Hostname: page-component-76fb5796d-22dnz Total loading time: 0 Render date: 2024-04-26T08:44:01.951Z Has data issue: false hasContentIssue false
  • English
  • Français

Spatiotemporal expression profiling of the farnesyl diphosphate synthase genes in aphids and analysis of their associations with the biosynthesis of alarm pheromone

Published online by Cambridge University Press:  01 October 2018

Y.-J. Cheng  and
Z.-X. Li
Y.-J. Cheng
Affiliation:
Department of Entomology and MOA Key Laboratory for Monitoring and Environment-Friendly Control of Crop Pests, College of Plant Protection, China Agricultural University, Beijing 100193, China
Z.-X. Li*
Affiliation:
Department of Entomology and MOA Key Laboratory for Monitoring and Environment-Friendly Control of Crop Pests, College of Plant Protection, China Agricultural University, Beijing 100193, China
*
*Author for correspondence Phone/Fax: +86 10 62733608 E-mail: zxli@cau.edu.cn
Get access Rights & Permissions [Opens in a new window]

Abstract

The alarm behavior plays a key role in the ecology of aphids, but the site and molecular mechanism for the biosynthesis of aphid alarm pheromone are largely unknown. Farnesyl diphosphate synthase (FPPS) catalyzes the synthesis of FPP, providing the precursor for the alarm pheromone (E)-β-farnesene (EβF), and we speculate that FPPS is closely associated with the biosynthetic pathway of EβF. We firstly analyzed the spatiotemporal expression of FPPS genes by using quantitative reverse transcription-polymerase chain reaction, showing that they were expressed uninterruptedly from the embryonic stage to adult stage, with an obvious increasing trend from embryo to 4th-instar in the green peach aphid Myzus persicae, but FPPS1 had an overall significantly higher expression level than FPPS2; both FPPS1 and FPPS2 exhibited the highest expression in the cornicle area. This expression pattern was verified in Acyrthosiphon pisum, suggesting that FPPS1 may play a more important role in aphids and the cornicle area is most likely the site for EβF biosynthesis. We thus conducted a quantitative measurement of EβF in M. persicae by gas chromatography-mass spectrometry. The data obtained were used to perform an association analysis with the expression data, revealing that the content of EβF per aphid was significantly correlated with the mean weight per aphid (r = 0.8534, P = 0.0307) and the expression level of FPPS1 (r = 0.9134, P = 0.0109), but not with that of FPPS2 (r = 0.4113, P = 0.4179); the concentration of EβF per milligram of aphid was not correlated with the mean weight per aphid or the expression level of FPPS genes. These data suggest that FPPS1 may play a key role in the biosynthesis of aphid alarm pheromone.

Keywords

farnesyl diphosphate synthasespatiotemporal expressionaphid alarm pheromone(E)-β-farneseneMyzus persicaeAcyrthosiphon pisum
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 109 , Issue 3 , June 2019 , pp. 398 - 407
Check for updates
Copyright
Copyright © Cambridge University Press 2018 

