Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-27T10:53:25.011Z Has data issue: false hasContentIssue false

Aldehyde oxidases mediate plant toxicant susceptibility and fecundity in the red flour beetle, Tribolium castaneum

Published online by Cambridge University Press:  16 February 2022

Yonglei Zhang
Affiliation:
College of Biology and Food Engineering, Anyang Institute of Technology, Anyang 455000, China Jiangsu Key Laboratory for Biodiversity and Biotechnology, College of Life Sciences, Nanjing Normal University, Nanjing 210023, China
Jiahao Zhang
Affiliation:
College of Biology and Food Engineering, Anyang Institute of Technology, Anyang 455000, China
Dongyu Li
Affiliation:
College of Biology and Food Engineering, Anyang Institute of Technology, Anyang 455000, China
Haidi Sun
Affiliation:
College of Biology and Food Engineering, Anyang Institute of Technology, Anyang 455000, China
Ruixue Lu
Affiliation:
College of Biology and Food Engineering, Anyang Institute of Technology, Anyang 455000, China
Se Yin
Affiliation:
College of Biology and Food Engineering, Anyang Institute of Technology, Anyang 455000, China
Xinlong Guo
Affiliation:
College of Biology and Food Engineering, Anyang Institute of Technology, Anyang 455000, China
Shanshan Gao*
Affiliation:
College of Biology and Food Engineering, Anyang Institute of Technology, Anyang 455000, China
*
Author for correspondence: Shanshan Gao, Email: gaoshanshanky2012@163.com

Abstract

Aldehyde oxidases (AOXs) are a group of metabolic enzymes that play critical roles in the degradation of xenobiotics and chemicals. However, the physiological function of this enzyme in insects remains poorly understood. In this study, three TcAOX genes (TcAOX1, TcAOX2, TcAOX3) were identified and characterized from Tribolium castaneum genome. Spatiotemporal expression profiling showed that TcAOX1 expression was most highly expressed at the early pupal stage and was predominantly expressed in the antennae of adults, indicating that TcAOX1 was involved in the degradation of chemical signals; TcAOX2 expression was most highly expressed at the late pupal stage and was mainly expressed in the fat body, epidermis of larvae and adults, respectively; and TcAOX3 expression was in all stages and was primarily expressed in the head of adults. Moreover, the transcripts of TcAOX2 and TcAOX3 were significantly induced after exposure to plant oil, and RNA interference (RNAi) targeting of each of them enhanced the susceptibility of beetles to this plant toxicant, suggesting that these two genes are associated with plant toxicant detoxification. Intriguingly, knockdown of the TcAOX1 led to reductions in female egg-laying but unchanged the hatchability and the development of genital organs, suggesting that this gene may mediate fecundity by effecting the inactivation of chemical signals in T. castaneum. Overall, these results shed new light on the function of AOX genes in insects, and could facilitate the development of research on pest control management.

Type
Research Paper
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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

