棉铃虫围食膜的蛋白质组鉴定
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摘要
【目的】围食膜(peritrophic membrane, PM)是昆虫抵御随食物摄入的病原微生物入侵的第一道天然屏障。本研究旨在鉴定出农业重大害虫棉铃虫Helicoverpa armigera围食膜的总蛋白成分,为进一步揭示昆虫围食膜的形成机制及研发新颖的害虫控制策略奠定基础。【方法】剥离棉铃虫5龄幼虫PM,用三氟甲磺酸(trifluoromethane-sulfonic acid, TFMS)处理,采用液质联用技术(LC-MS/MS)鉴定围食膜蛋白质组,然后对鉴定结果进行生物信息学分析。【结果】本研究共鉴定出棉铃虫幼虫围食膜蛋白质169个,是目前鉴定最多的棉铃虫围食膜蛋白。通过GO分析,可以将这些鉴定的蛋白分为细胞组分、分子功能和生物学过程三大类;KEGG富集结果显示,鉴定蛋白可以富集在12条代谢通路中;蛋白互作分析(protein-protein interaction, PPI)结果表明,以ACC和CG3011等蛋白为核心可以形成蛋白互作网络。【结论】本研究鉴定了169个棉铃虫幼虫围食膜蛋白质,并对其进行了GO, KEGG和PPI分析,结果有助于人们全面理解昆虫围食膜的分子结构和功能。
【Aim】 The peritrophic membrane(PM) is the first natural barrier against the invasion of microbes ingested with foods in insects. This study aims to identify the total protein constituents of the peritrophic membrane of the cotton bollworm, Helicoverpa armigera, a major agricultural insect, so as to lay a foundation for further revealing the formation mechanism of PM and developing novel pest control strategies. 【Methods】 The PMs of the 5 th instar larvae of H. armigera were peeled off and then treated with trifluoromethane-sulfonic acid(TFMS). The peritrophic membrane proteome of larvae was identified by liquid chromatography and mass spectrometry(LC-MS/MS), and the identified results were subjected to bioinformatics analysis.【Results】 In this study we identified a total of 169 peritrophic membrane proteins from H. armigera larvae, which is the highest number of PM proteins identified in H. armigera up to date. GO analysis revealed that these identified proteins could be divided into three major categories, i.e., cellular component(CC), molecular function(MF) and biological process(BP). The KEGG enrichment results showed that the identified proteins could be enriched in 12 metabolic pathways. The results of protein-protein interaction(PPI) analysis indicated that ACC and CG3011 proteins could serve as the core protein-protein interaction network. 【Conclusion】 In this study 169 peritrophic membrane proteins were identified from H. armigera larvae and subjected to GO, KEGG and PPI analyses. The results are helpful to comprehensively understand the molecular structure and function of PM in insects.
【Aim】 The peritrophic membrane(PM) is the first natural barrier against the invasion of microbes ingested with foods in insects. This study aims to identify the total protein constituents of the peritrophic membrane of the cotton bollworm, Helicoverpa armigera, a major agricultural insect, so as to lay a foundation for further revealing the formation mechanism of PM and developing novel pest control strategies. 【Methods】 The PMs of the 5 th instar larvae of H. armigera were peeled off and then treated with trifluoromethane-sulfonic acid(TFMS). The peritrophic membrane proteome of larvae was identified by liquid chromatography and mass spectrometry(LC-MS/MS), and the identified results were subjected to bioinformatics analysis.【Results】 In this study we identified a total of 169 peritrophic membrane proteins from H. armigera larvae, which is the highest number of PM proteins identified in H. armigera up to date. GO analysis revealed that these identified proteins could be divided into three major categories, i.e., cellular component(CC), molecular function(MF) and biological process(BP). The KEGG enrichment results showed that the identified proteins could be enriched in 12 metabolic pathways. The results of protein-protein interaction(PPI) analysis indicated that ACC and CG3011 proteins could serve as the core protein-protein interaction network. 【Conclusion】 In this study 169 peritrophic membrane proteins were identified from H. armigera larvae and subjected to GO, KEGG and PPI analyses. The results are helpful to comprehensively understand the molecular structure and function of PM in insects.
