悬铃木方翅网蝽触角气味结合蛋白基因鉴定
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摘要
【目的】悬铃木方翅网蝽Corythucha ciliata是专性危害悬铃木属Platanus植物的外来入侵害虫,本研究旨在获得该害虫触角中气味结合蛋白(OBPs)基因信息,以期寻求有效控制害虫的嗅觉分子靶标。【方法】利用Illumina HiSeq~(TM) 4000高通量测序技术对悬铃木方翅网蝽雌雄成虫触角进行转录组测序并对测序结果进行生物信息学分析;通过实时荧光定量PCR(qPCR)方法,分析OBP基因在悬铃木方翅网蝽雌雄成虫触角中的表达模式。【结果】对悬铃木方翅网蝽雌雄成虫触角6个样品的转录组测序,共获得40.87 Gb clean reads,各样品的序列长度均达到6.31 Gb。转录组数据分析共鉴定出26个推测的悬铃木方翅网蝽OBP基因,其编码蛋白中24个(CcilOBP1-24)属于Classic OBPs,CcilOBP25/26属于Plus-C OBPs;与半翅目其他昆虫相关OBPs系统发育分析表明,大部分CcilOBPs形成独立一簇,少数与其他半翅目昆虫OBPs直系同源。qPCR分析显示,有11个OBP基因在雌雄成虫触角中表达量差异显著,其中有9个OBP基因(CcilOBP5/6/9/10/17/18/21/24/25)在雄成虫触角中显著高表达,有2个OBP基因(CcilOBP14/16)在雌成虫触角中显著高表达。【结论】本研究获得了悬铃木方翅网蝽成虫触角气味结合蛋白基因信息,研究结果为生物控制该害虫提供了重要基础数据和候选分子靶标。
【Aim】 The sycamore lace bug, Corythucha ciliata(Hemiptera: Tingidae), is an invasive and specific forestry pest of Platanus spp. The objective of this study is to obtain the gene information of odorant binding proteins(OBPs) in C. ciliata antennae and to seek effective olfactory molecular targets for pest control. 【Methods】 The antennal transcriptomes of male and female adults of C. ciliata were sequenced using Illumina HiSeq~(TM) 4000 platform and subjected to bioinformatics analysis. The expression patterns of OBP genes in female and male antennae of C. ciliata adults were analyzed by real-time quantitative PCR(qPCR). 【Results】 In total, 40.87 Gb clean reads were obtained from six samples of male and female antennal transcripts of C. ciliata adults, the sequences of all of the samples are more than 6.31 Gb in length. By further screening and identification, we obtained 26 putative OBP genes from C. ciliata, whose encoded proteins correspond to 24 Classic OBPs(CcilOBP1-24) and 2 Plus-C OBPs(CcilOBP25/26). Phylogenetic analysis of OBPs from C. ciliata(CcilOBPs) and other closely related Hemiptera species revealed that most CcilOBPs form a unique cluster, and a few form ortholog groups with OBPs from other hemipterous insects. qPCR analysis showed that there were significant differences in the expression levels of 11 OBP genes in the antennae of male and female adults, including 9 OBP genes(CcilOBP5/6/9/10/17/18/21/24/25) highly expressed in the male antennae, and 2 OBP genes(CcilOBP14/16) highly expressed in the female antennae. 【Conclusion】 This study acquired the molecular information of OBP genes from C. ciliata adult antennae. The results provide valuable basic data and candidate molecular targets for biological control of C. ciliata.
【Aim】 The sycamore lace bug, Corythucha ciliata(Hemiptera: Tingidae), is an invasive and specific forestry pest of Platanus spp. The objective of this study is to obtain the gene information of odorant binding proteins(OBPs) in C. ciliata antennae and to seek effective olfactory molecular targets for pest control. 【Methods】 The antennal transcriptomes of male and female adults of C. ciliata were sequenced using Illumina HiSeq~(TM) 4000 platform and subjected to bioinformatics analysis. The expression patterns of OBP genes in female and male antennae of C. ciliata adults were analyzed by real-time quantitative PCR(qPCR). 【Results】 In total, 40.87 Gb clean reads were obtained from six samples of male and female antennal transcripts of C. ciliata adults, the sequences of all of the samples are more than 6.31 Gb in length. By further screening and identification, we obtained 26 putative OBP genes from C. ciliata, whose encoded proteins correspond to 24 Classic OBPs(CcilOBP1-24) and 2 Plus-C OBPs(CcilOBP25/26). Phylogenetic analysis of OBPs from C. ciliata(CcilOBPs) and other closely related Hemiptera species revealed that most CcilOBPs form a unique cluster, and a few form ortholog groups with OBPs from other hemipterous insects. qPCR analysis showed that there were significant differences in the expression levels of 11 OBP genes in the antennae of male and female adults, including 9 OBP genes(CcilOBP5/6/9/10/17/18/21/24/25) highly expressed in the male antennae, and 2 OBP genes(CcilOBP14/16) highly expressed in the female antennae. 【Conclusion】 This study acquired the molecular information of OBP genes from C. ciliata adult antennae. The results provide valuable basic data and candidate molecular targets for biological control of C. ciliata.
