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| Transcriptome analysis of hsp18.3 functions and regulatory systems using RNA-sequencing in the red flour beetle, Tribolium castaneum |
| XIONG Wen-feng*, XIE Jia*, WEI Lu-ting, ZHANG Si-si, SONG Xiao-wen, GAO Shan-shan, LI Bin |
| Jiangsu Key Laboratory for Biodiversity and Biotechnology, College of Life Sciences, Nanjing Normal University, Nanjing 210023, P.R.China |
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Abstract The red flour beetle, Tribolium castaneum, is a major agriculture pest of stored grain, cereal products and peanuts for human consumption. It is reported that heat shock protein 18.3 of T. castaneum (Tchsp18.3) plays a significant role in stress resistance, development and reproduction. However, the regulatory systems of Tchsp18.3 remain unknown. Therefore, we compared the global transcriptome profiles of RNA interference (RNAi)-treated larvae (ds-Tchsp18.3) and control larvae of T. castaneum using RNA sequencing. Overall, we obtained 14 154 435 sequence reads aligned with 13 299 genes. Additionally, 569 differentially expressed genes (DEGs) were identified from the ds-Tchsp18.3 and control groups, of which 246 DEGs were annotated in the 47 Gene Ontology (GO) functional groups and 282 DEGs were assigned to 147 Kyoto Encyclopedia of Genes and Genomes (KEGG) biological signaling pathways. The DEGs encoding viperin, dorsal, Hdd11, PGRP2, defensin1 and defensin2 were simultaneously related to immunity and stress responses, which suggests that cross-talk might exist between the immunity and stress responses of T. castaneum. The knockdown of Tchsp18.3gene expression suppressed the antioxidant activity process, which most likely modulated the effects of Tchsp18.3 on development and reproduction. Furthermore, the DEGs, including Blimp-1, Gld, Drm, Kinesin-14, Pthr2, Delta(11)-like and EGF-like domain protein 2, were also associated with the development and reproduction of ds-Tchsp18.3 insects. Additionally, knockdown of Tchsp18.3 amplified the serine protease (SP) signaling pathway to further regulate stress responses and innate immunity as well as development and reproduction of the red flour beetles. These results provide valuable insight into the molecular regulatory mechanism of Tchsp18.3 involved in insect physiology and further facilitate the research of suitable and sustainable management for pest control.
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Received: 06 August 2017
Accepted:
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| Fund: This work was supported by the National Natural Science Foundation of China (31572326 and 31172146) and the Priority Academic Program Development (PAPD) of Jiangsu Higher Education Institutions, China. |
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Corresponding Authors:
Correspondence LI Bin, E-mail: libin@njnu.edu.cn, libinlb@hotmail.com
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| About author: XIONG Wen-feng, E-mail: 13182919223@163.com; XIE Jia, E-mail: xiejia666666@163.com; * These authors contributed equally to this work |
Cite this article:
XIONG Wen-feng, XIE Jia, WEI Lu-ting, ZHANG Si-si, SONG Xiao-wen, GAO Shan-shan, LI Bin.
2018.
Transcriptome analysis of hsp18.3 functions and regulatory systems using RNA-sequencing in the red flour beetle, Tribolium castaneum. Journal of Integrative Agriculture, 17(05): 1040-1056.
