Hostname: page-component-848d4c4894-hfldf Total loading time: 0 Render date: 2024-05-01T02:36:59.187Z Has data issue: false hasContentIssue false

Molecular mechanism of Serratia marcescens Bizio infection in Reticulitermes chinensis Snyder based on full-length SMRT transcriptome sequencing

Published online by Cambridge University Press:  08 February 2024

Ling Zhang
Affiliation:
Co-Innovation Center for Sustainable Forestry in Southern China, Nanjing Forestry University, Nanjing 210037, People's Republic of China College of Forestry, Nanjing Forestry University, Nanjing 210037, People's Republic of China
Fang Tang*
Affiliation:
Co-Innovation Center for Sustainable Forestry in Southern China, Nanjing Forestry University, Nanjing 210037, People's Republic of China College of Forestry, Nanjing Forestry University, Nanjing 210037, People's Republic of China
*
Corresponding author: Fang Tang; Email: tangfang76@sohu.com

Abstract

Reticulitermes chinensis Snyder is an important pest in forestry and construction and is widely distributed in China. We found that Serratia marcescens Bizio strain SM1 has insecticidal activity to R. chinensis, but the pathogenic mechanism of SM1 to R. chinensis is not clear. Therefore, full-length transcriptome sequencing was performed on R. chinensis infected with SM1 and the control group. A total of 230 differentially expressed genes were identified by comparing SM1 infection group and the control group, among which 103 were downregulated and 127 were upregulated. We found downregulated genes in nine metabolic pathway categories, among which carbohydrate metabolism had the most downregulated genes, followed by energy metabolism and amino acid metabolism. We also found that some downregulated genes were related to pattern recognition receptors, cellular immunity, and humoral immunity, indicating that R. chinensis immunity was negatively affected by SM1 infection. In addition, some genes in signal transduction and genetic information processing pathways were downregulated. In this study, high-throughput full-length transcriptome analysis was used to analyse the pathogenic mechanism of SM1 to R. chinensis. The results of this study provide useful information for exploring the relationship between SM1 and R. chinensis, and provide theoretical support for the future application of SM1 and the prevention and treatment of R. chinensis.

Type
Research Paper
Copyright
Copyright © The Author(s), 2024. 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

Advedissian, T, Deshayes, F and Viguier, M (2017) Galectin-7 in epithelial homeostasis and carcinomas. International Journal of Molecular Sciences 18, 2760.CrossRefGoogle ScholarPubMed
Akira, S, Uematsu, S and Takeuchi, O (2006) Pathogen recognition and innate immunity. Cell 124, 783801.CrossRefGoogle ScholarPubMed
Armstrong, GAB, Shoemaker, KL, Money, TGA and Robertson, RM (2006) Octopamine mediates thermal preconditioning of the locust ventilatory central pattern generator via a cAMP/protein kinase A signaling pathway. Journal of Neuroscience 26, 1211812126.CrossRefGoogle Scholar
Ballabio, A (2016) The awesome lysosome. EMBO Molecular Medicine 8, 7376.CrossRefGoogle ScholarPubMed
Basnet, S and Kamble, ST (2018) RNAi-mediated knockdown of vATPase subunits affects survival and reproduction of bed bugs (Hemiptera: Cimicidae). Journal of Medical Entomology 55, 540546.CrossRefGoogle ScholarPubMed
