Hostname: page-component-8448b6f56d-qsmjn Total loading time: 0 Render date: 2024-04-23T22:27:54.532Z Has data issue: false hasContentIssue false
  • English
  • Français

Identification and expression patterns of Halloween genes encoding cytochrome P450s involved in ecdysteroid biosynthesis in the cotton bollworm Helicoverpa armigera

Published online by Cambridge University Press:  22 August 2016

J. Zheng ,
K. Tian ,
Y. Yuan ,
M. Li  and
X. Qiu
J. Zheng
Affiliation:
State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China University of Chinese Academy of Sciences, Beijing 100049, China
K. Tian
Affiliation:
State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China University of Chinese Academy of Sciences, Beijing 100049, China
Y. Yuan
Affiliation:
State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China
M. Li
Affiliation:
State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China
X. Qiu*
Affiliation:
State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China University of Chinese Academy of Sciences, Beijing 100049, China
*
*Author for correspondence Phone: 86-10-64807231 Fax: +86-10-64807099 E-mail: qiuxh@ioz.ac.cn
Get access Rights & Permissions [Opens in a new window]

Abstract

20-Hydroxyecdysone (20E) is a key hormone which regulates growth, development and reproduction in insects. Although cytochrome P450 enzymes (P450s) participating in the ecdysteroid biosynthesis of 20E have been characterized in a few model insects, no work has been published on the molecular entity of their orthologs in the cotton bollworm Helicoverpa armigera, a major pest insect in agriculture worldwide. In this study, four cytochrome P450 homologs, namely HarmCYP302A1, HarmCYP306A1, HarmCYP314A1 and HarmCYP315A1 from H. armigera, were identified and evolutional conservation of these Halloween genes were revealed among lepidopteran. Expression analyses showed that HarmCYP302A1 and HarmCYP315A1 were predominantly expressed in larval prothoracic glands, whereas this predominance was not always observed for HarmCYP306A1 and CYP314A1. The expression patterns of Halloween genes indicate that the fat bodies may play an important role in the conversion of ecdysone into 20E in larval–larval molt and in larval–pupal metamorphosis, and raise the possibility that HarmCYP315A1 plays a role in tissue-specific regulation in the steroid biosynthesis in H. armigera. These findings represent the first identification and expression characterization of four steriodogenic P450 genes and provide the groundwork for future functional and evolutionary study of steroid biosynthesis in this agriculturally important pest.

Keywords

Cytochrome P450EcysteroidExpression patternHalloween genesHelicoverpa armigera
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 107 , Issue 1 , February 2017 , pp. 85 - 95
Check for updates
Copyright
Copyright © Cambridge University Press 2016 

