Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-22T19:10:07.014Z Has data issue: false hasContentIssue false

Chemosensory genes in the head of Spodoptera litura larvae

Published online by Cambridge University Press:  26 February 2021

Lu-Lu Li
Affiliation:
College of Life Sciences, Huaibei Normal University, 100 Dongshan Road, Huaibei235000, China
Ji-Wei Xu
Affiliation:
College of Life Sciences, Huaibei Normal University, 100 Dongshan Road, Huaibei235000, China
Wei-Chen Yao
Affiliation:
College of Life Sciences, Huaibei Normal University, 100 Dongshan Road, Huaibei235000, China
Hui-Hui Yang
Affiliation:
College of Life Sciences, Huaibei Normal University, 100 Dongshan Road, Huaibei235000, China
Youssef Dewer
Affiliation:
Bioassay Research Department, Central Agricultural Pesticide Laboratory, Agricultural Research Center, 7 Nadi El-Seid Street, Dokki 12618Giza, Egypt
Fan Zhang
Affiliation:
Key Laboratory of Animal Resistance Research, College of Life Science, Shandong Normal University, 88 East Wenhua Road, Jinan250014, China
Xiu-Yun Zhu*
Affiliation:
College of Life Sciences, Huaibei Normal University, 100 Dongshan Road, Huaibei235000, China
Ya-Nan Zhang*
Affiliation:
College of Life Sciences, Huaibei Normal University, 100 Dongshan Road, Huaibei235000, China
*
Author for correspondence: Xiu-Yun Zhu, Email: [email protected]; Ya-Nan Zhang, Email: [email protected]
Author for correspondence: Xiu-Yun Zhu, Email: [email protected]; Ya-Nan Zhang, Email: [email protected]

Abstract

The tobacco cutworm Spodoptera litura (Lepidoptera: Noctuidae) is a polyphagous pest with a highly selective and sensitive chemosensory system involved in complex physiological behaviors such as searching for food sources, feeding, courtship, and oviposition. However, effective management strategies for controlling the insect pest populations under threshold levels are lacking. Therefore, there is an urgent need to formulate eco-friendly pest control strategies based on the disruption of the insect chemosensory system. In this study, we identified 158 putative chemosensory genes based on transcriptomic and genomic data for S. litura, including 45 odorant-binding proteins (OBPs, nine were new), 23 chemosensory proteins (CSPs), 60 odorant receptors (ORs, three were new), and 30 gustatory receptors (GRs, three were new), a number higher than those reported by previous transcriptome studies. Subsequently, we constructed phylogenetic trees based on these genes in moths and analyzed the dynamic expression of various genes in head capsules across larval instars using quantitative real-time polymerase chain reaction. Nine genes–SlitOBP8, SlitOBP9, SlitOBP25, SlitCSP1, SlitCSP7, SlitCSP18, SlitOR34, SlitGR240, and SlitGR242–were highly expressed in the heads of 3- to 5-day-old S. litura larvae. The genes differentially expressed in olfactory organs during larval development might play crucial roles in the chemosensory system of S. litura larvae. Our findings substantially expand the gene inventory for S. litura and present potential target genes for further studies on larval feeding in S. litura.

