|
|
|
|
|
| Expression profiles and functional prediction of ionotropic receptors in Asian corn borer, Ostrinia furnacalis (Lepidoptera: Crambidae) |
| ZHANG Yu1, 2, YANG Bin2, YU Jie2, PANG Bao-ping1, WANG Gui-rong2, 3 |
1 Research Center for Grassland Entomology, Inner Mongolia Agricultural University, Hohhot 010018, 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
3 Guangdong Laboratory of Lingnan Modern Agriculture (Shenzhen Branch)/Genome Analysis Laboratory of the Ministry of Agriculture and Rural Affairs/Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen 518116, P.R.China
|
|
|
|
|
Abstract Genes involved in chemosensation are essential for odorant-mediated insect behaviors. Odorant receptors (ORs) bind and respond to pheromones and plant volatiles, regulating insect behaviors such as mating and host-plant selection, while ionotropic receptors (IRs), which are present at lower levels in insects than ORs, influence ion channels, especially in agricultural pests. Asian corn borer, Ostrinia furnacalis, is the main pest of maize that causes huge economic losses in Asia. Twenty-one OfurIRs have been identified, but none has been characterized. In this study, tissue-specific expression profiling, phylogenetic analysis, and electroantennography (EAG) analysis were applied to characterize the evolution, expression, and the potential function of OfurIRs. It was found that 20 OfurIRs were highly expressed in the antennae, except for OfurIR75p3, whereas 10 and nine OfurIRs were highly expressed in the proboscis and genitalia, respectively, indicating that these OfurIRs were functionally associated with feeding and oviposition. EAG results showed that seven acids elicited responses in the antennae of O. furnacalis and that 2-oxopentanoic acid displayed a significant female-biased response. Combined with the phylogenetic analysis, 10 OfurIRs in clade 4 were roughly predicted to be candidate receptors for 2-oxopentanoic acid and other tested acids. These results provide basic information about OfurIRs and may help advance the knolwedge on the olfactory system of O. furnacalis.
|
|
Received: 06 June 2020
Accepted: 12 September 2020
|
Fund: This work was supported by the National Natural Science Foundation of China (31701859, 31725023 and 31621064).
|
| About author:
ZHANG Yu, E-mail: zhangyu15326050747@163.com; Correspondence PANG Bao-ping, E-mail: pangbp@imau.edu.cn; YANG Bin, Tel: +86-10-62810689, E-mail: byang@ippcass.cn |
Cite this article:
ZHANG Yu, YANG Bin, YU Jie, PANG Bao-ping, WANG Gui-rong.
2022.
Expression profiles and functional prediction of ionotropic receptors in Asian corn borer, Ostrinia furnacalis (Lepidoptera: Crambidae). Journal of Integrative Agriculture, 21(2): 474-485.
|
Abuin L, Bargeton B, Ulbrich M H, Isacoff E Y, Kellenberger S, Benton R. 2011. Functional architecture of olfactory ionotropic glutamate receptors. Neuron, 69, 44–60.
Abuin L, Prieto-Godino L L, Pan H, Gutierrez C, Huang L, Jin R, Benton R. 2019. In vivo assembly and trafficking of olfactory ionotropic receptors. BMC Biology, 17, 34.
Afidchao M M, Musters C, de Snoo G R. 2013. Asian corn borer (ACB) and non-ACB pests in GM corn (Zea mays L.) in the Philippines. Pest Management Science, 69, 792–801.
Ai M, Blais S, Park J Y, Min S, Neubert T A, Suh G S B. 2013. Ionotropic glutamate receptors IR64a and IR8a form a functional odorant receptor complex in vivo in Drosophila. The Journal of Neuroscience, 33, 10741–10749.
Bai P H, Wang H M, Liu B S, Li M, Liu B M, Gu X S, Tang R. 2020. Botanical volatiles selection in mediating electrophysiological responses and reproductive behaviors for the fall webworm moth Hyphantria cunea. Frontiers in Physiology, 11, 486.
Bengtsson J M, Trona F, Montagné N, Anfora G, Ignell R, Witzgall P, Jacquin-Joly E. 2012. Putative chemosensory receptors of the codling moth, Cydia pomonella, identified by antennal transcriptome analysis. PLoS ONE, 7, e31620.
Benton R, Sachse S, Michnick S W, Vosshall L B. 2006. Atypical membrane topology and heteromeric function of Drosophila odorant receptors in vivo. PLoS Biology, 4, e20.
Benton R, Vannice K S, Gomez-Diaz C, Vosshall L B. 2009. Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila. Cell, 136, 149–162.
de Bruyne M, Baker T C. 2018. Odor detection in insects: Volatile codes. Journal of Chemical Ecology, 34, 882–897.
Budelli G, Ni L, Berciu C, van Giesen L, Knecht Z A, Chang E C, Kaminski B, Silbering A F, Samuel A, Klein M, Benton R, Nicastro D, Garrity P A. 2019. Ionotropic receptors specify the morphogenesis of phasic sensors controlling rapid thermal preference in Drosophila. Neuron, 101, 738–747.
