[en] Herbivore-induced plant volatiles (HIPVs) play a key role in the interactions between plants and herbivorous insects, as HIPVs can promote or deter herbivorous insects’ behavior. While aphids are common and serious phloem-feeding pests in farmland ecosystems, little is known about how aphids use their sensitive olfactory system to detect HIPVs. In this study, the antennal transcriptomes of the aphid species Megoura crassicauda were sequenced, and expression level analyses of M. crassicauda odorant receptors (ORs) were carried out. To investigate the chemoreception mechanisms that M. crassicauda uses to detect HIPVs, we performed in vitro functional studies of the ORs using 11 HIPVs reported to be released by aphid-infested plants. In total, 54 candidate chemosensory genes were identified, among which 20 genes were ORs. McraOR20 and McraOR43 were selected for further functional characterization because their homologs in aphids were quite conserved and their expression levels in antennae of M. crassicauda were relatively high. The results showed that McraOR20 specifically detected cis-jasmone, as did its ortholog ApisOR20 from the pea aphid Acyrthosiphon pisum, while McraOR43 did not respond to any of the HIPV chemicals that were tested. This study characterized the ability of the homologous OR20 receptors in the two aphid species to detect HIPV cis-jasmone, and provides a candidate olfactory target for mediating aphid behaviors.
Disciplines :
Entomology & pest control
Author, co-author :
WANG, Bo ✱; Tianjin Key Laboratory of Conservation and Utilization of Animal Diversity, Tianjin Normal University, Tianjin, China ; 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 ; 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
YAO, Yuan; Tianjin Key Laboratory of Conservation and Utilization of Animal Diversity, Tianjin Normal University, Tianjin, China
Francis, Frédéric ; Université de Liège - ULiège > TERRA Research Centre > Gestion durable des bio-agresseurs
YAN, Chun-cai; Tianjin Key Laboratory of Conservation and Utilization of Animal Diversity, Tianjin Normal University, Tianjin, China
WANG, Gui-rong; 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
WANG, Bing; 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 :
A conserved odorant receptor identified from antennal transcriptome of Megoura crassicauda that specifically responds to cis-jasmone
Publication date :
July 2022
Journal title :
Journal of Integrative Agriculture
ISSN :
2095-3119
Publisher :
Editorial Department of Scientia Agricultura Sinica
This work was funded by the National Natural Science Foundation of China (31572072 and 31801994), the Shenzhen Science and Technology Program, China (KQTD20180411143628272), the Natural Science Foundation of Tianjin, China (18JCYBJC96100), and the Tianjin Normal University Foundation, China (135305JF79).
Abuin, L, Bargeton, B, Ulbrich, M H, Isacoff, E Y, Kellenberger, S, Benton, R, Functional architecture of olfactory ionotropic glutamate receptors. Neuron 69 (2011), 44–60.
Benton, R, Vannice, K S, Gomez-Diaz, C, Vosshall, L B, Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila. Cell 136 (2009), 149–162.
De Biasio, F, Riviello, L, Bruno, D, Grimaldi, A, Congiu, T, Sun, Y F, Falabella, P, Expression pattern analysis of odorant-binding proteins in the pea aphid Acyrthosiphon pisum. Insect Science 22 (2015), 220–234.
Birkett, M A, Campbell, C A, Chamberlain, K, Guerrieri, E, Hick, A J, Martin, J L, Michaela, M, Napier, J A, Pettersson, J, Pickett, J A, Poppy, G M, Pow, E M, Pye, B J, Smart, L E, Wadhams, G H, Wadhams, L J, Woodcock, C M, New roles for cis-jasmone as an insect semiochemical and in plant defense. Proceedings of the National Academy of Sciences of the United States of America 97 (2000), 9329–9334.
Bruce, T J, Martin, J L, Pickett, J A, Pye, B J, Smart, L E, Wadhams, L J, cis-Jasmone treatment induces resistance in wheat plants against the grain aphid, Sitobion avenae (Fabricius) (Homoptera: Aphididae). Pest Management Science 59 (2003), 1031–1036.
Bruce, T J, Wadhams, L J, Woodcock, C M, Insect host location: A volatile situation. Trends in Plant Science 10 (2005), 269–274.
Bruno, D, Grossi, G, Salvia, R, Scala, A, Farina, D, Grimaldi, A, Zhou, J J, Bufo, S A, Vogel, H, Grosse-Wilde, E, Hansson, B S, Falabella, P, Sensilla morphology and complex expression pattern of odorant binding proteins in the vetch aphid Megoura viciae (Hemiptera: Aphididae). Frontiers in Physiology, 9, 2018, 777.
