Please wait a minute...
Journal of Integrative Agriculture  2023, Vol. 22 Issue (7): 2162-2172    DOI: 10.1016/j.jia.2022.11.004
Plant Protection Advanced Online Publication | Current Issue | Archive | Adv Search |

Mutagenesis of odorant coreceptor Orco reveals the distinct role of olfaction between sexes in Spodoptera frugiperda

CAO Song1, 2, SUN Dong-dong2, LIU Yang2, YANG Qing1, WANG Gui-rong1, 2#
1 Shenzhen Branch, Guangdong Laboratory for Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of
Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen
518120, P.R.China
2 State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of
Agricultural Sciences, Beijing 100193, P.R.China
Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
摘要  

昆虫的气味受体(Odorant receprotOR)是它们探测和识别与其生存密切相关的外部化学线索的关键。昆虫识别配体的特异性受体与一个广泛存在的气味受体共受体(Odorant receptor coreceptorOrco构成了异聚体复合体。本研究运用CRISPR/Cas9基因敲除技术对我国重大入侵害虫草地贪夜蛾的Orco基因进行了敲除,并揭示了该基因在气味受体调控的嗅觉行为中的重要作用。触角电位结果表明,Orco基因敲除之后,雌雄成虫对8种测试的植物挥发物和两种性信息素的电生理反应均丧失。然而,Orco基因对雌雄虫交配行为的影响却存在明显的差异:雄虫Orco突变体的交配行为完全被干扰而雌虫Orco突变体的交配行为却不受影响。产卵实验结果表明,Orco突变体雌虫的产卵量比野生型雌虫的产卵量减少了24.1%。总之,这些结果表明了Orco是一个干扰草地贪夜蛾正常行为的优良靶标,并为害虫的防治提供了一种可行的方法。



Abstract  

Odorant receptor (OR) is crucial for insects to detect and recognize external chemical cues closely related to their survival.  The insect OR forms a heteromeric complex composed of a ligand-specific receptor and a ubiquitously odorant receptor coreceptor (Orco).  This study used the CRISPR/Cas9 technique to knock out (KO) Orco and reveal its essential role in acting on OR-meditated olfactory behavior in a critical invasive agricultural pest, the fall armyworm (FAW), Spodoptera frugiperda.  Electroantennogram (EAG) results suggested that the Orco mutants of both male and female moths severely reduced their electrophysiological responses to the eight tested plant volatiles and two sex pheromones.  However, the Orco gene played distinct roles in mating behavior between sexes: the mating behavior was fully disrupted in mutated males but not in mutated females.  The oviposition result indicated that the Orco KO females displayed reduced egg laying by 24.1% compared with the mated wild type (WT) females.  Overall, these results strongly suggest that Orco is an excellent target for disrupting FAW’s normal behavior and provides a feasible pest control approach.


Keywords:  Spodoptera frugiperda        Orco        CRISPR/Cas9        EAG        olfactory behavior  
Received: 08 August 2022   Accepted: 27 September 2022
Fund: This work was funded by the National Natural Science Foundation of China (32130089), the China Postdoctoral Science Foundation (2020M680785), and the Shenzhen Science and Technology Program, China (KQTD20180411143628272), the Central Public-interest Scientific Institution Basal Research Fund of Chinese Academy of Agricultural Sciences (CAAS-ZDRW202108), the Special Funds for Science Technology Innovation and Industrial Development of Shenzhen Dapeng New District, China (PT202101-02), and the Agricultural Science and Technology Innovation Program of Chinese Academy of Agricultural Sciences (ASTIP).
About author:  CAO Song, E-mail: csong_onnz@163.com; #Correspondence WANG Gui-rong, E-mail: wangguirong@caas.cn

Cite this article: 

CAO Song, SUN Dong-dong, LIU Yang, YANG Qing, WANG Gui-rong. 2023.

Mutagenesis of odorant coreceptor Orco reveals the distinct role of olfaction between sexes in Spodoptera frugiperda . Journal of Integrative Agriculture, 22(7): 2162-2172.

Baker T C, Nishida R, Roelofs W L. 1981. Close-range attraction of female oriental fruit moths to herbal scent of male hairpencils. Science214, 1359–1361.

Bastin-Héline L, de Fouchier A, Cao S, Koutroumpa F, Caballero-Vidal G, Robakiewicz S, Monsempes C, François M C, Ribeyre T, Maria A, Chertemps T, de Cian A, Walker W B, Wang G, Jacquin-Joly E, Montagné N. 2019. A novel lineage of candidate pheromone receptors for sex communication in moths. eLife8, e49826.

