Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-26T08:22:52.128Z Has data issue: false hasContentIssue false
  • English
  • Français

Molecular characterization of prophenoloxidase-1 (PPO1) and the inhibitory effect of kojic acid on phenoloxidase (PO) activity and on the development of Zeugodacus tau (Walker) (Diptera: Tephritidae)

Published online by Cambridge University Press:  22 June 2018

H.-H. Zhang ,
M.-J. Luo ,
Q.-W. Zhang ,
P.-M. Cai ,
A. Idrees ,
Q.-E. Ji ,
J.-Q. Yang  and
J.-H. Chen
H.-H. Zhang
Affiliation:
Institute of Beneficial Insects, Plant Protection College, Fujian Agriculture and Forestry University, Fuzhou 350002, PR, China UN (China) Center for Fruit Fly Prevention and Treatment, Fuzhou 350002, China State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fuzhou 350002, China Key Lab of Biopesticide and Chemical Biology, Ministry of Education, Fuzhou 350002, China
M.-J. Luo
Affiliation:
Institute of Beneficial Insects, Plant Protection College, Fujian Agriculture and Forestry University, Fuzhou 350002, PR, China UN (China) Center for Fruit Fly Prevention and Treatment, Fuzhou 350002, China State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fuzhou 350002, China Key Lab of Biopesticide and Chemical Biology, Ministry of Education, Fuzhou 350002, China
Q.-W. Zhang
Affiliation:
Institute of Beneficial Insects, Plant Protection College, Fujian Agriculture and Forestry University, Fuzhou 350002, PR, China UN (China) Center for Fruit Fly Prevention and Treatment, Fuzhou 350002, China State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fuzhou 350002, China Key Lab of Biopesticide and Chemical Biology, Ministry of Education, Fuzhou 350002, China
P.-M. Cai
Affiliation:
Institute of Beneficial Insects, Plant Protection College, Fujian Agriculture and Forestry University, Fuzhou 350002, PR, China UN (China) Center for Fruit Fly Prevention and Treatment, Fuzhou 350002, China State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fuzhou 350002, China Key Lab of Biopesticide and Chemical Biology, Ministry of Education, Fuzhou 350002, China
A. Idrees
Affiliation:
Institute of Beneficial Insects, Plant Protection College, Fujian Agriculture and Forestry University, Fuzhou 350002, PR, China UN (China) Center for Fruit Fly Prevention and Treatment, Fuzhou 350002, China State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fuzhou 350002, China Key Lab of Biopesticide and Chemical Biology, Ministry of Education, Fuzhou 350002, China
Q.-E. Ji
Affiliation:
Institute of Beneficial Insects, Plant Protection College, Fujian Agriculture and Forestry University, Fuzhou 350002, PR, China UN (China) Center for Fruit Fly Prevention and Treatment, Fuzhou 350002, China State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fuzhou 350002, China Key Lab of Biopesticide and Chemical Biology, Ministry of Education, Fuzhou 350002, China
J.-Q. Yang
Affiliation:
Institute of Beneficial Insects, Plant Protection College, Fujian Agriculture and Forestry University, Fuzhou 350002, PR, China UN (China) Center for Fruit Fly Prevention and Treatment, Fuzhou 350002, China State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fuzhou 350002, China Key Lab of Biopesticide and Chemical Biology, Ministry of Education, Fuzhou 350002, China
J.-H. Chen*
Affiliation:
Institute of Beneficial Insects, Plant Protection College, Fujian Agriculture and Forestry University, Fuzhou 350002, PR, China UN (China) Center for Fruit Fly Prevention and Treatment, Fuzhou 350002, China State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fuzhou 350002, China Key Lab of Biopesticide and Chemical Biology, Ministry of Education, Fuzhou 350002, China
*
*Author for correspondence Phone: (0591)83789421, 87270998 Fax: (0591)83789421 E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Phenoloxidase (PO) plays a key role in melanin biosynthesis during insect development. Here, we isolated the 2310-bp full-length cDNA of PPO1 from Zeugodacus tau, a destructive horticultural pest. qRT-polymerase chain reaction showed that the ZtPPO1 transcripts were highly expressed during larval–prepupal transition and in the haemolymph. When the larvae were fed a 1.66% kojic acid (KA)-containing diet, the levels of the ZtPPO1 transcripts significantly increased by 2.79- and 3.39-fold in the whole larvae and cuticles, respectively, while the corresponding PO activity was significantly reduced; in addition, the larval and pupal durations were significantly prolonged; pupal weights were lowered; and abnormal phenotypes were observed. An in vitro inhibition experiment indicated that KA was an effective competitive inhibitor of PO in Z. tau. Additionally, the functional analysis showed that 20E could significantly up-regulate the expression of ZtPPO1, induce lower pupal weight, and advance pupation. Knockdown of the ZtPPO1 gene by RNAi significantly decreased mRNA levels after 24 h and led to low pupation rates and incomplete pupae with abnormal phenotypes during the larval-pupal interim period. These results proved that PO is important for the normal growth of Z. tau and that KA can disrupt the development of this pest insect.

