Hostname: page-component-77c89778f8-sh8wx Total loading time: 0 Render date: 2024-07-17T06:06:26.703Z Has data issue: false hasContentIssue false

Production of alarm pheromone starts at embryo stage and is modulated by rearing conditions and farnesyl diphosphate synthase genes in the bird cherry-oat aphid Rhopalosiphum padi

Published online by Cambridge University Press:  10 April 2019

C.-X. Sun
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: +86 10 62732539 Fax: +86 10 6273 3608 E-mail: zxli@cau.edu.cn

Abstract

The major component of aphid alarm pheromone is (E)-β-farnesene (EβF), but the molecular mechanisms of EβF synthesis are poorly understood. Here we established a biological model to study the modulation of EβF synthesis in the bird cherry-oat aphid Rhopalosiphum padi by using quantitative polymerase chain reaction, gas chromatography/mass spectrometry and RNA interference. Our results showed that the rearing conditions significantly affected the weight of adult and modulated EβF synthesis in a transgenerational manner. Specifically, the quantity of EβF per milligram of aphid was significantly reduced in the individually reared adult or 1st-instar nymphs derived from 1-day-old adult reared individually, but EβF in the nymph derived from 2-day-old adult that experienced collective conditions returned to normal. Further study revealed that the production of EβF started in embryo and was extended to early nymphal stage, which was modulated by farnesyl diphosphate synthase genes (RpFPPS1 and RpFPPS2) and rearing conditions. Knockdown of RpFPPS1 and RpFPPS2 confirmed the role played by FPPS in the biosynthesis of aphid alarm pheromone. Our results suggested that the production of EβF starts at the embryo stage and is modulated by FPPS and rearing conditions in R. padi, which sheds lights on the modulatory mechanisms of EβF in the aphid.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2019 