Anderson, SM and Barnett, SE (1991) The involvement of alcohol dehydrogenase and aldehyde dehydrogenase in alcohol/aldehyde metabolism in Drosophila melanogaster. Genetica 83, 99106.CrossRefGoogle ScholarPubMed
Asakawa, T, Itoh, K, Adachi, M, Hoshino, K, Watanabe, N and Tanaka, Y (2008) Properties of 130 kDa subunit of monkey aldehyde oxidase. Biological Pharmaceutical Bulletin 31, 380385.CrossRefGoogle ScholarPubMed
Barrero, JM, Rodríguez, PL, Quesada, V, Piqueras, P, Ponce, MR and Micol, JL (2006) Both abscisic acid (ABA)-dependent and ABA-independent pathways govern the induction of NCED3, AAO3 and ABA1 in response to salt stress. Plant Cell Environment 29, 20002008.CrossRefGoogle ScholarPubMed
Beedham, C, Peet, CF, Panoutsopoulos, GI, Carter, H and Smith, JA (1995) Role of aldehyde oxidase in biogenic amine metabolism. Progress in Brain Research 106, 345353.CrossRefGoogle ScholarPubMed
Begum, K, Li, B, Beeman, RW and Park, Y (2009) Functions of ion transport peptide and ion transport peptide-like in the red flour beetle Tribolium castaneum. Insect Biochemistry and Molecular Biology 39, 717725.CrossRefGoogle ScholarPubMed
Calzi, ML, Raviolo, C, Ghibaudi, E, de Gioia, L, Salmona, M, Cazzaniga, G, Kurosaki, M, Terao, M and Garattini, E (1995) Purification, cDNA cloning, and tissue distribution of bovine liver aldehyde oxidase. Journal of Biological Chemistry 270, 3103731045.CrossRefGoogle ScholarPubMed
Choo, YM, Pelletier, J, Atungulu, E and Leal, WS (2013) Identification and characterization of an antennae-specific aldehyde oxidase from the navel orangeworm. PLoS One 8, e67794.CrossRefGoogle ScholarPubMed
Coleman, M, Vontas, JG and Hemingway, J (2002) Molecular characterization of the amplified aldehyde oxidase from insecticide-resistant Culex quinquefasciatus. European Journal of Biochemistry 269, 768779.CrossRefGoogle ScholarPubMed
Enroth, C, Eger, BT, Okamoto, K, Nishino, T, Nishino, T and Pai, EF (2000) Crystal structures of bovine milk xanthine dehydrogenase and xanthine oxidase: structure-based mechanism of conversion. Proceedings of the National Academy of Sciences of the United States of America 97, 1072310728.CrossRefGoogle ScholarPubMed
Garattini, E and Terao, M (2011) Increasing recognition of the importance of aldehyde oxidase in drug development and discovery. Drug Metabolism Reviews 43, 374386.CrossRefGoogle ScholarPubMed
Garattini, E, Mendel, R, Romão, MJ, Wright, R and Terao, M (2003) Mammalian molybdo-flavoenzymes, an expanding family of proteins: structure, genetics, regulation, function and pathophysiology. Biochemical Journal 372, 1532.CrossRefGoogle ScholarPubMed
Garattini, E, Fratelli, M and Terao, M (2008) Mammalian aldehyde oxidases: genetics, evolution and biochemistry. Cellular and Molecular Life Sciences 65, 10191048.CrossRefGoogle ScholarPubMed
González-Mas, MC, Rambla, JL, Alamar, MC, Gutiérrez, A and Granell, A (2011) Comparative analysis of the volatile fraction of fruit juice from different Citrus species. PLoS One 6, e22016.CrossRefGoogle ScholarPubMed
Hammond, DG, Rangel, S and Kubo, I (2000) Volatile aldehydes are promising broad-spectrum postharvest insecticides. Journal of Agricultural and Food Chemistry 48, 44104417.CrossRefGoogle ScholarPubMed
He, P, Zhang, YF, Hong, DY, Wang, J, Wang, XL, Zuo, LH, Tang, XF, Xu, WM and He, M (2017) A reference gene set for sex pheromone biosynthesis and degradation genes from the diamondback moth, Plutella xylostella, based on genome and transcriptome digital gene expression analyses. BMC Genomics 18, 219.CrossRefGoogle ScholarPubMed
Heinstra, PW, Geer, BW, Seykens, D and Langevin, M (1989) The metabolism of ethanol-derived acetaldehyde by alcohol dehydrogenase (EC 1.1.1.1) and aldehyde dehydrogenase (EC 1.2.1.3) in Drosophila melanogaster larvae. Biochemical Journal 259, 791797.CrossRefGoogle Scholar