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

Brown, M.R., Sieglaff, D.H. & Rees, H.H. (2009) Gonadal ecdysteroidogenesis in Arthropoda: occurrence and regulation. Annual Review of Entomology 54, 105–125.Google Scholar
Bustin, S.A., Benes, V., Garson, J.A., Hellemans, J., Huggett, J., Kubista, M., Mueller, R., Nolan, T., Pfaffl, M.W., Shipley, G.L., Vandesompele, J. & Wittwer, C.T. (2009) The MIQE guidelines-minimum information for publication of quantitative real-time PCR experiments. Clinical Chemistry 55, 611–622.CrossRefGoogle ScholarPubMed
Cabrera, A.R., Shirk, P.D., Evans, J.D., Hung, K., Sims, J., Alborn, H. & Teal, P.E.A. (2015) Three Halloween genes from the Varroa mite, Varroa destructor (Anderson & Trueman) and their expression during reproduction. Insect Molecular Biology 24, 277–292.CrossRefGoogle ScholarPubMed
Chavez, V.M., Marques, G., Delbecque, J.P., Kobayashi, K., Hollingsworth, M., Burr, J., Natzle, J.E. & O'Connor, M.B. (2000) The Drosophila disembodied gene controls late embryonic morphogenesis and codes for a cytochrome P450 enzyme that regulates embryonic ecdysone levels. Development 127, 4115–4126.Google Scholar
Christiaens, O., Iga, M., Velarde, R.A., Rougé, P. & Smagghe, G. (2010) Halloween genes and nuclear receptors in ecdysteroid biosynthesis and signalling in the pea aphid. Insect Molecular Biology 19, 187–200.CrossRefGoogle ScholarPubMed
Dubrovsky, E.B. (2005) Hormonal cross talk in insect development. Trends in Endocrinology and Metabolism 16, 6–11.Google Scholar
Enya, S., Ameku, T., Igarashi, F., Iga, M., Kataoka, H., Shinoda, T. & Niwa, R. (2014) A Halloween gene noppera-bo encodes a glutathione S-transferase essential for ecdysteroid biosynthesis via regulating the behaviour of cholesterol in Drosophila . Science Reports 4, 6586.Google Scholar
Enya, S., Daimon, T., Igarashi, F., Kataoka, H., Uchibori, M., Sezutsu, H., Shinoda, T. & Niwa, R. (2015) The silkworm glutathione S-transferase gene noppera-bo is required for ecdysteroid biosynthesis and larval development. Insect Biochemistry and Molecular Biology 61, 1–7.Google Scholar
Feyereisen, R. (2012) Insect CYP genes and P450 enzymes. In Gilbert, L.I. (ed.), Insect Molecular Biology and Biochemistry. Elsevier Academic Press, San Diego, pp. 236–316.Google Scholar
Feyereisen, R. (2015) Insect P450 inhibitors and insecticides: challenges and opportunities. Pest Management Science 71, 793–800.Google Scholar
Fitt, G.P. (1989) The ecology of Heliothis species in relation to agroecosystems. Annual Review of Entomology 34, 17–53.Google Scholar
Gilbert, L.I., Rybczynski, R. & Warren, J.T. (2002) Control and biochemical nature of the ecdysterroidogenic pathway. Annual Review of Entomology 47, 883–916.Google Scholar
Iga, M. & Smagghe, G. (2010) Identification and expression profile of Halloween genes involved in ecdysteroid biosynthesis in Spodoptera littoralis . Peptides 31, 456–467.Google Scholar
Jia, S., Wan, P.J., Zhou, L.T., Mu, L.L. & Li, G.Q. (2013) Knockdown of a putative Halloween gene Shade reveals its role in ecdysteroidogenesis in the small brown planthopper Laodelphax striatellus . Gene 531, 168–174.Google Scholar
Kong, Y., Liu, X.P., Wan, P.J., Shi, X.Q., Guo, W.C. & Li, G.Q. (2014) The P450 enzyme Shade mediates the hydroxylation of ecdysone to 20-hydroxyecdysone in the Colorado potato beetle, Leptinotarsa decemlineata . Insect Molecular Biology 23, 632–643.Google Scholar
Liu, D., Zhou, X., Li, M., Zhu, S. & Qiu, X. (2014) Characterization of NADPH–cytochrome P450 reductase gene from the cotton bollworm, Helicoverpa armigera . Gene 545, 262–270.Google Scholar
Livak, K.L. & Schmittgen, T.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402–408.CrossRefGoogle Scholar
Luan, J.B., Ghanim, M., Liu, S.S. & Czosnek, H. (2013) Silencing the ecdysone synthesis and signaling pathway genes disrupts nymphal development in the whitefly. Insect Biochemistry and Molecular Biology 43, 740–746.Google Scholar
Namiki, T., Niwa, R., Sakudoh, T., Shirai, K., Takeuchi, H. & Kataoka, H. (2005) Cytochrome P450CYP307A1/spook: a regulator for ecdysone synthesis in insects. Biochemical and Biophysical Research Communications 337, 367–374.Google Scholar
Niwa, R. & Niwa, Y.S. (2014) Enzymes for ecdysteroid biosynthesis: their biological functions in insects and beyond. Bioscience, Biotechnology, and Biochemistry 78, 1283–1292.Google Scholar
Niwa, R., Sakudoh, T., Namiki, T., Saida, K., Fujimoto, Y. & Kataoka, H. (2005) The ecdysteroidogenic P450 Cyp302a1/disembodied from the silkworm, Bombyx mori, is transcriptionally regulated by prothoracicotropic hormone. Insect Molecular Biology 14, 563–571.Google Scholar