Keywords

developmentinhibitorkojic acidphenoloxidase activitytranscriptional levels
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 109 , Issue 2 , April 2019 , pp. 236 - 247
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

Aguilera, F., McDougall, C. & Degnan, B.M. (2013) Origin, evolution and classification of type-3 copper proteins: lineage-specific gene expansions and losses across the Metazoa. BMC Evolutionary Biology 13, 96.Google Scholar
Arakane, Y., Muthukrishnan, S., Beeman, R.W., Kanost, M.R. & Kramer, K.J. (2005) Laccase 2 is the phenoloxidase gene required for beetle cuticle tanning. Proceedings of the National Academy of Sciences of the United States of America 102, 11337–11342.Google Scholar
Ashida, M. & Brey, P.T. (1997) Recent advances in research on the insect prophenoloxidase cascade. pp. 135–172 in Brey, P.T. & Hultmark, D.E. (Eds) Molecular Mechanism of Immune Responses in Insects. London, Chapman & Hall.Google Scholar
Aspán, A., Huang, T.S., Cerenius, L. & Söderhäll, K. (1995) cDNA cloning of prophenoloxidase from the freshwater crayfish pacifastacus leniusculus and its activation. Proceedings of the National Academy of Sciences 92(4), 939–943.Google Scholar
Bai, P.P., Xie, Y.F., Shen, G.M., Wei, D.D. & Wang, J.J. (2014) Phenoloxidase and its zymogen are required for the larval-pupal transition in Bactrocera dorsalis (Diptera: Tephritidae). Journal of Insect Physiolohy 71, 137–146.Google Scholar
Barrett, F.M. (1987) Phenoloxidases from larval cuticle of the sheep blowfly, Lucilia cuprina: characterization, developmental changes, and inhibition by antiphenoloxidase antibodies. Archives of Insect Biochemistry and Physiology 5, 99–118.Google Scholar
Binggeli, O., Neyen, C., Poidevin, M. & Lemaitre, B. (2014) Prophenoloxidase activation is required for survival to microbial infections in Drosophila. PLoS Pathogens 10, e1004067.Google Scholar
Cerenius, L., Lee, B.L. & Söderhäll, K. (2008) The proPO-system: pros and cons for its role in invertebrate immunity. Trends in Immunology 29, 263–271.Google Scholar
Chase, M.R., Raina, K., Bruno, J. & Sugumaran, M. (2000) Purification, characterization and molecular cloning of prophenoloxidases from Sarcophaga bullata. Insect Biochemistry and Molecular Biology 30, 953–967.Google Scholar
Chen, Y., Liu, F., Yang, B., Lu, A., Wang, S., Wang, J., Ling, Q.-Z., Li, X., Beerntsen, B.T. & Ling, E. (2012) Specific amino acids affecting Drosophila melanogaster prophenoloxidase activity in vitro. Developmental & Comparative Immunology 38, 88–97.Google Scholar
Cui, L., Luckhart, S. & Rosenberg, R. (2000) Molecular characterization of a prophenoloxidase cDNA from the malaria mosquito Anopheles stephensi. Insect Molecular Biology 9, 127–137.Google Scholar
Dominick, O.S. & Truman, J.W. (1985) The physiology of wandering behaviour in manduca sexta. ii. the endocrine control of wandering behaviour. Journal of Experimental Biology 117(3), 45.Google Scholar
Du, L., Li, B., Gao, L., Xue, C.-B., Lin, J. & Luo, W.-C. (2010) Molecular characterization of the cDNA encoding prophenoloxidase-2 (PPO2) and its expression in diamondback moth Plutella xylostella. Pesticide Biochemistry and Physiology 98, 158–167.Google Scholar
Elias-Neto, M., Soares, M.P., Simões, Z.L., Hartfelder, K. & Bitondi, M.M. (2010) Developmental characterization, function and regulation of a Laccase2 encoding gene in the honey bee, Apis mellifera (Hymenoptera, Apinae). Insect Biochemistry and Molecular Biology 40, 241–251.Google Scholar
Fairhead, M. & Thöny-Meyer, L. (2012) Bacterial tyrosinases: old enzymes with new relevance to biotechnology. New Biotechnology 29, 183–191.Google Scholar
Franssens, V., Simonet, G., Breugelmans, B., Van Soest, S., Van Hoef, V. & Broeck, J.V. (2008) The role of hemocytes, serine protease inhibitors and pathogen-associated patterns in prophenoloxidase activation in the desert locust, Schistocerca gregaria. Peptides 29, 235–241.Google Scholar
