Identification and developmental expression of putative gene encoding juvenile hormone esterase(CpJHE-like) in codling moth, Cydia pomonella(L.)
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摘要
Juvenile hormone esterase(JHE) is a key enzyme for insects, playing an important role in the regulation of insect growth, development, diapause and reproduction. We identified a complete putative JHE of Cydia pomonella(CpJHE-like) which is comprised of a 1 761 bp coding sequence(CDS) encoding 587 amino acid residues from the transcriptome data. The deduced protein sequence of CpJHE-like showed the highest identity of 60.44% with the Adoxophyes honmai JHE(AhJHE) and the minimal identity of 25.81% with Aedes aegypti JHE(AaJHE). CpJHE-like exhibited all the seven typical motifs of the functional JHEs and had the highly consistent tertiary structure with Manduca sexta JHE(MsJHE). Phylogenetic analysis showed that the CpJHE-like was close to two JHEs from the family Tortricidae. The CpJHE-like transcript level take a leap in the 3-day-old fifth instar larva, increased about 300-fold compared to the basal level. Tissue-specific expression profile showed that the CpJHE-like transcript was expressed mainly in the fat body. This study indicates that the CpJHE-like is the functional JHE, which may play vital roles in the development and reproduction of C. pomonella.
Juvenile hormone esterase(JHE) is a key enzyme for insects, playing an important role in the regulation of insect growth, development, diapause and reproduction. We identified a complete putative JHE of Cydia pomonella(CpJHE-like) which is comprised of a 1 761 bp coding sequence(CDS) encoding 587 amino acid residues from the transcriptome data. The deduced protein sequence of CpJHE-like showed the highest identity of 60.44% with the Adoxophyes honmai JHE(AhJHE) and the minimal identity of 25.81% with Aedes aegypti JHE(AaJHE). CpJHE-like exhibited all the seven typical motifs of the functional JHEs and had the highly consistent tertiary structure with Manduca sexta JHE(MsJHE). Phylogenetic analysis showed that the CpJHE-like was close to two JHEs from the family Tortricidae. The CpJHE-like transcript level take a leap in the 3-day-old fifth instar larva, increased about 300-fold compared to the basal level. Tissue-specific expression profile showed that the CpJHE-like transcript was expressed mainly in the fat body. This study indicates that the CpJHE-like is the functional JHE, which may play vital roles in the development and reproduction of C. pomonella.
Juvenile hormone esterase(JHE) is a key enzyme for insects, playing an important role in the regulation of insect growth, development, diapause and reproduction. We identified a complete putative JHE of Cydia pomonella(CpJHE-like) which is comprised of a 1 761 bp coding sequence(CDS) encoding 587 amino acid residues from the transcriptome data. The deduced protein sequence of CpJHE-like showed the highest identity of 60.44% with the Adoxophyes honmai JHE(AhJHE) and the minimal identity of 25.81% with Aedes aegypti JHE(AaJHE). CpJHE-like exhibited all the seven typical motifs of the functional JHEs and had the highly consistent tertiary structure with Manduca sexta JHE(MsJHE). Phylogenetic analysis showed that the CpJHE-like was close to two JHEs from the family Tortricidae. The CpJHE-like transcript level take a leap in the 3-day-old fifth instar larva, increased about 300-fold compared to the basal level. Tissue-specific expression profile showed that the CpJHE-like transcript was expressed mainly in the fat body. This study indicates that the CpJHE-like is the functional JHE, which may play vital roles in the development and reproduction of C. pomonella.
引文
Agarwala R,Barrett T,Beck J,Benson D A,Bollin C,Bolton E,Bourexis D,Brister J R,Bryant S H,Canese K,Cavanaugh M,Charowhas C,Clark K,Dondoshansky I,Feolo M,Fitzpatrick L,Funk K,Geer L Y,Gorelenkov V,Graeff A,et al.2018.Database resources of the National Center for Biotechnology Information.Nucleic Acids Research,46,D8-D13.
Anand A,Crone E J,Zera A J.2008.Tissue and stage-specific juvenile hormone esterase(JHE)and epoxide hydrolase(JHEH)enzyme activities and Jhe transcript abundance in lines of the cricket Gryllus assimilis artificially selected for plasma JHE activity:Implications for JHE microevolution.Journal of Insect Physiology,54,1323-1331.
