Abstract
Aldehyde oxidases (AOXs) are a family of metabolic enzymes that oxidize aldehydes into carboxylic acids; therefore, they play critical roles in detoxification and degradation of chemicals. By using transcriptomic and genomic approaches, we successfully identified six putative AOX genes (HarmAOX1-6) from cotton bollworm, Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae). In silico expression profile, reverse transcription (RT)-PCR, and quantitative PCR (qPCR) analyses showed that HarmAOX1 is highly expressed in adult antennae, tarsi, and larval mouthparts, so they may play an important role in degrading plant-derived compounds. HarmAOX2 is highly and specifically expressed in adult antennae, suggesting a candidate pheromone-degrading enzyme (PDE) to inactivate the sex pheromone components (Z)-11-hexadecenal and (Z)-9-hexadecenal. RNA sequencing data further demonstrated that a number of host plants they feed on could significantly upregulate the expression levels of HarmAOX1 in larvae. This study improves our understanding of insect aldehyde oxidases and insect-plant interactions.
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References
Bentivenha JPF, Paula-Moraes SV et al (2016) Battle in the New World: Helicoverpa armigera versus Helicoverpa zea (Lepidoptera: Noctuidae). PLoS One 11(12):e0167182. https://doi.org/10.1371/journalpone0167182
Choi MY, Ahn SJ et al (2016) Tarsi of male Heliothine moths contain aldehydes and butyrate esters as potential pheromone components. J Chem Ecol 42(5):425–432. https://doi.org/10.1007/s10886-016-0701-3
Choo YM, Pelletier J et al (2013) Identification and characterization of an antennae-specific aldehyde oxidase from the navel orangeworm. PLoS One 8(6):e67794. https://doi.org/10.1371/journal.pone.0067794
Durand N, Carot-Sans G et al (2011) Degradation of pheromone and plant volatile components by a same odorant-degrading enzyme in the cotton leafworm, Spodoptera littoralis. PLoS One 6(12):e29147. https://doi.org/10.1371/journalpone0029147
Guo H, Del Corso A et al (2014) Aldehyde reductase activity in the antennae of Helicoverpa armigera. Insect Mol Biol 23(3):330–340. https://doi.org/10.1111/imb.12084
He P, Zhang YN et al (2015) An antenna-biased carboxylesterase is specifically active to plant volatiles in Spodoptera exigua. Pest Biochem Physiol 123:93–100. https://doi.org/10.1016/j.pestbp.2015.03.009
Ishida Y, Leal WS (2005) Rapid inactivation of a moth pheromone. Proc Natl Acad Sci U S A 102(39):14075–14079. https://doi.org/10.1073/pnas.0505340102
Ishida Y, Leal WS (2008) Chiral discrimination of the Japanese beetle sex pheromone and a behavioral antagonist by a pheromone-degrading enzyme. Proc Natl Acad Sci U S A 105(26):9076–9080. https://doi.org/10.1073/pnas.0802610105
Kasang G, Vonproff L et al (1988) Enzymatic conversion and degradation of sex-pheromones in antennae of the male silkworm moth Antheraea polyphemus. Z. Naturforsch C 43(3–4):275–284
Kasang G, Nicholls M et al (1989) Sex-pheromone conversion and degradation in antennae of the silkworm moth Bombyx mori L. Experientia 45(1):81–87. https://doi.org/10.1007/Bf01990456
Kearse M, Moir R et al (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28(12):1647–1649. https://doi.org/10.1093/bioinformatics/bts199
Leal WS (2013) Odorant reception in insects: roles of receptors, binding proteins, and degrading enzymes. Annu Rev Entomol 58:373–391. https://doi.org/10.1146/annurev-ento-120811-153635
Liu NY, Xu W et al (2014) Identification and characterization of three chemosensory receptor families in the cotton bollworm Helicoverpa armigera. BMC Genomics 15(1):597. https://doi.org/10.1186/1471-2164-15-597
Maibeche-Coisne M, Nikonov AA et al (2004) Pheromone anosmia in a scarab beetle induced by in vivo inhibition of a pheromone-degrading enzyme. Proc Natl Acad Sci U S A 101(31):11459–11464. https://doi.org/10.1073/pnas0403537101
Marelja Z, Dambowsky M et al (2014) The four aldehyde oxidases of Drosophila melanogaster have different gene expression patterns and enzyme substrate specificities. J Exp Biol 217(Pt 12):2201–2211. https://doi.org/10.1242/jeb.102129
Merlin C, Francois MC et al (2005) A new aldehyde oxidase selectively expressed in chemosensory organs of insects. Biochem. Bioph. Res Co 332(1):4–10. https://doi.org/10.1016/jbbrc200504.084
