Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-13T02:49:06.751Z Has data issue: false hasContentIssue false
  • English
  • Français

The identification and expression analysis of candidate chemosensory genes in the bird cherry-oat aphid Rhopalosiphum padi (L.)

Published online by Cambridge University Press:  04 December 2017

Z.-W. Kang ,
F.-H. Liu ,
R.-P. Pang ,
W.-B. Yu ,
X.-L. Tan ,
Z.-Q. Zheng ,
H.-G. Tian  and
T.-X. Liu
Z.-W. Kang
Affiliation:
State Key Laboratory of Crop Stress Biology for the Arid Areas, and Key Laboratory of Northwest Loess Plateau Crop Pest Management of Ministry of Agriculture, Northwest A&F University, Yangling, Shaanxi, 712100, China
F.-H. Liu
Affiliation:
State Key Laboratory of Integrated Management of Pest and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, 100101, China
R.-P. Pang
Affiliation:
State Key Laboratory of Crop Stress Biology for the Arid Areas, and Key Laboratory of Northwest Loess Plateau Crop Pest Management of Ministry of Agriculture, Northwest A&F University, Yangling, Shaanxi, 712100, China
W.-B. Yu
Affiliation:
State Key Laboratory of Crop Stress Biology for the Arid Areas, and Key Laboratory of Northwest Loess Plateau Crop Pest Management of Ministry of Agriculture, Northwest A&F University, Yangling, Shaanxi, 712100, China
X.-L. Tan
Affiliation:
State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China
Z.-Q. Zheng
Affiliation:
State Key Laboratory of Crop Stress Biology for the Arid Areas, and Key Laboratory of Northwest Loess Plateau Crop Pest Management of Ministry of Agriculture, Northwest A&F University, Yangling, Shaanxi, 712100, China
H.-G. Tian*
Affiliation:
State Key Laboratory of Crop Stress Biology for the Arid Areas, and Key Laboratory of Northwest Loess Plateau Crop Pest Management of Ministry of Agriculture, Northwest A&F University, Yangling, Shaanxi, 712100, China
T.-X. Liu*
Affiliation:
State Key Laboratory of Crop Stress Biology for the Arid Areas, and Key Laboratory of Northwest Loess Plateau Crop Pest Management of Ministry of Agriculture, Northwest A&F University, Yangling, Shaanxi, 712100, China
*
*Author for correspondence Tel/Fax: +86 29 87092663 E-mail: tianhg@nwsuaf.edu.cn; txliu@nwsuaf.edu.cn
*Author for correspondence Tel/Fax: +86 29 87092663 E-mail: tianhg@nwsuaf.edu.cn; txliu@nwsuaf.edu.cn
Get access Rights & Permissions [Opens in a new window]

Abstract

The bird cherry-oat aphid Rhopalosiphum padi (L.) is one of the most important wheat pests with polyphagia and autumn migrants. And, chemosensory genes were thought to play a key role in insect searching their hosts, food and mate. However, a systematic identification of the chemosensory genes in this pest has not been reported. Thus, in this study, we identified 14 odorant-binding proteins, nine chemosensory proteins, one sensory neuron membrane protein, 15 odorant receptors, 19 gustatory receptors and 16 ionotropic receptors from R. padi transcriptomes with a significantly similarity (E-value < 10−5) to known chemosensory genes in Acyrthosiphon pisum and Aphis gossypii. In addition, real-time quantitative polymerase chain reaction (RT-qPCR) was employed to determine the expression profiles of obtained genes. Among these obtained genes, we selected 23 chemosensory genes to analyze their expression patterns in different tissues, wing morphs and host plants. We found that except RpOBP1, RpOBP3, RpOBP4 and RpOBP5, the rest of the selected genes were highly expressed in the head with antennae compared with body without head and antennae. Besides that, the stimulation and depression of chemosensory genes by plant switch indicated that chemosensory genes might be involved in the plant suitability assessment. These results not only provide insights for the potential roles of chemosensory genes in plant search and perception of R. padi but also provide initial background information for the further research on the molecular mechanism of the polyphagia and autumn migrants of it. Furthermore, these chemosensory genes are also the candidate targets for pest management control in future.