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, Ionotropic receptors specify the morphogenesis of phasic sensors controlling rapid thermal preference in Drosophila. Neuron 101 (2019), 738–747.
Cao, D P, Liu, Y, Walker, W B, Li, J H, Wang, G R, Molecular characterization of the Aphis gossypii olfactory receptor gene families. PLoS ONE, 9, 2014, e101187.
Cao, S, Huang, T Y, Shen, J, Liu, Y, Wang, G R, An orphan pheromone receptor affects the mating behavior of Helicoverpa armigera. Frontiers in Physiology, 11, 2020, 413.
Chen, Y, Amrein, H, Ionotropic receptors mediate Drosophila oviposition preference through sour gustatory receptor neurons. Current Biology 27 (2017), 2741–2750.
Chen, Y, He, M, Li, Z Q, Zhang, Y N, He, P, Identification and tissue expression profile of genes from three chemoreceptor families in an urban pest, Periplaneta americana. Scientific Reports, 6, 2016, 27495.
Chyb, S, Drosophila gustatory receptors: From gene identification to functional expression. Journal of Insect Physiology 50 (2004), 469–477.
Clyne, P J, Warr, C G, Carlson, J R, Candidate taste receptors in Drosophila. Science 287 (2000), 1830–1834.
Clyne, P J, Warr, C G, Freeman, M R, Lessing, D, Kim, J, Carlson, J R, A novel family of divergent seven-transmembrane proteins. Neuron 22 (1999), 327–338.
Croset, V, Rytz, R, Cummins, S F, Budd, A, Brawand, D, Kaessmann, H, Gibson, T J, Benton, R, Ancient protostome origin of chemosensory ionotropic glutamate receptors and the evolution of insect taste and olfaction. PLoS Genetics, 6, 2010, e1001064.
Dahanukar, A, Lei, Y T, Kwon, J Y, Carlson, J R, Two Gr genes underlie sugar reception in Drosophila. Neuron 56 (2007), 503–516.
Dewhirst, S Y, Birkett, M A, Loza-Reyes, E, Martin, J L, Pye, B J, Smart, L E, Hardie, J, Pickett, J A, Activation of defence in sweet pepper, Capsicum annum, by cis-jasmone, and its impact on aphid and aphid parasitoid behaviour. Pest Management Science 68 (2012), 1419–1429.
Dus, M, Min, S, Keene, A C, Lee, G Y, Suh, G S B, Taste-independent detection of the caloric content of sugar in Drosophila. Proceedings of the National Academy of Sciences of the United States of America 108 (2011), 11644–11649.
El-Gebali, S, Mistry, J, Bateman, A, Eddy, S R, Luciani, A, Potter, S C, Qureshi, M, Richardson, L J, Salazar, G A, Smart, A, Sonnhammer, E L L, Hirsh, L, Paladin, L, Piovesan, D, Tosatto, S C E, Finn, R D, The Pfam protein families database in 2019. Nucleic Acids Research 47 (2018), D427–D432.
Fan, J, Xue, W X, Duan, H X, Jiang, X, Zhang, Y, Yu, W J, Jiang, S S, Sun, J R, Chen, J L, Identification of an intraspecific alarm pheromone and two conserved odorant-binding proteins associated with (E)-β-farnesene perception in aphid Rhopalosiphum padi. Journal of Insect Physiology 101 (2017), 151–160.
Fan, J, Zhang, Y, Francis, F, Cheng, D F, Sun, J R, Chen, J L, Orco mediates olfactory behaviors and winged morph differentiation induced by alarm pheromone in the grain aphid, Sitobion avenae. Insect Biochemistry and Molecular Biology 64 (2015), 16–24.
Fleischer, J, Krieger, J, Insect pheromone receptors - key elements in sensing intraspecific chemical signals. Frontiers in Cellular Neuroscience, 12, 2018, 425.
Galindo, K, Smith, D P, A large family of divergent Drosophila odorant-binding proteins expressed in gustatory and olfactory sensilla. Genetica 159 (2001), 1059–1072.
Grabherr, M G, Haas, B J, Yassour, M, Levin, J Z, Thompson, D A, Amit, I, Adiconis, X, Fan, L, Raychowdhury, R, Zeng, Q D, Chen, Z H, Mauceli, E, Hacohen, N, Gnirke, A, Rhind, N, di Palma, F, Birren, B W, Nusbaum, C, Lindblad-Toh, K, Friedman, N, et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnology 29 (2011), 644–652.