Ming QL, Yan YH et al (2007) Mechanisms of premating isolation between Helicoverpa armigera (Hubner) and Helicoverpa assulta (Guenee) (Lepidoptera: Noctuidae). J Insect Physiol 53(2):170–178. https://doi.org/10.1016/j.jinsphys.2006.11.007
Pearce SL, Clarke DF et al (2017) Genomic innovations, transcriptional plasticity and gene loss underlying the evolution and divergence of two highly polyphagous and invasive Helicoverpa pest species. BMC Biol 15(1):63. https://doi.org/10.1186/s12915-017-0402-6
Pelletier J, Bozzolan F et al (2007) Identification of candidate aldehyde oxidases from the silkworm Bombyx mori potentially involved in antennal pheromone degradation. Gene 404(1–2):31–40. https://doi.org/10.1016/j.gene.2007.08.022
Perkins LE, Cribb BW et al (2013) Generalist insects behave in a jasmonate-dependent manner on their host plants, leaving induced areas quickly and staying longer on distant parts. P Roy Soc Biol Sci 280(1756):1–9. https://doi.org/10.1098/Rspb2012.2646
Rybczynski R, Reagan J et al (1989) A pheromone-degrading aldehyde oxidase in the antennae of the moth Manduca sexta. J Neurosci 9(4):1341–1353
Rybczynski R, Vogt RG et al (1990) Antennal-specific pheromone-degrading aldehyde oxidases from the moths Antheraea polyphemus and Bombyx mori. J Biol Chem 265(32):19712–19715
Singh S, Brocker C et al (2013) Aldehyde dehydrogenases in cellular responses to oxidative/electrophilic stress. Free Radical Bio Med 56:89–101. https://doi.org/10.1016/j.freeradbiomed201211.010
Su H, Cheng Y et al (2015) Silk gland gene expression during larval-pupal transition in the cotton leaf roller Sylepta derogata (Lepidoptera: Pyralidae). PLoS One 10(9):e0136868. https://doi.org/10.1371/journal.pone.0136868
Tamura K, Peterson D et al (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28(10):2731–2739. https://doi.org/10.1093/molbev/msr121
van der Goes van Naters W, Carlson JR (2006) Insects as chemosensors of humans and crops. Nature 444(7117):302–307. https://doi.org/10.1038/nature05403
Vogt RG, Riddiford LM (1981) Pheromone binding and inactivation by moth antennae. Nature 293(5828):161–163. https://doi.org/10.1038/293161a0
Wang HL, Zhao CH et al (2005) Comparative study of sex pheromone composition and biosynthesis in Helicoverpa armigera, H. assulta and their hybrid. Insect Biochem Mol Biol 35(6):575–583. https://doi.org/10.1016/j.ibmb.2005.01.018
Wu H, Hou C et al (2013) Peripheral coding of sex pheromone blends with reverse ratios in two helicoverpa species. PLoS One 8(7):e70078. https://doi.org/10.1371/journal.pone.0070078
Xu W, Zhang HJ et al (2012) A sugar gustatory receptor identified from the foregut of cotton bollworm Helicoverpa armigera. J Chem Ecol 38(12):1513–1520. https://doi.org/10.1007/s10886-012-0221-8
Xu W, Papanicolaou A et al (2015) Chemosensory receptor genes in the Oriental tobacco budworm Helicoverpa assulta. Insect Mol Biol 24(2):253–263. https://doi.org/10.1111/imb.12153
Xu W, Papanicolaou A et al (2016) Expansion of a bitter taste receptor family in a polyphagous insect herbivore. Sci Rep 6:23666. https://doi.org/10.1038/srep23666
Zhang YF, van Loon JJ et al (2010) Tarsal taste neuron activity and proboscis extension reflex in response to sugars and amino acids in Helicoverpa armigera (Hubner). J Exp Biol 213(Pt 16):2889–2895. https://doi.org/10.1242/jeb.042705
Acknowledgements
We would like to thank all the members of Helicoverpa genome consortium for permission to use the genome sequences ahead of the publication. We also thank Professor Myron Zalucki of the University of Queensland providing us H. armigera pupae and Dr. Alexie Papanicolaou of Hawkesbury Institute for the Environment (HIE) in Western Sydney University for in silico expression analysis. Dr. Wei Xu is the recipient of an Australian Research Council Discovery Early Career Researcher Award (DECRA) (DE160100382).
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Xu, W., Liao, Y. Identification and characterization of aldehyde oxidases (AOXs) in the cotton bollworm. Sci Nat 104, 94 (2017). https://doi.org/10.1007/s00114-017-1515-z
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DOI: https://doi.org/10.1007/s00114-017-1515-z