Bai H,Ramaseshadri P,Palli S R.2007.Identification and characterization of juvenile hormone esterase gene from the yellow fever mosquito,Aedes aegypti.Insect Biochemistry and Molecular Biology,37,829-837.
Belles X,Martin D,Piulachs M D.2005.The mevalonate pathway and the synthesis of juvenile hormone in insects.Annual Review of Entomology,50,181-199.
Campbell P M,Harcourt R L,Crone E J,Claudianos C,Hammock B D,Russell R J,Oakeshott J G.2001.Identification of a juvenile hormone esterase gene by matching its peptide mass fingerprint with a sequence from the Drosophila genome project.Insect Biochemistry and Molecular Biology,31,513-520.
Chang E S.1993.Comparative endocrinology of molting and reproduction:Insects and crustaceans.Annual Review of Entomology,38,161-180.
Charmillot P J,Bloesch B,Benz M.1989.Control of the codling moth Cydia pomonella L.with fenoxycarb and teflubenzuron.Revue Suisse de Viticulture,d’Arboriculture et d’Horticulture,21,187-193.(in French)
Charmillot P J,Pasquier D,Hofer D.2002.Control of codling moth Cydia pomonella by autosterilisation.IOBC WPRSBulletin,25,117-120.
Crone E J,Zera A J,Anand A,Oakeshott J G,Sutherland T D,Russell R J,Harshman L G,Hoffmann F G,Claudianos C.2007.JHE in Gryllus assimilis:Cloning,sequence-activity associations and phylogeny.Insect Biochemistry and Molecular Biology,37,1359-1365.
Denlinger D L,Armbruster P A.2014.Mosquito diapause.Annual Review of Entomology,59,73-93.
Dorn S,Frischknecht M L,Martinez V,Zurflüh R,Fischer U.1981.A novel non-neurotoxic insecticide with a broad activity spectrum.Journal of Plant Diseases and Protection,88,269-275.
El-Sheikh E A,Mamtha M D,Ragheb D A,Ashour M B A.2011.Potential of juvenile hormone esterase as a bio-insecticide:An overview.Egyptian Journal of Biological Pest Control,21,103-110.
El-Sheikh E S A,Kamita S G,Vu K,Hammock B D.2011.Improved insecticidal efficacy of a recombinant baculovirus expressing mutated JH esterase from Manduca sexta.Biological Control,58,354-361.
Feng Q L,Ladd T R,Tomkins B L,Sundaram M,Sohi S S,Retnakaran A,Davey K G,Palli S R.1999.Spruce budworm(Choristoneura fumiferana)juvenile hormone esterase:Hormonal regulation,developmental expression and cDNAcloning.Molecular and Cellular Endocrinology,148,95-108.
Gelbi?I,Sehnal F.1973.Effects of juvenile hormone mimics on the codling moth Cydia pomonella(L.)(Lep.,Olethreutidae).Bulletin of Entomological Research,63,7-16.
Ghosh D,Wawrzak Z,Pletnev V Z,Li N Y,Kaiser R,Pangborn W,Jornvall H,Erman M,Duax W L.1995.Structure of uncomplexed and linoleate-bound Candida ylindracea cholesterol esterase.Structure,3,279-288.
Giray T,Giovanetti M,West-Eberhard M J.2005.Juvenile hormone,reproduction,and worker behavior in the neotropical social wasp Polistes canadensis.Proceedings of the National Academy of Sciences of the United States of America,102,3330-3335.
Gu X,Kumar S,Kim E,Kim Y.2015.A whole genome screening and RNA interference identify a juvenile hormone esteraselike gene of the diamondback moth,Plutella xylostella.Journal of Insect Physiology,80,81-87.
Hammock B D,Sparks T C.1977.A rapid assay for insect juvenile hormone esterase activity.Analytical Biochemistry,82,573-579.
Hanzlik T N,Abdel-Aal Y,Harshman L G,Hammock B D.1989.Isolation and sequencing of cDNA clones coding for juvenile hormone esterase from Heliothis virescens.Evidence for a catalytic mechanism for the serine carboxylesterases different from that of the serine proteases.Journal of Biological Chemistry,264,12419-12425.
Hinton A C,Hammock B D.2001.Purification of juvenile hormone esterase and molecular cloning of the cDNAfrom Manduca sexta.Insect Biochemistry and Molecular Biology,32,57-66.
