<strong>一个保守的豌豆修尾蚜气味受体的鉴定与特异性识别顺式-茉莉酮的功能研究</strong>

Journal of Integrative Agriculture ›› 2022, Vol. 21 ›› Issue (7): 2042-2054.DOI: 10.1016/S2095-3119(21)63712-7

• • 上一篇下一篇

一个保守的豌豆修尾蚜气味受体的鉴定与特异性识别顺式-茉莉酮的功能研究

收稿日期:2021-01-15 接受日期:2021-04-16 出版日期:2022-07-01 发布日期:2021-04-16

A conserved odorant receptor identified from antennal transcriptome of Megoura crassicauda that specifically responds to cis-jasmone

WANG Bo^{1, 2*}, HUANG Tian-yu^{2, 3, 4*}, YAO Yuan¹, Frederic FRANCIS⁴, YAN Chun-cai¹, WANG Gui-rong^{2, 3}, WANG Bing²

¹ Tianjin Key Laboratory of Conservation and Utilization of Animal Diversity, Tianjin Normal University, Tianjin 300387, 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 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 518120, P.R.China
⁴ Functional and Evolutionary Entomology, Gembloux Agro-Bio Tech, University of Liège, Gembloux 5030, Belgium

Received:2021-01-15 Accepted:2021-04-16 Online:2022-07-01 Published:2021-04-16
About author:WANG Bo, E-mail: wangboo_88@163.com; HUANG Tian-yu, E-mail: huangty_caas@hotmail.com; Correspondence YAN Chun-cai, E-mail: skyycc@tjnu.edu.cn; WANG Gui-rong, E-mail: wangguirong@caas.cn; WANG Bing, E-mail: bwang@ippcaas.cn * These authors contributed equally to this study.
Supported by:
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).

摘要/Abstract

摘要：

本研究首先对豌豆修尾蚜触角转录组进行测序，并对鉴定到的气味受体（odorant receptors, ORs）基因进行了表达水平分析。随后，为了研究豌豆修尾蚜识别HIPVs的化学感受机制，利用11种已鉴定的蚜虫为害诱导的HIPVs对ORs的体外功能进行了研究。研究结果表明，在豌豆修尾蚜触角转录组中共鉴定出54个化学感受基因。注释到20个ORs基因，与豌豆蚜ORs进行氨基酸相似性分析，发现McraOR20和McraOR43分别与豌豆蚜的同源受体序列具有较高的保守性，且在触角中的表达量较高。因此对McraOR20和McraOR43的体外功能进行了研究，结果显示豌豆修尾蚜McraOR20与豌豆蚜中的同源基因ApisOR20均能特异地识别一种HIPV顺式-茉莉酮，而McraOR43对测试的11种HIPVs均无电生理反应。本研究证实了两种蚜虫的同源受体OR20均能特异性识别虫害诱导的植物挥发物顺式-茉莉酮，为发展蚜虫的行为调控策略提供了候选的嗅觉受体靶标。

Abstract: 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.

Key words: Megoura crassicauda , transcriptome , chemosensory genes , odorant receptors , cis-jasmone

. 一个保守的豌豆修尾蚜气味受体的鉴定与特异性识别顺式-茉莉酮的功能研究[J]. Journal of Integrative Agriculture, 2022, 21(7): 2042-2054.

WANG Bo, HUANG Tian-yu, YAO Yuan, Frederic FRANCIS, YAN Chun-cai, WANG Gui-rong, WANG Bing. A conserved odorant receptor identified from antennal transcriptome of Megoura crassicauda that specifically responds to cis-jasmone[J]. Journal of Integrative Agriculture, 2022, 21(7): 2042-2054.