Benton R, Sachse S, Michnick S W, Vosshall L B. 2006. Atypical membrane topology and heteromeric function of Drosophila odorant receptors in vivoPLoS Biology4, e20.

Birch M C, Poppy G M, Baker T C. 1990. Scents and eversible scent structures of male moths. Annual Review of Entomology35, 25–54.

Bober R, Rafaeli A. 2010. Gene-silencing reveals the functional significance of pheromone biosynthesis activating neuropeptide receptor (PBAN-R) in a male moth. Proceedings of the National Academy of Sciences of the United States of America107, 16858–16862.

Cao S, Huang T, Shen J, Liu Y, Wang G. 2020. An orphan pheromone receptor affects the mating behavior of Helicoverpa armigeraFrontiers in Physiology11, 413.

Carroll M J, Schmelz E A, Meagher R L, Teal P E A. 2006. Attraction of Spodoptera frugiperda larvae to volatiles from herbivore-damaged maize seedlings. Journal of Chemical Ecology32, 1911–1924.

Cury K M, Prudhomme B, Gompel N. 2019. A short guide to insect oviposition: When, where and how to lay an egg. Journal of Neurogenetics33, 75–89.

DeGennaro M, McBride C S, Seeholzer L, Nakagawa T, Dennis E J, Goldman C, Jasinskiene N, James A A, Vosshall L B. 2013. orco mutant mosquitoes lose strong preference for humans and are not repelled by volatile DEET. Nature498, 487–491.

Fandino R A, Haverkamp A, Bisch-Knaden S, Zhang J, Bucks S, Nguyen T A T, Schroder K, Werckenthin A, Rybak J, Stengl M, Knaden M, Hansson B S, Grosse-Wilde E. 2019. Mutagenesis of odorant coreceptor Orco fully disrupts foraging but not oviposition behaviors in the hawkmoth Manduca sextaProceedings of the National Academy of Sciences of the United States of America116, 15677–15685.

Fitzpatrick S M, McNeil J N. 1988. Male scent in lepidopteran communication: the role of male pheromone in mating behaviour of Pseudaletia Unipuncta (Haw.) (Lepidoptera: Noctuidae). Memoirs of the Entomological Society of Canada120, 131–151.

Fleischer J, Pregitzer P, Breer H, Krieger J. 2017. Access to the odor world: Olfactory receptors and their role for signal transduction in insects. Cellular and Molecular Life Sciences75, 485–508.

Franco T A, Oliveira D S, Moreira M F, Leal W S, Melo A C. 2016. Silencing the odorant receptor co-receptor RproOrco affects the physiology and behavior of the Chagas disease vector Rhodnius prolixusInsect Biochemistry and Molecular Biology69, 82–90.

Ganiger P C, Yeshwanth H M, Muralimohan K, Vinay N, Kumar A R V, Chandrashekara K. 2018. Occurrence of the new invasive pest, fall armyworm, Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae), in the maize fields of Karnataka, India. Current Science115, 621–623.

Goergen G, Kumar P L, Sankung S B, Togola A, Tamo M. 2016. First report of outbreaks of the fall armyworm Spodoptera frugiperda (J E Smith) (Lepidoptera, Noctuidae), a new alien invasive pest in West and Central Africa. PLoS ONE11, e0165632.

Guo J, Liu X, Liu S, Wei Z, Han W, Guo Y, Dong S. 2020. Functional characterization of sex pheromone receptors in the fall armyworm (Spodoptera frugiperda). Insects11, 193.

Guo M, Ren X, Liu Y, Wang G. 2022. An odorant receptor from the proboscis of the cotton bollworm Helicoverpa armigera (Lepidoptera: Noctuidae) narrowly tuned to indole. Insects13, 385.

Hansson B S, Stensmyr M C. 2011. Evolution of insect olfaction. Neuron72, 698–711.

Hillier N K, Vickers N J. 2004. The role of heliothine hairpencil compounds in female Heliothis virescens (Lepidoptera: Noctuidae) behavior and mate acceptance. Chemical Senses29, 499–511.

Jacquin E, Nagnan P, Frerot B. 1991. Identification of hairpencil secretion from male Mamestra brassicae (L.) (Lepidoptera: Noctuidae) and electroantennogram studies. Journal of Chemical Ecology17, 239–246.