Keywords

Rhopalosiphum paditranscriptomechemosensory genephylogenetic analysisexpression pattern
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 108 , Issue 5 , October 2018 , pp. 645 - 657
Check for updates
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

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.Google Scholar
Agnihotri, A.R., Roy, A.A. & Joshi, R.S. (2016) Gustatory receptors in Lepidoptera: chemosensation and beyond. Insect Molecular Biology 25, 519–529.Google Scholar
Ahmed, T., Zhang, T.T., Wang, Z.Y., He, K.L. & Bai, S.X. (2016) Gene set of chemosensory receptors in the polyembryonic endoparasitoid Macrocentrus cingulum. Scientific Reports 6, 24078.Google Scholar
Ai, M., Min, S., Grosjean, Y., Leblanc, C., Bell, R., Benton, R. & Suh, G.S. (2010) Acid sensing by the Drosophila olfactory system. Nature 468, 691–695.Google Scholar
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.Google Scholar
Cao, H.H., Liu, H.R., Zhang, Z.F. & Liu, T.X. (2016) The green peach aphid Myzus persicae perform better on pre-infested Chinese cabbage Brassica pekinensis by enhancing host plant nutritional quality. Scientific Reports 6, 21954.Google Scholar
Carey, A.F., Wang, G., Su, C.Y., Zwiebel, L.J. & Carlson, J.R. (2010) Odorant reception in the malaria mosquito Anopheles gambiae. Nature 464, 66–71.Google Scholar
Chang, H., Liu, Y., Yang, T., Pelosi, P., Dong, S.L. & Wang, G.R. (2015) Pheromone binding proteins enhance the sensitivity of olfactory receptors to sex pheromones in Chilo suppressalis. Scientific Reports 5, 13093.Google Scholar
Cui, H.H., Gu, S.H., Zhu, X.Q., Wei, Y., Liu, H.W., Khalid, H.D., Guo, Y.Y. & Zhang, Y.J. (2017) Odorant-binding and chemosensory proteins identified in the antennal transcriptome of Adelphocoris suturalis Jakovlev. Comparative Biochemistry and Physiology 24, 139–145.Google Scholar
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.Google Scholar
Dewhirst, S.Y. & Pickett, J.A. (2009) Production of semiochemical and allelobiotic agents as a consequence of aphid feeding. Chemoecology 20, 89–96.Google Scholar
Dixon, A. (1971) The life-cycle and host preferences of the bird cherry-oat aphid, Rhopalosiphum padi L., and their bearing on the theories of host alternation in aphids. Annals of Applied Biology 68, 135–147.Google Scholar
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.Google Scholar
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 prolixus. Insect Biochemistry and Molecular Biology 69, 82–90.Google Scholar
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.Google Scholar
Gu, S.H., Zhou, J.J., Gao, S., Wang, D.H., Li, X.C., Guo, Y.Y. & Zhang, Y.J. (2015) Identification and comparative expression analysis of odorant binding protein genes in the tobacco cutworm Spodoptera litura. Scientific Reports 5, 13800.Google Scholar
Guo, S.S., Zhang, M. & Liu, T.X. (2016) Insulin-related peptide 5 is involved in regulating embryo development and biochemical composition in pea aphid with wing polyphenism. Frontier Physiology 7, 31.Google Scholar
Hallem, E.A., Dahanukar, A. & Carlson, J.R. (2006) Insect odor and taste receptors. Annual Review of Entomology 51, 113–135.Google Scholar
He, P., Zhang, J., Liu, N.Y., Zhang, Y.N., Yang, K. & Dong, S.L. (2011) Distinct expression profiles and different functions of odorant binding proteins in Nilaparvata lugens Stål. PLoS ONE 6, e28921.Google Scholar
Hojo, M.K., Ishii, K., Sakura, M., Yamaguchi, K., Shigenobu, S. & Ozaki, M. (2015) Antennal RNA-sequencing analysis reveals evolutionary aspects of chemosensory proteins in the carpenter ant, Camponotus japonicus. Scientific Reports 5, 13541.Google Scholar