Beyenbach, KW and Wieczorek, H (2006) The V-type H+ ATPase: molecular structure and function, physiological roles and regulation. Journal of Experimental Biology 209, 577589.CrossRefGoogle Scholar
Brubaker, SW, Bonham, KS, Zanoni, I and Kagan, JC (2015) Innate immune pattern recognition: a cell biological perspective. Annual Review of Immunology 33, 257290.CrossRefGoogle ScholarPubMed
Brummett, LM, Kanost, MR and Gorman, MJ (2017) The immune properties of Manduca sexta transferrin. Insect Biochemistry and Molecular Biology 81, 19.CrossRefGoogle ScholarPubMed
Buchfink, B, Xie, C and Huson, DH (2015) Fast and sensitive protein alignment using DIAMOND. Nature Methods 12, 5960.CrossRefGoogle ScholarPubMed
Cao, M, Gatehouse, JA and Fitches, EC (2018) A systematic study of RNAi effects and dsRNA stability in Tribolium castaneum and Acyrthosiphon pisum, following injection and ingestion of analogous dsRNAs. International Journal of Molecular Sciences 19, 1079.CrossRefGoogle ScholarPubMed
Chen, WW, Zhang, H, Chen, Y, Zeng, WH and Li, ZQ (2023) Combined use of lipopolysaccharide-binding protein dsRNA and Gram-negative bacteria for pest management of Coptotermes formosanus. Pest Management Science 79(7), 22872298.CrossRefGoogle ScholarPubMed
Cheng, CH, Ma, HL, Liu, GX, Deng, YQ, Jiang, JJ, Feng, J and Guo, ZX (2022) Biochemical, metabolic, and immune responses of mud crab (Scylla paramamosain) after mud crab reovirus infection. Fish and Shellfish Immunology 127, 437445.CrossRefGoogle ScholarPubMed
Cotter, SC, Myatt, JP, Benskin, CMH and Wilson, K (2008) Selection for cuticular melanism reveals immune function and life-history trade-offs in Spodoptera littoralis. Journal of Evolutionary Biology 21, 17441754.CrossRefGoogle ScholarPubMed
Covi, JA, Chang, ES and Mykles, DL (2012) Neuropeptide signaling mechanisms in crustacean and insect molting glands. Invertebrate Reproduction and Development 56, 3349.CrossRefGoogle Scholar
Ding, Z, Pan, J, Huang, H, Jiang, GC, Chen, JQ, Zhu, XS, Wang, RL and Xu, GH (2018) An integrated metabolic consequence of Hepatospora eriocheir infection in the Chinese mitten crab Eriocheir sinensis. Fish and Shellfish Immunology 72, 443451.CrossRefGoogle ScholarPubMed
Dong, YC, Chen, ZZ, Clarke, AR and Niu, CY (2019) Changes in energy metabolism trigger pupal diapause transition of Bactrocera minax after 20-hydroxyecdysone application. Frontiers in Physiology 10, 1288.CrossRefGoogle ScholarPubMed
Dunphy, G and Halwani, A (1997) Haemolymph proteins of larvae of Galleria mellonella detoxify endotoxins of the insect pathogenic bacteria Xenorhabdus nematophilus (Enterobacteriaceae). Journal of Insect Physiology 43, 10231029.CrossRefGoogle Scholar
Eliautout, R, Dubrana, MP, Vincent-Monégat, C, Vallier, A, Braquart-Varnier, C, Poirié, M, Saillard, C, Heddi, A and Arricau-Bouvery, N (2016) Immune response and survival of Circulifer haematoceps to Spiroplasma citri infection requires expression of the gene hexamerin. Developmental and Comparative Immunology 54, 719.CrossRefGoogle ScholarPubMed
Ferreira, APA and Boucrot, E (2018) Mechanisms of carrier formation during clathrin-independent endocytosis. Trends in cell Biology 28, 188200.CrossRefGoogle ScholarPubMed
