Abstract
The green mirid bug Apolygus lucorum is an agricultural pest that is known to cause damage to more than 150 plant species. Here, we report the transcriptomes of A. lucorum at three different developmental stages (the second and fifth instar nymphs and adults). A total of 98,236 unigenes with an average length of 1,335 nt was obtained, of which 50,640 were annotated, including those encoding digestive enzymes and cytochrome P450s. Comparisons with cotton bollworm and cotton aphid transcriptomes revealed distinct features of A. lucorum as a mesophyll feeder. The gene expression dynamics varied during development from young nymphs to adults. The high-quality transcriptome data and the gene expression dynamics reported here provide valuable data for a more comprehensive understanding of the physiology and development of mirid bugs, and for mining targets for their control.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Benjamini, Y., Drai, D., Elmer, G., Kafkafi, N., and Golani, I. (2001). Controlling the false discovery rate in behavior genetics research. Behav Brain Res 125, 279–284.
Benoit, J.B., Adelman, Z.N., Reinhardt, K., Dolan, A., Poelchau, M., Jennings, E.C., Szuter, E.M., Hagan, R.W., Gujar, H., Shukla, J.N., Zhu, F., Mohan, M., Nelson, D.R., Rosendale, A.J., Derst, C., Resnik, V., Wernig, S., Menegazzi, P., Wegener, C., Peschel, N., Hendershot, J.M., Blenau, W., Predel, R., Johnston, P.R., Ioannidis, P., Waterhouse, R.M., Nauen, R., Schorn, C., Ott, M.C., Maiwald, F., Johnston, J.S., Gondhalekar, A.D., Scharf, M.E., Peterson, B.F., Raje, K.R., Hottel, B.A., Armisén, D., Crumière, A.J.J., Refki, P.N., Santos, M.E., Sghaier, E., Viala, S., Khila, A., Ahn, S.J., Childers, C., Lee, C.Y., Lin, H., Hughes, D.S.T., Duncan, E.J., Murali, S.C., Qu, J., Dugan, S., Lee, S.L., Chao, H., Dinh, H., Han, Y., Doddapaneni, H., Worley, K.C., Muzny, D.M., Wheeler, D., Panfilio, K.A., Vargas Jentzsch, I.M., Vargo, E.L., Booth, W., Friedrich, M., Weirauch, M.T., Anderson, M.A.E., Jones, J.W., Mittapalli, O., Zhao, C., Zhou, J.J., Evans, J.D., Attardo, G.M., Robertson, H.M., Zdobnov, E.M., Ribeiro, J.M.C., Gibbs, R.A., Werren, J.H., Palli, S.R., Schal, C., and Richards, S. (2016). Unique features of a global human ectoparasite identified through sequencing of the bed bug genome. Nat Commun 7, 10165.
Canavoso, L.E., Jouni, Z.E., Karnas, K.J., Pennington, J.E., and Wells, M.A. (2001). Fat metabolism in insects. Annu Rev Nutr 21, 23–46.
Cao, D.P., Liu, Y., Wei, J.J., Li, J.H., and Wang, G.R. (2016). A de novotranscriptomic analysis to reveal functional genes in Apolygus lucorum. Insect Sci 23, 2–14.
Chen, G., Shi, T., and Shi, L. (2017). Characterizing and annotating the genome using RNA-seq data. Sci China Life Sci 60, 116–125.
Chen, Z.X., Sturgill, D., Qu, J., Jiang, H., Park, S., Boley, N., Suzuki, A.M., Fletcher, A.R., Plachetzki, D.C., FitzGerald, P.C., Artieri, C.G., Atallah, J., Barmina, O., Brown, J.B., Blankenburg, K.P., Clough, E., Dasgupta, A., Gubbala, S., Han, Y., Jayaseelan, J.C., Kalra, D., Kim, Y.A., Kovar, C.L., Lee, S.L., Li, M., Malley, J.D., Malone, J.H., Mathew, T., Mattiuzzo, N.R., Munidasa, M., Muzny, D.M., Ongeri, F., Perales, L., Przytycka, T.M., Pu, L.L., Robinson, G., Thornton, R.L., Saada, N., Scherer, S.E., Smith, H.E., Vinson, C., Warner, C.B., Worley, K.C., Wu, Y.Q., Zou, X., Cherbas, P., Kellis, M., Eisen, M.B., Piano, F., Kionte, K., Fitch, D.H., Sternberg, P.W., Cutter, A.D., Duff, M.O., Hoskins, R.A., Graveley, B.R., Gibbs, R.A., Bickel, P.J., Kopp, A., Carninci, P., Celniker, S.E., Oliver, B., and Richards, S. (2014). Comparative validation of the D. melanogaster modENCODE transcriptome annotation. Genome Res 24, 1209–1223.
