球孢白僵菌毒素对家蚕糖代谢水平的影响
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摘要
为明确球孢白僵菌毒素对宿主昆虫糖代谢水平的作用,本研究检测了家蚕幼虫感染球孢白僵菌和注射球孢白僵菌毒素之后组织中海藻糖和糖原含量的变化,以及糖代谢相关基因表达水平的变化;分析了注射毒素和添食海藻糖之后对家蚕幼虫存活率的影响、以及添加毒素之后对BmN细胞的损伤作用。结果表明,家蚕幼虫感染球孢白僵菌和注射毒素后海藻糖和糖原含量显著降低;Bombyxin A2和BmIBP2基因显著上调表达,而糖代谢酶系基因则显著下调表达。注射毒素显著降低家蚕5龄幼虫的存活时间,而补充海藻糖能够延长家蚕幼虫的存活时间。添加毒素能够使家蚕BmN细胞发生凝集作用而最终崩解死亡,并诱导Bombyxin A2和BmIBP2基因显著上调表达以及糖代谢酶系基因显著下调表达。以上结果说明,球孢白僵菌可能通过分泌毒素,作用于家蚕类胰岛素信号通路,调节家蚕自身糖类物质的代谢与合成,破坏家蚕能量代谢与储存平衡,引起家蚕组织细胞凋亡并最终导致家蚕死亡。本研究结果对农林害虫的生物防治、家蚕等经济昆虫僵病防治技术的研究以及球孢白僵菌毒素用于新型降糖药物的筛选和中药僵蚕的开发利用均具有重要意义。
In order to clarify the effect of mycotoxins on the glycometabolism of host insects, in this study, the changes of trehalose and glycogen contents as well as the changes of the expression levels of glycometabolism related genes in silkworm larvae infected with Beauveria bassiana or injected with mycotoxins were investigated.Besides, the effects on the survival rate of 5 thinstar silkworm larvae injected with mycotoxins and reared with trehalose were also investigated. In addition, the damage of BmN cells induced by mycotoxins was detected. The results showed that the trehalose and glycogen contention in silkworm larvae both infected with B. bassiana and injected with mycotoxins were all significantly decreased. The expression level of Bombyxin A2 and Bmibp2 gene was significantly up-regulated, while the glycometabolism related genes were significantly down-regulated. Moreover,the injection of mycotoxins could significantly reduce the survival time of the 5 thinstar silkworm larvae, while the supplementation of trehalose could significantly prolong the survival time. Furthermore, mycotoxins could induce the agglutination of BmN cells and finally encourage apoptosis and disintegration, the expression levels of Bombyxin A2 and Bmibp2 genes were significantly up-regulated, while the glycometabolism related genes were significantly down regulated. The above results indicated that B. bassiana might secrete the mycotoxins, which affected the silkworm insulin pathway by adjusting the expression level of Bombyxin A2 and Bmibp2 genes, and then regulated metabolism and synthesis of carbohydrate, upset the balance of storage of energy, leading to the cell apoptosis and the death of silkworm larvae. The finds yield insights for better understand the pathogenic mechanism of B. bassiana by studying the effects of mycotoxins on the glycometabolism of host insects, which have important significance for the study on bio-control and muscardine disease resistance of silkworm or other economic insects,the screening of Beauveria bassiana mycotoxin as a novel antidiabetic drugs, and the development and utilization of traditional Chinese medicine Bombyx batryticatus.