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

Bellés, X., Martín, D. & Piulachs, M.D. (2005) The mevalonate pathway and the synthesis of juvenile hormone in insects. Annual Review of Entomology 50, 181199.Google Scholar
Bhatia, V., Maisnam, J., Jain, A., Sharma, K.K. & Bhattacharya, R. (2015) Aphid-repellent pheromone e-β-farnesene is generated in transgenic Arabidopsis thaliana over-expressing farnesyl diphosphate synthase 2. Annals of Botany 115, 581591.Google Scholar
Bowers, W.S., Nault, L.R., Webb, R.E. & Dutky, S.R. (1972) Aphid alarm pheromone: isolation, identification, synthesis. Science 177, 11211122.Google Scholar
Byers, J.A. (2005) A cost of alarm pheromone production in cotton aphids, Aphis gossypii. Naturwissenschaften 92, 6972.Google Scholar
Crock, J., Wildung, M. & Croteau, R. (1997) Isolation and bacterial expression of a sesquiterpene synthase cDNA clone from peppermint (Mentha x piperita, L.) that produces the aphid alarm pheromone (E)-β-farnesene. Proceeding National Academy of Science USA 94, 1283312838.Google Scholar
De, V.M., Cheng, W.Y., Summers, H.E., Raguso, R.A. & Jander, G. (2010) Alarm pheromone habituation in Myzus persicae has fitness consequences and causes extensive gene expression changes. Proceeding National Academy of Science USA 107, 1467314678.Google Scholar
Edwards, L.J., Siddall, J.B., Dunham, L.L., Uden, P. & Kislow, C.J. (1973) Trans-β-farnesene, alarm pheromone of the green peach aphid, Myzus persicae (Sulzer). Nature 241, 126127.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, 611.Google Scholar
Goggin, F.L. (2007) Plant-aphid interactions: molecular and ecological perspectives. Current Opinion in Plant Biology 10, 399408.Google Scholar
Hardie, J. (1987) Juvenile hormone stimulation of oocyte development and embryogenesis in the parthenogenetic ovaries of an aphid, Aphis fabae. International Journal of Invertebrate Reproduction 11, 189202.Google Scholar
Joachim, C. & Weisser, W.W. (2013) Real-time monitoring of (E)-β-farnesene emission in colonies of the pea aphid, Acyrthosiphon pisum, under lacewing and ladybird predation. Journal of Chemical Ecology 39, 12541262.Google Scholar
Kislow, C.J. & Edwards, L.J. (1972) Repellent odour in aphids. Nature 235, 108109.Google Scholar
Lees, A.D. (1967) The production of the apterous and alate forms in the aphid Megoura viciae Buckton, with special reference to the role of crowding. Journal of Insect Physiology 13, 289318.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, 512.Google Scholar
Lewis, M.J., Prosser, I.M., Mohib, A. & Field, L.M. (2008) Cloning and characterisation of a prenyltransferase from the aphid Myzus persicae with potential involvement in alarm pheromone biosynthesis. Insect Molecular Biology 17, 437443.Google Scholar
Livak, K.J. & Schmittgen, T.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods 25, 402408.Google Scholar
Maruyama, T., Ito, M., Kiuchi, F. & Honda, G. (2001) Molecular cloning, functional expression and characterization of d-limonene synthase from Schizonepeta tenuifolia. Biological and Pharmaceutical Bulletin 24, 373377.Google Scholar
Mathers, T.C., Chen, Y., Kaithakottil, G., Legeai, F., Mugford, S.T., Baa-Puyoulet, P., Bretaudeau, A., Clavijo, B., Colella, S., Collin, O., Dalmay, T., Derrien, T., Feng, H., Gabaldón, T., Jordan, A., Julca, I., Kettles, G.J., Kowitwanich, K., Lavenier, D., Lenzi, P., Lopez-Gomollon, S., Loska, D., Mapleson, D., Maumus, F., Moxon, S., Price, D.R., Sugio, A., van Munster, M., Uzest, M., Waite, D., Jander, G., Tagu, D., Wilson, A.C., van Oosterhout, C., Swarbreck, D. & Hogenhout, S.A. (2017) Rapid transcriptional plasticity of duplicated gene clusters enables a clonally reproducing aphid to colonise diverse plant species. Genome Biology 18, 27.Google Scholar
Mondor, E.B. & Roitberg, B.D. (2011) Age-dependent fitness costs of alarm signaling in aphids. Canadian Journal of Zoology 81, 757762.Google Scholar
Mondor, E.B., Baird, D.S., Slessor, K.N. & Roitberg, B.D. (2000) Ontogeny of alarm pheromone secretion in pea aphid, Acyrthosiphon pisum. Journal of Chemical Ecology 26, 28752882.Google Scholar
Müller, C.B., Williams, I.S. & Hardie, J. (2001) The role of nutrition, crowding and interspecific interactions in the development of winged aphids. Ecological Entomology 26, 330340.Google Scholar
Picaud, S., Brodelius, M. & Brodelius, P.E. (2005) Expression, purification and characterization of recombinant (E)-beta-farnesene synthase from Artemisia annua. Phytochemistry 66, 961967.Google Scholar
Pickett, J.A. & Griffiths, D.C. (1980) Composition of aphid alarm pheromones. Journal of Chemical Ecology 6, 349360.Google Scholar
Robertson, I.C., Roitberg, B.D., Williamson, I. & Senger, S.E. (1995) Contextual chemical ecology: an evolutionary approach to the chemical ecology of insects. American Entomologist 41, 237240.Google Scholar
Ruzicka, L. (1953) The isoprene rule and the biogenesis of terpenic compounds. Experientia 50, 395405.Google Scholar
Schwartzberg, E.G., Grit, K., Claudia, S., Anja, D., Röse, U.S.R., Gershenzon, J., Boland, W. & Weisser, W.W. (2008) Real-time analysis of alarm pheromone emission by the pea aphid (Acyrthosiphon pisum) under predation. Journal of Chemical Ecology 34, 7681.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, 417424.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, 6041.Google Scholar
The International Aphid Genomics Consortium (2010) Genome sequence of the pea aphid Acyrthosiphon pisum. PLoS Biology 8, 124.Google Scholar
Turlings, T.C.J., Tumlinson, J.H., Heath, R.R., Proveaux, A.T. & Doolittle, R.E. (1991) Isolation and identification of allelochemicals that attract the larval parasitoid, Cotesia marginiventris (Cresson), to the microhabitat of one of its hosts. Journal of Chemical Ecology 17, 22352251.Google Scholar
van Emden, H.F., Dingley, J., Dewhirst, S.Y., Pickett, J.A., Woodcock, C.M. & Wadhams, L.J. (2015) The effect of artificial diet on the production of alarm pheromone by Myzus persicae. Physiological Entomology 39, 285291.Google Scholar
Vandermoten, S., Mescher, M.C., Francis, F., Haubruge, E. & Verheggen, F.J. (2012) Aphid alarm pheromone: an overview of current knowledge on biosynthesis and functions. Insect Biochemistry and Molecular Biology 42, 155163.Google Scholar
Verheggen, F.J., Ryne, C., Olsson, P.O.C., Arnaud, L., Lognay, G., Högberg, H.E., Persson, D., Haubruge, E. & Löfstedt, C. (2007) Electrophysiological and behavioral activity of secondary metabolites in the confused flour beetle, Tribolium confusum. Journal of Chemical Ecology 33, 525539.Google Scholar
Verheggen, F.J., Haubruge, E., Moraes, C.M.D. & Mescher, M.C. (2009) Social environment influences aphid production of alarm pheromone. Behavioral Ecology 20, 283288.Google Scholar
Watt, A.D. & Dixon, A.F.G. (1981) The role of cereal growth stages and crowding in the induction of alatae in Sitobion avenae and its consequences for population growth. Ecological Entomology 79, 441447.Google Scholar
Wientjens, W.H.J.M., Lakwijk, A.C. & Marel, T.D. (1973) Alarm pheromone of grain aphids. Cellular & Molecular Life Sciences 29, 658660.Google Scholar
Wynn, G.G. & Boudreaux, H.B. (1972) Structure and function of aphid cornicles. Annals of the Entomological Society of America 65, 157166.Google Scholar
Xiang, J.G., Zhang, F., Fang, Y.L., Kan, W., Zhang, G.X. & Zhang, Z.N. (2002) Behavioural response of aphids to the alarm pheromone component (E)-β-farnesene in the field. Physiological Entomology 27, 307311.Google Scholar