Dennis, E.A. (1994). Diversity of group types, regulation, and function of phospholipase A2. J Biol Chem 269, 13057–13060.
Eubanks, M.D., and Denno, R.F. (1999). The ecological consequences of variation in plants and prey for an omnivorous insect. Ecology 80, 1253–1266.
Feyereisen, R. (2006). Evolution of insect P450. Biochem Soc Trans 34, 1252–1255.
Finseth, F.R., and Harrison, R.G. (2014). A comparison of next generation sequencing technologies for transcriptome assembly and utility for RNASeq in a non-model bird. PLoS ONE 9, e108550.
Fleming, D.E., Krishnan, N., Catchot, A.L., and Musser, F.R. (2016). Susceptibility to insecticides and activities of glutathione S-transferase and esterase in populations of Lygus lineolaris (Hemiptera: Miridae) in Mississippi. Pest Manag Sci 72, 1595–1603.
Guo, H., Song, X., Wang, G., Yang, K., Wang, Y., Niu, L., Chen, X., and Fang, R. (2014). Plant-generated artificial small RNAs mediated aphid resistance. PLoS ONE 9, e97410.
Haas, B.J., Papanicolaou, A., Yassour, M., Grabherr, M., Blood, P.D., Bowden, J., Couger, M.B., Eccles, D., Li, B., Lieber, M., Macmanes, M.D., Ott, M., Orvis, J., Pochet, N., Strozzi, F., Weeks, N., Westerman, R., William, T., Dewey, C.N., Henschel, R., Leduc, R.D., Friedman, N., and Regev, A. (2013). De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc 8, 1494–1512.
Hull, J.J., Geib, S.M., Fabrick, J.A., and Brent, C.S. (2013). Sequencing and de novo assembly of the western tarnished plant bug (Lygus hesperus) transcriptome. PLoS ONE 8, e55105.
Kimmins, F.M., and Tjallingii, W.F. (1985). Ultrastructure of sieve element penetration by aphid stylets during electrical recording. Entomol Exp Appl 39, 135–141.
Labandeira, C.C., and Phillips, T.L. (1996). Insect fluid-feeding on upper Pennsylvanian tree ferns (Palaeodictyoptera, Marattiales) and the early history of the piercing-and-sucking functional feeding group. Ann Entomol Soc Am 89, 157–183.
Langmead, B., Trapnell, C., Pop, M., and Salzberg, S.L. (2009). Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10, R25.
Li, B., and Dewey, C.N. (2011). RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12, 323.
Liu, N., Li, M., Gong, Y., Liu, F., and Li, T. (2015). Cytochrome P450s—Their expression, regulation, and role in insecticide resistance. Pesticide Biochem Physiol 120, 77–81.
Lu, Y., Jiao, Z., and Wu, K. (2012). Early season host plants of Apolygus lucorum (Heteroptera: Miridae) in northern China. J Econ Entomol 105, 1603–1611.
Lu, Y., Wu, K., Jiang, Y., Xia, B., Li, P., Feng, H., Wyckhuys, K.A.G., and Guo, Y. (2010). Mirid bug outbreaks in multiple crops correlated with wide-scale adoption of Bt cotton in China. Science 328, 1151–1154.
Lu, Y.H., Qiu, F., Feng, H.Q., Li, H.B., Yang, Z.C., Wyckhuys, K.A.G., and Wu, K.M. (2008). Species composition and seasonal abundance of pestiferous plant bugs (Hemiptera: Miridae) on Bt cotton in China. Crop Protect 27, 465–472.
Maczkowiak, F., and Da Lage, J.L. (2006). Origin and evolution of the Amyrel gene in the a-amylase multigene family of Diptera. Genetica 128, 145–158.
Mao, Y.B., Cai, W.J., Wang, J.W., Hong, G.J., Tao, X.Y., Wang, L.J., Huang, Y.P., and Chen, X.Y. (2007). Silencing a cotton bollworm P450 monooxygenase gene by plant-mediated RNAi impairs larval tolerance of gossypol. Nat Biotechnol 25, 1307–1313.