引文
Campbell PM, Cao AT, Hines ER, East PD, Gordon KH, 2008. Proteomic analysis of the peritrophic matrix from the gut of the caterpillar, Helicoverpa armigera. Insect Biochem. Molec. Biol., 38(10): 950-958.
Dinglasan RR, Devenport M, Florens L, Johnson JR, McHugh CA, Donnelly-Doman M, Carucci DJ, Yates JR, Jacobs-Lorena M, 2009. The Anopheles gambiae adult midgut peritrophic matrix proteome. Insect Biochem. Molec. Biol., 39(2): 125-134.
Duan HR, Qiu DB, Gong CL, Huang ML, 2011. Analysis of horizontal transfer gene of Bombyx mori nuclear polyhedrosis virus. Hereditas (Beijing), 33(6): 636-647. [段海蓉, 丘德彬, 贡成良, 黄茉莉, 2011. 家蚕核型多角体病毒水平转移基因分析. 遗传, 33(6): 636-647]
Edge AS, 2003. Deglycosylation of glycoproteins with trifluoromethanesulphonic acid: elucidation of molecular structure and function. Biochem. J., 376(2): 339-350.
Faulkner P, Kuzio J, Williams GV, Wilson JA, 1997. Analysis of p74, a PDV envelope protein of Autographa californica nucleopolyhedrovirus required for occlusion body infectivity in vivo. J. Gen. Virol., 78(12): 3091-3100.
Gao ZR, Lin S, Guo XQ, Li QS, Qiu F, 2011. A study on the resurgence of cotton bollworm induced by chemical insecticides. J. Henan Agric. Sci., 30(1): 17-19. [高宗仁, 林松, 郭小奇, 李巧丝, 邱锋, 2001. 化学杀虫剂诱发棉铃虫再猖獗的研究. 河南农业科学, 30(1): 17-19]
Gilbert C, Peccoud J, Chateigner A, Moumen B, Cordaux R, Herniou EA, 2016. Continuous influx of genetic material from host to virus populations. PLoS Genet., 12(2): e1005838.
Goley ED, Ohkawa T, Mancuso J, Woodruff JB, D′Alessio JA, Cande WZ, Volkman LZ, Welch MD, 2006. Dynamic nuclear actin assembly by Arp2/3 complex and a baculovirus WAPS-like protein. Science, 314(5798): 464-467.
Grishin NV, 1998. The R3H motif: a domain that binds single-stranded nucleic acids. Trends Biochem. Sci., 23(9): 329-330.
Guarino LA, Mistretta TA, Dong W, 2002. Baculovirus lef-12 is not required for viral replication. J. Virol., 76(23): 12032-12043.
Gui L,Wang B, Wang LY, Li FH, Xiang JH, 2012. Review on structure and function of insect peritrophic membrane for facilitating research on prevention of WSSV disease in shrimp. Marine Sci., 36(4): 126-131. [桂朗, 王兵, 王丽燕, 李富花, 相建海, 2012. 昆虫围食膜结构与功能概述及其对对虾WSSV病防治研究的启示. 海洋科学, 36(4): 126-131]
Guo HF, Fang JC, Han ZJ, 2003. Advances in insect virus synergists. Acta Entomol. Sin., 46(6): 766-772. [郭慧芳, 方继朝, 韩召军, 2003. 昆虫病毒增效剂研究进展. 昆虫学报, 46(6): 766-772]
Hayakawa T, Shitomi Y, Miyamoto K, Hori H, 2004. GalNAc pretreatment inhibits trapping of Bacillus thuringiensis Cry1Ac on the peritrophic membrane of Bombyx mori. FEBS Lett., 576(3): 331-335.