Cao S, Liu Y, Guo M B, Wang G R. 2016. A conserved odorant receptor tuned to floral volatiles in three Heliothinae species. PLoS ONE, 11, e0155029.
Chen Y, Amrein H. 2017. Ionotropic receptors mediate Drosophila oviposition preference through sour gustatory receptor neurons. Current Biology, 27, 2741–2750.
Croset V, Rytz R, Cummins S F, Budd A, Brawand D, Kaessmann H, Gibson T J, Benton R. 2010. Ancient protostome origin of chemosensory ionotropic glutamate receptors and the evolution of insect taste and olfaction. PLoS Genetics, 6, e1001064.
Depetris-Chauvin A, Galagovsky D, Grosjean Y. 2015. Chemicals and chemoreceptors: Ecologically relevant signals driving behavior in Drosophila. Frontiers in Ecology & Evolution, 3, 41.
Dobritsa A A, van der Goes, van Naters W, Warr C G, Steinbrecht R A, Carlson J R. 2003. Integrating the molecular and cellular basis of odor coding in the Drosophila antenna. Neuron, 37, 827–841.
Du L X, Zhao X C, Liang X Z, Gao X W, Liu Y, Wang G R. 2018. Identification of candidate chemosensory genes in Mythimna separata by transcriptomic analysis. BMC Genomics, 19, 518.
Enjin A, Zaharieva E E, Frank D D, Mansourian S, Suh G S, Gallio M, Stensmyr M C. 2016. Humidity sensing in Drosophila. Current Biology, 26, 1352–1358.
Fox A N, Pitts R J, Zwiebel L J. 2002. A cluster of candidate odorant receptors from the malaria vector mosquito, Anopheles gambiae. Chemical Senses, 27, 453–459.
Ganguly A, Pang L, Duong V K, Lee A, Schoniger H, Varady E, Dahanukar A. 2017. A molecular and cellular context-dependent role for Ir76b in detection of amino acid taste. Cell Reports, 18, 737–750.
van Giesen L, Garrity P A. 2017. More than meets the IR: The expanding roles of variant ionotropic glutamate receptors in sensing odor, taste, temperature and moisture. F1000Research, 6, 1753.
Grosjean Y, Rytz R, Farine J P, Abuin L, Cortot J, Jefferis G S X E, Benton R. 2011. An olfactory receptor for food-derived odours promotes male courtship in Drosophila. Nature, 478, 236–240.
Guo L, Li G Q. 2009. Olfactory perception of oviposition-deterring fatty acids and their methyl esters by the Asian corn borer, Ostrinia furnacalis. Journal of Insect Science, 9, 1–9.
Healy T P, Copland M J. 2000. Human sweat and 2-oxopentanoic acid elicit a landing response from Anopheles gambiae. Medical & Veterinary Entomology, 14, 195–200.
Hussain A, Zhang M, Üçpunar H K, Svensson T, Quillery E, Gompel N, Ignell R, Grunwald K I C. 2016. Ionotropic chemosensory receptors mediate the taste and smell of polyamines. PLoS Biology, 14, e1002454.
Jacquin-Joly E, Merlin C. 2004. Insect olfactory receptors: Contributions of molecular biology to chemical ecology. Journal of Chemical Ecology, 30, 2359–2397.
Klun J A, Bierl-Leonhardt B A, Schwarz M, Litsinger J A, Barrion A T, Chiang H C, Jiang Z. 1980. Sex pheromone of the Asian corn borer moth. Life Science, 27, 1603–1606.
Knecht Z A, Silbering A F, Cruz J, Yang L, Croset V, Benton R, Garrity P A. 2017. Ionotropic receptor-dependent moist and dry cells control hygrosensation in Drosophila. Elife, 6, e26654.
Knecht Z A, Silbering A F, Ni L, Klein M, Budelli G, Bell R, Abuin L, Ferrer A J, Samuel A D, Benton R, Garrity P A. 2016. Distinct combinations of variant ionotropic glutamate receptors mediate thermosensation and hygrosensation in Drosophila. Elife, 5, e17879.
Larsson M C, Domingos A I, Jones W D, Chiappe M E, Amrein H L, Vosshall B. 2004. Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron, 43, 703–714.
Lee M J, Sung H Y, Jo H, Kim H W, Choi M S, Kwon J Y, Kang K. 2017. Ionotropic receptor 76b is required for gustatory aversion to excessive Na+ in Drosophila. Molecules Cells, 40, 787–795.
Liu W, Jiang X C, Cao S, Yang B, Wang G R. 2018. Functional studies of sex pheromone receptors in Asian corn borer Ostrinia furnacalis. Frontiers in Physiology, 9, 591.
Mombaerts P. 1999. Molecular biology of odorant receptors in vertebrates. Annual Review of Neuroscience, 22, 487–509.
Nault L R, Edwards L J, Styer W E. 1973. Aphid alarm pheromones: Secretion and reception. Environmental Entomology, 2, 101–105.