Miao, X.X., Xub, S.J., Li, M.H., Li, M.W., Huang, J.H., Dai, F.Y., Marino, S.W., Mills, D.R., Zeng, P., Mita, K., Jia, S.H., Zhang, Y., Liu, W.B., Xiang, H., Guo, Q.H., Xu, A.Y., Kong, X.Y., Lin, H.X., Shi, Y.Z., Lu, G., Zhang, X., Huang, W., Yasukochi, Y., Sugasaki, T., Shimada, T., Nagaraju, J., Xiang, Z.H., Wang, S.Y., Goldsmith, M.R., Lu, C., Zhao, G.P., and Huang, Y.P. (2005). Simple sequence repeat-based consensus linkage map of Bombyx mori. Proc Natl Acad Sci USA 102, 16303–16308.
Musser, R.O., Hum-Musser, S.M., Slaten-Bickford, S.E., Felton, G.W., and Gergerich, R.C. (2002). Evidence that ribonuclease activity present in beetle regurgitant is found to stimulate virus resistance in plants. J Chem Ecol 28, 1691–1696.
Pan, Y., Peng, T., Gao, X., Zhang, L., Yang, C., Xi, J., Xin, X., Bi, R., and Shang, Q. (2015a). Transcriptomic comparison of thiamethoxamresistance adaptation in resistant and susceptible strains of Aphis gossypii Glover. Comp Biochem Physiol Part D Genomics Proteomics 13, 10–15.
Pan, Y., Yang, C., Gao, X., Peng, T., Bi, R., Xi, J., Xin, X., Zhu, E., Wu, Y., and Shang, Q. (2015b). Spirotetramat resistance adaption analysis of Aphis gossypii Glover by transcriptomic survey. Pesticide Biochem Physiol 124, 73–80.
Papanicolaou, A., Schetelig, M.F., Arensburger, P., Atkinson, P.W., Benoit, J.B., Bourtzis, K., Castañ era, P., Cavanaugh, J.P., Chao, H., Childers, C., Curril, I., Dinh, H., Doddapaneni, H.V., Dolan, A., Dugan, S., Friedrich, M., Gasperi, G., Geib, S., Georgakilas, G., Gibbs, R.A., Giers, S.D., Gomulski, L.M., González-Guzmán, M., Guillem-Amat, A., Han, Y., Hatzigeorgiou, A.G., Hernández-Crespo, P., Hughes, D.S.T., Jones, J.W., Karagkouni, D., Koskinioti, P., Lee, S.L., Malacrida, A.R., Manni, M., Mathiopoulos, K., Meccariello, A., Murali, S.C., Murphy, T.D., Muzny, D.M., Oberhofer, G., Ortego, F., Paraskevopoulou, M.D., Poelchau, M., Qu, J., Reczko, M., Robertson, H.M., Rosendale, A.J., Rosselot, A.E., Saccone, G., Salvemini, M., Savini, G., Schreiner, P., Scolari, F., Siciliano, P., Sim, S.B., Tsiamis, G., Ureña, E., Vlachos, I.S., Werren, J.H., Wimmer, E.A., Worley, K.C., Zacharopoulou, A., Richards, S., and Handler, A.M. (2016). The whole genome sequence of the Mediterranean fruit fly, Ceratitis capitata (Wiedemann), reveals insights into the biology and adaptive evolution of a highly invasive pest species. Genome Biol 17, 192.
Pertea, G., Huang, X., Liang, F., Antonescu, V., Sultana, R., Karamycheva, S., Lee, Y., White, J., Cheung, F., Parvizi, B., Tsai, J., and Quackenbush, J. (2003). TIGR Gene Indices clustering tools (TGICL): a software system for fast clustering of large EST datasets. Bioinformatics 19, 651–652.
Ran, F.A., Hsu, P.D., Lin, C.Y., Gootenberg, J.S., Konermann, S., Trevino, A.E., Scott, D.A., Inoue, A., Matoba, S., Zhang, Y., and Zhang, F. (2013). Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell 154, 1380–1389.