引文
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Biessmann H, Nguyen QK, Le D, Walter MF, 2005. Microarray-based survey of a subset of putative olfactory genes in the mosquito Anopheles gambiae. Insect Mol. Biol., 14(6): 575-589.
Breer H, Raming K, Krieger J, 1994. Signal recognition and transduction in olfactory neurons. Biochem. Biophys. Acta, 1224(2): 277-287.
Cui HH, Gu SH, Zhu XQ, Wei Y, Liu HW, Khalid HD, Guo YY, Zhang YJ, 2016. Odorant-binding and chemosensory proteins identified in the antennal transcriptome of Adelphocoris suturalis Jakovlev. Comp. Biochem. Physiol. D, 24: 139-145.
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Field LM, Pickett JA, Wadhams LJ, 2000. Molecular studies in insect olfaction. Insect Mol. Biol., 9(6): 545-551.
Fu NN, Liu J, Qu C, Wang R, Xu YH, Luo C, Li FQ, 2017. Analysis of Corythucha ciliata CcilCSP1 structure and prediction of its binding to host-plant volatiles. Sci. Silv. Sin., 53(10): 109-117. [付宁宁, 刘佳, 渠成, 王然, 许奕华, 罗晨, 李峰奇, 2017. 悬铃木方翅网蝽化学感受蛋白CcilCSP1的结构及其结合寄主挥发物的预测分析. 林业科学, 53(10): 109-117]
Gu SH, Wang SP, Zhang XY, Wu KM, Guo YY, Zhou JJ, Zhang YJ, 2011. Identification and tissue distribution of odorant binding protein genes in the lucerne plant bug Adelphocoris lineolatus (Goeze). Insect Biochem. Mol., 41(4): 254-263.
Gu SH, Wu KM, Guo YY, Field LM, Pickett JA, Zhang YJ, Zhou JJ, 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(9): e73524.
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He M, He P, 2014. Molecular characterization, expression profiling, and binding properties of odorant binding protein genes in the whitebacked planthopper, Sogatella furcifera. Comp. Biochem. Physiol. B, 174(1): 1-8.
Hua JF, Zhang S, Cui JJ, Wang DJ, Wang CY, Luo JY, Lv LM, 2012. Identification and binding characterization of three odorant binding proteins and one chemosensory protein from Apolygus lucorum (Meyer-Dur). J. Chem. Ecol., 38(9): 1163-1170.
Hull JJ, Perera OP, Snodgrass GL, 2014. Cloning and expression profiling of odorant-binding proteins in the tarnished plant bug, Lygus lineolaris. Insect Mol. Biol., 23(1): 78-97.
Ji P, Gu SH, Liu JT, Zhu XQ, Guo YY, Zhou JJ, Zhang YJ, 2013. Identification and expression profile analysis of odorant-binding protein genes in Apolygus lucorum (Hemiptera: Miridae). Appl. Entomol. Zool., 48(3): 301-311.
Ju RT, Li B, 2010. Sycamore lace bug, Corythucha ciliata, an invasive alien pest rapidly spreading in urban China. Biodivers. Sci., 18(6): 638-646. [鞠瑞亭, 李博, 2010. 悬铃木方翅网蝽: 一种正在迅速扩张的城市外来入侵害虫. 生物多样性, 18(6): 638-646]
Kaissling KE, 2009. Olfactory perireceptor and receptor events in moths: a kinetic model revised. J. Comp. Physiol. A, 195(10): 895-922.
Leal WS, 2013. Odorant reception in insects: roles of receptors, binding proteins, and degrading enzymes. Annu. Rev. Entomol., 58(1): 373-391.
Li B, Dewey CN, 2011. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinform., 12(1): 93-99.