Forgac, M (1989) Structure and function of vacuolar class of ATP-driven proton pumps. Physiological Reviews 69, 765796.CrossRefGoogle ScholarPubMed
Forgac, M (2007) Vacuolar ATPases: rotary proton pumps in physiology and pathophysiology. Nature Reviews Molecular Cell Biology 8, 917929.CrossRefGoogle ScholarPubMed
Gatehouse, HS, Markwick, NP, Poulton, J, Ward, VK, Young, V, Wilson, S, Dellow, R, Sneddon, K, Gatehouse, LN, Simpson, RM, Janssen, BJ, Bishop, R, Schaffer, RJ and Christeller, JT (2007) Effects of EppoNPV infection on gene expression in Epiphyas postvittana larvae. New Zealand Plant Protection 60, 3341.CrossRefGoogle Scholar
Geiser, DL and Winzerling, JJ (2012) Insect transferrins: multifunctional proteins. Biochimica et Biophysica Acta (BBA)-General Subjects 1820, 437451.CrossRefGoogle ScholarPubMed
Ghazy, NA and Suzuki, T (2022) Environmental RNAi-based reverse genetics in the predatory mite Neoseiulus californicus: towards improved methods of biological control. Pesticide Biochemistry and Physiology 180, 104993.CrossRefGoogle ScholarPubMed
Ghosh, P, Dahms, NM and Kornfeld, S (2003) Mannose 6-phosphate receptors: new twists in the tale. Nature Reviews Molecular Cell Biology 4, 202213.CrossRefGoogle ScholarPubMed
Hamama, HM, Hussein, MA, Fahmy, AR and Fergani, YA (2016) A transferrin fragment isolated from the Egyptian cotton leaf worm, Spodoptera littoralis (Boisduval) (Lepidoptera: Noctuidae) in response to two commercial bioinsecticides. Egyptian Journal of Biological Pest Control 26, 5964.Google Scholar
Harvey, W (1992) Physiology of V-ATPases. Journal of Experimental Biology 172, 117.CrossRefGoogle ScholarPubMed
Hegazy, MI, Salama, ASA, El-Ashry, RM and Othman, AEI (2019) Serratia marcescens and Pseudomonas aeruginosa are promising candidates as biocontrol agents against root-knot nematodes (Meloidogyne spp.). Middle East Journal of Agriculture Research 8, 828838.Google Scholar
Hinton, A, Bond, S and Forgac, M (2009) V-ATPase functions in normal and disease processes. Pflugers Archiv-European Journal of Physiology 457, 589598.CrossRefGoogle ScholarPubMed
Hou, X, Chen, XW, Yang, H, Yue, WC, Wang, J, Han, H and Wang, CH (2020) V-ATPase subunit B plays essential roles in the molting process of the Chinese mitten crab, Eriocheir sinensis. Biology Open 9, bio048926.CrossRefGoogle ScholarPubMed
Houseley, J and Tollervey, D (2009) The many pathways of RNA degradation. Cell 136, 763776.CrossRefGoogle ScholarPubMed
Huang, FS, Zhu, SM, Ping, ZM, He, XS, Li, GX and Gao, DR (2000) Fauna Sinica: Insecta, Vol. 17: Isoptera. Beijing: Science Press.Google Scholar
Huang, LL, Cheng, TC, Xu, PZ, Cheng, DJ, Fang, T and Xia, QY (2009) A genome-wide survey for host response of silkworm, Bombyx mori during pathogen Bacillus bombyseptieus infection. PLoS ONE 4, e8098.CrossRefGoogle ScholarPubMed
Huang, ZJ, Tian, Z, Zhao, YL, Zhu, F, Liu, W and Wang, XP (2022) MAPK signaling pathway is essential for female reproductive regulation in the cabbage beetle, Colaphellus bowringi. Cells 11, 1602.CrossRefGoogle ScholarPubMed
Inglis, GD and Lawrence, AM (2001) Effects of Serratia marcescens on the F1 generation of laboratory-reared Heliothis virescens (Lepidoptera: Noctuidae). Journal of Economic Entomology 94, 362366.CrossRefGoogle ScholarPubMed
