Many insects can live on water and survive being caught in the rain. Current research has shown that insect cuticular hydrocarbons (CHC) confer desiccation resistance to maintain water balance. In this study, we identified a fatty acyl-CoA reductase gene (NlFAR) of the rice brown planthopper, Nilaparvata lugens that is essential for the production of CHCs, and found that NlFAR is essential for N. lugens to walk and jump on water when moving from one rice plant to another in paddy fields. NlFAR was mainly expressed in the integument at the beginning of each molt. Cuticular surface analysis by scanning electron microscopy and characterization of CHC extracts indicated that N. lugens with knockdown of NlFAR using RNA inference (RNAi) had a neater epicuticle layer and a significant decrease in CHC contents. Knockdown of NlFAR did not influence the desiccation resistance of N. lugens, but the dsNlFAR-treated insects were easily adhered and moistened by water droplets or their own secreted honeydew and unable to walk or jump on water. These results suggested that NlFAR is a crucial enzyme for CHC biosynthesis and cuticle waterproofing, but not for water retention of N. lugens, which may provide a potential strategy for pest management.
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Antony, B., Fujii, T., Moto, K., Matsumoto, S., Fukuzawa, M., Nakano, R., Tatsuki, S., and Ishikawa, Y. (2009). Pheromone–gland–specific fattyacyl reductase in the adzuki bean borer, Ostrinia scapulalis (Lepidoptera: Crambidae). Insect Biochem Mol Biol 39, 90–95.
Balabanidou, V., Kampouraki, A., MacLean, M., Blomquist, G.J., Tittiger, C., Juárez, M.P., Mijailovsky, S.J., Chalepakis, G., Anthousi, A., Lynd, A., et al. (2016). Cytochrome P450 associated with insecticide resistance catalyzes cuticular hydrocarbon production in Anopheles gambiae. Proc Natl Acad Sci USA 113, 9268–9273.
Bottrell, D.G., and Schoenly, K.G. (2012). Resurrecting the ghost of green revolutions past: The brown planthopper as a recurring threat to highyielding rice production in tropical Asia. J Asia–Pac Entomol 15, 122–140.
Chen, N., Fan, Y.L., Bai, Y., Li, X.D., Zhang, Z.F., and Liu, T.X. (2016). Cytochrome P450 gene, CYP4G51, modulates hydrocarbon production in the pea aphid, Acyrthosiphon pisum. Insect Biochem Mol Biol 76, 84–94.
Cheng, J.B., and Russell, D.W. (2004). Mammalian wax biosynthesis. J Biol Chem 279, 37798–37807.
Chung, H., and Carroll, S.B. (2015). Wax, sex and the origin of species: Dual roles of insect cuticular hydrocarbons in adaptation and mating. Bioessays 37, 822–830.
Dickinson, M. (2003). How to walk on water. Nature 424, 621–622.
Doan, T.T.P., Carlsson, A.S., Stymne, S., and Hofvander, P. (2016). Biochemical characteristics of AtFAR2, a fatty acid reductase from Arabidopsis thaliana that reduces fatty acyl–CoA and–ACP substrates into fatty alcohols. Acta Biochim Pol 63, 565–570.
Gao, X., and Jiang, L. (2004). Water–repellent legs of water striders. Nature 432, 36.
Ge, L.Q., Huang, L.J., Yang, G.Q., Song, Q.S., Stanley, D., Gurr, G.M., and Wu, J.C. (2013). Molecular basis for insecticide–enhanced thermotolerance in the brown planthopper Nilaparvata lugens Stål (Hemiptera:Delphacidae). Mol Ecol 22, 5624–5634.
Gibbs, A.G. (1998). Water–proofing properties of cuticular lipids. Am Zool 38, 471–482.
Gibbs, A.G. (2007). Waterproof cockroaches: The early work of J. A. Ramsay. J Exp Biol 210, 921–922.