Li CR, Xia WS, Wang FL, 2007. First records of Corythucha ciliata (Say) in China (Hemiptera, Tingidae). Acta Zootaxon. Sin., 32(4): 944-946. [李传仁, 夏文胜, 王福莲, 2007. 悬铃木方翅网蝽在中国的首次发现. 动物分类学报, 32(4): 944-946]
Li FQ, Wang R, Qu C, Fu NN, Luo C, Xu YH, 2016. Sequencing and characterization of the invasive sycamore lace bug Corythucha ciliata (Hemiptera: Tingidae) transcriptome. PLoS ONE, 11(8): e160609.
Li GW, Du J, Li YP, Wu JX, 2015. Identification of putative olfactory genes from the oriental fruit moth Grapholita molesta via an antennal transcriptome analysis. PLoS ONE, 10(11): e0142193.
Liu NY, Zhu JY, Ji M, Yang B, Ze SZ, 2017. Chemosensory genes from Pachypeltis micranthus, a natural enemy of the climbing hemp vine. J. Asia-Pac. Entomol., 20(2): 655-664.
Livak KJ, Schmittgen TD, 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCt method. Methods, 25(4): 402-408.
Maceljski M, 1986. Current status of Corythuca ciliata in Europe. EPPO Bull., 16(4): 621-624.
Oliveira DS, Brito NF, Nogueira FCS, Moreira MF, Leal WS, Soares MR, Melo ACA, 2017. Proteomic analysis of the kissing bug Rhodnius prolixus antenna. J. Insect Physiol., 100: 108-118.
szi B, Ladányi M, Hufnagel L, 2006. Population dynamics of the sycamore lace bug (Corythucha ciliata, Say, Heteroptera: Tingidae) in Hungary. Appl. Ecol. Env. Res., 4(1): 135-150.
Paula DP, Togawa RC, Costa MMC, Grynberg P, Martins NF, Andow DA, 2016. Identification and expression profile of odorant-binding proteins in Halyomorpha halys (Hemiptera: Pentatomidae). Insect Mol. Biol., 25(5): 580-594.
Pelletier J, Leal WS, 2011. Characterization of olfactory genes in the antennae of the Southern house mosquito, Culex quinquefasciatus. J. Insect Physiol., 57(7): 915-929.
Pelosi P, Iovinella I, Felicioli A, Dani FR, 2014. Soluble proteins of chemical communication: an overview across arthropods. Front. Physiol., 5: 320.
Picker C, Griffiths MD, 2015. Sycamore tree lace bug (Corythucha ciliata Say) (Hemiptera: Tingidae) reaches Africa. Afr. Entomol., 23(1): 247-249.
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Song YQ, Dong JF, Chen QX, Hu ZJ, Sun HZ, 2017. Analysis of the antennal transcriptome and chemoreception-related genes of the bean bug, Riptortus pedestris (Hemiptera: Alydidae). Acta Entomol. Sin., 60(10): 1120-1128. [宋月芹, 董钧锋, 陈庆霄, 胡振杰, 孙会忠, 2017. 点蜂缘蝽触角转录组及化学感受相关基因的分析. 昆虫学报, 60(10): 1120-1128]
Sun YL, Huang LQ, Pelosi P, Wang CZ, 2012. Expression in antennae and reproductive organs suggests a dual role of an odorant-binding protein in two sibling Helicoverpa species. PLoS ONE, 7(1): e30040.
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Tsitsanou KE, Drakou CE, Thireou T, Gruber AV, Kythreoti K, Azem A, Fessas D, Eliopoulos E, Iatrou K, Zographos SE, 2013. The crystal and solution studies of the “Plus-C”odorant binding protein 48 from Anopheles gambiae: control of binding specificity through 3D domain-swapping. J. Biol. Chem., 288(46): 33427-33438.
Vieira FG, Rozas J, 2011. Comparative genomics of the odorant-binding and chemosensory protein gene families across the Arthropoda: origin and evolutionary history of the chemosensory system. Genome Biol. Evol., 3(1): 476-490.
Vogt RG, Rybczynski R, Lerner MR, 1991. Molecular cloning and sequencing of general odorant-binding proteins GOBP1 and GOBP2 from the tobacco hawk moth Manduca sexta: comparisons with other insect OBPs and their signal peptides. J. Neurosci., 11(10): 2972-2984.
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Zhou JJ, 2010. Odorant-binding proteins in insects. Vitam. Horm., 83: 241-272.
Zhou JJ, Huang W, Zhang GA, Pickett JA, Field LM, 2004. "Plus-C" odorant-binding protein genes in two Drosophila species and the malaria mosquito Anopheles gambiae. Gene, 327(1): 117-129.