In order to clarify the effect of mycotoxins on the glycometabolism of host insects, in this study, the changes of trehalose and glycogen contents as well as the changes of the expression levels of glycometabolism related genes in silkworm larvae infected with Beauveria bassiana or injected with mycotoxins were investigated.Besides, the effects on the survival rate of 5 thinstar silkworm larvae injected with mycotoxins and reared with trehalose were also investigated. In addition, the damage of BmN cells induced by mycotoxins was detected. The results showed that the trehalose and glycogen contention in silkworm larvae both infected with B. bassiana and injected with mycotoxins were all significantly decreased. The expression level of Bombyxin A2 and Bmibp2 gene was significantly up-regulated, while the glycometabolism related genes were significantly down-regulated. Moreover,the injection of mycotoxins could significantly reduce the survival time of the 5 thinstar silkworm larvae, while the supplementation of trehalose could significantly prolong the survival time. Furthermore, mycotoxins could induce the agglutination of BmN cells and finally encourage apoptosis and disintegration, the expression levels of Bombyxin A2 and Bmibp2 genes were significantly up-regulated, while the glycometabolism related genes were significantly down regulated. The above results indicated that B. bassiana might secrete the mycotoxins, which affected the silkworm insulin pathway by adjusting the expression level of Bombyxin A2 and Bmibp2 genes, and then regulated metabolism and synthesis of carbohydrate, upset the balance of storage of energy, leading to the cell apoptosis and the death of silkworm larvae. The finds yield insights for better understand the pathogenic mechanism of B. bassiana by studying the effects of mycotoxins on the glycometabolism of host insects, which have important significance for the study on bio-control and muscardine disease resistance of silkworm or other economic insects,the screening of Beauveria bassiana mycotoxin as a novel antidiabetic drugs, and the development and utilization of traditional Chinese medicine Bombyx batryticatus.
引文
Eula Maria de M.B.C.,Fabiana Cristina P.,Christian L.,Valéria de O.,Marília O.,Elda B.,and Silvana P.,2011,Beauveria bassiana:quercetinase production and genetic diversity,Braz.J.Microbiol.,42(1):12-21
Fujiwara Y.,Tanaka Y.,Iwata K.,Rubio R.O.,Yaginuma T.,Yamashita O.,and Shiomi K.,2006,ERK/MAPK regulates ecdysteroid and sorbitol metabolism for embryonic diapause termination in the silkworm,Bombyx mori,J.Insect Physiol.,52(6):569-575
Gao K.,Deng X.Y.,Qian H.Y.,Wu P.,Qin G.X.,Liu T.,Shen Z.Y.,and Guo X.J.,2012,Novel protein of IBP from silkworm,Bombyx mori,involved in cytoplasmic polyhedrosis virus infection,J.Invertebr.Pathol.,110(1):83-91