Gu, S H, Wu, K M, Guo, Y Y, Field, L M, Pickett, J A, Zhang, Y J, Zhou, J J, Identification and expression profiling of odorant binding proteins and chemosensory proteins between two wingless morphs and a winged morph of the cotton aphid Aphis gossypii glover. PLoS ONE, 8, 2013, e73524.
Guo, M B, Du, L X, Chen, Q Y, Feng, Y L, Zhang, J, Zhang, X X, Tian, K, Cao, S, Huang, T Y, Jacquin-Joly, E, Wang, G R, Liu, Y, Odorant receptors for detecting flowering plant cues are functionally conserved across moths and butterflies. Molecular Biology and Evolution 38 (2020), 1413–1427.
Hassan, B A, Hussain, A, Zhang, M, Üçpunar, H K, Svensson, T, Quillery, E, Gompel, N, Ignell, R, Kadow, I C G, Ionotropic chemosensory receptors mediate the taste and smell of polyamines. PLoS Biology, 14, 2016, e1002454.
Hegde, M, Oliveira, J N, da Costa, J G, Loza-Reyes, E, Bleicher, E, Santana, A E, Caulfield, J C, Mayon, P, Dewhirst, S Y, Bruce, T J, Pickett, J A, Birkett, M A, Aphid antixenosis in cotton is activated by the natural plant defence elicitor cis-jasmone. Phytochemistry 78 (2012), 81–88.
Jacquin-Joly, E, Merlin, C, Insect olfactory receptors: Contributions of molecular biology to chemical ecology. Journal of Chemical Ecology 30 (2004), 2359–2397.
Jiao, Y C, Moon, S J, Montell, C, A Drosophila gustatory receptor required for the responses to sucrose, glucose, and maltose identified by mRNA tagging. Proceedings of the National Academy of Sciences of the United States of America 104 (2007), 14110–14115.
Jones, W D, Cayirlioglu, P, Grunwald Kadow, I, Vosshall, L B, Two chemosensory receptors together mediate carbon dioxide detection in Drosophila. Nature 445 (2006), 86–90.
Joseph, R M, Carlson, J R, Drosophila chemoreceptors: A molecular interface between the chemical world and the brain. Trends in Genetics 31 (2015), 683–695.
Katoh, K, Standley, D M, MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30 (2013), 772–780.
Kim, H, Lee, S, Molecular systematics of the genus Megoura (Hemiptera: Aphididae) using mitochondrial and nuclear DNA sequences. Molecules and Cells 25 (2008), 510–522.
Knecht, Z A, Silbering, A F, Cruz, J, Yang, L D, Croset, V, Benton, R, Garrity, P A, Ionotropic receptor-dependent moist and dry cells control hygrosensation in Drosophila. eLife, 6, 2017, e26654.
Knecht, Z A, Silbering, A F, Ni, L, Klein, M, Budelli, G, Bell, R, Abuin, L, Ferrer, A J, Samuel, A D T, Benton, R, Garrity, P A, Distinct combinations of variant ionotropic glutamate receptors mediate thermosensation and hygrosensation in Drosophila. Elife, 5, 2016, e17879.
Kroes, A, Weldegergis, B T, Cappai, F, Dicke, M, van Loon, J J A, Terpenoid biosynthesis in Arabidopsis attacked by caterpillars and aphids: Effects of aphid density on the attraction of a caterpillar parasitoid. Oecologia 185 (2017), 699–712.
Langmead, B, Salzberg, S L, Fast gapped-read alignment with Bowtie 2. Nature Methods 9 (2012), 357–359.
Li, B, Dewey, C N, RSEM: Accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics, 12, 2011, 323.
Li, Z Q, Zhang, S, Cai, X M, Luo, J Y, Dong, S L, Cui, J J, Chen, Z M, Distinct binding affinities of odorant-binding proteins from the natural predator Chrysoperla sinica suggest different strategies to hunt prey. Journal of Insect Physiology 111 (2018), 25–31.
Liu, Y P, Cui, Z Y, Si, P F, Liu, Y, Zhou, Q, Wang, G R, Characterization of a specific odorant receptor for linalool in the Chinese citrus fly Bactrocera minax (Diptera: Tephritidae). Insect Biochemistry and Molecular Biology, 122, 2020, 103389.
Liu, Y P, Cui, Z Y, Wang, G R, Zhou, Q, Liu, Y, Cloning and functional characterization of three odorant receptors from the Chinese citrus fly Bactrocera minax (Diptera: Tephritidae). Frontiers in Physiology, 11, 2020, 246.