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| Aevermann B D, Waters E R. 2008. A comparative genomic analysis of the small heat shock proteins in Caenorhabditis elegans and briggsae. Genetica, 133, 307–319.Agawa Y, Sarhan M, Kageyama Y, Akagi K, Takai M, Hashiyama K, Wada T, Handa H, Iwamatsu A, Hirose S, Ueda H. 2007. Drosophila Blimp-1 is a transient transcriptional repressor that controls timing of the ecdysone-induced developmental pathway. Molecular and Cellular Biology, 27, 8739–8747.Ahn H M, Lee K S, Lee D S, Yu K. 2012. JNK/FOXO mediated PeroxiredoxinV expression regulates redox homeostasis during Drosophila melanogaster gut infection. Developmental and Comparative Immunology, 38, 466–473.Altincicek B, Knorr E, Vilcinskas A. 2008. Beetle immunity: Identification of immune-inducible genes from the model insect Tribolium castaneum. Developmental and Comparative Immunology, 32, 585–595.Arrigo A P. 2000. sHsp as novel regulators of programmed cell death and tumorigenicity. Pathologie Biologie (Paris), 48, 280–288.Azad P, Zhou D, Russo E, Haddad G G. 2009. Distinct mechanisms underlying tolerance to intermittent and constant hypoxia in Drosophila melanogaster. PLoS ONE, 4, e5371.Bahia A C, Oliveira J H, Kubota M S, Araujo H R, Lima J B, Rios-Velasquez C M, Lacerda M V, Oliveira P L, Traub-Cseko Y M, Pimenta P F. 2013. The role of reactive oxygen species in Anopheles aquasalis response to Plasmodium vivax infection. PLoS ONE, 8, e57014.Bakthisaran R, Tangirala R, Rao C M. 2015. Small heat shock proteins: Role in cellular functions and pathology. Biochimica Biophysica Acta, 1854, 291–319.Bao Y, Mega K, Yamano Y, Morishima I. 2003. cDNA cloning and expression of bacteria-induced Hdd11 gene from eri-silkworm, Samia cynthia ricini. Comparative Biochemistry Physiology (Part C: Toxicology Pharmacolgy), 136, 337–342.Cavener D R, MacIntyre R J. 1983. Biphasic expression and function of glucose dehydrogenase in Drosophila melanogaster. Proceedings of the National Academy of Sciences of the United States of America, 80, 6286–6288.Cavener D R, Otteson D C, Kaufman T C. 1986. A rehabilitation of the genetic map of the 84B-D region in Drosophila melanogaster. Genetics, 114, 111–123.Chen X, Xiong W, Li C, Gao S, Song X, Wu W, Li B. 2016. Comparative RNA-sequencing profiling reveals novel Delta-class glutathione S-transferases relative genes expression patterns in Tribolium castaneum. Gene, 593, 13–20.Chen X, Zhang Y. 2015. Identification of multiple small heat-shock protein genes in Plutella xylostella (L.) and their expression profiles in response to abiotic stresses. Cell Stress Chaperones, 20, 23–35.Conesa A, Gotz S, Garcia-Gomez J M, Terol J, Talon M, Robles M. 2005. Blast2GO: A universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics, 21, 3674–3676.Contreras E, Benito-Jardon M, Lopez-Galiano M J, Real M D, Rausell C. 2015. Tribolium castaneum immune defense genes are differentially expressed in response to Bacillus thuringiensis toxins sharing common receptor molecules and exhibiting disparate toxicity. Developmental and Comparative Immunology, 50, 139–145.Contreras E, Rausell C, Real M D. 2013. Proteome response of Tribolium castaneum larvae to Bacillus thuringiensis toxin producing strains. PLoS ONE, 8, e55330.Csermely P, Schnaider T, Soti C, Prohaszka Z, Nardai G. 1998. The 90-kDa molecular chaperone family: structure, function, and clinical applications. A comprehensive review. Pharmacology Therapeutics, 79, 129–168.Davies S A, Overend G, Sebastian S, Cundall M, Cabrero P, Dow J A, Terhzaz S. 2012. Immune and stress response ‘cross-talk’ in the Drosophila Malpighian tubule. Journal of Insect Physiology, 58, 488–497.Deng F, He Q, Zhao Z. 2016. Suppressing a peroxidase gene reduces survival in the wheat aphid Sitobion avenae. Archives of Insect Biochemistry Physiology, 