Gao K.,Deng X.Y.,Zhu F.,Wang S.P.,Qian H.Y.,and Guo X.J.,2012,Prokaryotic expression of Bombyx mori insulin-related peptide-binding protein 2(Bm IBP2)and its tissue-specificity in silkworm,Zhongguo Nongye Kexue(Scientia Agricultura Sinica),45(23):4916-4923(高坤,邓祥元,朱峰,汪生鹏,钱荷英,郭锡杰,2012,家蚕类胰岛素相关肽结合蛋白2(Bm IBP2)的原核表达与组织特异性分析,中国农业科学,45(23):4916-4923)
Gao Y.,Xue J.L.,Fan S.H.,Fan J.H.,and Xie Y.P.,2010,Isolation and purification of toxins from a strain of Beauveria brongniartii and their toxicity to the larvae of Dendrolimus tabulaeformis,Zhongguo Nongye Kexue(Scientia Agricultura Sinica),43(15):3125-3133(高英,薛皎亮,范三红,樊金华,谢映平,2010,布氏白僵菌代谢毒素的分离纯化及其对油松毛虫幼虫的毒性研究,中国农业科学,43(15):3125-3133)
Grogan G.J.,and Holland H.L.,2000,The biocatalytic reactions of Beauveria spp.,Journal of Molecular Catalysis B:Enzymatic,9(1-3):1-32
Hage Hassan R.,Pacheco de Sousa A.C.,Mahfouz R.,Hainault I.,Blachnio-Zabielska A.,Bourron O.,Koskas F.,Górski J.,FerréP.,Foufelle F.,and Hajduch E.,2016,Sustained action of cera-
mide on the insulin signaling pathway in muscle cells:IMPL-ICATION OF THE DOUBLE-STRANDED RNA-ACTIVA-TED PROTEIN KINASE,J.Biol.Chem.,291(6):3019-3029
Ho C.K.,Rahib L.,Liao J.C.,Sriram G.,and Dipple K.M.,2015,Mathematical modeling of the insulin signal transduction pathway for prediction of insulin sensitivity from expression data,Mol.Genet.Metab.,114(1):66-72
Ishii K.,Hamamoto H.,Kamimura M.,Nakamura Y.,Noda H.,I-mamura K.,Mita K.,and Sekimizu K.,2010,Insect cytokine paralytic peptide(PP)induces cellular and humoral immune responses in the silkworm Bombyx mori,J.Biol.Chem.,285(37):28635-28642
Iwami M.,Kawakami A.,Ishizaki H.,Takahashi S.Y.,Adachi T.,SuzukiY.,Nagasawa H.,and Suzuki A.,1989,Cloning of a gene encoding bombyxin,an insulin-like brain secretory peptide of the silkmoth Bombyx mori with prothoracicotropic activity,Development Growth&Differentiation,31(1):31-37
Kong X.B.,and XüS.Q.,2010,Structure,signal transduction and function of insulin-like peptides(bombyxins)in the silkworm,Bombyx mori,Chanye Kexue(Science of Sericulture),36(3):458-464(孔祥宾,徐世清,2010,家蚕类胰岛素肽的结构及信号传导与作用,蚕业科学,36(3):458-464)
Livak K.J.,and Schmittgen T.D.,2001,Analysis of relative gene expression data using real-time quantitative PCR and the 2-△△CTmethod,Methods,25(4):402-408
Lozano-Tovar M.D.,Garrido-Jurado I.,Quesada-Moraga E.,RayaOrtega M.C.,and Trapero-Casas A.,2017,Metarhizium brunneum and Beauveria bassiana release secondary metabolites with antagonistic activity against Verticillium dahliae and Phytophthora megasperma olive pathogens,Crop Protection,100:186-195
Mascarin G.M.,and Jaronski S.T.,2016,The production and uses of Beauveria bassiana as a microbial insecticide,World J.Microbiol.Biotechnol.,32(11):177
Nabizadeh P.,and Kumar T.S.J.,2011,Fat body catalase activity as a biochemical index for the recognition of thermotolerant breeds of mulberry silkworm,Bombyx mori L.,Journal of Thermal Biology,36(1):1-6