Hegedus D, Erlandson M, Gillott C, Toprak U, 2009. New insights into peritrophic matrix synthesis, architecture, and function. Annu. Rev. Entomol., 54: 285-302.
Hu XL, Chen L, Xiang XW, Yang R, Yu SF, Wu XF, 2012. Proteomic analysis of peritrophic membrane (PM) from the midgut of fifth-instar larvae, Bombyx mori. Mol. Biol. Rep., 39(4): 3427-3434.
Jang MK, Kong BG, Jeong YI., Chang HL, Nah JW, 2004. Physicochemical characterization of α-chitin, β-chitin, and γ-chitin separated from natural resources. J. Polym. Sci. Pol. Chem., 42(14): 3423-3432.
Katsuma S, Kawaoka S, Mita K, Shimada T, 2008. Genome-wide survey for baculoviral host homologs using the Bombyx genome sequence. Insect Biochem. Molec. Biol., 38(12): 1080-1086.
Krantz DE, Zipursky SL, 1990. Drosophila chaoptin, a member of the leucine-rich repeat family, is a photoreceptor cell-specific adhesion molecule. EMBO J., 9(6): 1969-1977.
Kuzio J, Jaques R, Faulkner P, 1989. Identification of p74, a gene essential for virulence of baculovirus occlusion bodies. Virology, 173(2): 759-763.
Lepore LS, Roelvink PR, Granados RR, 1996. Enhancin, the granulosis virus protein that facilitates nucleopolyhedrovirus (NPV) infections, is a metalloprotease. J. Invertebr. Pathol., 68(2): 131-140.
Li K, Wang Y, Bai HM, Wang Q, Song JH, Zhou Y, Wu CC, Chen XW, 2010. The putative pocket protein binding site of Autographa californica nucleopolyhedrovirus BV/ODV-C42 is required for virus-induced nuclear actin polymerization. J. Virol., 84(15): 7857-7868.
Ling EJ, Yu XQ, 2006. Cellular encapsulation and melanization are enhanced by immulectins, pattern recognition receptors from the tobacco hornworm Manduca sexta. Dev. Comp. Immunol., 30(3): 289-299.
Ohkawa T, Volkman LE, Welch MD, 2010. Actin-based motility drives baculovirus transit to the nucleus and cell surface. J. Cell Biol., 190(2): 187-195.
Ono C, Kamagata T, Taka H, Sahara K, Asano S, Bando H, 2012. Phenotypic grouping of 141 BmNPVs lacking viral gene sequences. Virus Res., 165(2): 197-206.
Patankar AG, Giri AP, Harsulkar AM, Sainani MN, Deshpande VV, Ranjekar PK, Gupta VS, 2001. Complexity in specificities and expression of Helicoverpa armigera gut proteinases explains polyphagous nature of the insect pest. Insect Biochem. Molec. Biol., 31(4): 453-464.
Peng HY, Li X, Zhang SM, Arif BM, Chen XW, Hu ZH, 1998. Localization and cloning of the chitinase gene of, Heliothis armigera single nucleocapsid nucleopolyhedrovirus. Virol. Sin., 13(2): 139-143. [彭辉银, 李星, 张双民, Arif BM, 陈新文, 胡志红, 1998. 中国棉铃虫核型多角体病毒几丁质酶基因的定位与克隆. 中国病毒学, 13(2): 139-143]
Rose C, Belmonte R, Armstrong SD, Molyneux G, Haines LR, Lehane MJ, Wastling J, Acosta-Serrano A, 2014. An investigation into the protein composition of the teneral Glossina morsitans morsitans peritrophic matrix. PLoS Negl. Trop. Dis., 8(4): e2691.
Tellam RL, 1996. The peritrophic matrix. In: Lehane MJ, Billingsley PF eds. Biology of the Insect Midgut. Springer, Netherlands. 86-114.
