Characterization and functional analysis of chitinase family genes involved in nymph-adult transition of Sogatella furcifera.
Acetylglucosaminidase
/ genetics
Animal Shells
/ embryology
Animals
Chitinases
/ genetics
Gene Expression Regulation, Developmental
Genes, Insect
Hemiptera
/ embryology
Imaginal Discs
/ embryology
Intercellular Signaling Peptides and Proteins
/ genetics
Metamorphosis, Biological
/ genetics
Molting
/ genetics
Nymph
/ growth & development
Wings, Animal
/ embryology
RNA interference
Sogatella furcifera
chitin deacetylase
chitin synthesis
chitinase
wing development
Journal
Insect science
ISSN: 1744-7917
Titre abrégé: Insect Sci
Pays: Australia
ID NLM: 101266965
Informations de publication
Date de publication:
Aug 2021
Aug 2021
Historique:
revised:
04
06
2020
received:
25
04
2020
accepted:
07
06
2020
pubmed:
15
6
2020
medline:
10
8
2021
entrez:
15
6
2020
Statut:
ppublish
Résumé
Chitinase degrades chitin in the old epidermis or peritrophic matrix of insects, which ensures normal development and metamorphosis. In our previous work, we comprehensively studied the function of SfCht7 in Sogatella furcifera. However, the number and function of chitinase genes in S. furcifera remain unknown. Here, we identified 12 full-length chitinase transcripts from S. furcifera, which included nine chitinase (Cht), two imaginal disc growth factor (IDGF), and one endo-β-N-acetylglucosaminidase (ENGase) genes. Expression analysis results revealed that the expression levels of eight genes (SfCht3, SfCht5, SfCht6-1, SfCht6-2, SfCht7, SfCht8, SfCht10, and SfIDGF2) with similar transcript levels peaked prior to molting of each nymph and were highly expressed in the integument. Based on RNA interference (RNAi), description of the functions of each chitinase gene indicated that the silencing of SfCht5, SfCht10, and SfIDGF2 led to molting defects and lethality. RNAi inhibited the expressions of SfCht5, SfCht7, SfCht10, and SfIDGF2, which led to downregulated expressions of chitin synthase 1 (SfCHS1, SfCHS1a, and SfCHS1b) and four chitin deacetylase genes (SfCDA1, SfCDA2, SfCDA3, and SfCDA4), and caused a change in the expression level of two trehalase genes (TRE1 and TRE2). Furthermore, silencing of SfCht7 induced a significant decrease in the expression levels of three wing development-related genes (SfWG, SfDpp, and SfHh). In conclusion, SfCht5, SfCht7, SfCht10, and SfIDGF2 play vital roles in nymph-adult transition and are involved in the regulation of chitin metabolism, and SfCht7 is also involved in wing development; therefore, these genes are potential targets for control of S. furcifera.
Identifiants
pubmed: 32536018
doi: 10.1111/1744-7917.12839
doi:
Substances chimiques
Intercellular Signaling Peptides and Proteins
0
Chitinases
EC 3.2.1.14
Acetylglucosaminidase
EC 3.2.1.52
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
901-916Subventions
Organisme : National Natural Science Foundation of China
ID : 31960537
Organisme : National Natural Science Foundation of China
ID : 31560522
Organisme : Provincial Key Project for Agricultural Science and Technology of Guizhou
ID : NY 20133006
Organisme : International Cooperation Base for Insect Evolutionary Biology and Pest Control
ID : [2016] 5802
Informations de copyright
© 2020 Institute of Zoology, Chinese Academy of Sciences.
Références
Arakane, Y., Dixit, R., Begum, K., Park, Y. and Specht, C.A. (2009) Analysis of functions of the chitin deacetylase gene family in Tribolium castaneum. Insect Biochemistry and Molecular Biology, 39, 355-365.
Arakane, Y. and Muthukrishnan, S. (2010) Insect chitinase and chitinase-like proteins. Cellular and Molecular Life Sciences, 67, 201-216.
Chen, C., Yang, H., Tang, B., Yang W.J., Jin, D.C. (2017) Identification and functional analysis of chitinase 7 gene in white-backed planthopper, Sogatella furcifera. Comparative Biochemistry and Physiology, Part B, 208-209, 19-28.
Dong, W., Gao, Y.H., Zhang, X.B., Moussian, B. and Zhang, J.Z. (2020) Chitinase 10 controls chitin amounts and organization in the wing cuticle of Drosophila. Insect Science, 27, 1198-1207.
Funkhouser, J.D. and Aronson, N.N. (2007) Chitinase family GH18: evolutionary insights from the genomic history of a diverse protein family. BMC Evolutionary Biology, 7, 96.
Gu, X.Y., Li, Z.H., Su, Y., Zhao, Y. and Liu, L.J. (2019) Imaginal disc growth factor 4 regulates development and temperature adaptation in Bactrocera dorsalis. Scientific Reports, 9, 931. https://doi.org/10.1038/s41598-018-37414-9.