Jiang, DB, Lu, XY, Zhang, L and Tang, F (2023) Enhancement of pathogen toxicity by feeding Reticulitermes chinensis Snyder sonicated bacteria expressing double-stranded RNA that interferes with olfaction. Insect 14, 140.CrossRefGoogle ScholarPubMed
Jomori, T, Kubo, T and Natori, S (1990) Purification and characterization of lipopolysaccharide-binding protein from hemolymph of American cockroach Periplaneta americana. European Journal of Biochemistry 190, 201206.CrossRefGoogle ScholarPubMed
Kaksonen, M and Roux, A (2018) Mechanisms of clathrin-mediated endocytosis. Nature Reviews Molecular Cell Biology 19, 313326.CrossRefGoogle ScholarPubMed
Kim, J and Kim, Y (2010) A viral histone H4 suppresses expression of a transferrin that plays a role in the immune response of the diamondback moth, Plutella xylostella. Insect Molecular Biology 19, 567574.CrossRefGoogle Scholar
Kim, CH and Muturi, EJ (2013) Effect of larval density and Sindbis virus infection on immune responses in Aedes aegypti. Journal of Insect Physiology 59, 604610.CrossRefGoogle ScholarPubMed
Kimura, K, Kodama, A, Hayasaka, Y and Ohta, T (2004) Activation of the cAMP/PKA signaling pathway is required for post-ecdysial cell death in wing epidermal cells of Drosophila melanogaster. 131, 15971606.Google Scholar
Koizumi, N, Morozumi, A, Imamura, M, Tanaka, E, Iwahana, H and Sato, R (1997) Lipopolysaccharide-binding proteins and their involvement in the bacterial clearance from the hemolymph of the silkworm Bombyx mori. European Journal of Biochemistry 248, 217224.CrossRefGoogle ScholarPubMed
Koizumi, N, Imai, Y, Morozumi, A, Imamura, M, Kadotani, T, Yaoi, K, Iwahana, H and Sato, R (1999) Lipopolysaccharide-binding protein of Bombyx mori participates in a hemocyte-mediated defense reaction against Gram-negative bacteria. Journal of Insect Physiology 45, 853859.CrossRefGoogle Scholar
Kojour, MAM, Han, YS and Jo, YH (2020) An overview of insect innate immunity. Entomological Research 50, 282291.CrossRefGoogle Scholar
Kressler, D, Hurt, E and Baβler, J (2010) Driving ribosome assembly. Biochimica et Biophysica Acta (BBA)-Molecular Cell Research 1803, 673683.CrossRefGoogle ScholarPubMed
Kumar, H, Kawai, T and Akira, S (2011) Pathogen recognition by the innate immune system. International Reviews of Immunology 30, 1634.CrossRefGoogle ScholarPubMed
Kwak, KW, Han, MS, Nam, SH, Choi, JY, Lee, SH, Choi, YC and Park, KH (2014) Detection of insect pathogen Serratia marcescens in Protaetia brevitarsis seulensis (Kolbe) from Korea. International Journal of Industrial Entomology 28, 2531.CrossRefGoogle Scholar
Langmead, B (2010) Aligning short sequencing reads with bowtie. Current Protocols in Bioinformatics 32, 1117.CrossRefGoogle Scholar
Lanz, H, Tsutsumi, V and Aréchiga, H (1993) Morphological and biochemical characterization of Procambarus clarki blood cells. Developmental and Comparative Immunology 17, 389397.CrossRefGoogle ScholarPubMed
Lemaitre, B and Hoffmann, J (2007) The host defense of Drosophila melanogaster. Annual Review of Immunology 25, 697743.CrossRefGoogle ScholarPubMed
Li, B and Dewey, CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12, 116.CrossRefGoogle ScholarPubMed
Li, WZ and Godzik, A (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics (Oxford, England) 22, 16581659.Google ScholarPubMed
Li, P, Yin, YL, Li, DF and Kim, SW (2007) Amino acids and immune function. British Journal of Nutrition 98, 237252.CrossRefGoogle ScholarPubMed