Zhou JJ, Vieira FG, He XL, Smadia C, Liu R, Rozas J, Field LM, 2010. Genome annotation and comparative analysis of the odorant-binding proteins and chemosensory proteins in the pea aphid Acyrthosiphon pisum. Insect Mol. Biol., 19(Suppl. 2): 113-122.
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Zhu J, Guo MB, Ban LP, Song LM, Liu Y, Pelosi P, Wang GR, 2018. Niemann-Pick C2 proteins: a new function for an old family. Front. Physiol., 9: 52.
Benton R, Vannice KS, Gomezdiaz C, Vosshall LB, 2009. Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila. Cell, 136(1): 149-162.
Biessmann H, Nguyen QK, Le D, Walter MF, 2005. Microarray-based survey of a subset of putative olfactory genes in the mosquito Anopheles gambiae. Insect Mol. Biol., 14(6): 575-589.
Breer H, Raming K, Krieger J, 1994. Signal recognition and transduction in olfactory neurons. Biochem. Biophys. Acta, 1224(2): 277-287.
Cui HH, Gu SH, Zhu XQ, Wei Y, Liu HW, Khalid HD, Guo YY, Zhang YJ, 2016. Odorant-binding and chemosensory proteins identified in the antennal transcriptome of Adelphocoris suturalis Jakovlev. Comp. Biochem. Physiol. D, 24: 139-145.
Dickens JC, Callahan FE, Wergin WP, Erbe EF, 1995. Olfaction in a hemimetabolous insect: antennal-specific protein in adult Lygus lineolaris (Heteroptera: Miridae). J. Insect Physiol., 41(10): 857-867.
Field LM, Pickett JA, Wadhams LJ, 2000. Molecular studies in insect olfaction. Insect Mol. Biol., 9(6): 545-551.
Fu NN, Liu J, Qu C, Wang R, Xu YH, Luo C, Li FQ, 2017. Analysis of Corythucha ciliata CcilCSP1 structure and prediction of its binding to host-plant volatiles. Sci. Silv. Sin., 53(10): 109-117. [付宁宁, 刘佳, 渠成, 王然, 许奕华, 罗晨, 李峰奇, 2017. 悬铃木方翅网蝽化学感受蛋白CcilCSP1的结构及其结合寄主挥发物的预测分析. 林业科学, 53(10): 109-117]
Gu SH, Wang SP, Zhang XY, Wu KM, Guo YY, Zhou JJ, Zhang YJ, 2011. Identification and tissue distribution of odorant binding protein genes in the lucerne plant bug Adelphocoris lineolatus (Goeze). Insect Biochem. Mol., 41(4): 254-263.
Gu SH, Wu KM, Guo YY, Field LM, Pickett JA, Zhang YJ, Zhou JJ, 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(9): e73524.
Halbert SE, Meekef JR, 1998. The sycamore lace bug, Corythucha ciliata (Say) (Hemiptera: Tingidae). Florida Department of Agriculture and Consumer Services, Division of Plant Industry. Entomol. Circ., 387: 1-2.
He M, He P, 2014. Molecular characterization, expression profiling, and binding properties of odorant binding protein genes in the whitebacked planthopper, Sogatella furcifera. Comp. Biochem. Physiol. B, 174(1): 1-8.
Hua JF, Zhang S, Cui JJ, Wang DJ, Wang CY, Luo JY, Lv LM, 2012. Identification and binding characterization of three odorant binding proteins and one chemosensory protein from Apolygus lucorum (Meyer-Dur). J. Chem. Ecol., 38(9): 1163-1170.
Hull JJ, Perera OP, Snodgrass GL, 2014. Cloning and expression profiling of odorant-binding proteins in the tarnished plant bug, Lygus lineolaris. Insect Mol. Biol., 23(1): 78-97.
Ji P, Gu SH, Liu JT, Zhu XQ, Guo YY, Zhou JJ, Zhang YJ, 2013. Identification and expression profile analysis of odorant-binding protein genes in Apolygus lucorum (Hemiptera: Miridae). Appl. Entomol. Zool., 48(3): 301-311.
Ju RT, Li B, 2010. Sycamore lace bug, Corythucha ciliata, an invasive alien pest rapidly spreading in urban China. Biodivers. Sci., 18(6): 638-646. [鞠瑞亭, 李博, 2010. 悬铃木方翅网蝽: 一种正在迅速扩张的城市外来入侵害虫. 生物多样性, 18(6): 638-646]
Kaissling KE, 2009. Olfactory perireceptor and receptor events in moths: a kinetic model revised. J. Comp. Physiol. A, 195(10): 895-922.