Hinton A C,Hammock B D.2003.Juvenile hormone esterase(JHE)from Tenebrio molitor:full-length cDNA sequence,in vitro expression,and characterization of the recombinant protein.Insect Biochemistry and Bolecular Biology,33,477-487.
Hirai M,Kamimura M,Kikuchi K,Yasukochi Y,Kiuchi M,Shinoda T,Shiotsuki T.2002.cDNA cloning and characterization of Bombyx mori juvenile hormone esterase:An inducible gene by the imidazole insect growth regulator KK-42.Insect Biochemistry and Molecular Biology,32,627-635.
Huang X L,Liu L,Su X J,Feng J N.2016.Identification of biotransformation enzymes in the antennae of codling moth Cydia pomonella.Gene,580,73-79.
Jindra M,Palli S R,Riddiford L M.2013.The juvenile hormone signaling pathway in insect development.Annual Review of Entomology,58,181-204.
Kamita S G,Hammock B D.2010.Juvenile hormone esterase:Biochemistry and structure.Journal of Pesticide Science,35,265-274.
Kamita S G,Samra A I,Liu J Y,Cornel A J,Hammock B D.2011.Juvenile hormone(JH)esterase of the mosquito Culex quinquefasciatus is not a target of the JH analog insecticide methoprene.PLoS ONE,6,e28392.
Kamita S G,Wogulis M D,Law C S,Morisseau C,Tanaka H,Huang H Z,Wilson D K,Hammock B D.2010.Function of phenylalanine 259 and threonine 314 within the substrate binding pocket of the juvenile hormone esterase of Manduca sexta.Biochemistry,49,3733-3742.
Katoh K,Standley D M.2013.MAFFT multiple sequence alignment software version 7:Improvements in performance and usability.Molecular Biology and Evolution,30,772-780.
Kelley L A,Mezulis S,Yates C M,Wass M N,Sternberg M J E.2015.The Phyre2 web portal for protein modeling,prediction and analysis.Nature Protocols,10,845-858.
de Kort C A D,Granger N A.1996.Regulation of JH titers:The relevance of degradative enzymes and binding proteins.Archives of Insect Biochemistry and Physiology,33,1-26.
Kumar S,Neven L G,Zhu H,Zhang R.2015.Assessing the global risk of establishment of Cydia pomonella(Lepidoptera:Tortricidae)using CLIMEX and MaxEnt niche models.Journal of Economic Entomology,108,1708-1719.
Kumar S,Stecher G,Tamura K.2016.MEGA7:Molecular evolutionary genetics analysis version 7.0 for bigger datasets.Molecular Biology and Evolution,33,1870-1874.
LeBoeuf A C,Cohanim A B,Stoffel C,Brent C S,Waridel P,Privman E,Keller L,Benton R.2018.Molecular evolution of juvenile hormone esterase-like proteins in a socially exchanged fluid.Scientific Reports,8,17830.
Li S,Falabella P,Kuriachan I,Vinson S B,Borst D W,Malva C,Pennacchio F.2003.Juvenile hormone synthesis,metabolism,and resulting haemolymph titre in Heliothis virescens larvae parasitized by Toxoneuron nigriceps.Journal of Insect Physiology,49,1021-1030.
Li S,Zhang Q R,Xu W H,Schooley D A.2005.Juvenile hormone diol kinase,a calcium-binding protein with kinase activity,from the silkworm,Bombyx mori.Insect Biochemistry and Molecular Biology,35,1235-1248.
Liu S H,Yangb B J,Go J H,Yao X M,Zhang Y X,Song F,Liu Z W.2008.Molecular cloning and characterization of a juvenile hormone esterase gene from brown planthopper,Nilaparvata lugens.Journal of Insect Physiology,54,1495-1502.
Long C,Guo J,Wan F.2013.Molecular cloning,sequence analysis and developmental expression of cDNA fragment of juvenile hormone esterase from the whitefly Bemisia tabaci MED(Hemiptera:Aleyrodidae).Acta Entomologica Sinica,56,234-242.(in Chinese)
Mackert A,do Nascimento A M,Bitondi M M G,Hartfelder K,Simoes Z L P.2008.Identification of a juvenile hormone esterase-like gene in the honey bee,Apis mellifera L.-Expression analysis and functional assays.Comparative Biochemistry and Physiology(B:Biochemistry&Molecular Biology),150,33-44.
