved with the tube-like proboscis, and has maintained functional stability throughout the long-term coexistence of Lepidoptera with angiosperms. Thus, beyond providing a rich empirical resource for delineating the precise functions of H. armigera ORs, our results enable a comparative analysis of insect ORs that have apparently facilitated and currently sustain the intimate adaptations and ecological interactions among nectar feeding insects and flowering plants.
Disciplines :
Entomology & pest control
Author, co-author :
Guo, Mengbo ✱; State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China ; Guangdong Laboratory for Lingnan Modern Agriculture (Shenzhen Branch), Genome Analysis Laboratory of the Ministry of Agriculture, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China
Du, Lixiao ✱; State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China
Chen, Qiuyan; State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China
Feng, Yilu; State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China
Zhang, Jin; State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China
Zhang, Xiaxuan; State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China
Tian, Ke; State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China
Cao, Song; State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China
Huang, Tianyu ; Université de Liège - ULiège > TERRA Research Centre ; State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China
Jacquin-Joly, Emmanuelle; INRAE, Sorbonne Université, CNRS, IRD, UPEC, Université de Paris, Institute of Ecology and Environmental Sciences of Paris, Versailles, France
Wang, Guirong ; State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China ; Guangdong Laboratory for Lingnan Modern Agriculture (Shenzhen Branch), Genome Analysis Laboratory of the Ministry of Agriculture, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China
Liu, Yang ; State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China
✱ These authors have contributed equally to this work.
Language :
English
Title :
Odorant Receptors for Detecting Flowering Plant Cues Are Functionally Conserved across Moths and Butterflies.
Publication date :
13 April 2021
Journal title :
Molecular Biology and Evolution
ISSN :
0737-4038
eISSN :
1537-1719
Publisher :
Oxford University Press, United States
Volume :
38
Issue :
4
Pages :
1413 - 1427
Peer reviewed :
Peer Reviewed verified by ORBi
Funding text :
We thank Dr Peter C. Gregg (University of New England) for providing valuable suggestions for setting up two-choice olfactometer system; Dr Yidong Wu and Dr Huidong Wang (Nanjing Agricultural University) for offering advices about gene knock-out by using CRISPR-Cas9 system; Dr Hu Li and Dr Xin Zhou (China Agricultural University) and Dr Fangluan Gao (Fujian Agriculture and Forestry University) for providing valuable suggestions for selection pressure analysis; Ms Chunyan Wang for giving assistance insect rearing. This work was funded by National Natural Science Foundation of China (31725023, 31621064, 31861133019 to G.W., and 31672095 to Y.L.), Shenzhen Science and Technology Program (Grant No. KQTD20180411143628272), and the French National Research Agency (ANR-16-CE21-0002-01 to E.J.-J.) and with the support of the International Associated Laboratory for Plant Protection INRA-CAAS. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the article.
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