Type
Research Paper
Copyright
Copyright © The Author(s), 2021. 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

Agnihotri, AR, Roy, AA and Joshi, RS (2016) Gustatory receptors in Lepidoptera: chemosensation and beyond. Insect Molecular Biology 25, 519529.CrossRefGoogle ScholarPubMed
Ahmad, M, Ghaffar, A and Rafiq, M (2013) Host plants of leaf worm, Spodoptera Litura (Fabricius) (Lepidoptera: noctuidae) in Pakistan. Asian Journal of Agriculture and Biology 1, 2328.Google Scholar
Bastin-Heline, L, de Fouchier, A, Cao, S, Koutroumpa, F, Caballero-Vidal, G, Robakiewicz, S, Monsempes, C, Francois, MC, Ribeyre, T, Maria, A, Chertemps, T, de Cian, A, Walker, WB III, Wang, G, Jacquin-Joly, E and Montagne, N (2019) A novel lineage of candidate pheromone receptors for sex communication in moths. Elife 8, e49826.CrossRefGoogle ScholarPubMed
CABI (2018) Invasive species compendium: data sheet Spodoptera litura (taro caterpillar). Available at https://www.cabi.org/isc/datasheet/44520.Google Scholar
Carraher, C, Dalziel, J, Jordan, MD, Christie, DL, Newcomb, RD and Kralicek, AV (2015) Towards an understanding of the structural basis for insect olfaction by odorant receptors. Insect Biochemistry and Molecular Biology 66, 3141.CrossRefGoogle ScholarPubMed
Celorio-Mancera Mde, L, Sundmalm, SM, Vogel, H, Rutishauser, D, Ytterberg, AJ, Zubarev, RA and Janz, N (2012) Chemosensory proteins, major salivary factors in caterpillar mandibular glands. Insect Biochemistry and Molecular Biology 42, 796805.CrossRefGoogle ScholarPubMed
Chen, GL, Pan, YF, Ma, YF, Wang, J, He, M and He, P (2018) Binding affinity characterization of an antennae-enriched chemosensory protein from the white-backed planthopper, Sogatella furcifera (Horvath), with host plant volatiles. Pesticide Biochemistry and Physiology 152, 17.CrossRefGoogle Scholar
Cheng, D, Lu, Y, Zeng, L, Liang, G and He, X (2015) Si-CSP9 regulates the integument and moulting process of larvae in the red imported fire ant, Solenopsis invicta. Scientific Reports 5, 9245.CrossRefGoogle ScholarPubMed
Cheng, T, Wu, J, Wu, Y, Chilukuri, RV, Huang, L, Yamamoto, K, Feng, L, Li, W, Chen, Z, Guo, H, Liu, J, Li, S, Wang, X, Peng, L, Liu, D, Guo, Y, Fu, B, Li, Z, Liu, C, Chen, Y, Tomar, A, Hilliou, F, Montagne, N, Jacquin-Joly, E, d'Alencon, E, Seth, RK, Bhatnagar, RK, Jouraku, A, Shiotsuki, T, Kadono-Okuda, K, Promboon, A, Smagghe, G, Arunkumar, KP, Kishino, H, Goldsmith, MR, Feng, Q, Xia, Q and Mita, K (2017) Genomic adaptation to polyphagy and insecticides in a major east Asian noctuid pest. Nature Ecology & Evolution 1, 17471756.CrossRefGoogle Scholar
Chyb, S, Dahanukar, A, Wickens, A and Carlson, JR (2003) Drosophila Gr5a encodes a taste receptor tuned to trehalose. Proceedings of the National Academy of Sciences of the United States of America 100(suppl. 2), 1452614530.CrossRefGoogle ScholarPubMed
Clark, JT and Ray, A (2016) Olfactory mechanisms for discovery of odorants to reduce insect-host contact. Journal of Chemical Ecology 42, 919930.CrossRefGoogle ScholarPubMed
Dahanukar, A, Lei, YT, Kwon, JY and Carlson, JR (2007) Two Gr genes underlie sugar reception in Drosophila. Neuron 56, 503516.CrossRefGoogle ScholarPubMed
De Fouchier, A, Sun, X, Caballero-Vidal, G, Travaillard, S, Jacquin-Joly, E and Montagné, N (2018) Behavioral effect of plant volatiles binding to Spodoptera littoralis Larval odorant receptors. Frontiers in Behavioral Neuroscience 12, 264.CrossRefGoogle ScholarPubMed
Dinesh-Kumar, A, Srimaan, E, Chellappandian, M, Vasantha-Srinivasan, P, Karthi, S, Thanigaivel, A, Ponsankar, A, Muthu-Pandian Chanthini, K, Shyam-Sundar, N, Annamalai, M, Kalaivani, K, Hunter, WB and Senthil-Nathan, S (2018) Target and non-target response of Swietenia Mahagoni Jacq. chemical constituents against tobacco cutworm Spodoptera litura Fab. and earthworm, Eudrilus eugeniae Kinb. Chemosphere 199, 3543.CrossRefGoogle ScholarPubMed