Leal WS, 2013. Odorant reception in insects: roles of receptors, binding proteins, and degrading enzymes. Annu. Rev. Entomol., 58(1): 373-391.
Li B, Dewey CN, 2011. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinform., 12(1): 93-99.
Li CR, Xia WS, Wang FL, 2007. First records of Corythucha ciliata (Say) in China (Hemiptera, Tingidae). Acta Zootaxon. Sin., 32(4): 944-946. [李传仁, 夏文胜, 王福莲, 2007. 悬铃木方翅网蝽在中国的首次发现. 动物分类学报, 32(4): 944-946]
Li FQ, Wang R, Qu C, Fu NN, Luo C, Xu YH, 2016. Sequencing and characterization of the invasive sycamore lace bug Corythucha ciliata (Hemiptera: Tingidae) transcriptome. PLoS ONE, 11(8): e160609.
Li GW, Du J, Li YP, Wu JX, 2015. Identification of putative olfactory genes from the oriental fruit moth Grapholita molesta via an antennal transcriptome analysis. PLoS ONE, 10(11): e0142193.
Liu NY, Zhu JY, Ji M, Yang B, Ze SZ, 2017. Chemosensory genes from Pachypeltis micranthus, a natural enemy of the climbing hemp vine. J. Asia-Pac. Entomol., 20(2): 655-664.
Livak KJ, Schmittgen TD, 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCt method. Methods, 25(4): 402-408.
Maceljski M, 1986. Current status of Corythuca ciliata in Europe. EPPO Bull., 16(4): 621-624.
Oliveira DS, Brito NF, Nogueira FCS, Moreira MF, Leal WS, Soares MR, Melo ACA, 2017. Proteomic analysis of the kissing bug Rhodnius prolixus antenna. J. Insect Physiol., 100: 108-118.
szi B, Ladányi M, Hufnagel L, 2006. Population dynamics of the sycamore lace bug (Corythucha ciliata, Say, Heteroptera: Tingidae) in Hungary. Appl. Ecol. Env. Res., 4(1): 135-150.
Paula DP, Togawa RC, Costa MMC, Grynberg P, Martins NF, Andow DA, 2016. Identification and expression profile of odorant-binding proteins in Halyomorpha halys (Hemiptera: Pentatomidae). Insect Mol. Biol., 25(5): 580-594.
Pelletier J, Leal WS, 2011. Characterization of olfactory genes in the antennae of the Southern house mosquito, Culex quinquefasciatus. J. Insect Physiol., 57(7): 915-929.
Pelosi P, Iovinella I, Felicioli A, Dani FR, 2014. Soluble proteins of chemical communication: an overview across arthropods. Front. Physiol., 5: 320.
Picker C, Griffiths MD, 2015. Sycamore tree lace bug (Corythucha ciliata Say) (Hemiptera: Tingidae) reaches Africa. Afr. Entomol., 23(1): 247-249.
Prado CE, 1990. Presencia en chile de Corythucha ciliata (Say) (Hemiptera: Heteroptera: Tingidae). Rev. Chilena Ent., 18: 53-55.
Song YQ, Dong JF, Chen QX, Hu ZJ, Sun HZ, 2017. Analysis of the antennal transcriptome and chemoreception-related genes of the bean bug, Riptortus pedestris (Hemiptera: Alydidae). Acta Entomol. Sin., 60(10): 1120-1128. [宋月芹, 董钧锋, 陈庆霄, 胡振杰, 孙会忠, 2017. 点蜂缘蝽触角转录组及化学感受相关基因的分析. 昆虫学报, 60(10): 1120-1128]
Sun YL, Huang LQ, Pelosi P, Wang CZ, 2012. Expression in antennae and reproductive organs suggests a dual role of an odorant-binding protein in two sibling Helicoverpa species. PLoS ONE, 7(1): e30040.
Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, Van BMJ, Salzberg SL, Wold BJ, Pachter L, 2010. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol., 28(5): 511-515.
Tsitsanou KE, Drakou CE, Thireou T, Gruber AV, Kythreoti K, Azem A, Fessas D, Eliopoulos E, Iatrou K, Zographos SE, 2013. The crystal and solution studies of the “Plus-C”odorant binding protein 48 from Anopheles gambiae: control of binding specificity through 3D domain-swapping. J. Biol. Chem., 288(46): 33427-33438.
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