Tellam RL, Wijffels G, Willadsen P, 1999. Peritrophic matrix proteins. Insect Biochem. Molec. Biol., 29(2): 87-101.
Thiem SM, Miller LK, 1989. A baculovirus gene with a novel transcription pattern encodes a polypeptide with a zinc finger and a leucine zipper. J. Virol., 63(11): 4489-4497.
Toprak U, Erlandson M, Baldwin D, Karcz S, Wan L, Coutu C, Gillott C, Hegedus DD, 2016. Identification of the Mamestra configurata (Lepidoptera: Noctuidae) peritrophic matrix proteins and enzymes involved in peritrophic matrix chitin metabolism. Insect Sci., 23(5): 656-674.
Wang P, Granados RR, 1997. An intestinal mucin is the target substrate for a baculovirus enhancin. Proc. Natl. Acad. Sci. USA, 94(13): 6977-6982.
Wang P, Granados RR, 1998. Observations on the presence of the peritrophic membrane in larval Trichoplusia ni and its role in limiting baculovirus infection. J. Invertebr. Pathol., 72(1): 57-62.
Wang P, Granados RR, 2001. Molecular structure of the peritrophic membrane (PM): identification of potential PM target sites for insect control. Arch. Insect Biochem., 47(2): 110-118.
Wang Y, Wang Q, Liang CY, Song JH, Li N, Shi H, Chen XW, 2008. Autographa californica multiple nucleopolyhedrovirus nucleocapsid protein BV/ODV-C42 mediates the nuclear entry of P78/83. J. Virol., 82(9): 4554-4561.
Wang Y, Xiu JF, Cheng JZ, Luo M, Zhao P, Shang XL, Wang T, Wu JW, 2016. Proteomic analysis of the peritrophic matrix from the midgut of third instar larvae, Musca domestica. Biomed. Environ. Sci., 29(1): 56-65.
Zhang J, Zhang R, Ye CL, Xie X, 2011. Drosophila-derived GPCR Methuselah G protein coupled signal transduction pathway. Chin. J. Cell Biol., 33(8): 847-854. [张静, 张儒, 叶晨立, 谢欣, 2011. 果蝇来源的GPCR Methuselah G蛋白偶联信号转导通路研究. 中国细胞生物学学报, 33(8): 847-854]
Zhang N, Ge J, Zhou ZQ, Yin J, Zhong J, 2016. Expression and role of AcMNPV bro gene. J. Fudan Univ. (Nat. Sci.), 55(1): 128-132. [张楠, 葛晶, 周子谦, 尹隽, 钟江, 2016. AcMNPV bro基因的表达和作用研究. 复旦学报(自然科学版), 55(1): 128-132]
Zhang XX, Liang ZP, Peng HY, Zhang ZX, Tang XC, Li G, Zhao SL, Xiao YZ, Zhang WJ, 2006. Effect of Congo red on peritrophic membrane of Helicoverpa armigera (Hübner) and its viral-enhancing activity. Acta Entomol. Sin., 49(1): 45-49. [张小霞, 梁振普, 彭辉银, 张忠信, 汤显春, 李罡, 赵淑玲, 肖宇宙, 张万菊, 2006. 刚果红对棉铃虫中肠围食膜的影响及其病毒增效作用. 昆虫学报, 49(1): 45-49]
Zhong XW, Zhang LP, Zou Y, Yi QY, Zhao P, Xia QY, Xiang ZH, 2012. Shotgun analysis on the peritrophic membrane of the silkworm Bombyx mori. BMB Rep., 45(11): 665-670.