Durand, N, Carot-Sans, G, Bozzolan, F, Rosell, G, Siaussat, D, Debernard, S, Chertemps, T and Maibeche-Coisne, M (2011) Degradation of pheromone and plant volatile components by a same odorant-degrading enzyme in the cotton leafworm, Spodoptera littoralis. PLoS One 6, e29147.CrossRefGoogle ScholarPubMed
Feng, B, Lin, X, Zheng, K, Qian, K, Chang, Y and Du, Y (2015) Transcriptome and expression profiling analysis link patterns of gene expression to antennal responses in Spodoptera litura. BMC Genomics 16, 269.CrossRefGoogle ScholarPubMed
Field, LM, Pickett, JA and Wadhams, LJ (2000) Molecular studies in insect olfaction. Insect Molecular Biology 9, 545551.CrossRefGoogle ScholarPubMed
Getahun, MN, Thoma, M, Lavista-Llanos, S, Keesey, I, Fandino, RA, Knaden, M and Hansson, BS (2016) Intracellular regulation of the insect chemoreceptor complex impacts odour localization in flying insects. Journal of Experimental Biology 219, 34283438.Google ScholarPubMed
Gu, SH, Zhou, JJ, Gao, S, Wang, DH, Li, XC, Guo, YY and Zhang, YJ (2015) Identification and comparative expression analysis of odorant binding protein genes in the tobacco cutworm Spodoptera litura. Scientific Reports 5, 13800.CrossRefGoogle ScholarPubMed
Guo, H, Huang, LQ, Pelosi, P and Wang, CZ (2012) Three pheromone-binding proteins help segregation between two Helicoverpa species utilizing the same pheromone components. Insect Biochemistry and Molecular Biology 42, 708716.CrossRefGoogle ScholarPubMed
Hallem, EA, Dahanukar, A and Carlson, JR (2006) Insect odor and taste receptors. Annual Review of Entomology 51, 113135.CrossRefGoogle ScholarPubMed
He, P, Zhang, YN, Li, ZQ, Yang, K, Zhu, JY, Liu, SJ and Dong, SL (2014) An antennae-enriched carboxylesterase from Spodoptera exigua displays degradation activity in both plant volatiles and female sex pheromones. Insect Molecular Biology 23, 475486.CrossRefGoogle ScholarPubMed
He, P, Zhang, YN, Yang, K, Li, ZQ and Dong, SL (2015) An antenna-biased carboxylesterase is specifically active to plant volatiles in Spodoptera exigua. Pesticide Biochemistry and Physiology 123, 93100.CrossRefGoogle ScholarPubMed
He, P, Engsontia, P, Chen, GL, Yin, Q, Wang, J, Lu, X, Zhang, YN, Li, ZQ and He, M (2018) Molecular characterization and evolution of a chemosensory receptor gene family in three notorious rice planthoppers, Nilaparvata lugens, Sogatella furcifera and Laodelphax striatellus, based on genome and transcriptome analyses. Pest Management Science 74, 21562167.CrossRefGoogle Scholar
He, P, Durand, N and Dong, SL (2019a) Editorial: insect olfactory proteins (from gene identification to functional characterization). Frontiers in Physiology 10, 1313.CrossRefGoogle Scholar
He, P, Chen, GL, Li, S, Wang, J, Ma, YF, Pan, YF and He, M (2019b) Evolution and functional analysis of odorant-binding proteins in three rice planthoppers: Nilaparvata lugens, Sogatella furcifera, and Laodelphax striatellus. Pest Management Science 75, 16061620.CrossRefGoogle Scholar
He, P, Mang, DZ, Wang, H, Wang, MM, Ma, YF, Wang, J, Chen, GL, Zhang, F and He, M (2020) Molecular characterization and functional analysis of a novel candidate of cuticle carboxylesterase in Spodoptera exigua degrading sex pheromones and plant volatile esters. Pesticide Biochemistry and Physiology 163, 227234.CrossRefGoogle ScholarPubMed
Hopf, TA, Morinaga, S, Ihara, S, Touhara, K, Marks, DS and Benton, R (2015) Amino acid coevolution reveals three-dimensional structure and functional domains of insect odorant receptors. Nature Communications 6, 6077.CrossRefGoogle ScholarPubMed