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

Almohamad, R., Verheggen, F.J., Francis, F., Lognay, G. & Haubruge, E. (2008) Emission of alarmpheromone by non-preyed aphid colonies. Journal of Applied Entomology 132, 601–604.Google Scholar
Beale, M.H., Birkett, M.A., Bruce, T.J., Chamberlain, K., Field, L.M., Huttly, A.K., Martin, J.L., Parker, R., Phillips, A.L., Pickett, J.A., Prosser, I.M., Shewry, P.R., Smart, L.E., Wadhams, L.J., Woodcock, C.M. & Zhang, Y. (2006) Aphid alarm pheromone produced by transgenic plants affects aphid and parasitoid behavior. Proceeding National Academy of Science USA 103, 10509–10513.Google Scholar
Bogaert, N.V., Jonghe, K.D., Damme, E.J.M.V., Maes, M. & Smagghe, G. (2015) Quantitation and localization of pospiviroids in aphids. Journal of Virological Methods 211, 51–54.Google Scholar
Bomtorin, A.D., Mackert, A., Rosa, G.C.C., Moda, L.M., Martins, J.R., Bitondi, M.M.G., Hartfelder, K. & Simões, Z.L. (2014) Juvenile hormone biosynthesis gene expression in the corpora allata of honey bee (Apis mellifera L.) female castes. PLoS ONE 9, e86923.Google Scholar
Bruce, T.J., Aradottr, G.I., Smart, L.E., Martin, J.L., Caulfield, J.C., Doherty, A., Sparks, C.A., Woodcock, C.M., Birkett, M.A., Napier, J.A., Jones, H.D. & Pickett, J.A. (2015) The first crop plant genetically engineered to release an insect pheromone for defence. Scientific Reports 5, 11183.Google Scholar
Byers, J.A. (2005) A cost of alarm pheromone production in cotton aphids, Aphis gossypii. Naturwissenschaften 92, 69–72.Google Scholar
Castillo-Gracia, M. & Couillaud, F. (1999) Molecular cloning and tissues expression of an insect farnesyl diphosphate synthase. European Journal of Biochemistry 262, 365–370.Google Scholar
Chen, S.W. & Edwards, J.S. (1972) Observations on the structure of secretory cells associated with aphid cornicles. Zeitschrift Für Zellforschung Und Mikroskopische Anatomie 130, 312–317.Google Scholar
Cheng, D., Meng, M., Peng, J., Qian, W.L., Kang, L.X. & Xia, Q.Y. (2014) Genome-wide comparison of genes involved in the biosynthesis, metabolism, and signaling of juvenile hormone between silkworm and other insects. Genetics and Molecular Biology 37, 444–459.Google Scholar
Cook, S.M., Khan, Z.R. & Pickett, J.A. (2007) The use of push-pull strategies in integrated pest management. Annual Review of Entomology 52, 375–400.Google Scholar
Cusson, M., Béliveau, C., Sen, S.E., Vandermoten, S., Rutledge, R.G., Stewart, D., Francis, F., Haubruge, E., Rehse, P., Huggins, D.J., Dowling, A.P. & Grant, G.H. (2006) Characterization and tissue-specific expression of two Lepidopteran farnesyl diphosphate synthase homologs: implications for the biosynthesis of ethyl-substituted juvenile hormones. PROTEINS: Structure, Function, and Bioinformatics 65, 742–758.Google Scholar
Dixon, A.F.G. & Agarwala, B.K. (1999) Ladybird-induced lifehistory changes in aphids. Proceedings of the Royal Society B Biological Sciences 266, 1549–1553.Google Scholar
Edwards, J.S. (1966) Defence by smear: supercooling in the cornicle wax of aphids. Nature 211, 73–74.Google Scholar
Francis, F., Vandermoten, S., Verheggen, F., Lognay, G. & Haubruge, E. (2005) Is the (E)-β-farnesene only volatile terpenoid in aphids? Journal of Applied Entomology 129, 6–11.Google Scholar
Gilg, A.B., Tittiger, C. & Blomquist, G.J. (2009) Unique animal prenyltransferase with monoterpene synthase activity. Naturwissenschaften 96, 731–735.Google Scholar
Green, S., Friel, E.N., Matich, A., Beuning, L.L., Cooney, J.M., Rowan, D.D. & MacRae, E. (2007) Unusual features of a recombinant apple alpha-farnesene synthase. Phytochemistry 68, 176–188.Google Scholar
Griffiths, D.C. & Pickett, J.A. (1980) A potential application of aphid alarm pheromones. Entomologia Experimentalis et Applicata 27, 199–201.Google Scholar
Huang, J., Marchal, E., Hult, E.F. & Tobe, S.S. (2015) Characterization of the juvenile hormone pathway in the viviparous cockroach, Diploptera punctata. PLoS ONE 10, e0117291.Google Scholar
Kang, Z.W., Liu, F.H., Tian, H.G., Zhang, M., Guo, S.S. & Liu, T.X. (2017) 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
Kaitala, A. (1991) Phenotypic plasticity in reproductive behaviour of waterstriders: trade-offs between reproduction and longevity during food stress. Functional Ecology 5, 12–18.Google Scholar
Kinjoh, T., Kaneko, Y., Itoyama, K., Mita, K., Hiruma, K. & Shinoda, T. (2007) Control of juvenile hormone biosynthesis in Bombyx mori: cloning of the enzymes in the mevalonate pathway and assessment of their developmental expression in the corpora allata. Insect Biochemistry and Molecular Biology 37, 808–818.Google Scholar
Kunert, G., Otto, S., Röse, U.S.R., Gershenzon, J. & Weisser, W.W. (2005) Alarm pheromone mediates production of winged dispersal morphs in aphids. Ecology Letters 8, 596–603.Google Scholar
Legeai, F., Shigenobu, S., Gauthier, J.P., Colbourne, J., Rispe, C., Collin, O., Richards, S, Wilson, A.C., Murphy, T. & Tagu, D. (2010) Aphidbase: a centralized bioinformatic resource for annotation of the pea aphid genome. Insect Molecular Biology 19, 5–12.Google Scholar
Lewis, M.J., Prosser, I.M., Mohib, A. & Field, L.M. (2008) Cloning and characterization of a prenyltransferase from the aphid Myzus persicae with potential involvement in alarm pheromone biosynthesis. Insect Molecular Biology 17, 437–443.Google Scholar