Niwa, R., Namiki, T., Ito, K., Shimada-Niwa, Y., Kiuchi, M., Kawaoka, S., Kayukawa, T., Banno, Y., Fujimoto, Y., Shigenobu, S., Kobayashi, S., Shimada, T., Katsuma, S. & Shinoda, T. (2010) Non-molting glossy/shroud encodes a short-chain dehydrogenase/reductase that functions in the ‘Black Box’ of the ecdysteroid biosynthesis pathway. Development 137, 1991–1999.Google Scholar
Ono, H., Rewitz, K.F., Shinoda, T., Itoyama, K., Petryk, A., Rybczynski, R., Jarcho, M., Warren, J.T., Marques, G., Shimell, M.J., Gilbert, L.I. & O'Connor, M.B. (2006) spook and spookier code for stage-specific components of the ecdysone biosynthetic pathway in Diptera. Developmental Biology 298, 555–570.CrossRefGoogle ScholarPubMed
Rewitz, K.F., Rybczynski, R., Warren, J.T. & Gilbert, L.I. (2006 a) Identification, characterization and developmental expression of Halloween genes encoding P450 enzymes mediating ecdysone biosynthesis in the tobacco hornworm, Manduca sexta . Insect Biochemistry and Molecular Biology 36, 188–199.Google Scholar
Rewitz, K.F., Rybczynski, R., Warren, J.T. & Gilbert, L.I. (2006 b) The Halloween genes code for cytochrome P450 enzymes mediating synthesis of the insect moulting hormone. Biochemical Society Transactions 34, 1256–1260.CrossRefGoogle ScholarPubMed
Shakeel, M., Zhu, X., Kang, T., Wan, H. & Li, J. (2015) Selection and evaluation of reference genes for quantitative gene expression studies in cotton bollworm, Helicoverpa armigera (Lepidoptera: Noctuidae). Journal of Asia-Pacific Entomology 2, 123–130.Google Scholar
Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 2725–2729.Google Scholar
Wan, P.J., Jia, S., Li, N., Fan, J.M. & Li, G.Q. (2014 a) The putative Halloween gene phantom involved in ecdysteroidogenesis in the white-backed planthopper Sogatella furcifera . Gene 548, 112–118.Google Scholar
Wan, P.J., Jia, S., Li, N., Fan, J.M. & Li, G.Q. (2014 b) RNA interference depletion of the halloween gene Disembodied implies its potential application for management of planthopper Sogatella furcifera and Laodelphax striatellus . PLoS ONE 9, e86675.Google Scholar
Wan, P.J., Jia, S., Li, N., Fan, J.M. & Li, G.Q. (2015) A Halloween gene shadow is a potential target for RNA-interference-based pest management in the small brown planthopper Laodelphax striatellus . Pest Management Science 71, 199–206.Google Scholar
Warren, J.T., Petryk, A., Marques, G., Jarcho, M., Parvy, J.P., Dauphin-Villemant, C., O'Connor, M.B. & Gilbert, L.I. (2002) Molecular and biochemical characterization of two P450 enzymes in the ecdysteroidogenic pathway of Drosophila melanogaster . Proceedings of the National Academy of Sciences of the United States of America 99, 11043–11048.CrossRefGoogle ScholarPubMed
Warren, J.T., Petryk, A., Marques, G., Parvy, J.P., Shinoda, T., Itoyama, K., Kobayashi, J., Jarcho, M., Li, Y.T., O'Connor, M.B., Dauphin-Villemant, C. & Gilbert, L.I. (2004) Phantom encodes the 25-hydroxylase of Drosophila melanogaster and Bombyx mori: a P450 enzyme critical in ecdysone biosynthesis. Insect Biochemistry and Molecular Biology 34, 991–1010.Google Scholar
Wu, K. & Gong, P. (1997) A new and practical artificial diet for the cotton bollworm. Insect Science 4, 277–282.Google Scholar
Yoshiyama, T., Namiki, T., Mita, K., Kataoka, H. & Niwa, R. (2006) Neverland is an evolutionally conserved Rieske-domain protein that is essential for ecdysone synthesis and insect growth. Development 133, 2565–2574.Google Scholar
Yoshiyama-Yanagawa, T., Enya, S., Shimada-Niwa, Y., Yaguchi, S., Haramoto, Y., Matsuya, T., Shiomi, K., Sasakura, Y., Takahashi, S., Asashima, M., Kataoka, H. & Niwa, R. (2011) The conserved Rieske oxygenase DAF-36/Neverland is a novel cholesterol-metabolizing enzyme. Journal of Biological Chemistry 286, 25756–25762.Google Scholar
Zhou, X., Ma, C., Li, M., Sheng, C., Liu, H. & Qiu, X. (2009) CYP9A12 and CYP9A17 in the cotton bollworm, Helicoverpa armigera: sequence similarity, expression profile and xenobiotic response. Pest Management Science 66, 65–73.Google Scholar
Supplementary material: Image

Zheng supplementary material S1

Supplementary Figure

Download Zheng supplementary material S1(Image)
Image 236.3 KB
Supplementary material: File

Zheng supplementary material S2

Supplementary Table

Download Zheng supplementary material S2(File)
File 58.4 KB
Supplementary material: File

Zheng supplementary material S3

Supplementary Table

Download Zheng supplementary material S3(File)
File 44.5 KB