Mancheno J M,Pernas M A,Martinez M J,Ochoa B,Rua ML,Hermoso J A.2003.Structural insights into the lipase/esterase behavior in the Candida rugosa lipases family:Crystal structure of the lipase 2 isoenzyme at 1.97 angstrom resolution.Journal of Molecular Biology,332,1059-1069.
Munyiri F N,Ishikawa Y.2007.Molecular cloning and developmental expression of the gene encoding juvenile hormone esterase in the yellow-spotted longicorn beetle,Psacothea hilaris.Insect Biochemistry and Molecular Biology,37,497-505.
Pasquier D,Charmillot P J.2004.Effectiveness of twelve insecticides applied topically to diapausing larvae of the codling moth,Cydia pomonella L.Pest Management Science,60,305-308.
Reuveny H,Cohen E.2004.Resistance of the codling moth Cydia pomonella(L.)(Lep.,Tortricidae)to pesticides in Israel.Journal of Applied Entomology,128,645-651.
Robert X,Gouet P.2014.Deciphering key features in protein structures with the new ENDscript server.Nucleic Acids Research,42,W320-W324.
Rodriguez M A,Bosch D,Avilla J.2011.Resistance of Spanish codling moth(Cydia pomonella)populations to insecticides and activity of detoxifying enzymatic systems.Entomologia Experimentalis et Applicata,138,184-192.
Saito Y,Kamita S G,Hammock B D,Kunimi Y,Inoue M N,Nakai M.2015.Juvenile hormone(JH)esterase activity but not JH epoxide hydrolase activity is downregulated in larval Adoxophyes honmai following nucleopolyhedroviruses infection.Journal of Insect Physiology,80,71-80.
Sauphanor B,Bouvier J C.1995.Cross-resistance between benzoylureas and benzoylhydrazines in the codling moth,Cydia pomonella L.Pesticide Science,45,369-375.
Seino A,Ogura T,Tsubota T,Shimomura M,Nakakura T,Tan A,Mita K,Shinoda T,Nakagawa Y,Shiotsuki T.2010.Characterization of juvenile hormone epoxide hydrolase and related genes in the larval development of the silkworm Bombyx mori.Bioscience Biotechnology and Biochemistry,74,1421-1429.
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Anand A,Crone E J,Zera A J.2008.Tissue and stage-specific juvenile hormone esterase(JHE)and epoxide hydrolase(JHEH)enzyme activities and Jhe transcript abundance in lines of the cricket Gryllus assimilis artificially selected for plasma JHE activity:Implications for JHE microevolution.Journal of Insect Physiology,54,1323-1331.
Bai H,Ramaseshadri P,Palli S R.2007.Identification and characterization of juvenile hormone esterase gene from the yellow fever mosquito,Aedes aegypti.Insect Biochemistry and Molecular Biology,37,829-837.
Belles X,Martin D,Piulachs M D.2005.The mevalonate pathway and the synthesis of juvenile hormone in insects.Annual Review of Entomology,50,181-199.
Campbell P M,Harcourt R L,Crone E J,Claudianos C,Hammock B D,Russell R J,Oakeshott J G.2001.Identification of a juvenile hormone esterase gene by matching its peptide mass fingerprint with a sequence from the Drosophila genome project.Insect Biochemistry and Molecular Biology,31,513-520.
Chang E S.1993.Comparative endocrinology of molting and reproduction:Insects and crustaceans.Annual Review of Entomology,38,161-180.
Charmillot P J,Bloesch B,Benz M.1989.Control of the codling moth Cydia pomonella L.with fenoxycarb and teflubenzuron.Revue Suisse de Viticulture,d’Arboriculture et d’Horticulture,21,187-193.(in French)
Charmillot P J,Pasquier D,Hofer D.2002.Control of codling moth Cydia pomonella by autosterilisation.IOBC WPRSBulletin,25,117-120.
Crone E J,Zera A J,Anand A,Oakeshott J G,Sutherland T D,Russell R J,Harshman L G,Hoffmann F G,Claudianos C.2007.JHE in Gryllus assimilis:Cloning,sequence-activity associations and phylogeny.Insect Biochemistry and Molecular Biology,37,1359-1365.
Denlinger D L,Armbruster P A.2014.Mosquito diapause.Annual Review of Entomology,59,73-93.