93, 86–95.Deng F, Zhao Z. 2014. Influence of catalase gene silencing on the survivability of Sitobion avenae. Archives of Insect Biochemistry Physiology, 86, 46–57.Diaz-Albiter H, Mitford R, Genta F A, Sant’Anna M R, Dillon R J. 2011. Reactive oxygen species scavenging by catalase is important for female Lutzomyia longipalpis fecundity and mortality. PLoS ONE, 6, e17486.Donitz J, Schmitt-Engel C, Grossmann D, Gerischer L, Tech M, Schoppmeier M, Klingler M, Bucher G. 2015. iBeetle-Base: A database for RNAi phenotypes in the red flour beetle Tribolium castaneum. Nucleic Acids Research, 43, D720–D725.Erler S, Popp M, Lattorff H M. 2011. Dynamics of immune system gene expression upon bacterial challenge and wounding in a social insect (Bombus terrestris). PLoS ONE, 6, e18126.Fu X, Jiao W, Chang Z. 2006. Phylogenetic and biochemical studies reveal a potential evolutionary origin of small heat shock proteins of animals from bacterial class A. Journal of Molecular Evolution, 62, 257–266.Gao Y, Tang T, Gu J, Sun L, Gao X, Ma X, Wang X, Liu F, Wang J. 2015. Downregulation of the Musca domestica peptidoglycan recognition protein SC (PGRP-SC) leads to overexpression of antimicrobial peptides and tardy pupation. Molecular Immunology, 67, 465–474.Garcia-Reina A, Rodriguez-Garcia M J, Ramis G, Galian J. 2017. Real-time cell analysis and heat shock protein gene expression in the TcA Tribolium castaneum cell line in response to environmental stress conditions. Insect Science, 24, 358–370.Gorman M J, Andreeva O V, Paskewitz S M. 2000. Sp22D: A multidomain serine protease with a putative role in insect immunity. Gene, 251, 9–17.Gotenstein J R, Swale R E, Fukuda T, Wu Z, Giurumescu C A, Goncharov A, Jin Y, Chisholm A D. 2010. The C. elegans peroxidasin PXN-2 is essential for embryonic morphogenesis and inhibits adult axon regeneration. Development, 137, 3603–3613.Hao X, Zhang S, Timakov B, Zhang P. 2007. The Hsp27 gene is not required for Drosophila development but its activity is associated with starvation resistance. Cell Stress Chaperones, 12, 364–372.Haslbeck M, Franzmann T, Weinfurtner D, Buchner J. 2005. Some like it hot: The structure and function of small heat-shock proteins. Nature Structural Molecular Biology, 12, 842–846.Hee J S, Cresswell P. 2017. Viperin interaction with mitochondrial antiviral signaling protein (MAVS) limits viperin-mediated inhibition of the interferon response in macrophages. PLoS ONE, 12, e0172236.Iida K, Cavener D R. 2004. Glucose dehydrogenase is required for normal sperm storage and utilization in female Drosophila melanogaster. Journal of Experimental Biology, 207, 675–681.Iwaki D D, Johansen K A, Singer J B, Lengyel J A. 2001. Drumstick, bowl, and lines are required for patterning and cell rearrangement in the Drosophila embryonic hindgut. Developmental Biology, 240, 611–626.Kawasaki F, Koonce N L, Guo L, Fatima S, Qiu C, Moon M T, Zheng Y, Ordway R W. 2016. Small heat shock proteins mediate cell-autonomous and -nonautonomous protection in a Drosophila model for environmental-stress-induced degeneration. Disease Models & Mechanisms, 9, 953–964.Kegel K B, Iwaki A, Iwaki T, Goldman J E. 1996. AlphaB-crystallin protects glial cells from hypertonic stress. American Journal of Physiologly, 270, C903-C909.Kim H, Kim J, Lee Y, Yang J, Han K. 2006. Transcriptional regulation of the methuselah gene by dorsal protein in Drosophila melanogaster. Molecules and Cells, 21, 261–268.Kim K K, Kim R, Kim S H. 1998. Crystal structure of a small heat-shock protein. Nature, 394, 595–599.Kim S H, Lee W J. 2014. Role of DUOX in gut inflammation: Lessons from Drosophila model of gut-microbiota interactions. Frontiers in Cellular and Infection Microbiology, 3, 116.Lee G J, Pokala N, Vierling E. 1995. Structure and in vitro molecular chaperone activity of cytosolic small heat shock proteins