Li, Q., Meng, Q.W., Lu, F.G., Guo, W.C. & Li, G.Q. (2016) Identification of ten mevalonate enzyme-encoding genes and their expression in response to juvenile hormone levels in Leptinotarsa decemlineata (Say). Gene 584, 136–147.Google Scholar
Livak, K.J. & Schmittgen, T.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C (T)) method. Methods 25, 402–408.Google Scholar
Ma, G.Y., Sun, X.F., Zhang, Y.L., Li, Z.X. & Shen, Z.R. (2010) Molecular cloning and characterization of a prenyltransferase from the cotton aphid, Aphis gossypii. Insect Biochemistry and Molecular Biology 40, 552–561.Google Scholar
Mutti, N.S., Park, Y., Reese, J.C. & Reeck, G.R. (2006) RNAi knockdown of a salivary transcript leading to lethality in the pea aphid, Acyrthosiphon pisum. Journal of Insect Science 6, 1–7.Google Scholar
Pfaffl, M.W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research 29, e45.Google Scholar
Picaud, S., Brodelius, M. & Brodelius, P.E. (2005) Expression, purification and characterization of recombinant (E)-β-farnesene synthase from Artemisia annua. Phytochemistry 66, 961–967.Google Scholar
Sallaud, C., Rontein, D., Onillon, S., Jabès, F., Duffé, P., Giacalone, C., Thoraval, S., Escoffier, C., Herbette, G., Leonhardt, N., Causse, M. & Tissier, A. (2009) A novel pathway for sesquiterpene biosynthesis from Z,Z-farnesyl pyrophosphate in the wild tomato Solanum habrochaites. Plant Cell 21, 301–317.Google Scholar
Sen, S.E., Trobaugh, C., Béliveau, C., Richard, T. & Cusson, M. (2007) Cloning, expression and characterization of a dipteran farnesyl diphosphate synthase. Insect Biochemistry and Molecular Biology 37, 1198–1206..Google Scholar
Sun, X.F. & Li, Z.X. (2012) In silico and in vitro analyses identified three amino acid residues critical to the catalysis of two aphid farnesyl diphosphate synthase. Protein Journal 31, 417–424.Google Scholar
Sun, Z.J. & Li, Z.X. (2017) Host plants and obligate endosymbionts are not the sources for biosynthesis of the aphid alarm pheromone. Scientific Reports 7, 6461.Google Scholar
Taban, A.H., Tittiger, C., Blomquist, G.J. & Welch, W.H. (2009) Isolation and characterization of farnesyl diphosphate synthase from the cotton boll weevil, Anthonomus grandis. Archives of Insect Biochemistry and Physiology 71, 88–104.Google Scholar
The International Aphid Genomics Consortium (2010) Genome sequence of the pea aphid Acyrthosiphon pisum. PLoS Biology 8, 1–24.Google Scholar
Truman, J.W. & Riddiford, L.M. (2002) Endocrine insights into the evolution of metamorphosis in insects. Annual Review of Entomology 47, 467–500.Google Scholar
van Emden, H.F., Dingley, J., Dewhirst, S.Y., Pickett, J.A., Woodcock, C.M. & Wadhams, L.J. (2014) The effect of artificial diet on the production of alarm pheromone by Myzus persicae. Physiological Entomology 39, 285–291.Google Scholar
Verheggen, F.J., Haubruge, E., Moraes, C.M.D. & Mescher, M.C. (2009) Social enviroment influences aphid production of alarmpheromone. Behavioral Ecology 20, 283–288.Google Scholar
Yang, C., Pan, H., Liu, Y. & Zhou, X. (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.Google Scholar
Yu, X.D., Jones, H.D., Ma, Y., Wang, G., Xu, Z., Zhang, B., Zhang, Y., Ren, G., Pickett, J.A. & Xia, L. (2012) (E)-β-farnesene synthase genes affect aphid (Myzus persicae) infestation in tobacco (Nicotiana tabacum). Functional and Integrative Genomics 12, 207–213.Google Scholar
Zha, S., Yin, Y., Wang, Y., Huang, Y., Li, Y. & Wang, Z. (2017) Cloning and functional analysis of farnesyl pyrophosphate synthase (FPPS) gene from Mylabris cichorii. Biotechnology and Applied Biochemistry 64, 667–676.Google Scholar
Zhang, Y.L. & Li, Z.X. (2008) Two different farnesyl diphosphate synthase genes exist in the genome of the green peach aphid, Myzus persicae. Genome 51, 501–510.Google Scholar
Zhang, Y.L. & Li, Z.X. (2012) Functional analysis and molecular docking identify two active short-chain prenyltransferases in the green peach aphid, Myzus persicae. Archives of Insect Biochemistry Physiology 81, 63–76.Google Scholar
Zhang, H. & Li, Z.X. (2013) In vitro, and in vivo, characterization of a novel insect decaprenyl diphosphate synthase: a two-major step catalytic mechanism is proposed. Biochemical and Biophysical Research Communication 442, 105–111.Google Scholar
Zhang, H. & Li, Z.X. (2014) A type-III insect geranylgeranyl diphosphate synthase with a novel catalytic property. Protein and Peptide Letters 21, 615–623.Google Scholar
Zhang, W., Ma, L., Xiao, H., Liu, C., Chen, L., Wu, S. & Liang, G. (2017) Identification and characterization of genes involving the early step of juvenile hormone pathway in Helicoverpa armigera. Scientific Reports 7, 16542.Google Scholar
Zhao, B., Lei, L., Vassylyev, D.G., Lin, X., Cane, D.E., Kelly, S.L., Yuan, H., Lamb, D.C. & Waterman, M.R. (2009) Crystal structure of albaflavenone monooxygenase containing a moonlighting terpene synthase active site. Journal of Biological Chemistry 284, 36711–36719.Google Scholar
Supplementary material: File

Cheng and Li supplementary material

Cheng and Li supplementary material 1

Download Cheng and Li supplementary material(File)
File 372.3 KB