Hussain, A., Zhang, M., Ucpunar, H.K., Svensson, T., Quillery, E., Gompel, N., Ignell, R. & Grunwald Kadow, I.C. (2016) Ionotropic chemosensory receptors mediate the taste and smell of polyamines. PLoS Biology 14, e1002454.Google Scholar
Jacobs, S.P., Liggins, A.P., Zhou, J.J., Pickett, J.A., Jin, X. & Field, L.M. (2005) OS-D-like genes and their expression in aphids (Hemiptera: Aphididae). Insect Molecular Biology 14, 423–432.Google Scholar
Jiang, X.J., Ning, C., Guo, H., Jia, Y.Y., Huang, L.Q., Qu, M.J. & Wang, C.Z. (2015) A gustatory receptor tuned to D-fructose in antennal sensilla chaetica of Helicoverpa armigera. Insect Biochemistry and Molecular Biology 60, 39–46.Google Scholar
Jiang, X., Pregitzer, P., Grosse-Wilde, E., Breer, H. & Krieger, J. (2016) Identification and characterization of two “Sensory Neuron Membrane Proteins” (SNMPs) of the desert locust, Schistocerca gregaria (Orthoptera: Acrididae). Journal of Insect Science 16, 33.Google Scholar
Kang, Z.W., Tian, H.G., Liu, F.H., Liu, X., Jing, X.F & Liu, T.X. (2017 a) Identification and expression analysis of chemosensory receptor genes in an aphid endoparasitoid Aphidius gifuensis. Scientific Reports 7, 3939.Google Scholar
Kang, Z.W., Liu, F.H., Tian, H.G., Zhang, M., Guo, S.S & Liu, T.X. (2017 b) Evaluation of the reference genes for expression analysis using quantitative real-time polymerase chain reaction in the green peach aphid, Myzus persicae. Insect Science 24, 222–234.Google Scholar
Kim, J.H. & Jander, G. (2007) Myzus persicae (green peach aphid) feeding on Arabidopsis induces the formation of a deterrent indole glucosinolate. Plant Journal 49, 1008–1019.Google Scholar
Li, H.L, Wu, F., Zhao, L., Tan, J., Jiang, H.T. & Hu, F.L. (2015 a) Neonicotinoid insecticide interact with honeybee odorant-binding protein: implication for olfactory dysfunction. International Journal of Biological Macromolecules 81, 624–630.Google Scholar
Li, X.M., Zhu, X.Y., Wang, Z.Q., Wang, Y., He, P., Chen, G., Sun, L., Deng, D.G. & Zhang, Y.N. (2015 b) Candidate chemosensory genes identified in Colaphellus bowringi by antennal transcriptome analysis. BMC Genomics 16, 1028.Google Scholar
Li, Z.Q., Zhang, S., Luo, J.Y., Wang, S.B., Wang, C.Y., Lv, L.M., Dong, S.L. & Cui, J.J. (2015 c) Identification and expression pattern of candidate olfactory genes in Chrysoperla sinica by antennal transcriptome analysis. Comparative Biochemistry and Physiology 15, 28–38.Google Scholar
Liu, C., Pitts, R.J., Bohbot, J.D., Jones, P.L., Wang, G. & Zwiebel, L.J. (2010) Distinct olfactory signaling mechanisms in the malaria vector mosquito Anopheles gambiae. PLoS Biology 8, e1000467.Google Scholar
Liu, C., Zhang, J., Liu, Y., Wang, G.R. & Dong, S.L. (2014) Expression of SNMP1 and SNMP2 genes in antennal sensilla of Spodoptera exigua (Hubner). Archives of Insect Biochemistry and Physiology 85, 114–126.Google Scholar
Liu, S., Rao, X.J., Li, M.Y., Feng, M.F., He, M.Z. & Li, S.G. (2015) Identification of candidate chemosensory genes in the antennal transcriptome of Tenebrio molitor (Coleoptera: Tenebrionidae). Comparative Biochemistry and Physiology 13, 44–51.Google Scholar
Liu, Y.H., Kang, Z.W., Guo, Y., Zhu, G.S., Rahman Shah, M.M., Song, Y., Fan, Y.L., Jing, X.F. & Liu, T.X. (2016) Nitrogen hurdle of host alternation for a polyphagous aphid and the associated changes of endosymbionts. Scientific Reports 6, 24781.Google Scholar
Mang, D., Shu, M., Endo, H., Yoshizawa, Y., Nagata, S., Kikuta, S. & Sato, R. (2016) Expression of a sugar clade gustatory receptor, BmGr6, in the oral sensory organs, midgut, and central nervous system of larvae of the silkworm Bombyx mori. Insect Biochemistry and Molecular Biology 70, 85–98.Google Scholar