Zhu R, Peng JX, Hong HZ, 2003. Effects of fluorescent brightener on the peritrophic membrane structure of Spodoptera exigua. Acta Entomol. Sin., 46(4): 424-428. [朱蓉, 彭建新, 洪华珠, 2003. 光增白剂对甜菜夜蛾围食膜结构的作用与影响. 昆虫学报, 46(4): 424-428]
Zhuo LX, Huang YL, Yang JR, 1981. Study on artificial feed of Helicoverpa armigera. Acta Entomol. Sin., 24(1): 110-112. [卓乐姒, 黄月兰, 杨家荣, 1981. 棉铃虫人工饲料的研究. 昆虫学报, 24(1): 110-112]
Dinglasan RR, Devenport M, Florens L, Johnson JR, McHugh CA, Donnelly-Doman M, Carucci DJ, Yates JR, Jacobs-Lorena M, 2009. The Anopheles gambiae adult midgut peritrophic matrix proteome. Insect Biochem. Molec. Biol., 39(2): 125-134.
Duan HR, Qiu DB, Gong CL, Huang ML, 2011. Analysis of horizontal transfer gene of Bombyx mori nuclear polyhedrosis virus. Hereditas (Beijing), 33(6): 636-647. [段海蓉, 丘德彬, 贡成良, 黄茉莉, 2011. 家蚕核型多角体病毒水平转移基因分析. 遗传, 33(6): 636-647]
Edge AS, 2003. Deglycosylation of glycoproteins with trifluoromethanesulphonic acid: elucidation of molecular structure and function. Biochem. J., 376(2): 339-350.
Faulkner P, Kuzio J, Williams GV, Wilson JA, 1997. Analysis of p74, a PDV envelope protein of Autographa californica nucleopolyhedrovirus required for occlusion body infectivity in vivo. J. Gen. Virol., 78(12): 3091-3100.
Gao ZR, Lin S, Guo XQ, Li QS, Qiu F, 2011. A study on the resurgence of cotton bollworm induced by chemical insecticides. J. Henan Agric. Sci., 30(1): 17-19. [高宗仁, 林松, 郭小奇, 李巧丝, 邱锋, 2001. 化学杀虫剂诱发棉铃虫再猖獗的研究. 河南农业科学, 30(1): 17-19]
Gilbert C, Peccoud J, Chateigner A, Moumen B, Cordaux R, Herniou EA, 2016. Continuous influx of genetic material from host to virus populations. PLoS Genet., 12(2): e1005838.
Goley ED, Ohkawa T, Mancuso J, Woodruff JB, D′Alessio JA, Cande WZ, Volkman LZ, Welch MD, 2006. Dynamic nuclear actin assembly by Arp2/3 complex and a baculovirus WAPS-like protein. Science, 314(5798): 464-467.
Grishin NV, 1998. The R3H motif: a domain that binds single-stranded nucleic acids. Trends Biochem. Sci., 23(9): 329-330.
Guarino LA, Mistretta TA, Dong W, 2002. Baculovirus lef-12 is not required for viral replication. J. Virol., 76(23): 12032-12043.
Gui L,Wang B, Wang LY, Li FH, Xiang JH, 2012. Review on structure and function of insect peritrophic membrane for facilitating research on prevention of WSSV disease in shrimp. Marine Sci., 36(4): 126-131. [桂朗, 王兵, 王丽燕, 李富花, 相建海, 2012. 昆虫围食膜结构与功能概述及其对对虾WSSV病防治研究的启示. 海洋科学, 36(4): 126-131]
Guo HF, Fang JC, Han ZJ, 2003. Advances in insect virus synergists. Acta Entomol. Sin., 46(6): 766-772. [郭慧芳, 方继朝, 韩召军, 2003. 昆虫病毒增效剂研究进展. 昆虫学报, 46(6): 766-772]
Hayakawa T, Shitomi Y, Miyamoto K, Hori H, 2004. GalNAc pretreatment inhibits trapping of Bacillus thuringiensis Cry1Ac on the peritrophic membrane of Bombyx mori. FEBS Lett., 576(3): 331-335.
Hegedus D, Erlandson M, Gillott C, Toprak U, 2009. New insights into peritrophic matrix synthesis, architecture, and function. Annu. Rev. Entomol., 54: 285-302.