Hemingway, J, Coleman, M, Paton, M, McCarroll, L, Vaughan, A and Desilva, D (2000) Aldehyde oxidase is coamplified with the world's most common Culex mosquito insecticide resistance-associated esterases. Insect Molecular Biology 9, 9399.CrossRefGoogle ScholarPubMed
Hille, R (2005) Molybdenum-containing hydroxylases. Archives of Biochemistry and Biophysics 433, 107116.CrossRefGoogle ScholarPubMed
Huang, DY and Ichikawa, Y (1994) Two different enzymes are primarily responsible for retinoic acid synthesis in rabbit liver cytosol. Biochemical and Biophysical Research Communications 205, 12781283.CrossRefGoogle ScholarPubMed
Huang, X, Liu, L, Su, X and Feng, J (2016) Identification of biotransformation enzymes in the antennae of codling moth Cydia pomonella. Gene 580, 7379.CrossRefGoogle ScholarPubMed
Hubert, J, Münzbergová, Z and Santino, A (2008) Plant volatile aldehydes as natural insecticides against stored-product beetles. Pest Managemant Science 64, 5764.CrossRefGoogle ScholarPubMed
Kim, YH, Soumaila Issa, M, Cooper, AM and Zhu, KY (2015) RNA interference: applications and advances in insect toxicology and insect pest management. Pesticide Biochemistry Physiology 120, 109117.CrossRefGoogle ScholarPubMed
Kimmerer, TW and Macdonald, RC (1987) Acetaldehyde and ethanol biosynthesis in leaves of plants. Plant Physiology 84, 12041209.CrossRefGoogle Scholar
Kurosaki, M, Terao, M, Barzago, MM, Bastone, A, Bernardinello, D, Salmona, M and Garattini, E (2004) The aldehyde oxidase gene cluster in mice and rats. Aldehyde oxidase homologue 3, a novel member of the molybdo-flavoenzyme family with selective expression in the olfactory mucosa. Journal of Biological Chemistry 279, 5048250498.CrossRefGoogle ScholarPubMed
Leal, WS (2013) Odorant reception in insects: roles of receptors, binding proteins, and degrading enzymes. Annual Review of Entomology 58, 373391.CrossRefGoogle ScholarPubMed
Li, B, Beeman, RW and Park, Y (2011) Functions of duplicated genes encoding CCAP receptors in the red flour beetle, Tribolium castaneum. Journal of Insect Physiology 57, 11901197.CrossRefGoogle ScholarPubMed
Livak, KJ and Schmittgen, TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Methods (San Diego, Calif.) 25, 402408.CrossRefGoogle ScholarPubMed
Mahro, M, Coelho, C, Trincão, J, Rodrigues, D, Terao, M, Garattini, E, Saggu, M, Lendzian, F, Hildebrandt, P, Romão, MJ and Leimkühler, S (2011) Characterization and crystallization of mouse aldehyde oxidase 3: from mouse liver to Escherichia coli heterologous protein expression. Drug Metabolism and Disposition 39, 19391945.CrossRefGoogle ScholarPubMed
Marelja, Z, Dambowsky, M, Bolis, M, Georgiou, ML, Garattini, E, Missirlis, F and Leimkühler, S (2014) The four aldehyde oxidases of Drosophila melanogaster have different gene expression patterns and enzyme-substrate specificities. Journal of Experimental Biology 217, 22012211.Google ScholarPubMed
Meister, G and Tuschl, T (2004) Mechanisms of gene silencing by double-stranded RNA. Nature 431, 343349.CrossRefGoogle ScholarPubMed
Mendel, RR and Hänsch, R (2002) Molybdoenzymes and molybdenum cofactor in plants. Journal of Experimental Botany 53, 16891698.CrossRefGoogle ScholarPubMed
Merlin, C, François, MC, Bozzolan, F, Pelletier, J, Jacquin-Joly, E and Maïbèche-Coisne, M (2005) A new aldehyde oxidase selectively expressed in chemosensory organs of insects. Biochemical and Biophysical Research Communications 332, 410.CrossRefGoogle ScholarPubMed
Okamura, Y, Inada, M, Elshopakey, GE and Itami, T (2018) Characterization of xanthine dehydrogenase and aldehyde oxidase of Marsupenaeus japonicus and their response to microbial pathogen. Molecular Biology Reports 45, 419432.CrossRefGoogle ScholarPubMed