Nath B.S.,2000,Changes in carbohydrate metabolism in hemolymph and fat body of the silkworm,Bombyx mori L.,exposed to organophosphorus insecticides,Pesticide Biochemistry and Physiology,68(3):127-137
Saegusa H.,Mizoguchi A.,Kitahora H.,Nagasawa H.,Suzuki A.,and Ishizaki H.,2010,Changes in the titer of bombyxin-immunoreactive material in hemolymph during the postembryonic development of the silkmoth Bombyx mori,Development Growth&Differentiation,34(5):595-605
Satake S.,Kawabe Y.,and Mizoguchi A.,2010,Carbohydrate metabolism during starvation in the silkworm Bombyx mori L.,Arch.Insect Biochem.Physiol.,44(2):90-98
Sun L.Y.,Xv X.,Yang Y.,Wu Y.Q.,Liu Q.X.,and Cui W.Z.,2015,Effects of diabetogenic agent streptozotocin and the bombyxinⅡderived from prokaryotic expression on content of blood sugar in the silkworm,Bombyx mori,Chanye Kexue(Science of Sericulture),41(3):442-449(孙凌云,徐欣,杨洋,吴亚群,刘庆信,崔为正,2015,糖尿病诱导剂链脲佐菌素与原核表达的家蚕素Ⅱ对家蚕血糖含量的影响,蚕业科学,41(3):442-449)
Tamayo-Mejía F.,Tamez-Guerr a P.,Guzmn-Franco A.W.,and Gomez-Flores R.,2016,Developmental stage affects survival of the ectoparasitoid Tamarixia triozae exposed to the fungus Beauveria bassiana,Biological Control,93:30-36
Tao H.,Liu H.J.,Cheng Y.Q.,Sima Y.H.,Yin W.M.,and Xu S.Q.,2015,Parental environmental exposure leads to glycometabolic disturbances that affect fertilization of eggs in the silkworm Bombyx mori:the parental transcript legacy,J.Comp.Physiol.B.,185(1):47-55
Tatun N.,Singtripop T.,and Osugi S.,2009,Possible involvement of proteinaceous and non-proteinaceous trehalase inhibitors in the regulation of hemolymph trehalose concentration in Bombyx mori,Appl.Entomol.Zool.,44(1):85-94
Wu Y.,Huang X.L.,Deng J.X.,and Hong J.,1998,Isolation,detection toxicity and structure of toxin from Beauveria Bassiana,Weishengwu Xuebao(Acta Microbiologica Sinica),38(6):468-474(武艺,黄秀梨,邓继先,洪泂,1998,球孢白僵菌毒素的分离,毒力检测及结构鉴定,微生物学报,38(6):468-474)
Xia Q.,Guo Y.R.,Zhang Z.,Li D.,Xuan Z.L.,Li Z.,Dai F.Y.,Li Y.R.,Cheng D.J.,Li R.Q.,Cheng T.C.,Jiang T.,Becquet C.,Xu X.,Liu C.,Zha X.F.,Fan W.,Lin Y.,Shen Y.H.,Jiang L.,Jensen J.,Hellmann I.,Tang S.,Zhao.P,Xu H.F.,Yu C.,Zhang G.J.,Li J.,Cao J.J.,Liu S.P.,He N.J.,Zhou Y.,Liu H.,Zhao J.,Ye C.,Du Z.H.,Pan G.Q.,Zhao A.C.,Shao H.J.,Zeng W.,Wu P.,Li C.F.,Pan M.H.,Li J.J.,Yin X.Y.,Li D.W.,Wang J.,Zheng H.S.,Wang W.,Zhang X.Q.,Li S.G.,Yang H.M.,Lu C.,Nielsen R.,Zhou Z.Y.,Wang J.,Xiang Z.H.,and Wang J.,2009,Complete resequencing of 40 genomes reveals domestication events and genes in silkworm(Bombyx mori),Science,326(5951):433-436