Richards, S., Gibbs, R.A., Weinstock, G.M., Brown, S.J., Denell, R., Beeman, R.W., Gibbs, R., Beeman, R.W., Brown, S.J., Bucher, G., Friedrich, M., Grimmelikhuijzen, C.J.P., Klingler, M., Lorenzen, M., Richards, S., Roth, S., Schrö der, R., Tautz, D., Zdobnov, E.M., Muzny, D., Gibbs, R.A., Weinstock, G.M., Attaway, T., Bell, S., Buhay, C.J., Chandrabose, M.N., Chavez, D., Clerk-Blankenburg, K.P., Cree, A., Dao, M., Davis, C., Chacko, J., Dinh, H., Dugan-Rocha, S., Fowler, G., Garner, T.T., Garnes, J., Gnirke, A., Hawes, A., Hernandez, J., Hines, S., Holder, M., Hume, J., Jhangiani, S.N., Joshi, V., Khan, Z.M., Jackson, L.R., Kovar, C., Kowis, A., Lee, S., Lewis, L.R., Margolis, J., Morgan, M., Nazareth, L.V., Nguyen, N., Okwuonu, G., Parker, D., Richards, S., Ruiz, S.J., Santibanez, J., Savard, J., Scherer, S.E., Schneider, B., Sodergren, E., Tautz, D., Vattahil, S., Villasana, D., White, C.S., Wright, R., Park, Y., Beeman, R.W., Lord, J., Oppert, B., Lorenzen, M., Brown, S., Wang, L., Savard, J., Tautz, D., Richards, S., Weinstock, G., Gibbs, R.A., Liu, Y., Worley, K., Weinstock, G., Elsik, C.G., Reese, J.T., Elhaik, E., Landan, G., Graur, D., Arensburger, P., Atkinson, P., Beeman, R.W., Beidler, J., Brown, S.J., Demuth, J.P., Drury, D.W., Du, Y.Z., Fujiwara, H., Lorenzen, M., Maselli, V., Osanai, M., Park, Y., Robertson, H.M., Tu, Z., Wang, J., Wang, S., Richards, S., Song, H., Zhang, L., Sodergren, E., Werner, D., Stanke, M., Morgenstern, B., Solovyev, V., Kosarev, P., Brown, G., Chen, H.C., Ermolaeva, O., Hlavina, W., Kapustin, Y., Kiryutin, B., Kitts, P., Maglott, D., Pruitt, K., Sapojnikov, V., Souvorov, A., Mackey, A.J., Waterhouse, R.M., Wyder, S., Zdobnov, E.M., Zdobnov, E.M., Wyder, S., Kriventseva, E.V., Kadowaki, T., Bork, P., Aranda, M., Bao, R., Beermann, A., Berns, N., Bolognesi, R., Bonneton, F., Bopp, D., Brown, S.J., Bucher, G., Butts, T., Chaumot, A., Denell, R.E., Ferrier, D.E.K., Friedrich, M., Gordon, C.M., Jindra, M., Klingler, M., Lan, Q., Lattorff, H.M.G., Laudet, V., von Levetsow, C., Liu, Z., Lutz, R., Lynch, J.A., da Fonseca, R.N., Posnien, N., Reuter, R., Roth, S., Savard, J., Schinko, J.B., Schmitt, C., Schoppmeier, M., Schrö der, R., Shippy, T.D., Simonnet, F., Marques-Souza, H., Tautz, D., Tomoyasu, Y., Trauner, J., Van der Zee, M., Vervoort, M., Wittkopp, N., Wimmer, E.A., Yang, X., Jones, A.K., Sattelle, D.B., Ebert, P.R., Nelson, D., Scott, J.G., Beeman, R.W., Muthukrishnan, S., Kramer, K.J., Arakane, Y., Beeman, R.W., 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, C.J.P., 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, K.K.O., Robertson, H.M., Angeli, S., Forêt, S., Bucher, G., Schuetz, S., Maleszka, R., Wimmer, E.A., Beeman, R.W., Lorenzen, M., Tomoyasu, Y., Miller, S.C., Grossmann, D., and Bucher, G. (2008). The genome of the model beetle and pest Tribolium castaneum. Nature 452, 949–955.
Rodriguez-Saona, C., Crafts-Brandner, S.J., Williams III, L., and Paré, P.W. (2002). Lygus hesperus feeding and salivary gland extracts induce volatile emissions in plants. J Chem Ecol 28, 1733–1747.
Sharma, P.C., Grover, A., and Kahl, G. (2007). Mining microsatellites in eukaryotic genomes. Trends Biotech 25, 490–498.