Ni L, Klein M, Svec K V, Budelli G, Chang E C, Ferrer A J, Benton R, Samuel A D, Garrity P A. 2016. The ionotropic receptors IR21a and IR25a mediate cool sensing in Drosophila. Elife, 5, e13254.
Olivier V, Monsempes C, Francois M C, Poivet E, Jacquin-Joly E. 2011. Candidate chemosensory ionotropic receptors in a Lepodoptera. Insect Molecular Biology, 20, 189–199.
Pelosi P, Iovinella I, Zhu J, Wang G, Dani F R. 2018. Beyond chemoreception: Diverse tasks of soluble olfactory proteins in insects. Biology Reviews of the Cambridge Philosophical Society, 93, 184–200.
Pitts R J, Derryberry S L, Zhang Z, Zwiebel L J. 2017. Variant ionotropic receptors in the malaria vector mosquito Anopheles gambiae tuned to amines and carboxylic acids. Scientific Reports, 7, 40297.
Renthal R, Velasquez D, Olmos D, Hampton J, Wergin W P. 2003. Structure and distribution of antennal sensilla of the red imported fire ant. Micron, 34, 405–413.
Rimal S, Lee Y. 2018. The multidimensional ionotropic receptors of Drosophila melanogaster. Insect Molecular Biology, 27, 1–7.
Rytz R, Croset V, Benton R. 2013. Ionotropic receptors (IRs): Chemosensory ionotropic glutamate receptors in Drosophila and beyond. Insect Biochemistry & Molecular Biology, 43, 888–897.
Schmittgen T D, Livak K J. 2008. Analyzing real-time PCR data by the comparative CT method. Nature Protocols, 3, 1101–1108.
Shan S, Wang S N, Song X, Khashaveh A, Lu Z Y, Dhiloo K H, Li R J, Gao X W, Zhang Y J. 2019. Antennal ionotropic receptors IR64a1 and IR64a2 of the parasitoid wasp Microplitis mediator (Hymenoptera: Braconidate) collaboratively perceive habitat and host cues. Insect Biochemistry & Molecular Biology, 114, 103204.
Silbering A F, Rytz R, Grosjean Y, Abuin L, Ramdya P, Jefferis G S X E, Benton R. 2011. Complementary function and integrated wiring of the evolutionarily distinct Drosophila olfactory subsystems. The Journal of Neuroscience, 31, 13357–13375.
Stamatakis A. 2014. RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30, 1312–1313.
Vogt R G, Riddiford L M. 1981. Pheromone binding and inactivation by moth antennae. Nature, 293, 161–163.
Wang J, Hu P, Gao P, Tao J, Luo Y. 2017. Antennal transcriptome analysis and expression profiles of olfactory genes in Anoplophora chinensis. Scientific Reports, 7, 15470.
Wang S N, Peng Y, Lu Z Y, Dhiloo K H, Gu S H, Li R J, Zhou J J, Zhang Y J, Guo Y Y. 2015. Identification and expression analysis of putative chemosensory receptor genes in Microplitis mediator by antennal transcriptome screening. International Journal of Biology Sciences, 11, 737–751.
Wang T T, Si F L, He Z B, Chen B. 2018. Genome-wide identification, characterization and classification of ionotropic glutamate receptor genes (iGluRs) in the malaria vector Anopheles sinensis (Diptera: Culicidae). Parasites Vectors, 11, 34.
Yang B, Ozaki K, Ishikawa Y, Matsuo T. 2015. Identification of candidate odorant receptors in Asian corn borer Ostrinia furnacalis. PLoS ONE, 10, e0121261.
Yang B, Ozaki K, Ishikawa Y, Matsuo T. 2016. Sexually biased expression of odorant-binding proteins and chemosensory proteins in Asian corn borer Ostrinia furnacalis (Lepidoptera: Crambidae). Applied Entomology & Zoology, 51, 373–383.
Yu J, Yang B, Chang Y J, Zhang Y, Wang G R. 2020. Identification of a general odorant receptor for repellents in the Asian corn borer Ostrinia furnacalis. Frontiers in Physiology, 11, 176.
Zhang J, Bisch-Knaden S, Fandino R A, Yan S, Obiero G F, Grosse-Wilde E, Hansson B S, Knaden M. 2019. The olfactory coreceptor IR8a governs larval feces-mediated competition avoidance in a hawkmoth. Proceedings of the National Academy of Sciences of the United States of America, 116, 21828–21833.
Zhang T T, Coates B S, Ge X, Bai S X, He K L, Wang Z Y. 2015. Male- and female-biased gene expression of olfactory-related genes in the antennae of Asian Corn Borer, Ostrinia furnacalis (Guenée) (Lepidoptera: Crambidae). PLoS ONE, 10, e0128550.
Zhang Y V, Ni J, Montell C. 2013. The molecular basis for attractive salt-taste coding in Drosophila. Science, 340, 1334–1338.
|
| No Suggested Reading articles found! |
|
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
| |
Shared |
|
|
|
|
| |
Discussed |
|
|
|
|