Xia Q.,Zhou Z.,Lu C.,Cheng D.,Dai F.,Li B.,Zhao P.,Zha X.,Cheng T.,Chai C.,Pan G.,Xu J.,Liu C.,Lin Y.,Qian J.,Hou Y.,Wu Z.,Li G.,Pan M.,Li C.,Shen Y.,Lan X.,Yuan L.,Li T.,Xu H.,Yang G.,Wan Y.,Zhu Y.,Yu M.,Shen W.,Wu D.,Xiang Z.,Yu J.,Wang J.,Li R.,Shi J.,Li H.,Li G.,Su J.,Wang X.,Li G.,Zhang Z.,Wu Q.,Li J.,Zhang Q.,Wei N.,Xu J.,Sun H.,Dong L.,Liu D.,Zhao S.,Zhao X.,Meng Q.,Lan F.,Huang X.,Li Y.,Fang L.,Li C.,Li D.,Sun Y.,Zhang Z.,Yang Z.,Huang Y.,Xi Y.,Qi Q.,He D.,Huang H.,Zhang X.,Wang Z.,Li W.,Cao Y.,Yu Y.,Yu H.,Li J.,Ye J.,Chen H.,Zhou Y.,Liu B.,Wang J.,Ye J.,Ji H.,Li S.,Ni P.,Zhang J.,Zhang Y.,Zheng H.,Mao B.,Wang W.,Ye C.,Li S.,Wang J.,Wong G.K.,and Yang H.,2004,A draft sequence for the genome of the domesticated silkworm(Bombyx mori),Science,306(5703):1937-1940
Xie Y.,Wang B.,Li F.,Ma L.,Ni M.,Shen W.,Hong F.,and Li B.,2014,Molecular mechanisms of reduced nerve toxicity by titanium dioxide nanoparticles in the phoxim-exposed brain of Bombyx mori,PLoS One,9(6):e101062
Xv W.S.,Hu M.Y.,and Zhong G.H.,2005,The studies of mycotoxins as pesticides in agricultural pests control,Yunnan Nongye Daxue Xuebao(Journal of Yunnan Agricultural University),20(3):339-342(徐伟松,胡美英,钟国华,2005,真菌杀虫毒素的研究,云南农业大学学报,20(3):339-342)
Zhang H.,Wu S.,Xing Z.,Wang X.,and Lei Z.,2016,Bioassay and scanning electron microscopic observations reveal high virulence of entomopathogenic fungus,Beauveria bassiana,on the onion maggot(Diptera:Anthomyiidae)adults,J.Econ.Entomol.,109(6):2309-2316
Fujiwara Y.,Tanaka Y.,Iwata K.,Rubio R.O.,Yaginuma T.,Yamashita O.,and Shiomi K.,2006,ERK/MAPK regulates ecdysteroid and sorbitol metabolism for embryonic diapause termination in the silkworm,Bombyx mori,J.Insect Physiol.,52(6):569-575
Gao K.,Deng X.Y.,Qian H.Y.,Wu P.,Qin G.X.,Liu T.,Shen Z.Y.,and Guo X.J.,2012,Novel protein of IBP from silkworm,Bombyx mori,involved in cytoplasmic polyhedrosis virus infection,J.Invertebr.Pathol.,110(1):83-91
Gao K.,Deng X.Y.,Zhu F.,Wang S.P.,Qian H.Y.,and Guo X.J.,2012,Prokaryotic expression of Bombyx mori insulin-related peptide-binding protein 2(Bm IBP2)and its tissue-specificity in silkworm,Zhongguo Nongye Kexue(Scientia Agricultura Sinica),45(23):4916-4923(高坤,邓祥元,朱峰,汪生鹏,钱荷英,郭锡杰,2012,家蚕类胰岛素相关肽结合蛋白2(Bm IBP2)的原核表达与组织特异性分析,中国农业科学,45(23):4916-4923)
Gao Y.,Xue J.L.,Fan S.H.,Fan J.H.,and Xie Y.P.,2010,Isolation and purification of toxins from a strain of Beauveria brongniartii and their toxicity to the larvae of Dendrolimus tabulaeformis,Zhongguo Nongye Kexue(Scientia Agricultura Sinica),43(15):3125-3133(高英,薛皎亮,范三红,樊金华,谢映平,2010,布氏白僵菌代谢毒素的分离纯化及其对油松毛虫幼虫的毒性研究,中国农业科学,43(15):3125-3133)
Grogan G.J.,and Holland H.L.,2000,The biocatalytic reactions of Beauveria spp.,Journal of Molecular Catalysis B:Enzymatic,9(1-3):1-32
Hage Hassan R.,Pacheco de Sousa A.C.,Mahfouz R.,Hainault I.,Blachnio-Zabielska A.,Bourron O.,Koskas F.,Górski J.,FerréP.,Foufelle F.,and Hajduch E.,2016,Sustained action of cera-
mide on the insulin signaling pathway in muscle cells:IMPL-ICATION OF THE DOUBLE-STRANDED RNA-ACTIVA-TED PROTEIN KINASE,J.Biol.Chem.,291(6):3019-3029