Jiang N, Mo B, Guo H, Yang J, Tang R, Wang C. 2021. Revisiting the sex pheromone of the fall armyworm Spodoptera frugiperda, a new invasive pest in South China. Insect Science29, 865–878.

Kimura T, Honda H. 1999. Identification and possible functions of the hairpencil scent of the yellow peach moth, Conogethes punctiferalis (Guenée) (Lepidoptera: Pyralidae). Applied Entomology and Zoology34, 147–153.

Koutroumpa F A, Monsempes C, François M C, de Cian A, Royer C, Concordet J P, Jacquin-Joly E. 2016. Heritable genome editing with CRISPR/Cas9 induces anosmia in a crop pest moth. Scientific Reports, 6, 29620.

Larsson M C, Domingos A I, Jones W D, Chiappe M E, Amrein H, Vosshall L B. 2004. Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron43, 703–714.

Leal W S. 2013. Odorant reception in insects: Roles of receptors, binding proteins, and degrading enzymes. Annual Review of Entomology58, 373–391.

Li R, Huang L, Dong J, Wang C. 2020. A moth odorant receptor highly expressed in the ovipositor is involved in detecting host-plant volatiles. eLife9, e53706.

Li Y, Zhang J, Chen D, Yang P, Jiang F, Wang X, Kang L. 2016. CRISPR/Cas9 in locusts: successful establishment of an olfactory deficiency line by targeting the mutagenesis of an odorant receptor co-receptor (Orco). Insect Biochemistry and Molecular Biology79, 27–35.

Liu Q, Liu W, Zeng B, Wang G, Hao D, Huang Y. 2017. Deletion of the Bombyx mori odorant receptor co-receptor (BmOrco) impairs olfactory sensitivity in silkworms. Insect Biochemistry and Molecular Biology86, 58–67.

Liu X, Zhang J, Yan Q, Miao C, Han W, Hou W, Yang K, Hansson B S, Peng Y, Guo J, Xu H, Wang C, Dong S, Knaden M. 2020. The molecular basis of host selection in a crucifer-specialized moth. Current Biology30, 4476–4482.

Löfstedt C. 1993. Moth pheromone genetics and evolution. Philosophical Transactions of the Royal Society of London (Series B: Biological Sciences), 340, 167–177.

Montezano D G, Specht A, Sosa-Gómez D R, Roque-Specht V F, Hunt T. 2018. Host plants of Spodoptera frugiperda (Lepidoptera: Noctuidae) in the Americas. African Entomology26, 286–300.

Neuhaus E M, Gisselmann G, Zhang W, Dooley R, Störtkuhl K, Hatt H. 2005. Odorant receptor heterodimerization in the olfactory system of Drosophila melanogasterNature Neuroscience8, 15–17.

Riabinina O, Task D, Marr E, Lin C C, Alford R, O’Brochta D A, Potter C J. 2016. Organization of olfactory centres in the malaria mosquito Anopheles gambiaeNature Communications7, 13010.

Sato K, Pellegrino M, Nakagawa T, Nakagawa T, Vosshall L B, Touhara K. 2008. Insect olfactory receptors are heteromeric ligand-gated ion channels. Nature452, 1002–1006.

Silbering A F, Rytz R, Grosjean Y, Abuin L, Ramdya P, Jefferis G S, Benton R. 2011. Complementary function and integrated wiring of the evolutionarily distinct Drosophila olfactory subsystems. Journal of Neuroscience31, 13357–13375.

Sparks A N. 1979. A review of the biology of the fall armyworm. The Florida Entomologist62, 82–87.

Stengl M. 2010. Pheromone transduction in moths. Frontiers in Cellular Neuroscience4, 133.

Stokstad E. 2017. New crop pest takes Africa at lightning speed. Science56, 473–474.

Suh E, Bohbot J, Zwiebel L J. 2014. Peripheral olfactory signaling in insects. Current Opinion in Insect Science6, 86–92.

Sun X, Hu C, Jia H, Wu Q, Shen X, Zhao S, Jiang Y, Wu K. 2021. Case study on the first immigration of fall armyworm, Spodoptera frugiperda invading into China. Journal of Integrative Agriculture20, 664–672.

Tateishi K, Watanabe T, Nishino H, Mizunami M, Watanabe H. 2022. Silencing the odorant receptor co-receptor impairs olfactory reception in a sensillum-specific manner in the cockroach. iScience25, 104272.