from pea. Journal of Biological Chemistry, 270, 10432–10438.Lei M, Liu H, Liu S, Zhang Y, Zhang S. 2015. Identification and functional characterization of viperin of amphioxus Branchiostoma japonicum: Implications for ancient origin of viperin-mediated antiviral response. Developmental and Comparative Immunology, 53, 293–302.Lemaitre B, Meister M, Govind S, Georgel P, Steward R, Reichhart J M, Hoffmann J A. 1995. Functional analysis and regulation of nuclear import of dorsal during the immune response in Drosophila. The EMBO Journal, 14, 536–545.Li C, Wu W, Sang M, Liu X, Hu X, Yun X, Li B. 2014. Comparative RNA-sequencing analysis of mthl1 functions and signal transductions in Tribolium castaneum. Gene, 547, 310–318.Li C J, Yun X P, Yu X J, Li B. 2017. Functional analysis of the circadian clock gene timeless in Tribolium castaneum. Insect Science, doi: 10.1111/1744-7917.12441Li R, Yu C, Li Y, Lam T W, Yiu S M, Kristiansen K, Wang J. 2009. SOAP2: An improved ultrafast tool for short read alignment. Bioinformatics, 25, 1966–1967.Li Z W, Li X, Yu Q Y, Xiang Z H, Kishino H, Zhang Z. 2009. The small heat shock protein (sHSP) genes in the silkworm, Bombyx mori, and comparative analysis with other insect sHSP genes. BMC Evolution Biology, 9, 215.Liang D, Benko Z, Agbottah E, Bukrinsky M, Zhao R Y. 2007. Anti-Vpr activities of heat shock protein 27. Molecular Medicine, 13, 229–239.Lindquist S, Craig E A. 1988. The heat-shock proteins. Annual Review of Genetics, 22, 631–677.Liu B, Jiang G, Zhang Y, Li J, Li X, Yue J, Chen F, Liu H, Li H, Zhu S, Wang J, Ran C. 2011. Analysis of transcriptome differences between resistant and susceptible strains of the citrus red mite Panonychus citri (Acari: Tetranychidae). PLoS ONE, 6, e28516.Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-??CT method. Methods, 25, 402–408.Marioni J C, Mason C E, Mane S M, Stephens M, Gilad Y. 2008. RNA-seq: An assessment of technical reproducibility and comparison with gene expression arrays. Genome Research, 18, 1509–1517.Martinez-Paz P, Morales M, Martin R, Martinez-Guitarte J L, Morcillo G. 2014. Characterization of the small heat shock protein Hsp27 gene in Chironomus riparius (Diptera) and its expression profile in response to temperature changes and xenobiotic exposures. Cell Stress Chaperones, 19, 529–540.Michaud S, Marin R, Westwood J T, Tanguay R M. 1997. Cell-specific expression and heat-shock induction of Hsps during spermatogenesis in Drosophila melanogaster. Journal of Cell Science, 110, 1989–1997.Van Montfort R, Slingsby C, Vierling E. 2001. Structure and function of the small heat shock protein/alpha-crystallin family of molecular chaperones. Advances in Protein Chemistry, 59, 105–156.van Montfort R L M, Basha E, Friedrich K L, Slingsby C, Vierling E. 2001. Crystal structure and assembly of a eukaryotic small heat shock protein. Nature Structural Biology, 8, 1025–1030.Morrow G, Battistini S, Zhang P, Tanguay R M. 2004. Decreased lifespan in the absence of expression of the mitochondrial small heat shock protein Hsp22 in Drosophila. Journal of Biological Chemistry, 279, 43382–43385.Mortazavi A, Williams B A, McCue K, Schaeffer L, Wold B. 2008. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nature Methods, 5, 621–628.Muturi E J, Kim C H, Alto B W, Berenbaum M R, Schuler M A. 2011. Larval environmental stress alters Aedes aegypti competence for Sindbis virus. Tropical Medicine & International Health, 16, 955–964.Muturi E J, Nyakeriga A, Blackshear M. 2012. Temperature-mediated differential expression of immune and stress-related genes in Aedes aegypti larvae. Journal of the American Mosquito Control Association, 28, 79–83.Nakamoto H, Vigh L. 2007. The small heat shock proteins and their clients. Cellular and Molecular Life Sciences, 64, 294–306.Oppert B, Elpidina E N, Toutges M, Mazumdar-Leighton