Showmaker, K.C., Bednárová, A., Gresham, C., Hsu, C.Y., Peterson, D.G., and Krishnan, N. (2016). Insight into the salivary gland transcriptome of Lygus lineolaris (Palisot de Beauvois). PLoS ONE 11, e0147197.
Stolle, E., Kidner, J.H., and Moritz, R.F.A. (2013). Patterns of evolutionary conservation of microsatellites (SSRs) suggest a faster rate of genome evolution in Hymenoptera than in Diptera. Genome Biol Evol 5, 151–162.
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28, 2731–2739.
Tao, X.Y., Xue, X.Y., Huang, Y.P., Chen, X.Y., and Mao, Y.B. (2012). Gossypol- enhanced P450 gene pool contributes to cotton bollworm tolerance to a pyrethroid insecticide. Mol Ecol 21, 4371–4385.
Tatusov, R.L., Fedorova, N.D., Jackson, J.D., Jacobs, A.R., Kiryutin, B., Koonin, E.V., Krylov, D.M., Mazumder, R., Mekhedov, S.L., Nikolskaya, A.N., Rao, B.S., Smirnov, S., Sverdlov, A.V., Vasudevan, S., Wolf, Y.I., Yin, J.J., and Natale, D.A. (2003). The COG database: an updated version includes eukaryotes. BMC Bioinformatics 4, 41.
Thompson, J., Gibson, T.J., Plewniak, F., Jeanmougin, F., and Higgins, D.G. (1997). The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25, 4876–4882.
Tian, C., Tek Tay, W., Feng, H., Wang, Y., Hu, Y., and Li, G. (2015). Characterization of Adelphocoris suturalis (Hemiptera: Miridae) transcriptome from different developmental stages. Sci Rep 5, 11042.
Wang, X., Fang, X., Yang, P., Jiang, X., Jiang, F., Zhao, D., Li, B., Cui, F., Wei, J., Ma, C., Wang, Y., He, J., Luo, Y., Wang, Z., Guo, X., Guo, W., Wang, X., Zhang, Y., Yang, M., Hao, S., Chen, B., Ma, Z., Yu, D., Xiong, Z., Zhu, Y., Fan, D., Han, L., Wang, B., Chen, Y., Wang, J., Yang, L., Zhao, W., Feng, Y., Chen, G., Lian, J., Li, Q., Huang, Z., Yao, X., Lv, N., Zhang, G., Li, Y., Wang, J., Wang, J., Zhu, B., and Kang, L. (2014). The locust genome provides insight into swarm formation and long-distance flight. Nat Commun 5, 2957.
Wang, Y.M., Ding, Y., Yu, D.W., Xue, W., and Liu, J.Y. (2015). Highthroughput sequencing-based genome-wide identification of microRNAs expressed in developing cotton seeds. Sci China Life Sci 58, 778–786.
Watanabe, K. (1996). Characteristic of Damages of Lygocoris (Apolygus) lucorum (Meyer-Dür) (Heteroptera Miridae) and Halyomorpha halys (Stål) (Heteroptera: Pentatomidae) on Cherry. Annual Report of the Society of Agricultural Chemicals of North Japan, pp. 143–144.
Weiberg, A., Wang, M., Lin, F.M., Zhao, H., Zhang, Z., Kaloshian, I., Huang, H.D., and Jin, H. (2013). Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways. Science 342, 118–123.
Wu, K.M., Lu, Y.H., Feng, H.Q., Jiang, Y.Y., and Zhao, J.Z. (2008). Suppression of cotton bollworm in multiple crops in China in areas with Bt toxin-containing cotton. Science 321, 1676–1678.
Wu, X.M., Yang, C.Q., Mao, Y.B., Wang, L.J., Shangguan, X.X., and Chen, X.Y. (2016). Targeting insect mitochondrial complex I for plant protection. Plant Biotechnol J 14, 1925–1935.