Pelletier, J, Bozzolan, F, Solvar, M, François, MC, Jacquin-Joly, E and Maïbèche-Coisne, M (2007) Identification of candidate aldehyde oxidases from the silkworm Bombyx mori potentially involved in antennal pheromone degradation. Gene 404, 3140.CrossRefGoogle ScholarPubMed
Pryde, DC, Dalvie, D, Hu, Q, Jones, P, Obach, RS and Tran, TD (2010) Aldehyde oxidase: an enzyme of emerging importance in drug discovery. Journal of Medicinal Chemistry 53, 84418460.CrossRefGoogle ScholarPubMed
Richards, S, Gibbs, RA, Weinstock, GM, Brown, SJ, Denell, R, Beeman, RW, Gibbs, R, Beeman, RW, Brown, SJ, Bucher G, Friedrich M, Grimmelikhuijzen CJ, Klingler M, Lorenzen M, Richards S, Roth S, Schröder R, Tautz D, Zdobnov EM, Muzny D, Gibbs RA, Weinstock GM, Attaway T, Bell S, Buhay CJ, Chandrabose MN, Chavez D, Clerk-Blankenburg KP, Cree A, Dao M, Davis C, Chacko J, Dinh H, Dugan-Rocha S, Fowler G, Garner TT, Garnes J, Gnirke A, Hawes A, Hernandez J, Hines S, Holder M, Hume J, Jhangiani SN, Joshi V, Khan ZM, Jackson, L, Kovar C, Kowis A, Lee S, Lewis LR, Margolis J, Morgan M, Nazareth LV, Nguyen N, Okwuonu G, Parker D, Richards S, Ruiz SJ, Santibanez J, Savard J, Scherer SE, Schneider B, Sodergren E, Tautz D, Vattahil S, Villasana D, White CS, Wright R, Park Y, Beeman RW, Lord J, Oppert B, Lorenzen M, Brown S, Wang L, Savard J, Tautz D, Richards S, Weinstock G, Gibbs RA, Liu Y, Worley K, Weinstock G, Elsik CG, Reese JT, Elhaik E, Landan G, Graur D, Arensburger P, Atkinson P, Beeman RW, Beidler J, Brown SJ, Demuth JP, Drury DW, Du YZ, Fujiwara H, Lorenzen M, Maselli V, Osanai M, Park Y, Robertson HM, Tu Z, Wang JJ, Wang S, Richards S, Song H, Zhang L, Sodergren E, Werner D, Stanke M, Morgenstern B, Solovyev V, Kosarev P, Brown G, Chen HC, Ermolaeva O, Hlavina W, Kapustin Y, Kiryutin B, Kitts P, Maglott D, Pruitt K, Sapojnikov V, Souvorov A, Mackey AJ, Waterhouse RM, Wyder S, Zdobnov EM, Zdobnov EM, Wyder S, Kriventseva EV, Kadowaki T, Bork P, Aranda M, Bao R, Beermann A, Berns N, Bolognesi R, Bonneton F, Bopp D, Brown SJ, Bucher G, Butts T, Chaumot A, Denell RE, Ferrier DE, Friedrich M, Gordon CM, Jindra M, Klingler M, Lan Q, Lattorff HM, Laude, V, von Levetsow C, Liu Z, Lutz R, Lynch JA, da Fonseca RN, Posnien N, Reuter R, Roth S, Savard J, Schinko JB, Schmitt C, Schoppmeier M, Schröder R, Shippy TD, Simonnet F, Marques-Souza H, Tautz D, Tomoyasu Y, Trauner J, Van der Zee M, Vervoort M, Wittkopp N, Wimmer EA, Yang X, Jones AK, Sattelle DB, Ebert PR, Nelson D, Scott JG, Beeman RW, Muthukrishnan S, Kramer KJ, Arakane Y, Beeman RW, Zhu Q, Hogenkamp D, Dixit R, Oppert B, Jiang H, Zou Z, Marshall J, Elpidina E, Vinokurov K, Oppert C, Zou Z, Evans J, Lu Z, Zhao P, Sumathipala N, Altincicek B, Vilcinskas A, Williams M, Hultmark D, Hetru C, Jiang H, Grimmelikhuijzen CJ, Hauser F, Cazzamali G, Williamson M, Park Y, Li B, Tanaka Y, Predel R, Neupert S, Schachtner J, Verleyen P, Raible F, Bork P, Friedrich M, Walden KK, Robertson HM, Angeli S, Forêt S, Bucher G, Schuetz S, Maleszka R, Wimmer EA, Beeman RW, Lorenzen M, Tomoyasu Y, Miller SC, Grossmann D and Bucher, G (2008) The genome of the model beetle and pest Tribolium castaneum. Nature 452, 949955.Google ScholarPubMed
Rybczynski, R, Reagan, J and Lerner, MR (1989) A pheromone-degrading aldehyde oxidase in the antennae of the moth Manduca sexta. The Journal of Neuroscience 9, 13411353.CrossRefGoogle ScholarPubMed
Sagi, M, Scazzocchio, C and Fluhr, R (2002) The absence of molybdenum cofactor sulfuration is the primary cause of the flacca phenotype in tomato plants. The Plant Journal 31, 305317.CrossRefGoogle ScholarPubMed
Schumann, S, Terao, M, Garattini, E, Saggu, M, Lendzian, F, Hildebrandt, P and Leimkühler, S (2009) Site directed mutagenesis of amino acid residues at the active site of mouse aldehyde oxidase AOX1. PLoS One 4, e5348.CrossRefGoogle ScholarPubMed