Dorn S,Frischknecht M L,Martinez V,Zurflüh R,Fischer U.1981.A novel non-neurotoxic insecticide with a broad activity spectrum.Journal of Plant Diseases and Protection,88,269-275.
El-Sheikh E A,Mamtha M D,Ragheb D A,Ashour M B A.2011.Potential of juvenile hormone esterase as a bio-insecticide:An overview.Egyptian Journal of Biological Pest Control,21,103-110.
El-Sheikh E S A,Kamita S G,Vu K,Hammock B D.2011.Improved insecticidal efficacy of a recombinant baculovirus expressing mutated JH esterase from Manduca sexta.Biological Control,58,354-361.
Feng Q L,Ladd T R,Tomkins B L,Sundaram M,Sohi S S,Retnakaran A,Davey K G,Palli S R.1999.Spruce budworm(Choristoneura fumiferana)juvenile hormone esterase:Hormonal regulation,developmental expression and cDNAcloning.Molecular and Cellular Endocrinology,148,95-108.
Gelbi?I,Sehnal F.1973.Effects of juvenile hormone mimics on the codling moth Cydia pomonella(L.)(Lep.,Olethreutidae).Bulletin of Entomological Research,63,7-16.
Ghosh D,Wawrzak Z,Pletnev V Z,Li N Y,Kaiser R,Pangborn W,Jornvall H,Erman M,Duax W L.1995.Structure of uncomplexed and linoleate-bound Candida ylindracea cholesterol esterase.Structure,3,279-288.
Giray T,Giovanetti M,West-Eberhard M J.2005.Juvenile hormone,reproduction,and worker behavior in the neotropical social wasp Polistes canadensis.Proceedings of the National Academy of Sciences of the United States of America,102,3330-3335.
Gu X,Kumar S,Kim E,Kim Y.2015.A whole genome screening and RNA interference identify a juvenile hormone esteraselike gene of the diamondback moth,Plutella xylostella.Journal of Insect Physiology,80,81-87.
Hammock B D,Sparks T C.1977.A rapid assay for insect juvenile hormone esterase activity.Analytical Biochemistry,82,573-579.
Hanzlik T N,Abdel-Aal Y,Harshman L G,Hammock B D.1989.Isolation and sequencing of cDNA clones coding for juvenile hormone esterase from Heliothis virescens.Evidence for a catalytic mechanism for the serine carboxylesterases different from that of the serine proteases.Journal of Biological Chemistry,264,12419-12425.
Hinton A C,Hammock B D.2001.Purification of juvenile hormone esterase and molecular cloning of the cDNAfrom Manduca sexta.Insect Biochemistry and Molecular Biology,32,57-66.
Hinton A C,Hammock B D.2003.Juvenile hormone esterase(JHE)from Tenebrio molitor:full-length cDNA sequence,in vitro expression,and characterization of the recombinant protein.Insect Biochemistry and Bolecular Biology,33,477-487.
Hirai M,Kamimura M,Kikuchi K,Yasukochi Y,Kiuchi M,Shinoda T,Shiotsuki T.2002.cDNA cloning and characterization of Bombyx mori juvenile hormone esterase:An inducible gene by the imidazole insect growth regulator KK-42.Insect Biochemistry and Molecular Biology,32,627-635.
Huang X L,Liu L,Su X J,Feng J N.2016.Identification of biotransformation enzymes in the antennae of codling moth Cydia pomonella.Gene,580,73-79.
Jindra M,Palli S R,Riddiford L M.2013.The juvenile hormone signaling pathway in insect development.Annual Review of Entomology,58,181-204.
Kamita S G,Hammock B D.2010.Juvenile hormone esterase:Biochemistry and structure.Journal of Pesticide Science,35,265-274.
Kamita S G,Samra A I,Liu J Y,Cornel A J,Hammock B D.2011.Juvenile hormone(JH)esterase of the mosquito Culex quinquefasciatus is not a target of the JH analog insecticide methoprene.PLoS ONE,6,e28392.
Kamita S G,Wogulis M D,Law C S,Morisseau C,Tanaka H,Huang H Z,Wilson D K,Hammock B D.2010.Function of phenylalanine 259 and threonine 314 within the substrate binding pocket of the juvenile hormone esterase of Manduca sexta.Biochemistry,49,3733-3742.