Hu XL, Chen L, Xiang XW, Yang R, Yu SF, Wu XF, 2012. Proteomic analysis of peritrophic membrane (PM) from the midgut of fifth-instar larvae, Bombyx mori. Mol. Biol. Rep., 39(4): 3427-3434.
Jang MK, Kong BG, Jeong YI., Chang HL, Nah JW, 2004. Physicochemical characterization of α-chitin, β-chitin, and γ-chitin separated from natural resources. J. Polym. Sci. Pol. Chem., 42(14): 3423-3432.
Katsuma S, Kawaoka S, Mita K, Shimada T, 2008. Genome-wide survey for baculoviral host homologs using the Bombyx genome sequence. Insect Biochem. Molec. Biol., 38(12): 1080-1086.
Krantz DE, Zipursky SL, 1990. Drosophila chaoptin, a member of the leucine-rich repeat family, is a photoreceptor cell-specific adhesion molecule. EMBO J., 9(6): 1969-1977.
Kuzio J, Jaques R, Faulkner P, 1989. Identification of p74, a gene essential for virulence of baculovirus occlusion bodies. Virology, 173(2): 759-763.
Lepore LS, Roelvink PR, Granados RR, 1996. Enhancin, the granulosis virus protein that facilitates nucleopolyhedrovirus (NPV) infections, is a metalloprotease. J. Invertebr. Pathol., 68(2): 131-140.
Li K, Wang Y, Bai HM, Wang Q, Song JH, Zhou Y, Wu CC, Chen XW, 2010. The putative pocket protein binding site of Autographa californica nucleopolyhedrovirus BV/ODV-C42 is required for virus-induced nuclear actin polymerization. J. Virol., 84(15): 7857-7868.
Ling EJ, Yu XQ, 2006. Cellular encapsulation and melanization are enhanced by immulectins, pattern recognition receptors from the tobacco hornworm Manduca sexta. Dev. Comp. Immunol., 30(3): 289-299.
Ohkawa T, Volkman LE, Welch MD, 2010. Actin-based motility drives baculovirus transit to the nucleus and cell surface. J. Cell Biol., 190(2): 187-195.
Ono C, Kamagata T, Taka H, Sahara K, Asano S, Bando H, 2012. Phenotypic grouping of 141 BmNPVs lacking viral gene sequences. Virus Res., 165(2): 197-206.
Patankar AG, Giri AP, Harsulkar AM, Sainani MN, Deshpande VV, Ranjekar PK, Gupta VS, 2001. Complexity in specificities and expression of Helicoverpa armigera gut proteinases explains polyphagous nature of the insect pest. Insect Biochem. Molec. Biol., 31(4): 453-464.
Peng HY, Li X, Zhang SM, Arif BM, Chen XW, Hu ZH, 1998. Localization and cloning of the chitinase gene of, Heliothis armigera single nucleocapsid nucleopolyhedrovirus. Virol. Sin., 13(2): 139-143. [彭辉银, 李星, 张双民, Arif BM, 陈新文, 胡志红, 1998. 中国棉铃虫核型多角体病毒几丁质酶基因的定位与克隆. 中国病毒学, 13(2): 139-143]
Rose C, Belmonte R, Armstrong SD, Molyneux G, Haines LR, Lehane MJ, Wastling J, Acosta-Serrano A, 2014. An investigation into the protein composition of the teneral Glossina morsitans morsitans peritrophic matrix. PLoS Negl. Trop. Dis., 8(4): e2691.
Tellam RL, 1996. The peritrophic matrix. In: Lehane MJ, Billingsley PF eds. Biology of the Insect Midgut. Springer, Netherlands. 86-114.
Tellam RL, Wijffels G, Willadsen P, 1999. Peritrophic matrix proteins. Insect Biochem. Molec. Biol., 29(2): 87-101.
Thiem SM, Miller LK, 1989. A baculovirus gene with a novel transcription pattern encodes a polypeptide with a zinc finger and a leucine zipper. J. Virol., 63(11): 4489-4497.