Guillem, R.M., Drijfhout, F.P., and Martin, S.J. (2016). Species–specific cuticular hydrocarbon stability within European Myrmica ants. J Chem Ecol 42, 1052–1062.
Hadley, N.F. (1981). Cuticular lipids of terrestrial plants and arthropods: a comparison of their structure, composition, and waterproofing function. Biol Rev 56, 23–47.
Hadley, N.F. (1991). Integumental lipids of plants and animals: comparative function and biochemistry. Adv Lipid Res 24, 303–320.
Hellenbrand, J., Biester, E.M., Gruber, J., Hamberg, M., and Frentzen, M. (2011). Fatty acyl–CoA reductases of birds. BMC Biochem 12, 64.
Hu, D.L., Chan, B., and Bush, J.W.M. (2003). The hydrodynamics of water strider locomotion. Nature 424, 663–666.
Hu, Y.H., Chen, X.M., Yang, P., and Ding, W.F. (2018). Characterization and functional assay of a fatty acyl–CoA reductase gene in the scale insect, Ericerus pela Chavannes (Hemiptera: Coccoidae). Arch Insect Biochem Physiol 97, e21445.
Huang, H.J., Liu, C.W., Xu, H.J., Bao, Y.Y., and Zhang, C.X. (2017a). Mucin–like protein, a saliva component involved in brown planthopper virulence and host adaptation. J Insect Physiol 98, 223–230.
Huang, H.J., Xue, J., Zhuo, J.C., Cheng, R.L., Xu, H.J., and Zhang, C.X. (2017b). Comparative analysis of the transcriptional responses to low and high temperatures in three rice planthopper species. Mol Ecol 26, 2726–2737.
Jaspers, M.H.J., Pflanz, R., Riedel, D., Kawelke, S., Feussner, I., and Schuh, R. (2014). The fatty acyl–CoA reductase waterproof mediates airway clearance in Drosophila. Dev Biol 385, 23–31.
Li, X., Zheng, T., Zheng, X., Han, N., Chen, X., and Zhang, D. (2016). Molecular characterization of two fatty Acyl–CoA reductase genes from Phenacoccus solenopsis (Hemiptera: Pseudococcidae). J Insect Sci 16, 49.
Liénard, M.A., Hagström, A.K., Lassance, J.M., and Löfstedt, C. (2010). Evolution of multicomponent pheromone signals in small ermine moths involves a single fatty–acyl reductase gene. Proc Natl Acad Sci USA 107, 10955–10960.
Liu, R., Zhu, F., Lu, L., Fu, A., Lu, J., Deng, Z., and Liu, T. (2014). Metabolic engineering of fatty acyl–ACP reductase–dependent pathway to improve fatty alcohol production in Escherichia coli. Metab Eng 22, 10–21.
Lockey, K.H. (1991). Insect hydrocarbon classes: Implications for chemotaxonomy. Insect Biochem 21, 91–97.
Metz, J.G., Pollard, M.R., Anderson, L., Hayes, T.R., and Lassner, M.W. (2000). Purification of a jojoba embryo fatty acyl–coenzyme A reductase and expression of its cDNA in high erucic acid rapeseed. Plant Physiol 122, 635–644.
Moto, K., Yoshiga, T., Yamamoto, M., Takahashi, S., Okano, K., Ando, T., Nakata, T., and Matsumoto, S. (2003). Pheromone gland–specific fattyacyl reductase of the silkmoth, Bombyx mori. Proc Natl Acad Sci USA 100, 9156–9161.
Pan, P.L., Ye, Y.X., Lou, Y.H., Lu, J.B., Cheng, C., Shen, Y., Moussian, B., and Zhang, C.X. (2018). A comprehensive omics analysis and functional survey of cuticular proteins in the brown planthopper. Proc Natl Acad Sci USA 115, 5175–5180.