Loughrin, J H, Manukian, A, Heath, R R, Tumlinson, J H, Volatiles emitted by different cotton varieties damaged by feeding beet armyworm larvae. Journal of Chemical Ecology 21 (1995), 1217–1227.
Matthes, M C, Bruce, T J A, Ton, J, Verrier, P J, Pickett, J A, Napier, J A, The transcriptome of cis-jasmone-induced resistance in Arabidopsis thaliana and its role in indirect defence. Planta 232 (2010), 1163–1180.
Mistry, J, Finn, R D, Eddy, S R, Bateman, A, Punta, M, Challenges in homology search: HMMER3 and convergent evolution of coiled-coil regions. Nucleic Acids Research, 41, 2013, e121.
Moon, S J, Kottgen, M, Jiao, Y C, Xu, H, Montell, C, A taste receptor required for the caffeine response in vivo. Current Biology 16 (2006), 1812–1817.
Northey, T, Venthur, H, De Biasio, F, Chauviac, F X, Cole, A, Lisboa Ribeiro Junior, K A, Grossi, G, Falabella, P, Field, L M, Keep, N H, Zhou, J J, Crystal structures and binding dynamics of odorant-binding protein 3 from two aphid species Megoura viciae and Nasonovia ribisnigri. Scientific Reports, 6, 2016, 24739.
Pelosi, P, Iovinella, I, Zhu, J, Wang, G R, Dani, F R, Beyond chemoreception: diverse tasks of soluble olfactory proteins in insects. Biological Reviews 93 (2018), 184–200.
Pelosi, P, Zhou, J J, Ban, L, Calvello, M, Soluble proteins in insect chemical communication. Cellular and Molecular Life Sciences 63 (2006), 1658–1676.
Pertea, G, Huang, X, Liang, F, Antonescu, V, Sultana, R, Karamycheva, S, Lee, Y, White, J, Cheung, F, Parvizi, B, Tsai, J, Quackenbush, J, TIGR Gene Indices clustering tools (TGICL): A software system for fast clustering of large EST datasets. Bioinformatics 19 (2003), 651–652.
Petersen, T N, Brunak, S, von Heijne, G, Nielsen, H, SignalP 4.0: Discriminating signal peptides from transmembrane regions. Nature Methods 8 (2011), 785–786.
Pickett, J A, Rasmussen, H B, Woodcock, C M, Matthes, M, Napier, J A, Plant stress signalling: Understanding and exploiting plant–plant interactions. Biochemical Society Transactions 31 (2003), 123–127.
Powell, W, Pickett, J A, Manipulation of parasitoids for aphid pest management: Progress and prospects. Pest Management Science 59 (2003), 149–155.
Prieto-Godino, L L, Rytz, R, Cruchet, S, Bargeton, B, Abuin, L, Silbering, A F, Ruta, V, Dal Peraro, M, Benton, R, Evolution of acid-sensing olfactory circuits in Drosophilids. Neuron 93 (2017), 1–16.
Qiao, H, Tuccori, E, He, X L, Gazzano, A, Field, L, Zhou, J J, Pelosi, P, Discrimination of alarm pheromone (E)-β-farnesene by aphid odorant-binding proteins. Insect Biochemistry and Molecular Biology 39 (2009), 414–419.
Qin, Y G, Yang, Z K, Song, D L, Wang, Q, Gu, S H, Li, W H, Duan, H X, Zhou, J J, Yang, X L, Bioactivities of synthetic salicylate-substituted carboxyl (E)-β-farnesene derivatives as ecofriendly agrochemicals and their binding mechanism with potential targets in aphid olfactory system. Pest Management Science 76 (2020), 2465–2472.
Robertson, H M, The insect chemoreceptor superfamily is ancient in animals. Chemical Senses 40 (2015), 609–614.
Robertson, H M, Robertson, E C N, Walden, K K O, Enders, L S, Miller, N J, The chemoreceptors and odorant binding proteins of the soybean and pea aphids. Insect Biochemistry and Molecular Biology 105 (2019), 69–78.
Rose, U S, Tumlinson, J H, Volatiles released from cotton plants in response to Helicoverpa zea feeding damage on cotton flower buds. Planta 218 (2004), 824–832.
Sandler, B H, Nikonova, L, Leal, W S, Clardy, J, Sexual attraction in the silkworm moth: Structure of the pheromone-binding-protein–bombykol complex. Chemistry & Biology 7 (2000), 143–151.
Schwartzberg, E G, Boroczky, K, Tumlinson, J H, Pea aphids, Acyrthosiphon pisum, suppress induced plant volatiles in broad bean, Vicia faba. Journal of Chemical Ecology 37 (2011), 1055–1062.