Li, ZQ, Yu, H and Huang, GH (2018) Changes in lipid, protein and carbohydrate metabolism in Spodoptera exigua larvae associated with infection by Heliothis virescens ascovirus 3h. Journal of Invertebrate Pathology 155, 5563.CrossRefGoogle ScholarPubMed
Li, Z, Yang, HJ, Zhang, L, Zhang, CY, Hu, YS and Fan, D (2021) Cloning and biological functional analysis of juvenile hormone epoxide hydrolase gene MsJHEH2 from Mythimna separata. Chinese Journal of Biological Control 37, 970981.Google Scholar
Li, RS, Xiao, Y, Li, K and Tian, L (2022) Transcription and post-translational regulation of autophagy in insects. Frontiers in Physiology 13, 825202.CrossRefGoogle ScholarPubMed
Lin, Y (2015) The research development of termite prevention and elimination in China. Chinese Journal of Hygienic Insecticides and Equipments 21, 537544.Google Scholar
Liu, YZ (2003) Study on Reticulitermes chinensis in China. Chinese Journal of Hygienic Insecticide and Equipment 9, 812.Google Scholar
Liu, YH, Wang, L and Yu, L (2015) The principle and application of the single-molecule real-time sequencing technology. Hereditas 37, 259268.Google ScholarPubMed
Liu, Y, Xin, ZZ, Zhu, XY, Wang, Y, Zhang, DZ, Jiang, SH, Zhang, HB, Zhou, CL, Liu, QN and Tang, BP (2018) Transcriptomic analysis of immune-related genes in the lipopolysaccharide-stimulated hepatopancreas of the mudflat crab Helice tientsinensis. Fish and Shellfish Immunology 83, 272282.CrossRefGoogle ScholarPubMed
Love, MI, Huber, W and Anders, S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology 15, 121.CrossRefGoogle ScholarPubMed
Lu, MM, Tian, XW, Yang, XC, Yuan, C, Ehsan, M, Liu, XC, Yan, RF, Xu, LX, Song, XK and Li, XR (2017) The N- and C-terminal carbohydrate recognition domains of Haemonchus contortus galectin bind to distinct receptors of goat PBMC and contribute differently to its immunomodulatory functions in host–parasite interactions. Parasites and Vectors 10, 111.CrossRefGoogle Scholar
Lucas, C and Ben-Shahar, Y (2021) The foraging gene as a modulator of division of labour in social insects. Journal of Neurogenetics 35, 168178.CrossRefGoogle ScholarPubMed
Luo, J, Wang, ZQ, Tang, F and Feng, K (2022) Immune defense mechanism of Reticulitermes chinensis Snyder (Blattodea: Isoptera) against Serratia marcescens Bizio. Insects 13, 226.CrossRefGoogle ScholarPubMed
Ma, JY, Zhang, MC, Ruan, LW, Shi, H and Xu, X (2010) Characterization of two novel ADP ribosylation factors from the shrimp Marsupenaeus japonicus. Fish and Shellfish Immunology 29, 956962.CrossRefGoogle ScholarPubMed
Malhotra, JD and Kaufman, RJ (2007) The endoplasmic reticulum and the unfolded protein response. Seminars in Cell and Developmental Biology 18, 716731.CrossRefGoogle ScholarPubMed
Matsumoto, Y, Hatano, A, Unoki, S and Mizunami, M (2009) Stimulation of the cAMP system by the nitric oxide–cGMP system underlying the formation of long-term memory in an insect. Neuroscience Letters 467, 8185.CrossRefGoogle ScholarPubMed
Mayeur, GL (2001) Examination of the Structure, Function and Regulation of Eukaryotic Translation Initiation Factor 3 (eIF3). Davis: University of California.Google Scholar
McGuire, C, Stransky, L, Cotter, K and Forgac, M (2017) Regulation of V-ATPase activity. Frontiers in Bioscience Landmark 22, 609622.Google ScholarPubMed