Toprak U, Erlandson M, Baldwin D, Karcz S, Wan L, Coutu C, Gillott C, Hegedus DD, 2016. Identification of the Mamestra configurata (Lepidoptera: Noctuidae) peritrophic matrix proteins and enzymes involved in peritrophic matrix chitin metabolism. Insect Sci., 23(5): 656-674.
Wang P, Granados RR, 1997. An intestinal mucin is the target substrate for a baculovirus enhancin. Proc. Natl. Acad. Sci. USA, 94(13): 6977-6982.
Wang P, Granados RR, 1998. Observations on the presence of the peritrophic membrane in larval Trichoplusia ni and its role in limiting baculovirus infection. J. Invertebr. Pathol., 72(1): 57-62.
Wang P, Granados RR, 2001. Molecular structure of the peritrophic membrane (PM): identification of potential PM target sites for insect control. Arch. Insect Biochem., 47(2): 110-118.
Wang Y, Wang Q, Liang CY, Song JH, Li N, Shi H, Chen XW, 2008. Autographa californica multiple nucleopolyhedrovirus nucleocapsid protein BV/ODV-C42 mediates the nuclear entry of P78/83. J. Virol., 82(9): 4554-4561.
Wang Y, Xiu JF, Cheng JZ, Luo M, Zhao P, Shang XL, Wang T, Wu JW, 2016. Proteomic analysis of the peritrophic matrix from the midgut of third instar larvae, Musca domestica. Biomed. Environ. Sci., 29(1): 56-65.
Zhang J, Zhang R, Ye CL, Xie X, 2011. Drosophila-derived GPCR Methuselah G protein coupled signal transduction pathway. Chin. J. Cell Biol., 33(8): 847-854. [张静, 张儒, 叶晨立, 谢欣, 2011. 果蝇来源的GPCR Methuselah G蛋白偶联信号转导通路研究. 中国细胞生物学学报, 33(8): 847-854]
Zhang N, Ge J, Zhou ZQ, Yin J, Zhong J, 2016. Expression and role of AcMNPV bro gene. J. Fudan Univ. (Nat. Sci.), 55(1): 128-132. [张楠, 葛晶, 周子谦, 尹隽, 钟江, 2016. AcMNPV bro基因的表达和作用研究. 复旦学报(自然科学版), 55(1): 128-132]
Zhang XX, Liang ZP, Peng HY, Zhang ZX, Tang XC, Li G, Zhao SL, Xiao YZ, Zhang WJ, 2006. Effect of Congo red on peritrophic membrane of Helicoverpa armigera (Hübner) and its viral-enhancing activity. Acta Entomol. Sin., 49(1): 45-49. [张小霞, 梁振普, 彭辉银, 张忠信, 汤显春, 李罡, 赵淑玲, 肖宇宙, 张万菊, 2006. 刚果红对棉铃虫中肠围食膜的影响及其病毒增效作用. 昆虫学报, 49(1): 45-49]
Zhong XW, Zhang LP, Zou Y, Yi QY, Zhao P, Xia QY, Xiang ZH, 2012. Shotgun analysis on the peritrophic membrane of the silkworm Bombyx mori. BMB Rep., 45(11): 665-670.
Zhu R, Peng JX, Hong HZ, 2003. Effects of fluorescent brightener on the peritrophic membrane structure of Spodoptera exigua. Acta Entomol. Sin., 46(4): 424-428. [朱蓉, 彭建新, 洪华珠, 2003. 光增白剂对甜菜夜蛾围食膜结构的作用与影响. 昆虫学报, 46(4): 424-428]
Zhuo LX, Huang YL, Yang JR, 1981. Study on artificial feed of Helicoverpa armigera. Acta Entomol. Sin., 24(1): 110-112. [卓乐姒, 黄月兰, 杨家荣, 1981. 棉铃虫人工饲料的研究. 昆虫学报, 24(1): 110-112]