Trible W, Olivos-Cisneros L, McKenzie S K, Saragosti J, Chang N, Matthews B J, Oxley P R, Kronauer D J C. 2017. orco mutagenesis causes loss of antennal lobe glomeruli and impaired social behavior in ants. Cell170, 727–735.

Vosshall L B, Hansson B S. 2011. A unified nomenclature system for the insect olfactory coreceptor. Chemical Senses36, 497–498.

Wang B, Dong W, Li H, D’Onofrio C, Bai P, Chen R, Yang L, Wu J, Wang X, Wang B, Ai D, Knoll W, Pelosi P, Wang G. 2022. Molecular basis of (E)-β-farnesene-mediated aphid location in the predator Eupeodes corollaeCurrent Biology32, 951–962.

Wang C, Zhang S, Guo M, Hou X, Yang B, Wang G. 2022. Optimization of a pheromone lure by analyzing the peripheral coding of sex pheromones of Spodoptera frugiperda in China. Pest Management Science78, 2995–3004.

Wicher D, Schäfer R, Bauernfeind R, Stensmyr M C, Heller R, Heinemann S H, Hansson B S. 2008. Drosophila odorant receptors are both ligand-gated and cyclic-nucleotide-activated cation channels. Nature452, 1007–1011.

Wu K, Shirk P D, Taylor C E, Furlong R B, Shirk B D, Pinheiro D H, Siegfried B D. 2018. CRISPR/Cas9 mediated knockout of the abdominal-A homeotic gene in fall armyworm moth (Spodoptera frugiperda). PLoS ONE13, e0208647.

Wu M, Qi G, Chen H, Ma J, Liu J, Jiang Y, Lee G S, Otuka A, Hu G. 2022. Overseas immigration of fall armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae), invading Korea and Japan in 2019. Insect Science29, 505–520.

Xiao H, Ye X, Xu H, Mei Y, Yang Y, Chen X, Yang Y, Liu T, Yu Y, Yang W, Lu Z, Li F. 2020. The genetic adaptations of fall armyworm Spodoptera frugiperda facilitated its rapid global dispersal and invasion. Molecular Ecology Resources20, 1050–1068.

Yan H, Opachaloemphan C, Mancini G, Yang H, Gallitto M, Mlejnek J, Leibholz A, Haight K, Ghaninia M, Huo L, Perry M, Slone J, Zhou X, Traficante M, Penick C A, Dolezal K, Gokhale K, Stevens K, Fetter-Pruned I, Bonasio R, et al. 2017. An engineered orco mutation produces aberrant social behavior and defective neural development in ants. Cell170, 736–747.

Zhang L, Liu B, Zheng W, Liu C, Zhang D, Zhao S, Li Z, Xu P, Wilson K, Withers A, Jones C M, Smith J A, Chipabika G, Kachigamba D L, Nam K, d’Alençon E, Liu B, Liang X, Jin M, Wu C, et al. 2020. Genetic structure and insecticide resistance characteristics of fall armyworm populations invading China. Molecular Ecology Resources20, 1682–1696.

Zhang R, Gao G, Chen H. 2016. Silencing of the olfactory co-receptor gene in Dendroctonus armandi leads to EAG response declining to major host volatiles. Scientific Reports6, 23136.

Zhang R, Wang B, Grossi G, Falabella P, Liu Y, Yan S, Lu J, Xi J, Wang G. 2017. Molecular basis of alarm pheromone detection in aphids. Current Biology27, 55–61.

Zhao W, Li L, Zhang Y, Liu X, Wei J, Xie Y, Du M, An S. 2018. Calcineurin is required for male sex pheromone biosynthesis and female acceptance. Insect Molecular Biology27, 373–382.

Zhou Y L, Zhu X Q, Gu S H, Cui H H, Guo Y Y, Zhou J J, Zhang Y J. 2014. Silencing in Apolygus lucorum of the olfactory coreceptor Orco gene by RNA interference induces EAG response declining to two putative semiochemicals. Journal of Insect Physiology60, 31–39.

Zhu G, Chereddy S C R R, Howell J L, Palli S R. 2020. Genome editing in the fall armyworm, Spodoptera frugiperda: multiple sgRNA/Cas9 method for identification of knockouts in one generation. Insect Biochemistry and Molecular Biology122, 103373.

Zweerus N L, van Wijk M, Schal C, Groot A T. 2021. Experimental evidence for female mate choice in a noctuid moth. Animal Behaviour179, 1–13.

No related articles found!
No Suggested Reading articles found!