S. 2010. Microarray analysis reveals strategies of Tribolium castaneum larvae to compensate for cysteine and serine protease inhibitors. Comparative Biochemistry Physiology (Part D: Genomics Proteomics), 5, 280–287.Pandey A, Saini S, Khatoon R, Sharma D, Narayan G, Kar Chowdhuri D. 2016. Overexpression of hsp27 rescued neuronal cell death and reduction in life- and health-span in Drosophila melanogaster against prolonged exposure to dichlorvos. Molecular Neurobiology, 53, 3179–3193.Perkin L C, Elpidina E N, Oppert B. 2017. RNA interference and dietary inhibitors induce a similar compensation response in Tribolium castaneum larvae. Insect Molecular Biology, 26, 35–45.Ponnuvel K M, Murthy G N, Awasthi A K, Rao G, Vijayaprakash N B. 2010. Differential gene expression during early embryonic development in diapause and non-diapause eggs of multivoltine silkworm Bombyx mori. Indian Journal of Experimintal Biology, 48, 1143–1151.Van Raamsdonk J M, Hekimi S. 2009. Deletion of the mitochondrial superoxide dismutase sod-2 extends lifespan in Caenorhabditis elegans. PLoS Genetics, 5, e1000361.Reichhart J M, Georgel P, Meister M, Lemaitre B, Kappler C, Hoffmann J A. 1993. Expression and nuclear translocation of the rel/NF-kappa B-related morphogen dorsal during the immune response of Drosophila. Comptes Rendus Academie Sciences III, 316, 1218–1224.Ritossa F M, Vonborstel R C. 1964. Chromosome puffs in Drosophila induced by ribonuclease. Science, 145, 513–514.Sang M, Li C, Wu W, Li B. 2016. Identification and evolution of two insulin receptor genes involved in Tribolium castaneum development and reproduction. Gene, 585, 196–204.Sang W, Ma W H, Qiu L, Zhu Z H, Lei C L. 2012. The involvement of heat shock protein and cytochrome P450 genes in response to UV-A exposure in the beetle Tribolium castaneum. Journal of Insect Physiology, 58, 830–836.Singh M K, Tiwari P K. 2016. Cloning & sequence identification of Hsp27 gene and expression analysis of the protein on thermal stress in Lucilia cuprina. Insect Science, 23, 555–568.Song X, Huang F, Liu J, Li C, Gao S, Wu W, Zhai M, Yu X, Xiong W, Xie J, Li B. 2017. Genome-wide DNA methylomes from discrete developmental stages reveal the predominance of non-CpG methylation in Tribolium castaneum. DNA Research, 24, 445–457.Storey J D, Tibshirani R. 2003. Statistical significance for genomewide studies. Proceedings of the National Academy of Sciences of the United States of America, 100, 9440–9445.Sultan A R, Oish Y, Ueda H. 2014. Function of the nuclear receptor FTZ-F1 during the pupal stage in Drosophila melanogaster. Development Growth & Differentiation, 56, 245–253.Sun C C, Dong W R, Zhao J, Nie L, Xiang L X, Zhu G, Shao J Z. 2015. Cysteine-independent catalase-like activity of vertebrate Peroxiredoxin 1 (Prx1). Journal of Biological Chemistry, 290, 19942–19954.Taracena M L, Oliveira P L, Almendares O, Umana C, Lowenberger C, Dotson E M, Paiva-Silva G O, Pennington P M. 2015. Genetically modifying the insect gut microbiota to control Chagas disease vectors through systemic RNAi. PLoS Neglected Tropical Diseases, 9, e0003358.Tomei E J, Wolniak S M. 2016. Transcriptome analysis reveals a diverse family of kinesins essential for spermatogenesis in the fern Marsilea. Cytoskeleton (Hoboken), 73, 145–159.Tsvetkova N M, Horvath I, Torok Z, Wolkers W F, Balogi Z, Shigapova N, Crowe L M, Tablin F, Vierling E, Crowe J H, Vigh L. 2002. Small heat-shock proteins regulate membrane lipid polymorphism. Proceedings of the National Academy of Sciences of the United States of America, 99, 13504–13509.Uddin S N, Yano M, Murakami R. 2011. The drumstick gene acts cell-non-autonomously and triggers specification of the small intestine in the Drosophila hindgut. International Journal of Developmental Biology, 55, 945–952.Wang D, Zhang Y, Dong Z, Guo P, Ma S, Guo K, Xia Q, Zhao