Katoh K,Standley D M.2013.MAFFT multiple sequence alignment software version 7:Improvements in performance and usability.Molecular Biology and Evolution,30,772-780.
Kelley L A,Mezulis S,Yates C M,Wass M N,Sternberg M J E.2015.The Phyre2 web portal for protein modeling,prediction and analysis.Nature Protocols,10,845-858.
de Kort C A D,Granger N A.1996.Regulation of JH titers:The relevance of degradative enzymes and binding proteins.Archives of Insect Biochemistry and Physiology,33,1-26.
Kumar S,Neven L G,Zhu H,Zhang R.2015.Assessing the global risk of establishment of Cydia pomonella(Lepidoptera:Tortricidae)using CLIMEX and MaxEnt niche models.Journal of Economic Entomology,108,1708-1719.
Kumar S,Stecher G,Tamura K.2016.MEGA7:Molecular evolutionary genetics analysis version 7.0 for bigger datasets.Molecular Biology and Evolution,33,1870-1874.
LeBoeuf A C,Cohanim A B,Stoffel C,Brent C S,Waridel P,Privman E,Keller L,Benton R.2018.Molecular evolution of juvenile hormone esterase-like proteins in a socially exchanged fluid.Scientific Reports,8,17830.
Li S,Falabella P,Kuriachan I,Vinson S B,Borst D W,Malva C,Pennacchio F.2003.Juvenile hormone synthesis,metabolism,and resulting haemolymph titre in Heliothis virescens larvae parasitized by Toxoneuron nigriceps.Journal of Insect Physiology,49,1021-1030.
Li S,Zhang Q R,Xu W H,Schooley D A.2005.Juvenile hormone diol kinase,a calcium-binding protein with kinase activity,from the silkworm,Bombyx mori.Insect Biochemistry and Molecular Biology,35,1235-1248.
Liu S H,Yangb B J,Go J H,Yao X M,Zhang Y X,Song F,Liu Z W.2008.Molecular cloning and characterization of a juvenile hormone esterase gene from brown planthopper,Nilaparvata lugens.Journal of Insect Physiology,54,1495-1502.
Long C,Guo J,Wan F.2013.Molecular cloning,sequence analysis and developmental expression of cDNA fragment of juvenile hormone esterase from the whitefly Bemisia tabaci MED(Hemiptera:Aleyrodidae).Acta Entomologica Sinica,56,234-242.(in Chinese)
Mackert A,do Nascimento A M,Bitondi M M G,Hartfelder K,Simoes Z L P.2008.Identification of a juvenile hormone esterase-like gene in the honey bee,Apis mellifera L.-Expression analysis and functional assays.Comparative Biochemistry and Physiology(B:Biochemistry&Molecular Biology),150,33-44.
Mancheno J M,Pernas M A,Martinez M J,Ochoa B,Rua ML,Hermoso J A.2003.Structural insights into the lipase/esterase behavior in the Candida rugosa lipases family:Crystal structure of the lipase 2 isoenzyme at 1.97 angstrom resolution.Journal of Molecular Biology,332,1059-1069.
Munyiri F N,Ishikawa Y.2007.Molecular cloning and developmental expression of the gene encoding juvenile hormone esterase in the yellow-spotted longicorn beetle,Psacothea hilaris.Insect Biochemistry and Molecular Biology,37,497-505.
Pasquier D,Charmillot P J.2004.Effectiveness of twelve insecticides applied topically to diapausing larvae of the codling moth,Cydia pomonella L.Pest Management Science,60,305-308.
Reuveny H,Cohen E.2004.Resistance of the codling moth Cydia pomonella(L.)(Lep.,Tortricidae)to pesticides in Israel.Journal of Applied Entomology,128,645-651.
Robert X,Gouet P.2014.Deciphering key features in protein structures with the new ENDscript server.Nucleic Acids Research,42,W320-W324.
Rodriguez M A,Bosch D,Avilla J.2011.Resistance of Spanish codling moth(Cydia pomonella)populations to insecticides and activity of detoxifying enzymatic systems.Entomologia Experimentalis et Applicata,138,184-192.
Saito Y,Kamita S G,Hammock B D,Kunimi Y,Inoue M N,Nakai M.2015.Juvenile hormone(JH)esterase activity but not JH epoxide hydrolase activity is downregulated in larval Adoxophyes honmai following nucleopolyhedroviruses infection.Journal of Insect Physiology,80,71-80.
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