Smadja, C, Shi, P, Butlin, R K, Robertson, H M, Large gene family expansions and adaptive evolution for odorant and gustatory receptors in the pea aphid, Acyrthosiphon pisum. Molecular Biology and Evolution 26 (2009), 2073–2086.
Sobhy, I S, Woodcock, C M, Powers, S J, Caulfield, J C, Pickett, J A, Birkett, M A, cis-Jasmone elicits aphid-induced stress signalling in potatoes. Journal of Chemical Ecology 43 (2017), 39–52.
Stamatakis, A, RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30 (2014), 1312–1313.
Sun, J S, Xiao, S K, Carlson, J R, The diverse small proteins called odorant-binding proteins. Open Biology, 8, 2018, 180208.
Sung, H Y, Jeong, Y T, Lim, J Y, Kim, H, Oh, S M, Hwang, S W, Kwon, J Y, Moon, S J, Heterogeneity in the Drosophila gustatory receptor complexes that detect aversive compounds. Nature Communications, 8, 2017, 1484.
Takemoto, H, Takabayashi, J, Parasitic wasps Aphidius ervi are more attracted to a blend of host-induced plant volatiles than to the independent compounds. Journal of Chemical Ecology 41 (2015), 801–807.
Turlings, T C J, Erb, M, Tritrophic interactions mediated by herbivore-induced plant volatiles: mechanisms, ecological relevance, and application potential. Annual Review of Entomology 63 (2018), 433–452.
Turlings, T C J, Tumlinson, J H, Systemic release of chemical signals by herbivore-injured corn. Proceedings of the National Academy of Sciences of the United States of America 89 (1992), 8399–8402.
Untergasser, A, Cutcutache, I, Koressaar, T, Ye, J, Faircloth, B C, Remm, M, Rozen, S G, Primer3 - new capabilities and interfaces. Nucleic Acids Research, 40, 2012, e115.
Wang, B, Liu, Y, Wang, G R, Chemosensory genes in the antennal transcriptome of two syrphid species, Episyrphus balteatus and Eupeodes corollae (Diptera: Syrphidae). BMC Genomics, 18, 2017, 586.
Wang, Q, Zhou, J J, Liu, J T, Huang, G Z, Xu, W Y, Zhang, Q, Chen, J L, Zhang, Y J, Li, X C, Gu, S H, Integrative transcriptomic and genomic analysis of odorant binding proteins and chemosensory proteins in aphids. Insect Molecular Biology 28 (2019), 1–22.
Xue, W X, Fan, J, Zhang, Y, Xu, Q X, Han, Z L, Sun, J R, Chen, J L, Identification and expression analysis of candidate odorant-binding protein and chemosensory protein genes by antennal transcriptome of Sitobion avenae. PLoS ONE, 11, 2016, e0161839.
Yang, C X, Pan, H P, Liu, Y, Zhou, X G, Selection of reference genes for expression analysis using quantitative real-time PCR in the pea aphid, Acyrthosiphon pisum (Harris) (Hemiptera, Aphidiae). PLoS ONE, 9, 2014, e110454.
Zhang, R B, Liu, Y, Yan, S C, Wang, G R, Identification and functional characterization of an odorant receptor in pea aphid, Acyrthosiphon pisum. Insect Science 26 (2019), 58–67.
Zhang, R B, Wang, B, Grossi, G, Falabella, P, Liu, Y, Yan, S C, Lu, J, Xi, J H, Wang, G R, Molecular basis of alarm pheromone detection in aphids. Current Biology 27 (2017), 55–61.
Zhao, J J, Zhang, Y, Fan, D S, Feng, J N, Identification and expression profiling of odorant-binding proteins and chemosensory proteins of Daktulosphaira vitifoliae (Hemiptera: Phylloxeridae). Journal of Economic Entomology 110 (2017), 1813–1820.
Zhong, T, Yin, J, Deng, S S, Li, K B, Cao, Y Z, Fluorescence competition assay for the assessment of green leaf volatiles and trans-β-farnesene bound to three odorant-binding proteins in the wheat aphid Sitobion avenae (Fabricius). Journal of Insect Physiology 58 (2012), 771–781.
Zhou, J J, Vieira, F G, He, X L, Smadja, C, Liu, R, Rozas, J, Field, L M, Genome annotation and comparative analyses of the odorant-binding proteins and chemosensory proteins in the pea aphid Acyrthosiphon pisum. Insect Molecular Biology 19 (2010), 113–122.