参考文献

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.
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 Biasio F, Riviello L, Bruno D, Grimaldi A, Congiu T, Sun Y F, Falabella P. 2015. Expression pattern analysis of odorant-binding proteins in the pea aphid Acyrthosiphon pisum. Insect Science, 22, 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. 2000. 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, 9329–9334.
Bruce T J, Martin J L, Pickett J A, Pye B J, Smart L E, Wadhams L J. 2003. cis-Jasmone treatment induces resistance in wheat plants against the grain aphid, Sitobion avenae (Fabricius) (Homoptera: Aphididae). Pest Management Science, 59, 1031–1036.
Bruce T J, Wadhams L J, Woodcock C M. 2005. Insect host location: A volatile situation. Trends in Plant Science, 10, 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. 2018. Sensilla morphology and complex expression pattern of odorant binding proteins in the vetch aphid Megoura viciae (Hemiptera: Aphididae). Frontiers in Physiology, 9, 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. 2019. Ionotropic receptors specify the morphogenesis of phasic sensors controlling rapid thermal preference in Drosophila. Neuron, 101, 738–747.
Cao D P, Liu Y, Walker W B, Li J H, Wang G R. 2014. Molecular characterization of the Aphis gossypii olfactory receptor gene families. PLoS ONE, 9, e101187.
Cao S, Huang T Y, Shen J, Liu Y, Wang G R. 2020. An orphan pheromone receptor affects the mating behavior of Helicoverpa armigera. Frontiers in Physiology, 11, 413.
Chen Y, Amrein H. 2017. Ionotropic receptors mediate Drosophila oviposition preference through sour gustatory receptor neurons. Current Biology, 27, 2741–2750.
Chen Y, He M, Li Z Q, Zhang Y N, He P. 2016. Identification and tissue expression profile of genes from three chemoreceptor families in an urban pest, Periplaneta americana. Scientific Reports, 6, 27495.
Chyb S. 2004. Drosophila gustatory receptors: From gene identification to functional expression. Journal of Insect Physiology, 50, 469–477.
Clyne P J, Warr C G, Carlson J R. 2000. Candidate taste receptors in Drosophila. Science, 287, 1830–1834.
Clyne P J, Warr C G, Freeman M R, Lessing D, Kim J, Carlson J R. 1999. A novel family of divergent seven-transmembrane proteins. Neuron, 22, 327–338.
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.
Dahanukar A, Lei Y T, Kwon J Y, Carlson J R. 2007. Two Gr genes underlie sugar reception in Drosophila. Neuron, 56, 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. 2012. Activation of defence in sweet pepper, Capsicum annum, by cis-jasmone, and its impact on aphid and aphid parasitoid behaviour. Pest Management Science, 68, 1419–1429.
Dus M, Min S, Keene A C, Lee G Y, Suh G S B. 2011. 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, 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. 2018. The Pfam protein families database in 2019. Nucleic Acids Research, 47, 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. 2017. 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, 151–160.
Fan J, Zhang Y, Francis F, Cheng D F, Sun J R, Chen J L. 2015. Orco mediates olfactory behaviors and winged morph differentiation induced by alarm pheromone in the grain aphid, Sitobion avenae. Insect Biochemistry and Molecular Biology, 64, 16–24.
Fleischer J, Krieger J. 2018. Insect pheromone receptors - key elements in sensing intraspecific chemical signals. Frontiers in Cellular Neuroscience, 12, 425.
Galindo K, Smith D P. 2001. A large family of divergent Drosophila odorant-binding proteins expressed in gustatory and olfactory sensilla. Genetica, 159, 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. 2011. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnology, 29, 644–652.
Gu S H, Wu K M, Guo Y Y, Field L M, Pickett J A, Zhang Y J, Zhou J J. 2013. 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, 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. 2020. Odorant receptors for detecting flowering plant cues are functionally conserved across moths and butterflies. Molecular Biology and Evolution, 38, 1413–1427.
Hassan B A, Hussain A, Zhang M, Üçpunar H K, Svensson T, Quillery E, Gompel N, Ignell R, Kadow I C G. 2016. Ionotropic chemosensory receptors mediate the taste and smell of polyamines. PLoS Biology, 14, 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. 2012. Aphid antixenosis in cotton is activated by the natural plant defence elicitor cis-jasmone. Phytochemistry, 78, 81–88.