Qiu, Y., Tittiger, C., Wicker–Thomas, C., Le Goff, G., Young, S., Wajnberg, E., Fricaux, T., Taquet, N., Blomquist, G.J., and Feyereisen, R. (2012). An insect–specific P450 oxidative decarbonylase for cuticular hydrocarbon biosynthesis. Proc Natl Acad Sci USA 109, 14858–14863.
Teerawanichpan, P., Robertson, A.J., and Qiu, X. (2010). A fatty acyl–CoA reductase highly expressed in the head of honey bee (Apis mellifera) involves biosynthesis of a wide range of aliphatic fatty alcohols. Insect Biochem Mol Biol 40, 641–649.
Wang, Y., Carballo, R.G., and Moussian, B. (2017). Double cuticle barrier in two global pests, the whitefly Trialeurodes vaporariorum and the bedbug Cimex lectularius. J Exp Biol 220, 1396–1399.
Wang, Y., Yu, Z., Zhang, J., and Moussian, B. (2016). Regionalization of surface lipids in insects. Proc R Soc B 283, 20152994.
Wigglesworth, V.B. (1933). The physiology of the cuticle and of ecdysis in Rhodnius prolixus (Triatomidae, Hemiptera) with special reference to the function of the oenocytes and of the dermal glands. Quart J Microsc Sci 76, 269–318.
Wigglesworth, V.B. (1945). Transpiration through the cuticle of insects. J Exp Biol 21, 97–113.
Xu, H.J., Xue, J., Lu, B., Zhang, X.C., Zhuo, J.C., He, S.F., Ma, X.F., Jiang, Y.Q., Fan, H.W., Xu, J.Y., et al. (2015). Two insulin receptors determine alternative wing morphs in planthoppers. Nature 519, 464–467.
Xue, J., Zhou, X., Zhang, C.X., Yu, L.L., Fan, H.W., Wang, Z., Xu, H.J., Xi, Y., Zhu, Z.R., Zhou, W.W., et al. (2014). Genomes of the rice pest brown planthopper and its endosymbionts reveal complex complementary contributions for host adaptation. Genome Biol 15, 521.
Xue, J., Bao, Y.Y., Li, B.L., Cheng, Y.B., Peng, Z.Y., Liu, H., Xu, H.J., Zhu, Z.R., Lou, Y.G., Cheng, J.A., et al. (2010). Transcriptome analysis of the brown planthopper Nilaparvata lugens. PLoS ONE 5, e14233.
Yu, Z., Wang, Y., Zhao, X., Liu, X., Ma, E., Moussian, B., and Zhang, J. (2017). The ABC transporter ABCH–9C is needed for cuticle barrier construction in Locusta migratoria. Insect Biochem Mol Biol 87, 90–99.
Yu, Z., Zhang, X., Wang, Y., Moussian, B., Zhu, K.Y., Li, S., Ma, E., and Zhang, J. (2016). LmCYP4G102: An oenocyte–specific cytochrome P450 gene required for cuticular waterproofing in the migratory locust, Locusta migratoria. Sci Rep 6, 29980.
This work was supported by the National Natural Science Foundation of China (31630057 and 31471765). We thank Dr. Yong-Liang Fan and Nan Chen for their kind help in CHC analysis.
Compliance and ethics The author(s) declare that they have no conflict of interest.
Figure S1 GC-MS analysis of CHCs.
Table S1 Primers used in this work
Table S2 NCBI accession numbers of sequences used for phylogenetic analysis
Table S3 Effect of RNAi suppression of NlFAR on the hydrocarbons of N. lugens
Video 1 Waterproofing experiment of dsNlFAR- and dsGFP-treated N. lugens
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Li, DT., Chen, X., Wang, XQ. et al. FAR gene enables the brown planthopper to walk and jump on water in paddy field. Sci. China Life Sci. 62, 1521–1531 (2019). https://doi.org/10.1007/s11427-018-9462-4
- Nilaparvata lugens
- fatty acyl-CoA reductase
- cuticular hydrocarbon