Mohan, M, Selvakumar, G, Sushil, SN, Bhatt, JC and Gupta, HS (2011) Entomopathogenicity of endophytic Serratia marcescens strain SRM against larvae of Helicoverpa armigera (Noctuidae: Lepidoptera). World Journal of Microbiology and Biotechnology 27, 25452551.CrossRefGoogle Scholar
Peisker, K, Braun, D, Wölfle, T, Hentschel, J, Fünfschilling, U, Fischer, G, Sickmann, A and Rospert, S (2008) Ribosome-associated complex binds to ribosomes in close proximity of Rpl31 at the exit of the polypeptide tunnel in yeast. Molecular Biology of the Cell 19, 52795288.CrossRefGoogle ScholarPubMed
Praparatana, R, Maskaew, S, Thongsoi, R, Runsaeng, P and Utarabhand, P (2022) Galectin, another lectin from Fenneropenaeus merguiensis, contributed in shrimp immune defense. Journal of Invertebrate Pathology 190, 107738.CrossRefGoogle ScholarPubMed
Rust, MK and Su, NY (2012) Managing social insects of urban importance. Annual Review of Entomology 57, 355375.CrossRefGoogle ScholarPubMed
Saftig, P and Klumperman, J (2009) Lysosome biogenesis and lysosomal membrane proteins: trafficking meets function. Nature Reviews Molecular Cell Biology 10, 623635.CrossRefGoogle ScholarPubMed
Sajjadian, SM and Kim, Y (2020) PGE2 upregulates gene expression of dual oxidase in a lepidopteran insect midgut via cAMP signalling pathway. Open Biology 10, 200197.CrossRefGoogle Scholar
Sanders, SL, Garbett, KA and Weil, PA (2002) Molecular characterization of Saccharomyces cerevisiae TFIID. Molecular and Cellular Biology 22, 60006013.CrossRefGoogle ScholarPubMed
Sezen, K, Yaman, M and Demirbag, Z (2001) Insecticidal potential of Serratia marcescenes Bn10. Biologia 56, 333336.Google Scholar
Shi X, Z, Wang, L, Xu, S, Zhang, XW, Zhao, XF, Vasta, GR and Wang, JX (2014) A galectin from the kuruma shrimp (Marsupenaeus japonicus) functions as an opsonin and promotes bacterial clearance from hemolymph. PLoS ONE 9, e91794.CrossRefGoogle ScholarPubMed
Someya, N, Nakajima, M, Hirayae, K, Hibi, T and Akutsu, K (2001) Synergistic antifungal activity of chitinolytic enzymes and prodigiosin produced by biocontrol bacterium, Serratia marcescens strain B2 against gray mold pathogen, Botrytis cinerea. Journal of General Plant Pathology 67, 312317.CrossRefGoogle Scholar
Stokes, BA, Yadav, S, Shokal, U, Smith, LC and Eleftherianos, I (2015) Bacterial and fungal pattern recognition receptors in homologous innate signaling pathways of insects and mammals. Frontiers in Microbiology 6, 19.CrossRefGoogle ScholarPubMed
Tan, SD (2022) Effects of Fungal Infection on the Allo-Grooming Behavior of Social Immunity in Reticulitermes chinensis. Wuhan: Hubei University.Google Scholar
Tang, T, Li, X, Yang, X, Yu, X, Wang, JH, Liu, FS and Huang, DW (2014) Transcriptional response of Musca domestica larvae to bacterial infection. PLoS One 9, e104867.CrossRefGoogle ScholarPubMed
Tao, AL, Wang, T, Pang, FH, Zheng, XL, Ayra-Pardo, C, Huang, SL, Xu, RX, Liu, FQ, Li, JK, Wei, YB, Wang, ZQ, Niu, QH and Li, DD (2022) Characterization of a novel chitinolytic Serratia marcescens strain TC-1 with broad insecticidal spectrum. AMB Express 12, 113.CrossRefGoogle ScholarPubMed
Teets, NM, Yi, SX, Lee, RE Jr and Denlinger, DL (2013) Calcium signaling mediates cold sensing in insect tissues. Proceedings of the National Academy of Sciences of the United States of America 110, 91549159.CrossRefGoogle ScholarPubMed