Huang, CF, Huang, DX, Zheng, QW and Shen, YQ (2009) The features and control discussion on Chinese cabbage Spodoptera Litura's occurrence and harm. Journal of Guangxi Agriculture 24, 3637.Google Scholar
Ingham, VA, Anthousi, A, Douris, V, Harding, NJ, Lycett, G, Morris, M, Vontas, J and Ranson, H (2020) A sensory appendage protein protects malaria vectors from pyrethroids. Nature 577, 376380.CrossRefGoogle ScholarPubMed
Jacquin-Joly, E and Merlin, C (2004) Insect olfactory receptors: contributions of molecular biology to chemical ecology. Journal of Chemical Ecology 30, 23592397.CrossRefGoogle ScholarPubMed
Jacquin-Joly, E, Vogt, RG, Francois, MC and Nagnan-Le Meillour, P (2001) Functional and expression pattern analysis of chemosensory proteins expressed in antennae and pheromonal gland of Mamestra brassicae. Chemical Senses 26, 833844.CrossRefGoogle ScholarPubMed
Jeong, YT, Shim, J, Oh, SR, Yoon, HI, Kim, CH, Moon, SJ and Montell, C (2013) An odorant-binding protein required for suppression of sweet taste by bitter chemicals. Neuron 79, 725737.CrossRefGoogle ScholarPubMed
Jiang, XJ, Ning, C, Guo, H, Jia, YY, Huang, LQ, Qu, MJ and Wang, CZ (2015) A gustatory receptor tuned to d-fructose in antennal sensilla chaetica of Helicovera armigera. Insect Biochemistry and Molecular Biology 60, 3946.CrossRefGoogle Scholar
Jin, R, Liu, NY, Liu, Y and Dong, SL (2015) A larval specific OBP able to bind the major female sex pheromone component in Spodoptera exigua (Hübner). Journal of Integrative Agriculture 14, 13561366.CrossRefGoogle Scholar
Jones, WD, Cayirlioglu, P, Kadow, IG and Vosshall, LB (2007) Two chemosensory receptors together mediate carbon dioxide detection in Drosophila. Nature 445, 8690.CrossRefGoogle ScholarPubMed
Kwon, JY, Dahanukar, A, Weiss, LA and Carlson, JR (2007) The molecular basis of CO2 reception in Drosophila. Proceedings of the National Academy of Sciences of the United States of America 104, 35743578.CrossRefGoogle ScholarPubMed
Larsson, MC, Domingos, AI, Jones, WD, Chiappe, ME, Amrein, H and Vosshall, LB (2004) Or83b encodes a broadly expressed odorant receptor essential for Drosophila Olfaction. Neuron 43, 703714.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, K, Chen, J, Jin, P, Li, J, Wang, J and Shu, Y (2018) Effects of Cd accumulation on cutworm Spodoptera Litura larvae via Cd treated Chinese flowering cabbage Brassica campestris and artificial diets. Chemosphere 200, 151163.CrossRefGoogle Scholar
Liu, NY, Xu, W, Papanicolaou, A, Dong, SL and Anderson, A (2014a) Identification and characterization of three chemosensory receptor families in the cotton bollworm Helicoverpa armigera. BMC Genomics 15, 597.CrossRefGoogle Scholar
Liu, YL, Guo, H, Huang, LQ, Pelosi, P and Wang, CZ (2014b) Unique function of a chemosensory protein in the proboscis of two Helicoverpa species. Journal of Experimental Biology 217, 18211826.Google Scholar
Liu, NY, Zhang, T, Ye, ZF, Li, F and Dong, SL (2015a) Identification and characterization of candidate chemosensory gene families from Spodoptera exigua Developmental transcriptomes. International Journal of Biological Sciences 11, 10361048.CrossRefGoogle Scholar
Liu, NY, Yang, F, Yang, K, He, P, Niu, XH, Xu, W, Anderson, A and Dong, SL (2015b) Two subclasses of odorant-binding proteins in Spodoptera exigua display structural conservation and functional divergence. Insect Molecular Biology 24, 167182.CrossRefGoogle Scholar
Liu, Q, Liu, W, Zeng, B, Wang, G, Hao, D and Huang, Y (2017) Deletion of the Bombyx mori Odorant receptor co-receptor (BmOrco) impairs olfactory sensitivity in silkworms. Insect Biochemistry and Molecular Biology 86, 5867.CrossRefGoogle ScholarPubMed