Nam, K.J. & Hardie, J. (2014) Chemical aspects of host-acceptance behaviour in the bird cherry-oat aphid Rhopalosiphum padi: host-acceptance signals used by different morphs with the same genotype. Physiological Entomology 39, 143–152.Google Scholar
Nicholson, S.J., Nickerson, M.L., Dean, M., Song, Y., Hoyt, P.R., Rhee, H., Kim, C. & Puterka, G.J. (2015) The genome of Diuraphis noxia, a global aphid pest of small grains. BMC Genomics 16, 429.Google Scholar
Ning, C., Yang, K., Xu, M., Huang, L.Q. & Wang, C.Z. (2016) Functional validation of the carbon dioxide receptor in labial palps of Helicoverpa armigera moths. Insect Biochemistry and Molecular Biology 73, 12–19.Google Scholar
Niu, D.J., Liu, Y., Dong, X.T. & Dong, S.L. (2016) Transcriptome based identification and tissue expression profiles of chemosensory genes in Blattella germanica (Blattaria: Blattidae). Comparative Biochemistry and Physiology 18, 30–43.Google Scholar
Northey, T., Venthur, H., De Biasio, F., Chauviac, F.X., Cole, A., Ribeiro, K.A.J., 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.Google Scholar
Park, K.C., Elias, D., Donato, B. & Hardie, J. (2000) Electroantennogram and behavioural responses of different forms of the bird cherry-oat aphid, Rhopalosiphum padi, to sex pheromone and a plant volatile. Journal of Insect Physiology 46, 597–604.Google Scholar
Pescod, K.V., Quick, W.P & Douglas, A.E. 2007. Aphid responses to plants with genetically manipulated phloem nutrient levels. Physiological Entomology 32, 253–258.Google Scholar
Pettersson, J.P., Pickett, J.A., Pye, B.J., Quiroz, A., Smart, L.E., Wadhams, L.J & Woodcock, C.M. (1994). Winter host component reduces colonization by bird-cherry-oat aphid, Rhopalosiphum padi (L.) (Homoptera, Aphididae), and other aphids in cereal fields. Journal of Chemical Ecology 20, 2565–2574.Google Scholar
Qiao, H., Tuccori, E., He, X., Gazzano, A., Field, L., Zhou, J.J. & Pelosi, P. (2009) Discrimination of alarm pheromone (E)-beta-farnesene by aphid odorant-binding proteins. Insect Biochemistry and Molecular Biology 39, 414–419.Google Scholar
Sato, K., Tanaka, K & Touhara, K. (2011) Sugar-regulated cation channel formed by an insect gustatory receptor. Proceedings of the National Academy of Science of the USA 108, 11680–11685.Google Scholar
Sheng, S., Liao, C.W., Zheng, Y., Zhou, Y., Xu, Y., Song, W.M., He, P., Zhang, J. & Wu, F.A. (2017) Candidate chemosensory genes identified in the endoparasitoid Meteorus pulchricornis (Hymenoptera: Braconidae) by antennal transcriptome analysis. Comparative Biochemistry and Physiology 22, 20–31.Google Scholar
Sempruch, C., Marczuk, W., Leszczyński, B. & Czerniewicz, P. (2013) Participation of amino acid decarboxylases in biochemical interactions between triticale (Triticosecale; Poaceae) and bird cherry-oat aphid (Rhopalosiphum padi; Aphididae). Biochemical Systematics and Ecology 51, 349–356.Google Scholar
Sempruch, C., Golawska, S., Osinski, P., Leszczynski, B., Czerniewicz, P., Sytykiewicz, H. & Matok, H. (2016) Influence of selected plant amines on probing behaviour of bird cherry-oat aphid (Rhopalosiphum padi L.). Bulletin of Entomological Research 106, 368–377.Google Scholar
Takemura, M., Kuwahara, Y. & Nishida., R. (2006) Feeding responses of an oligophagous bean aphid, Megoura crassicauda, to primary and secondary substances in Vicia angustifolia. Entomologia Experimentalis et Applicata 121, 51–57.Google Scholar
Tan, K., Chen, W.W., Dong, S.H., Liu, X.W., Wang, Y.H. & Nieh, J.C. (2015) A neonicotinoid impairs olfactory learning in Asian honey bees (Apis cerana) exposed as larvae or as adults. Scientific Reports 5, 10989.Google Scholar
Vellichirammal, N.N., Madayiputhiya, N. & Brisson, J.A. (2016) The genomewide transcriptional response underlying the pea aphid wing polyphenism. Molecular Ecology 25, 4146–4160.Google Scholar