Sekimoto, H, Seo, M, Dohmae, N, Takio, K, Kamiya, Y and Koshiba, T (1997) Cloning and molecular characterization of plant aldehyde oxidase. Journal of Biological Chemistry 272, 1528015285.CrossRefGoogle ScholarPubMed
Sekimoto, H, Seo, M, Kawakami, N, Komano, T, Desloire, S, Liotenberg, S, Marion-Poll, A, Caboche, M, Kamiya, Y and Koshiba, T (1998) Molecular cloning and characterization of aldehyde oxidases in Arabidopsis thaliana. Plant Cell Physiology 39, 433442.CrossRefGoogle ScholarPubMed
Silver, K, Cooper, AM and Zhu, KY (2021) Strategies for enhancing the efficiency of RNA interference in insects. Pest Management Science 77, 26452658.CrossRefGoogle ScholarPubMed
Takei, M, Kogure, S, Yokoyama, C, Kouzuma, Y and Suzuki, Y (2019) Identification of an aldehyde oxidase involved in indole-3-acetic acid synthesis in Bombyx mori silk gland. Bioscience Biotechnology and Biochemistry 83, 129136.CrossRefGoogle ScholarPubMed
Terao, M, Kurosaki, M, Saltini, G, Demontis, S, Marini, M, Salmona, M and Garattini, E (2000) Cloning of the cDNAs coding for two novel molybdo-flavoproteins showing high similarity with aldehyde oxidase and xanthine oxidoreductase. Journal of Biological Chemistry 275, 3069030700.CrossRefGoogle ScholarPubMed
Terao, M, Kurosaki, M, Barzago, MM, Varasano, E, Boldetti, A, Bastone, A, Fratelli, M and Garattini, E (2006) Avian and canine aldehyde oxidases. Novel insights into the biology and evolution of molybdo-flavoenzymes. Journal of Biological Chemistry 281, 1974819761.CrossRefGoogle ScholarPubMed
Terao, M, Romão, MJ, Leimkühler, S, Bolis, M, Fratelli, M, Coelho, C, Santos-Silva, T and Garattini, E (2016) Structure and function of mammalian aldehyde oxidases. Archives of Toxicology 90, 753780.CrossRefGoogle ScholarPubMed
van der Goes van Naters, W and Carlson, JR (2006) Insects as chemosensors of humans and crops. Nature 444, 302307.CrossRefGoogle ScholarPubMed
Wang, MM, He, M, Wang, H, Ma, YF, Dewer, Y, Zhang, F and He, P (2021) A candidate aldehyde oxidase in the antennae of the diamondback moth, Plutella xylostella (L.), is potentially involved in the degradation of pheromones, plant-derived volatiles and the detoxification of xenobiotics. Pesticide Biochemistry Physiology 171, 104726.CrossRefGoogle Scholar
Xu, W and Liao, Y (2017) Identification and characterization of aldehyde oxidases (AOXs) in the cotton bollworm. Die Naturwissenschaften 104, 1112.CrossRefGoogle ScholarPubMed
Yang, Y, Lin, Y, Yang, CW, Wang, YX and Xia, QY (2010) Identification and expression profiling of aldehyde oxidase genes in the silkworm, Bombyx mori. Acta Entomologica Sinica 53, 18.Google Scholar
Yoshihara, S and Tatsumi, K (1997) Purification and characterization of hepatic aldehyde oxidase in male and female mice. Archives of Biochemistry and Biophysics 338, 2934.CrossRefGoogle ScholarPubMed
Zdunek-Zastocka, E (2008) Molecular cloning, characterization and expression analysis of three aldehyde oxidase genes from Pisum sativum L. Plant Physiology and Biochemistry 46, 1928.CrossRefGoogle ScholarPubMed
Zhang, Y, Yang, Y, Shen, G, Mao, X, Jiao, M and Lin, Y (2020) Identification and characterization of aldehyde oxidase 5 in the pheromone gland of the silkworm (Lepidoptera: Bombycidae). Journal of Insect Science 20, 31.CrossRefGoogle Scholar
Zhang, YC, Gao, SS, Xue, S, An, SH and Zhang, KP (2021) Disruption of the cytochrome P450 CYP6BQ7 gene reduces tolerance to plant toxicants in the red flour beetle, Tribolium castaneum. International Journal of Biological Macromolecules 172, 263269.CrossRefGoogle ScholarPubMed
Supplementary material: File

Zhang et al. supplementary material

Tables S1 and S2

Download Zhang et al. supplementary material(File)
File 17.1 KB