Thomson, E, Ferreira-Cerca, S and Hurt, E (2013) Eukaryotic ribosome biogenesis at a glance. Journal of Cell Science 126, 48154821.CrossRefGoogle ScholarPubMed
Tusun, A, Li, M, Liang, XZ, Yang, T, Yang, B and Wang, GR (2017) Juvenile hormone epoxide hydrolase: a promising target for hemipteran pest management. Scientific Reports 7, 789.CrossRefGoogle ScholarPubMed
Valles, SM and Pereira, RM (2005) Solenopsis invicta transferrin: cDNA cloning, gene architecture, and up-regulation in response to Beauveria bassiana infection. Gene 358, 6066.CrossRefGoogle ScholarPubMed
Venkatesh, K, Siddhartha, G, Joshi, R, Patel, S and Hasan, G (2001) Interactions between the inositol 1,4,5-trisphosphate and cyclic AMP signaling pathways regulate larval molting in Drosophila. Genetics 158, 309318.CrossRefGoogle ScholarPubMed
Verma, M, Sharma, S and Prasad, R (2009) Biological alternatives for termite control: a review. International Biodeterioration and Biodegradation 63, 959972.CrossRefGoogle Scholar
Wagner, CA, Finberg, KE, Breton, S, Marshansky, V, Brown, D and Geibel, JP (2004) Renal vacuolar H+-ATPase. Physiological Reviews 84, 12631314.CrossRefGoogle ScholarPubMed
Wang, W (2014) Group Resistance and Its Mechanism of Reticulitermes chinensis Infected by Metarhizium anisopliae. Wuhan: Huazhong Agricultural University.Google Scholar
Wang, P, Wang, W and , ZQ (2014) Expression, purification and characterization of a galectin in the silkworm (Bombyx mori). Acta Entomologica Sinica 57, 806814.Google Scholar
Weernink, PAO, de Jesús, ML and Schmidt, M (2007) Phospholipase D signaling: orchestration by PIP2 and small GTPases. Naunyn-Schmiedeberg's Archives of Pharmacology 374, 399411.CrossRefGoogle Scholar
Wen, DH, Wang, XL, Shang, L, Huang, Y, Li, TN, Wu, CF, Zhang, R and Zhang, JH (2016) Involvement of a versatile pattern recognition receptor, apolipophorin-III in prophenoloxidase activation and antibacterial defense of the Chinese oak silkworm, Antheraea pernyi. Developmental and Comparative Immunology 65, 124131.CrossRefGoogle ScholarPubMed
Wu, WM, Lin, S, Zhao, Z, Su, Y, Li, RL, Zhang, ZD and Guo, XJ (2021) Bombyx mori apolipophorin-III inhibits Beauveria bassiana directly and through regulating expression of genes relevant to immune signaling pathways. Journal of Invertebrate Pathology 184, 107647.CrossRefGoogle ScholarPubMed
Xing, LS, Yuan, CF, Wang, ML, Lin, Z, Shen, BC, Hu, ZH and Zou, Z (2017) Dynamics of the interaction between cotton bollworm Helicoverpa armigera and nucleopolyhedrovirus as revealed by integrated transcriptomic and proteomic analyses. Molecular and Cellular Proteomics 16, 10091028.CrossRefGoogle ScholarPubMed
Xu, HH, Hao, ZP, Wang, LF, Li, SJ, Guo, YR and Dang, XL (2020) Suppression of transferrin expression enhances the susceptibility of Plutella xylostella to Isaria cicadae. Insects 11, 281.CrossRefGoogle ScholarPubMed
Xue, HT, Liu, L, Zhao, ZH, Zhang, ZY, Guan, Y, Cheng, HR, Zhou, YF and Tai, GH (2017) The N-terminal tail coordinates with carbohydrate recognition domain to mediate galectin-3 induced apoptosis in T cells. Oncotarget 8, 49824.CrossRefGoogle ScholarPubMed
Yang, X, Deng, S, Wei, XG, Yang, J, Zhao, QN, Yin, C, Du, TH, Guo, ZJ, Xia, JX, Yang, ZZ, Xie, W, Wang, SL, Wu, QJ, Yang, FS, Zhou, XG, Nauen, R, Bass, C and Zhang, YJ (2020) MAPK-directed activation of the whitefly transcription factor CREB leads to P450-mediated imidacloprid resistance. Proceedings of the National Academy of Sciences of the United States of America 117, 1024610253.CrossRefGoogle ScholarPubMed