Wang, J., Li, D.Z., Min, S.F., Mi, F., Zhou, S.S. & Wang, M.Q. (2014) Analysis of chemosensory gene families in the beetle Monochamus alternatus and its parasitoid Dastarcus helophoroides. Comparative Biochemistry and Physiology 11, 1–8.Google Scholar
Wang, H., Wu, K.K., Liu, Y., Wu, Y.F. & Wang, X.F. (2015 a) Integrative proteomics to understand the transmission mechanism of Barley yellow dwarf virus-GPV by its insect vector Rhopalosiphum padi. Scientific Reports 5, 10971.Google Scholar
Wang, Z.F., Yang, P.P., Chen, D.F., Jiang, F., Li, Y., Wang, X.H. & Kang, L. (2015 b) Identification and functional analysis of olfactory receptor family reveal unusual characteristics of the olfactory system in the migratory locust. Cellular and Molecular Life Sciences 72, 4429–4443.Google Scholar
Xu, W., Papanicolaou, A., Zhang, H.J. & Anderson, A. (2016) Expansion of a bitter taste receptor family in a polyphagous insect herbivore. Scientific Reports 6, 23666.Google Scholar
Xue, W.X., Fan, J., Zhang, Y., Xu, Q.X., Han, Z., 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.Google Scholar
Zhang, R.R, Gao, G.Q. & Chen, H. (2016a) Silencing of the olfactory co-receptor gene in Dendroctonus armandi leads to EAG response declining to major host volatiles. Scientific Reports 6, 23136.Google Scholar
Zhang, R.B., Wang, B., Grossi, G., Falabella, P., Liu, Y., Yan, S.C., Lu, J., Xi, J.H. & Wang, G.R. (2016b) Molecular basis of alarm pheromone detection in aphids. Current Biology 27, 55–61.Google Scholar
Zheng, W.W., Peng, W., Zhu, C.P., Zhang, Q., Saccone, G & Zhang, H.Y. (2013). Identification and expression profile analysis of odorant binding proteins in the oriental fruit fly Bactrocera dorsalis. International Journal of Molecular Science 14, 14936–14949.Google Scholar
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-beta-farnesene bound to three odorant-binding proteins in the wheat aphid Sitobion avenae (Fabricius). Journal of Insect Physiology 58, 771–781.Google Scholar
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(Suppl 2), 113–122.Google Scholar
Zhou, C.X., Min, S.F., Tang, Y.L. & Wang, M.Q. (2015) Analysis of antennal transcriptome and odorant binding protein expression profiles of the recently identified parasitoid wasp, Sclerodermus sp. Comparative Biochemistry and Physiology 16, 10–19.Google Scholar
Zhu, F., Xu, P., Barbosa, R.M., Choo, Y.M. & Leal, W.S. (2013) RNAi-based demonstration of direct link between specific odorant receptors and mosquito oviposition behavior. Insect Biochemistry and Molecular Biology 43, 916–923.Google Scholar
Zhu, J., Ban, L.P., Song, L.M., Liu, Y., Pelosi, P. & Wang, G. R. (2016) General odorant-binding proteins and sex pheromone guide larvae of Plutella xylostella to better food. Insect Biochemistry and Molecular Biology 72, 10–19.Google Scholar
Zuo, Y.Y., Peng, X., Wang, K., Lin, F.F., Li, Y.T & Chen, M.H. (2016) Expression patterns, mutation detection and RNA interference of Rhopalosiphum padi voltage-gated sodium channel genes. Scientific Reports 6, 30166.Google Scholar
Supplementary material: File

Kang et al supplementary material 1

Supplementary Table

Download Kang et al supplementary material 1(File)
File 78.3 KB
Supplementary material: PDF

Kang et al supplementary material 2

Supplementary Figure

Download Kang et al supplementary material 2(PDF)
PDF 43 KB
Supplementary material: PDF

Kang et al supplementary material 3

Supplementary Figure

Download Kang et al supplementary material 3(PDF)
PDF 39.9 KB
Supplementary material: PDF

Kang et al supplementary material 4

Supplementary Figure

Download Kang et al supplementary material 4(PDF)
PDF 45 KB