Genta, F., Souza, R., Garcia, E. & Azambuja, P. (2010) Phenoloxidases from Rhodnius prolixus: temporal and tissue expression pattern and regulation by ecdysone. Journal of Insect Physiolohy 56, 1253–1259.Google Scholar
Hall, M., Scott, T., Sugumaran, M., Söderhäll, K. & Law, J.H. (1995) Proenzyme of Manduca sexta phenoloxidase: purification, activation, substrate specificity of the active enzyme, and molecular cloning. Proceedings of the National Academy of Sciences of the United States of America 92(17), 7764–7768.Google Scholar
Hartzer, K.L., Zhu, K.Y. & Baker, J.E. (2005) Phenoloxidase in larvae of Plodia interpunctella (Lepidoptera: Pyralidae): molecular cloning of the proenzyme cDNA and enzymatic activity in larvae paralyzed and parasitized by Habrobracon hebetor (Hymenoptera: Braconidae). Archives of Insect Biochemistry and Physiology 59, 67–79.Google Scholar
Hillyer, J.F., Schmidt, S.L. & Christensen, B.M. (2003) Hemocyte-mediated phagocytosis and melanization in the mosquito Armigeres subalbatus following immune challenge by bacteria. Cell and Iissue Research 313, 117–127.Google Scholar
Hillyer, J.F., Schmidt, S.L. & Christensen, B.M. (2004) The antibacterial innate immune response by the mosquito Aedes aegypti is mediated by hemocytes and independent of Gram type and pathogenicity. Microbes and Infection 6, 448–459.Google Scholar
Hiruma, K. & Riddiford, L.M. (1985) Hormonal regulation of dopa decarboxylase during a larval molt. Developmental Biology 110, 509–513.Google Scholar
Hiruma, K. & Riddiford, L.M. (2009) The molecular mechanisms of cuticular melanization: the ecdysone cascade leading to dopa decarboxylase expression in Manduca sexta. Insect Biochemistry and Molecular Biology 39, 245–253.Google Scholar
Hu, F., Dou, W., Wang, J.J., Jia, F.X. & Wang, J.J. (2011) Purification and biochemical characterization of glutathione S-transferases from four field populations of Bactrocera dorsalis (Hendel) (Diptera: Tephritidae). Archives of Insect Biochemistry and Physiology 78, 201–215.Google Scholar
Kanost, M.R. & Gorman, M.J. (2008) Phenoloxidases in insect immunity. pp. 69–96 in Beckage, N.E. (Ed.) Insect Immunology. San Diego, Academic Press.Google Scholar
Kinosita, R. & Shikata, R. (1965) On toxic moldy rice. pp. 111–132 in Wogan, G.N. (Ed.) In Mycotoxins in Foodstuffs. Cambridge, MA, MIT Press.Google Scholar
Li, J.Y. & Christensen, B.M. (1993) Involvement of L-tyrosine and phenoloxidase in the tanning of Aedes aegypti eggs. Insect Biochemistry and Molecular Biology 23, 739–748.Google Scholar
Li, Y., Wang, Y., Jiang, H. & Deng, J. (2009) Crystal structure of Manduca sexta prophenoloxidase provides insights into the mechanism of type 3 copper enzymes. Proceedings of the National Academy of Sciences 106, 17002–17006.Google Scholar
Lourenço, A.P., Zufelato, M.S., Bitondi, M.M.G. & Simões, Z.L.P. (2005) Molecular characterization of a cDNA encoding prophenoloxidase and its expression in Apis mellifera. IInsect Biochemistry and Molecular Biology 35, 541–552.Google Scholar
Lu, Y. L., Li, B., Gong, W., Gao, L., Zhang, X. & Xue, C. B. (2015) Identification and characterization of a prophenoloxidase-1 (PPO1) cDNA in the cabbage butterfly Pieris rapae L. Entomological Science 18, 94–103.Google Scholar
Marinotti, O., Ngo, T., Kojin, B.B., Chou, S.P., Nguyen, B. & Juhn, J. (2014) Integrated proteomic and transcriptomic analysis of the Aedes aegypti eggshell. BMC Developmental Biology 14, 15.Google Scholar
Mayer, A.M. (2006) Polyphenol oxidases in plants and fungi: going places? A review. Phytochemistry 67, 2318–2331.Google Scholar
Nakamura, A., Stiebler, R., Fantappié, M.R., Fialho, E., Masuda, H. & Oliveira, M.F. (2007) Effects of retinoids and juvenoids on moult and on phenoloxidase activity in the blood-sucking insect Rhodnius prolixus. Acta Tropica 103, 222–230.Google Scholar