Yang, YP, Ma, FJ, Dong, JJ, Li, LX, Ren, P, Zhang, YN, Wu, YT, Wang, YP, Liu, K and Zhang, F (2021) The innate immune response to infection by Polyascus gregaria in the male Chinese mitten crab (Eriocheir sinensis), revealed by proteomic analysis. Fishes 6, 57.CrossRefGoogle Scholar
Yoshiga, T, Georgieva, T, Dunkov, BC, Harizanova, N, Ralchev, K and Law, JH (1999) Drosophila melanogaster transferrin: cloning, deduced protein sequence, expression during the life cycle, gene localization and up-regulation on bacterial infection. European Journal of Biochemistry 260, 414420.CrossRefGoogle ScholarPubMed
Yue, JJ, Ma, YC, Liu, Q, Jiang, LL, Fei, DL, Zhang, H, Sun, L, Li, M and Ma, MX (2018) Expression, purification and characterization of galectin AcGalectin in Apis cerana cerana (Hymenoptera: Apidae). Acta Entomologica Sinica 61, 546554.Google Scholar
Yun, EY, Lee, JK, Kwon, OY, Hwang, JS, Kim, I, Kang, SW, Lee, WJ, Ding, JL, You, KH and Goo, TW (2009) Bombyx mori transferrin: genomic structure, expression and antimicrobial activity of recombinant protein. Developmental and Comparative Immunology 33, 10641069.CrossRefGoogle ScholarPubMed
Zänker, KS (2010) Immunology of Invertebrates: Humoral. Encyclopedia of Life Sciences. Chichester: John Wiley and Sons, Ltd.Google Scholar
Zhang, XW, Ji, BZ, Liu, SW, Cao, DD, Yang, JJ, Liu, JJ, Ji, SL, Soleymaninejadian, E and Wang, HJ (2015) Research progress in anatomic structures of digestive system and symbiotes in termites. Journal of Nanjing Forestry University (Natural Sciences Edition) 39, 155161.Google Scholar
Zhang, QL, Zhang, L, Yang, XZ, Wang, XT, Li, XP, Wang, J, Chen, JY and Yuan, ML (2017) Comparative transcriptomic analysis of Tibetan Gynaephora to explore the genetic basis of insect adaptation to divergent altitude environments. Scientific Reports 7, 16972.CrossRefGoogle ScholarPubMed
Zhang, W, Tettamanti, G, Bassal, T, Heryanto, C, Eleftherianos, I and Mohamed, A (2021) Regulators and signalling in insect antimicrobial innate immunity: functional molecules and cellular pathways. Cellular Signalling 83, 110003.CrossRefGoogle ScholarPubMed
Zhao, J, Luo, X, Chen, DH, Wang, JD and Yang, ZR (2004) Study on the locusts energy metabolizability inhibited by the insecticidal protein purified from Pseudomonas pseudoalcaligenes. Acta Microbiologia Sinica 44, 365368.Google Scholar
Zhao, JH, Benlekbir, S and Rubinstein, JL (2015) Electron cryomicroscopy observation of rotational states in a eukaryotic V-ATPase. Nature 521, 241245.CrossRefGoogle Scholar
Zhao, JY, Zhao, XT, Sun, JT, Zou, LF, Yang, SX, Han, X, Zhu, WC, Yin, Q and Hong, XY (2017) Transcriptome and proteome analyses reveal complex mechanisms of reproductive diapause in the two-spotted spider mite, Tetranychus urticae. Insect Molecular Biology 26, 215232.CrossRefGoogle ScholarPubMed
Supplementary material: File

Zhang and Tang supplementary material 1

Zhang and Tang supplementary material
Download Zhang and Tang supplementary material 1(File)
File 28.7 KB
Supplementary material: File

Zhang and Tang supplementary material 2

Zhang and Tang supplementary material
Download Zhang and Tang supplementary material 2(File)
File 33.9 KB