Jacquin-Joly E, Merlin C. 2004. Insect olfactory receptors: Contributions of molecular biology to chemical ecology. Journal of Chemical Ecology, 30, 2359–2397.
Jiao Y C, Moon S J, Montell C. 2007. 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, 14110–14115.
Jones W D, Cayirlioglu P, Grunwald Kadow I, Vosshall L B. 2006. Two chemosensory receptors together mediate carbon dioxide detection in Drosophila. Nature, 445, 86–90.
Joseph R M, Carlson J R. 2015. Drosophila chemoreceptors: A molecular interface between the chemical world and the brain. Trends in Genetics, 31, 683–695.
Katoh K, Standley D M. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution, 30, 772–780.
Kim H, Lee S. 2008. Molecular systematics of the genus Megoura (Hemiptera: Aphididae) using mitochondrial and nuclear DNA sequences. Molecules and Cells, 25, 510–522.
Knecht Z A, Silbering A F, Cruz J, Yang L D, 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 T, Benton R, Garrity P A. 2016. Distinct combinations of variant ionotropic glutamate receptors mediate thermosensation and hygrosensation in Drosophila. Elife, 5, e17879.
Kroes A, Weldegergis B T, Cappai F, Dicke M, van Loon J J A. 2017. Terpenoid biosynthesis in Arabidopsis attacked by caterpillars and aphids: Effects of aphid density on the attraction of a caterpillar parasitoid. Oecologia, 185, 699–712.
Langmead B, Salzberg S L. 2012. Fast gapped-read alignment with Bowtie 2. Nature Methods, 9, 357–359.
Li B, Dewey C N. 2011. RSEM: Accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics, 12, 323.
Li Z Q, Zhang S, Cai X M, Luo J Y, Dong S L, Cui J J, Chen Z M. 2018. Distinct binding affinities of odorant-binding proteins from the natural predator Chrysoperla sinica suggest different strategies to hunt prey. Journal of Insect Physiology, 111, 25–31.
Liu Y P, Cui Z Y, Si P F, Liu Y, Zhou Q, Wang G R. 2020a. Characterization of a specific odorant receptor for linalool in the Chinese citrus fly Bactrocera minax (Diptera: Tephritidae). Insect Biochemistry and Molecular Biology, 122, 103389.
Liu Y P, Cui Z Y, Wang G R, Zhou Q, Liu Y. 2020b. Cloning and functional characterization of three odorant receptors from the Chinese citrus fly Bactrocera minax (Diptera: Tephritidae). Frontiers in Physiology, 11, 246.
Loughrin J H, Manukian A, Heath R R, Tumlinson J H. 1995. Volatiles emitted by different cotton varieties damaged by feeding beet armyworm larvae. Journal of Chemical Ecology, 21, 1217–1227.
Matthes M C, Bruce T J A, Ton J, Verrier P J, Pickett J A, Napier J A. 2010. The transcriptome of cis-jasmone-induced resistance in Arabidopsis thaliana and its role in indirect defence. Planta, 232, 1163–1180.
Mistry J, Finn R D, Eddy S R, Bateman A, Punta M. 2013. Challenges in homology search: HMMER3 and convergent evolution of coiled-coil regions. Nucleic Acids Research, 41, e121.
Moon S J, Kottgen M, Jiao Y C, Xu H, Montell C. 2006. A taste receptor required for the caffeine response in vivo. Current Biology, 16, 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. 2016. Crystal structures and binding dynamics of odorant-binding protein 3 from two aphid species Megoura viciae and Nasonovia ribisnigri. Scientific Reports, 6, 24739.
Pelosi P, Iovinella I, Zhu J, Wang G R, Dani F R. 2018. Beyond chemoreception: diverse tasks of soluble olfactory proteins in insects. Biological Reviews, 93, 184–200.
Pelosi P, Zhou J J, Ban L, Calvello M. 2006. Soluble proteins in insect chemical communication. Cellular and Molecular Life Sciences, 63, 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. 2003. TIGR Gene Indices clustering tools (TGICL): A software system for fast clustering of large EST datasets. Bioinformatics, 19, 651–652.
Petersen T N, Brunak S, von Heijne G, Nielsen H. 2011. SignalP 4.0: Discriminating signal peptides from transmembrane regions. Nature Methods, 8, 785–786.
Pickett J A, Rasmussen H B, Woodcock C M, Matthes M, Napier J A. 2003. Plant stress signalling: Understanding and exploiting plant–plant interactions. Biochemical Society Transactions, 31, 123–127.
Powell W, Pickett J A. 2003. Manipulation of parasitoids for aphid pest management: Progress and prospects. Pest Management Science, 59, 149–155.
Prieto-Godino L L, Rytz R, Cruchet S, Bargeton B, Abuin L, Silbering A F, Ruta V, Dal Peraro M, Benton R. 2017. Evolution of acid-sensing olfactory circuits in Drosophilids. Neuron, 93, 1–16.