Ho C.K.,Rahib L.,Liao J.C.,Sriram G.,and Dipple K.M.,2015,Mathematical modeling of the insulin signal transduction pathway for prediction of insulin sensitivity from expression data,Mol.Genet.Metab.,114(1):66-72
Ishii K.,Hamamoto H.,Kamimura M.,Nakamura Y.,Noda H.,I-mamura K.,Mita K.,and Sekimizu K.,2010,Insect cytokine paralytic peptide(PP)induces cellular and humoral immune responses in the silkworm Bombyx mori,J.Biol.Chem.,285(37):28635-28642
Iwami M.,Kawakami A.,Ishizaki H.,Takahashi S.Y.,Adachi T.,SuzukiY.,Nagasawa H.,and Suzuki A.,1989,Cloning of a gene encoding bombyxin,an insulin-like brain secretory peptide of the silkmoth Bombyx mori with prothoracicotropic activity,Development Growth&Differentiation,31(1):31-37
Kong X.B.,and XüS.Q.,2010,Structure,signal transduction and function of insulin-like peptides(bombyxins)in the silkworm,Bombyx mori,Chanye Kexue(Science of Sericulture),36(3):458-464(孔祥宾,徐世清,2010,家蚕类胰岛素肽的结构及信号传导与作用,蚕业科学,36(3):458-464)
Livak K.J.,and Schmittgen T.D.,2001,Analysis of relative gene expression data using real-time quantitative PCR and the 2-△△CTmethod,Methods,25(4):402-408
Lozano-Tovar M.D.,Garrido-Jurado I.,Quesada-Moraga E.,RayaOrtega M.C.,and Trapero-Casas A.,2017,Metarhizium brunneum and Beauveria bassiana release secondary metabolites with antagonistic activity against Verticillium dahliae and Phytophthora megasperma olive pathogens,Crop Protection,100:186-195
Mascarin G.M.,and Jaronski S.T.,2016,The production and uses of Beauveria bassiana as a microbial insecticide,World J.Microbiol.Biotechnol.,32(11):177
Nabizadeh P.,and Kumar T.S.J.,2011,Fat body catalase activity as a biochemical index for the recognition of thermotolerant breeds of mulberry silkworm,Bombyx mori L.,Journal of Thermal Biology,36(1):1-6
Nath B.S.,2000,Changes in carbohydrate metabolism in hemolymph and fat body of the silkworm,Bombyx mori L.,exposed to organophosphorus insecticides,Pesticide Biochemistry and Physiology,68(3):127-137
Saegusa H.,Mizoguchi A.,Kitahora H.,Nagasawa H.,Suzuki A.,and Ishizaki H.,2010,Changes in the titer of bombyxin-immunoreactive material in hemolymph during the postembryonic development of the silkmoth Bombyx mori,Development Growth&Differentiation,34(5):595-605
Satake S.,Kawabe Y.,and Mizoguchi A.,2010,Carbohydrate metabolism during starvation in the silkworm Bombyx mori L.,Arch.Insect Biochem.Physiol.,44(2):90-98
Sun L.Y.,Xv X.,Yang Y.,Wu Y.Q.,Liu Q.X.,and Cui W.Z.,2015,Effects of diabetogenic agent streptozotocin and the bombyxinⅡderived from prokaryotic expression on content of blood sugar in the silkworm,Bombyx mori,Chanye Kexue(Science of Sericulture),41(3):442-449(孙凌云,徐欣,杨洋,吴亚群,刘庆信,崔为正,2015,糖尿病诱导剂链脲佐菌素与原核表达的家蚕素Ⅱ对家蚕血糖含量的影响,蚕业科学,41(3):442-449)
Tamayo-Mejía F.,Tamez-Guerr a P.,Guzmn-Franco A.W.,and Gomez-Flores R.,2016,Developmental stage affects survival of the ectoparasitoid Tamarixia triozae exposed to the fungus Beauveria bassiana,Biological Control,93:30-36