Maleszka, J, Forêt, S, Saint, R and Maleszka, R (2007) RNAi-induced phenotypes suggest a novel role for a chemosensory protein CSP5 in the development of embryonic integument in the honeybee (Apis mellifera). Development Genes and Evolution 217, 189196.CrossRefGoogle Scholar
Mang, D, Shu, M, Tanaka, S, Nagata, S, Takada, T, Endo, H, Kikuta, S, Tabunoki, H, Iwabuchi, K and Sato, R (2016) Expression of the fructose receptor BmGr9 and its involvement in the promotion of feeding, suggested by its co-expression with neuropeptide F1 in Bombyx mori. Insect Biochemistry and Molecular Biology 75, 5869.CrossRefGoogle ScholarPubMed
Mortazavi, A, Williams, BA, McCue, K, Schaeffer, L and Wold, B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nature Methods 5, 621628.CrossRefGoogle ScholarPubMed
Muller, PY, Janovjak, H and Miserez, AZ (2002) Processing of gene expression data generated by quantitative real-time RT-PCR. Biotechniques 32, 13721374.Google ScholarPubMed
Pelosi, P, Calvello, M and Ban, L (2005) Diversity of odorant-binding proteins and chemosensory proteins in insects. Chemical Senses 30(suppl. 1), i291i292.CrossRefGoogle ScholarPubMed
Pelosi, P, Mastrogiacomo, R, Iovinella, I, Tuccori, E and Persaud, KC (2014) Structure and biotechnological applications of odorant-binding proteins. Applied Microbiology and Biotechnology 98, 6170.CrossRefGoogle ScholarPubMed
Pelosi, P, Iovinella, I, Zhu, J, Wang, G and Dani, FR (2018) Beyond chemoreception: diverse tasks of soluble olfactory proteins in insects. Biological Reviews of the Cambridge Philosophical Society 93, 184200.CrossRefGoogle ScholarPubMed
Picimbon, JF and Gadenne, C (2002) Evolution of noctuid pheromone binding proteins: identification of PBP in the black cutworm moth, Agrotis ipsilon. Insect Biochemistry and Molecular Biology 32, 839846.CrossRefGoogle ScholarPubMed
Poivet, E, Rharrabe, K, Monsempes, C, Glaser, N, Rochat, D, Renou, M, Marion-Poll, F and Jacquin-Joly, E (2012) The use of the sex pheromone as an evolutionary solution to food source selection in caterpillars. Nature Communications 3, 1047.CrossRefGoogle ScholarPubMed
Raad, H, Ferveur, JF, Ledger, N, Capovilla, M and Robichon, A (2016) Functional gustatory role of chemoreceptors in Drosophila Wings. Cell Reports 15, 14421454.CrossRefGoogle ScholarPubMed
Sannino, L and Espinosa, B (1999) Morphological notes on Mamestra brassicae (Lepidoptera Noctuidae). Il Tabacco 7, 1324.Google Scholar
Sato, K, Tanaka, K and Touhara, K (2011) Sugar-regulated cation channel formed by an insect gustatory receptor. Proceedings of the National Academy of Sciences of the United States of America 108, 1168011685.CrossRefGoogle ScholarPubMed
Simon, P (2003) Q-Gene: processing quantitative real-time RT-PCR data. Bioinformatics (Oxford, England) 19, 14391440.CrossRefGoogle ScholarPubMed
Smith, IM, McNamara, DG, Scott, PR and Holderness, M (1997) Spodoptera littoralis and spodoptera litura. In Quarantine Pests for Europe, 2nd Edn. Wallingford, Oxon, UK: CAB International, pp. 518525.Google Scholar
Soffan, A, Subandiyah, S, Makino, H, Watanabe, T and Horiike, T (2018) Evolutionary analysis of the highly conserved insect odorant coreceptor (Orco) revealed a positive selection mode, implying functional flexibility. Journal of Insect Science (Online) 18, 18.CrossRefGoogle ScholarPubMed
Vogt, RG (2003) Biochemical diversity of odor detection:OBPs, ODEs and SNMPs. In Blomquist, GJ and Vogt, RG (eds), Insect Pheromone Biochemistry and Molecular Biology. London: Elsevier Academic Press, pp. 397451.Google Scholar