P. 2016. Serine protease P-IIc is responsible for the digestion of yolk proteins at the late stage of silkworm embryogenesis. Insect Biochemistry Molecular Biology, 74, 42–49.Wang J, Wu Y, Yang G, Aksoy S. 2009. Interactions between mutualist Wigglesworthia and tsetse peptidoglycan recognition protein (PGRP-LB) influence trypanosome transmission. Proceedings of the National Academy of Sciences of the United States of America, 106, 12133–12138.Wang L, Feng Z, Wang X, Zhang X. 2010. DEGseq: An R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics, 26, 136–138.Wang Z, Gerstein M, Snyder M. 2009. RNA-Seq: A revolutionary tool for transcriptomics. Nature Reviews Genetics, 10, 57–63.Waters E R, Aevermann B D, Sanders-Reed Z. 2008. Comparative analysis of the small heat shock proteins in three angiosperm genomes identifies new subfamilies and reveals diverse evolutionary patterns. Cell Stress Chaperones, 13, 127–142.Waters E R, Rioflorido I. 2007. Evolutionary analysis of the small heat shock proteins in five complete algal genomes. Journal of Molecular Evolution, 65, 162–174.Xie J, Hu X X, Zhai M F, Yu X J, Song X W, Gao S S, Wu W, Li B. 2017. Characterization and functional analysis of hsp18.3 gene in the red flour beetle, Tribolium castaneum. Insect Science, doi: 10.1111/1744-7917.12543Xiong W, Zhai M, Yu X, Wei L, Mao J, Liu J, Xie J, Li B. 2017. Comparative RNA-sequencing analysis of ER-based HSP90 functions and signal pathways in Tribolium castaneum. Cell Stress Chaperones, 23, 29–43.Xu J, Tan A, Palli S R. 2010. The function of nuclear receptors in regulation of female reproduction and embryogenesis in the red flour beetle, Tribolium castaneum. Journal of Insect Physiology, 56, 1471–1480.Yang J, Dong S, Jiang Q, Si Q, Liu X. 2013. Characterization and expression of cytoplasmic copper/zinc superoxide dismutase (CuZnSOD) gene under temperature and hydrogen peroxide (H2O2) in rotifer Brachionus calyciflorus. Gene, 518, 388–396.Ye J, Fang L, Zheng H, Zhang Y, Chen J, Zhang Z, Wang J, Li S, Li R, Bolund L. 2006. WEGO: A web tool for plotting GO annotations. Nucleic Acids Research, 34, W293–W297.Zhang B, Zheng J, Peng Y, Liu X, Hoffmann A A, Ma C S. 2015. Stress responses of small heat shock protein genes in Lepidoptera point to limited conservation of function across phylogeny. PLoS ONE, 10, e0132700.Zhang C, Dai L, Wang L, Qian C, Wei G, Li J, Zhu B, Liu C. 2015. Inhibitors of eicosanoid biosynthesis influencing the transcripts level of sHSP21.4 gene induced by pathogen infections, in Antheraea pernyi. PLoS ONE, 10, e0121296.Zhang C, Zhu B, Dai L S, Liu C, Luo X. 2016. Nucleopolyhedroviruses (NPV) induce the expression of small heat shock protein 25.4 in Antheraea pernyi. Gene, 591, 327–332.Zhang L, Kang H, Jin S, Zeng Q T, Yang Y. 2016. Hsp27 gene in Drosophila ananassae subgroup was split by a recently acquired intron. Journal of Genetics, 95, 257–262.Zhang Y, Liu Y, Guo X, Li Y, Gao H, Xu B. 2014. sHsp22.6, an intronless small heat shock protein gene, is involved in stress defence and development in Apis cerana cerana. Insect Biochemistry and Molecular Biology, 53, 1–12.Zhao H, Yi X, Hu Z, Hu M, Chen S, Muhammad R U, Dong X, Gong L. 2013. RNAi-mediated knockdown of catalase causes cell cycle arrest in SL-1 cells and results in low survival rate of Spodoptera litura (Fabricius). PLoS ONE, 8, e59527.Zhu M, Zhang W, Liu F, Chen X, Li H, Xu B. 2016. Characterization of an Apis cerana cerana cytochrome P450 gene (AccCYP336A1) and its roles in oxidative stresses responses. Gene, 584, 120–128.Zou Z, Lopez D L, Kanost M R, Evans J D, Jiang H. 2006. Comparative analysis of serine protease-related genes in the honey bee genome: Possible involvement in embryonic development and innate immunity. Insect Molecular Biology, 15, 603–614. |
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