Niwa, Y. & Akamatsu, H. (1991) Kojic acid scavenges free radicals while potentiating leukocyte functions including free radical generation. Inflammation 15, 303–315.Google Scholar
Olivares, C. & Solano, F. (2009) New insights into the active site structure and catalytic mechanism of tyrosinase and its related proteins. Pigment Cell & Melanoma Research 22, 750–760.Google Scholar
Owusu-Yaw, J., Cohen, M., Fernando, S. & Wei, C. (1990) An assessment of the genotoxicity of vanadium. Toxicology Letters 50, 327–336.Google Scholar
Park, D.-S., Shin, S.W., Kim, M.G., Park, S.S., Lee, W.-J., Brey, P.T. & Park, H.-Y. (1997) Isolation and characterization of the cDNA encoding the prophenoloxidase of fall webworm, Hyphantria cunea. Insect Biochemistry and Molecular Biology 27, 983–992.Google Scholar
Parrish, F.W., Wiley, B.J., Simmons, E.G. & Long, L.J. (1966) Production of aflatoxins and kojic acid by species of aspergillus and penicillium. Journal of Applied Microbiology 14, 139.Google Scholar
Phonpala, Y., Benjakul, S., Visessanguan, W. & Eun, J.B. (2009) Sulfur-containing compounds heated under alkaline condition: antibrowning, antioxidative activities, and their effect on quality of shrimp during iced storage. Journal of Food Science 74, 240–247.Google Scholar
Riddiford, L.M. (1976) Hormonal control of insect epidermal cell commitment in vitro. Nature 259, 115–117.Google Scholar
Riddiford, L.M. (1978) Ecdysone-induced change in cellular commitment of the epidermis of the tobacco hornworm, Manduca sexta, at the initiation of metamorphosis. General and Comparative Endocrinology 34, 438–446.Google Scholar
Sánchez-Ferrer, Á., Rodríguez-López, J.N., García-Cánovas, F. & García-Carmona, F. (1995) Tyrosinase: a comprehensive review of its mechanism. Biochimica et Biophysica Acta (BBA)-Protein Structure and Molecular Enzymology 1247, 1–11.Google Scholar
Shao, Q., Yang, B., Xu, Q., Li, X., Lu, Z. & Wang, C. (2012) Hindgut innate immunity and regulation of fecal microbiota through melanization in insects. Journal of Biological Chemistry 287, 14270–14279.Google Scholar
Söderhäll, K. & Cerenius, L. (1998) Role of the prophenoloxidase-activating system in invertebrate immunity. Current Opinion in Immunology 10, 23–28.Google Scholar
Söderhäll, K., Cerenius, L. & Johansson, M.W. (1994) The prophenoloxidase activating system and its role in invertebrate defence. Annals of the New York Academy of Sciences 712, 155–161.Google Scholar
Sritunyalucksana, K., Cerenius, L. & Söderhäll, K. (1999) Molecular cloning and characterization of prophenoloxidase in the black tiger shrimp, Penaeus monodon. Developmental & Comparative Immunology 23, 179–186.Google Scholar
Sugumaran, M. & Kanost, M.R. (1993) Regulation of insect hemolymph phenoloxidases. pp. 317–342 in Beckage, N.E., Thompson, S.N. & Fredric, B.A. (Eds) Parasites and Pathogens. San Diego, Academic Press.Google Scholar
Wang, M.X., Lu, Y., Cai, Z.Z., Liang, S., Niu, Y.S. & Miao, Y.G. (2013) Phenoloxidase is anecessary enzyme for the silkworm molting which is regulated by molting hormone. Molecular Biology Reports 40, 3549–3555.Google Scholar
Yatsu, J. & Asano, T. (2009) Cuticle laccase of the silkworm, Bombyx mori: purification, gene identification and presence of its inactive precursor in the cuticle. Insect Biochemistry and Molecular Biology 39, 254–262.Google Scholar
Zufelato, M.S., Lourenco, A.P., Simoes, Z.L., Jorge, J.A. & Bitondi, M.M. (2004) Phenoloxidase activity in Apis mellifera honey bee pupae, and ecdysteroid-dependent expression of the prophenoloxidase mRNA. Insect Biochemistry and Molecular Biology 34, 1257–1268.Google Scholar
Supplementary material: File

Zhang et al. supplementary material 1

Zhang et al. supplementary material

Download Zhang et al. supplementary material 1(File)
File 815.2 KB