Wu, CX, Liu, JF, Di, XY and Yang, MF (2018) Delay in mating reduces reproductivity but increases life span in tobacco cutworm, Spodoptera litura Fabricius (Lepidoptera: Noctuidae). Journal of Economic Entomology 111, 16501657.CrossRefGoogle Scholar
Xu, Z, Cao, GC and Dong, SL (2010) Changes of sex pheromone communication systems associated with tebufenozide and abamectin resistance in diamondback moth, Plutella Xylostella (L.). Journal of Chemical Ecology 36, 526534.CrossRefGoogle Scholar
Xu, W, Zhang, HJ and Anderson, A (2012) A sugar gustatory receptor identified from the foregut of cotton bollworm Helicoverpa armigera. Journal of Chemical Ecology 38, 15131520.CrossRefGoogle ScholarPubMed
Xu, W, Papanicolaou, A, Liu, NY, Dong, SL and Anderson, A (2015) Chemosensory receptor genes in the Oriental tobacco budworm Helicoverpa assulta. Insect Molecular Biology 24, 253263.CrossRefGoogle ScholarPubMed
Yan, H, Jafari, S, Pask, G, Zhou, X, Reinberg, D and Desplan, C (2020) Evolution, developmental expression and function of odorant receptors in insects. Journal of Experimenta Biology 223, jeb208215.Google ScholarPubMed
Yang, S, Cao, D, Wang, G and Liu, Y (2017) Identification of genes involved in chemoreception in Plutella Xyllostella by antennal transcriptome analysis. Scientific Reports 7, 11941.CrossRefGoogle ScholarPubMed
Zhang, HJ, Anderson, AR, Trowell, SC, Luo, AR, Xiang, ZH and Xia, QY (2011) Topological and functional characterization of an insect gustatory receptor. PLoS One 6, e24111.CrossRefGoogle ScholarPubMed
Zhang, YN, Ye, ZF, Yang, K and Dong, SL (2014) Antenna-predominant and male-biased CSP19 of Sesamia Inferens is able to bind the female sex pheromones and host plant volatiles. Gene 536, 279286.CrossRefGoogle ScholarPubMed
Zhang, J, Yan, S, Liu, Y, Jacquin-Joly, E, Dong, S and Wang, G (2015a) Identification and functional characterization of sex pheromone receptors in the common cutworm (Spodoptera litura). Chemical Senses 40, 716.CrossRefGoogle Scholar
Zhang, YN, Zhu, XY, Fang, LP, He, P, Wang, ZQ, Chen, G, Sun, L, Ye, ZF, Deng, DG and Li, JB (2015b) Identification and expression profiles of sex pheromone biosynthesis and transport related genes in Spodoptera litura. PLoS One 10, e0140019.CrossRefGoogle Scholar
Zhang, YN, Li, JB, He, P, Sun, L, Li, ZQ, Fang, LP, Ye, ZF, Deng, DG and Zhu, XY (2016) Molecular identification and expression patterns of carboxylesterase genes based on transcriptome analysis of the common cutworm, Spodoptera litura (Lepidoptera: Noctuidae). Journal of Asia-Pacific Entomology 19, 989994.CrossRefGoogle Scholar
Zhang, YN, Zhu, XY, Ma, JF, Dong, ZP, Xu, JW, Kang, K and Zhang, LW (2017) Molecular identification and expression patterns of odorant binding protein and chemosensory protein genes in Athetis lepigone (Lepidoptera: Noctuidae). PeerJ 5, e3157.CrossRefGoogle Scholar
Zhang, ZJ, Zhang, SS, Niu, BL, Ji, DF, Liu, XJ, Li, MW, Bai, H, Palli, SR, Wang, CZ and Tan, AJ (2019) A determining factor for insect feeding preference in the silkworm, Bombyx mori. PLoS Biology 17, e3000162.CrossRefGoogle ScholarPubMed
Zhou, JJ (2010) Odorant-binding proteins in insects. Vitamins and Hormones 83, 241272.CrossRefGoogle ScholarPubMed
Zhu, JY, Xu, ZW, Zhang, XM and Liu, NY (2018) Genome-based identification and analysis of ionotropic receptors in Spodoptera litura. Naturwissenschaften 105, 38.CrossRefGoogle ScholarPubMed
Zou, X, Xu, Z, Zou, H, Liu, J, Chen, S, Feng, Q and Zheng, S (2016) Glutathione S-transferase SlGSTE1 in Spodoptera litura may be associated with feeding adaptation of host plants. Insect Biochemistry and Molecular Biology 70, 3243.CrossRefGoogle ScholarPubMed
Supplementary material: File

Li et al. supplementary material

Li et al. supplementary material

Download Li et al. supplementary material(File)
File 71.2 KB