Xia, Q., Guo, Y., Zhang, Z., Li, D., Xuan, Z., Li, Z., Dai, F., Li, Y., Cheng, D., Li, R., Cheng, T., Jiang, T., Becquet, C., Xu, X., Liu, C., Zha, X., Fan, W., Lin, Y., Shen, Y., Jiang, L., Jensen, J., Hellmann, I., Tang, S., Zhao, P., Xu, H., Yu, C., Zhang, G., Li, J., Cao, J., Liu, S., He, N., Zhou, Y., Liu, H., Zhao, J., Ye, C., Du, Z., Pan, G., Zhao, A., Shao, H., Zeng, W., Wu, P., Li, C., Pan, M., Li, J., Yin, X., Li, D., Wang, J., Zheng, H., Wang, W., Zhang, X., Li, S., Yang, H., Lu, C., Nielsen, R., Zhou, Z., Wang, J., Xiang, Z., and Wang, J. (2009). Complete resequencing of 40 genomes reveals domestication events and genes in silkworm (Bombyx). Science 326, 433–436.
Xie, W., Guo, L., Jiao, X., Yang, N., Yang, X., Wu, Q., Wang, S., Zhou, X., and Zhang, Y. (2014). Transcriptomic dissection of sexual differences in Bemisia tabaci, an invasive agricultural pest worldwide. Sci Rep 4, 4088.
Xiong, G.H., Xing, L.S., Lin, Z., Saha, T.T., Wang, C., Jiang, H., and Zou, Z. (2015). High throughput profiling of the cotton bollworm Helicoverpa armigera immunotranscriptome during the fungal and bacterial infections. BMC Genomics 16, 321.
Yuan, H.B., Ding, Y.X., Gu, S.H., Sun, L., Zhu, X.Q., Liu, H.W., Dhiloo, K.H., Zhang, Y.J., and Guo, Y.Y. (2015). Molecular characterization and expression profiling of odorant-binding proteins in Apolygus lucorum. PLoS ONE 10, e0140562.
Yuan, W., Li, W., Li, Y., and Wu, K. (2013). Combination of plant and insect eggs as food sources facilitates ovarian development in an omnivorous bug Apolygus lucorum (Hemiptera: Miridae). J Econ Entomol 106, 1200–1208.
Zhai, Y., Zhang, J., Sun, Z., Dong, X., He, Y., Kang, K., Liu, Z., and Zhang, W. (2013). Proteomic and transcriptomic analyses of fecundity in the brown planthopper Nilaparvata lugens (Stål). J Proteome Res 12, 5199–5212.
Zhang, L., Hou, D., Chen, X., Li, D., Zhu, L., Zhang, Y., Li, J., Bian, Z., Liang, X., Cai, X., Yin, Y., Wang, C., Zhang, T., Zhu, D., Zhang, D., Xu, J., Chen, Q., Ba, Y., Liu, J., Wang, Q., Chen, J., Wang, J., Wang, M., Zhang, Q., Zhang, J., Zen, K., and Zhang, C.Y. (2012). Exogenous plant MIR168a specifically targets mammalian LDLRAP1: evidence of cross-kingdom regulation by microRNA. Cell Res 22, 107–126.
Zhang, L., Lu, Y., and Liang, G. (2013). A method for field assessment of plant injury elicited by the salivary proteins of Apolygus lucorum. Entomol Exp Appl 149, 292–297.
Zhen, C., and Gao, X. (2016). A point mutation (L1015F) of the voltage- sensitive sodium channel gene associated with lambda-cyhalothrin resistance in Apolygus lucorum (Meyer-Dür) population from the transgenic Bt cotton field of China. Pesticide Biochem Physiol 127, 82–89.
Zhen, C., Miao, L., Liang, P., and Gao, X. (2016). Survey of organophosphate resistance and an Ala216Ser substitution of acetylcholinesterase-1 gene associated with chlorpyrifos resistance in Apolygus lucorum (Meyer-Dür) collected from the transgenic Bt cotton fields in China. Pesticide Biochem Physiol 132, 29–37.
Acknowledgements
We thank K. Wu and L. Chao for help in collecting and rearing A. lucorum and M. Yan for language editing of this manuscript. This work was supported by the Strategic Priority Research Program of Chinese Academy of Sciences (XDB11030000), and the Ministry of Agriculture of China (2014ZX08009001-009).
Author information
Authors and Affiliations
Corresponding authors
Rights and permissions
About this article
Cite this article
Chen, D., Chen, F., Chen, C. et al. Transcriptome analysis of three cotton pests reveals features of gene expressions in the mesophyll feeder Apolygus lucorum . Sci. China Life Sci. 60, 826–838 (2017). https://doi.org/10.1007/s11427-017-9065-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11427-017-9065-3