Qiao H, Tuccori E, He X L, Gazzano A, Field L, Zhou J J, Pelosi P. 2009. Discrimination of alarm pheromone (E)-β-farnesene by aphid odorant-binding proteins. Insect Biochemistry and Molecular Biology, 39, 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. 2020. 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, 2465–2472.
Robertson H M. 2015. The insect chemoreceptor superfamily is ancient in animals. Chemical Senses, 40, 609–614.
Robertson H M, Robertson E C N, Walden K K O, Enders L S, Miller N J. 2019. The chemoreceptors and odorant binding proteins of the soybean and pea aphids. Insect Biochemistry and Molecular Biology, 105, 69–78.
Rose U S, Tumlinson J H. 2004. Volatiles released from cotton plants in response to Helicoverpa zea feeding damage on cotton flower buds. Planta, 218, 824–832.
Sandler B H, Nikonova L, Leal W S, Clardy J. 2000. Sexual attraction in the silkworm moth: Structure of the pheromone-binding-protein–bombykol complex. Chemistry & Biology, 7, 143–151.
Schwartzberg E G, Boroczky K, Tumlinson J H. 2011. Pea aphids, Acyrthosiphon pisum, suppress induced plant volatiles in broad bean, Vicia faba. Journal of Chemical Ecology, 37, 1055–1062.
Smadja C, Shi P, Butlin R K, Robertson H M. 2009. Large gene family expansions and adaptive evolution for odorant and gustatory receptors in the pea aphid, Acyrthosiphon pisum. Molecular Biology and Evolution, 26, 2073–2086.
Sobhy I S, Woodcock C M, Powers S J, Caulfield J C, Pickett J A, Birkett M A. 2017. cis-Jasmone elicits aphid-induced stress signalling in potatoes. Journal of Chemical Ecology, 43, 39–52.
Stamatakis A. 2014. RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30, 1312–1313.
Sun J S, Xiao S K, Carlson J R. 2018. The diverse small proteins called odorant-binding proteins. Open Biology, 8, 180208.
Sung H Y, Jeong Y T, Lim J Y, Kim H, Oh S M, Hwang S W, Kwon J Y, Moon S J. 2017. Heterogeneity in the Drosophila gustatory receptor complexes that detect aversive compounds. Nature Communications, 8, 1484.
Takemoto H, Takabayashi J. 2015. 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, 801–807.
Turlings T C J, Erb M. 2018. Tritrophic interactions mediated by herbivore-induced plant volatiles: mechanisms, ecological relevance, and application potential. Annual Review of Entomology, 63, 433–452.
Turlings T C J, Tumlinson J H. 1992. Systemic release of chemical signals by herbivore-injured corn. Proceedings of the National Academy of Sciences of the United States of America, 89, 8399–8402.
Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth B C, Remm M, Rozen S G. 2012. Primer3 - new capabilities and interfaces. Nucleic Acids Research, 40, e115.
Wang B, Liu Y, Wang G R. 2017. Chemosensory genes in the antennal transcriptome of two syrphid species, Episyrphus balteatus and Eupeodes corollae (Diptera: Syrphidae). BMC Genomics, 18, 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. 2019. Integrative transcriptomic and genomic analysis of odorant binding proteins and chemosensory proteins in aphids. Insect Molecular Biology, 28, 1–22.
Xue W X, Fan J, Zhang Y, Xu Q X, Han Z L, Sun J R, Chen J L. 2016. Identification and expression analysis of candidate odorant-binding protein and chemosensory protein genes by antennal transcriptome of Sitobion avenae. PLoS ONE, 11, e0161839.
Yang C X, Pan H P, Liu Y, Zhou X G. 2014. Selection of reference genes for expression analysis using quantitative real-time PCR in the pea aphid, Acyrthosiphon pisum (Harris) (Hemiptera, Aphidiae). PLoS ONE, 9, e110454.
Zhang R B, Liu Y, Yan S C, Wang G R. 2019. Identification and functional characterization of an odorant receptor in pea aphid, Acyrthosiphon pisum. Insect Science, 26, 58–67.
Zhang R B, Wang B, Grossi G, Falabella P, Liu Y, Yan S C, Lu J, Xi J H, Wang G R. 2017. Molecular basis of alarm pheromone detection in aphids. Current Biology, 27, 55–61.
Zhao J J, Zhang Y, Fan D S, Feng J N. 2017. Identification and expression profiling of odorant-binding proteins and chemosensory proteins of Daktulosphaira vitifoliae (Hemiptera: Phylloxeridae). Journal of Economic Entomology, 110, 1813–1820.
Zhong T, Yin J, Deng S S, Li K B, Cao Y Z. 2012. 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, 771–781.
Zhou J J, Vieira F G, He X L, Smadja C, Liu R, Rozas J, Field L M. 2010. Genome annotation and comparative analyses of the odorant-binding proteins and chemosensory proteins in the pea aphid Acyrthosiphon pisum. Insect Molecular Biology, 19, 113–122.

相关文章 0

编辑推荐

Metrics