Tao H.,Liu H.J.,Cheng Y.Q.,Sima Y.H.,Yin W.M.,and Xu S.Q.,2015,Parental environmental exposure leads to glycometabolic disturbances that affect fertilization of eggs in the silkworm Bombyx mori:the parental transcript legacy,J.Comp.Physiol.B.,185(1):47-55
Tatun N.,Singtripop T.,and Osugi S.,2009,Possible involvement of proteinaceous and non-proteinaceous trehalase inhibitors in the regulation of hemolymph trehalose concentration in Bombyx mori,Appl.Entomol.Zool.,44(1):85-94
Wu Y.,Huang X.L.,Deng J.X.,and Hong J.,1998,Isolation,detection toxicity and structure of toxin from Beauveria Bassiana,Weishengwu Xuebao(Acta Microbiologica Sinica),38(6):468-474(武艺,黄秀梨,邓继先,洪泂,1998,球孢白僵菌毒素的分离,毒力检测及结构鉴定,微生物学报,38(6):468-474)
Xia Q.,Guo Y.R.,Zhang Z.,Li D.,Xuan Z.L.,Li Z.,Dai F.Y.,Li Y.R.,Cheng D.J.,Li R.Q.,Cheng T.C.,Jiang T.,Becquet C.,Xu X.,Liu C.,Zha X.F.,Fan W.,Lin Y.,Shen Y.H.,Jiang L.,Jensen J.,Hellmann I.,Tang S.,Zhao.P,Xu H.F.,Yu C.,Zhang G.J.,Li J.,Cao J.J.,Liu S.P.,He N.J.,Zhou Y.,Liu H.,Zhao J.,Ye C.,Du Z.H.,Pan G.Q.,Zhao A.C.,Shao H.J.,Zeng W.,Wu P.,Li C.F.,Pan M.H.,Li J.J.,Yin X.Y.,Li D.W.,Wang J.,Zheng H.S.,Wang W.,Zhang X.Q.,Li S.G.,Yang H.M.,Lu C.,Nielsen R.,Zhou Z.Y.,Wang J.,Xiang Z.H.,and Wang J.,2009,Complete resequencing of 40 genomes reveals domestication events and genes in silkworm(Bombyx mori),Science,326(5951):433-436
Xia Q.,Zhou Z.,Lu C.,Cheng D.,Dai F.,Li B.,Zhao P.,Zha X.,Cheng T.,Chai C.,Pan G.,Xu J.,Liu C.,Lin Y.,Qian J.,Hou Y.,Wu Z.,Li G.,Pan M.,Li C.,Shen Y.,Lan X.,Yuan L.,Li T.,Xu H.,Yang G.,Wan Y.,Zhu Y.,Yu M.,Shen W.,Wu D.,Xiang Z.,Yu J.,Wang J.,Li R.,Shi J.,Li H.,Li G.,Su J.,Wang X.,Li G.,Zhang Z.,Wu Q.,Li J.,Zhang Q.,Wei N.,Xu J.,Sun H.,Dong L.,Liu D.,Zhao S.,Zhao X.,Meng Q.,Lan F.,Huang X.,Li Y.,Fang L.,Li C.,Li D.,Sun Y.,Zhang Z.,Yang Z.,Huang Y.,Xi Y.,Qi Q.,He D.,Huang H.,Zhang X.,Wang Z.,Li W.,Cao Y.,Yu Y.,Yu H.,Li J.,Ye J.,Chen H.,Zhou Y.,Liu B.,Wang J.,Ye J.,Ji H.,Li S.,Ni P.,Zhang J.,Zhang Y.,Zheng H.,Mao B.,Wang W.,Ye C.,Li S.,Wang J.,Wong G.K.,and Yang H.,2004,A draft sequence for the genome of the domesticated silkworm(Bombyx mori),Science,306(5703):1937-1940
Xie Y.,Wang B.,Li F.,Ma L.,Ni M.,Shen W.,Hong F.,and Li B.,2014,Molecular mechanisms of reduced nerve toxicity by titanium dioxide nanoparticles in the phoxim-exposed brain of Bombyx mori,PLoS One,9(6):e101062
Xv W.S.,Hu M.Y.,and Zhong G.H.,2005,The studies of mycotoxins as pesticides in agricultural pests control,Yunnan Nongye Daxue Xuebao(Journal of Yunnan Agricultural University),20(3):339-342(徐伟松,胡美英,钟国华,2005,真菌杀虫毒素的研究,云南农业大学学报,20(3):339-342)
Zhang H.,Wu S.,Xing Z.,Wang X.,and Lei Z.,2016,Bioassay and scanning electron microscopic observations reveal high virulence of entomopathogenic fungus,Beauveria bassiana,on the onion maggot(Diptera:Anthomyiidae)adults,J.Econ.Entomol.,109(6):2309-2316