Ganbaatar, O., Cao, B., Zhang, Y., Bao, D., Bao, W. and Wuriyanghan, H. (2017) Knockdown of Mythimna separata chitinase genes via bacterial expression and oral delivery of RNAi effectors. BMC Biotechnology, 17, 9.
Hale, R., Brittle, A.L., Fisher, K.H., Monk, N.A.M. and Strutt, D. (2015) Cellular interpretation of the long-range gradient of four-jointed activity in the Drosophila wing. eLife, 4, e05789.
Kramer, K.J., Corpuz, L., Choi, H.K. and Muthukrishnan, S. (1993) Sequence of a cDNA and expression of the gene encoding epidermal and gut chitinases of Manduca sexta. Insect Biochemistry and Molecular Biology, 23, 691-701.
Liu, S.H., Li, H.F., Yang, Y., Yang, R.L., Yang, W.J., Jiang, H.B. et al. (2018) Genome-wide identification of chitinase and chitin deacetylase gene families in the oriental fruit fly, Bactrocera dorsalis (Hendel). Comparative Biochemistry and Physiology-Part D, 27, 13-22.
Li, Y.L., Song, H.F., Zhang, X.Y., Li, D.Q., Zhang, T.T., Ma, EB. et al. (2016) Heterologous expression and characterization of two chitinase 5 enzymes from the migratory locust Locusta migratoria. Insect Science, 23, 406-416.
Li, D.Q., Zhang, J.Q., Wang, Y., Liu, X.J., Ma, E.B., Sun, T. et al. (2015) Two chitinase 5 genes from Locusta migratoria: molecular characteristics and functional differentiation. Insect Biochemistry and Molecular Biology, 58, 46-54.
Li, X., Liu, F.Z., Wu, C., Zhao, J., Cai, W.L. and Hua, H.X. (2019) Decapentaplegic function in wing vein development and wing morph transformation in brown planthopper, Nilaparvata lugens. Developmental Biology, 449, 143-150.
Livak, K.J. and Schmittgen, T.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCt Method. Methods, 25, 402-408.
Merzendorfer, H. (2013) Insect-derived Chitinases. Advances in Biochemical Engineering-biotechnology, 136, 19-50.
Muthukrishnan S, Arakane Y, Yang Q, Zhang CX, Zhang JZ, Zhang W. et al. (2018) Future questions in insect chitin biology: A microreview. Archives of Insect Biochemistry and Physiology, 98, e21454.
Mohamed, A.A., Omar, Y., Ao, M., Li, K., He, L., Xu, H. et al. (2019) The functional difference of eight chitinase genes between male and female of the cotton mealybug, Phenacoccus solenopsis. Insect Molecular Biology, 28, 550-567.
Nakabachi, A., Shigenobu, S. and Miyagishima, S. (2010) Chitinase-like proteins encoded in the genome of the pea aphid, Acyrthosiphon pisum. Insect Molecular Biology, 19, 175-185.
Nakao, T. (2017) Mechanisms of resistance to insecticides targeting RDL GABA receptors in planthoppers. NeuroToxicology, 60, 293-298.
Nakata, K.K., Chung, N.H. and Kobori, Y. (2019) Insecticide application and its effect on the density of rice planthoppers, Nilaparvata lugens and Sogatella furcifera, in paddy fields in the Red River Delta, Vietnam. Journal of Pesticide Science, 44, 129-135.
Niu, J., Shen, G., Christiaens, O., Smagghe, G., He, L. and Wang, J. (2018) Beyond insects: current status, achievements and future perspectives of RNAi in mite pests. Pest Management Science, 74, 2680-2687.
Neto-Silva, R.M., Wells, B S., Johnston, L.A. (2009) Mechanisms of growth and homeostasis in the Drosophila wing. Annual review of Cell and Developmental Biology, 25, 197-220.
Pan, Y., Lu, P., Wang, Y., Yin, L., Ma, H., Ma, H. et al. (2012) In silico identification of novel chitinase-like proteins in the silkworm, Bombyx mori, genome. Journal of Insect Science, 12, 1-14.
Pesch, Y.Y., Riedel, D., Patil, K.R., Loch, G. and Behr, M. (2016) Chitinases and Imaginal disc growth factors organize the extracellular matrix formation at barrier tissues in insects. Scientific Reports, 6, 18340.
Pesch, Y.Y., Riedel, D. and Behr, M. (2017) Drosophila Chitinase 2 is expressed in chitin producing organs for cuticle formation. Arthropod Structure & Development, 46, 4-12.
Su, C., Tu, G., Huang, S., Yang, Q., Shahzad, M.F. and Li, F. (2016) Genome-wide analysis of chitinase genes and their varied functions in larval moult, pupation and eclosion in the rice striped stem borer, Chilo suppressalis. Insect Molecular Biology, 25, 401-412.
Tang, B., Yang, M., Shen, Q., Xu, Y.X., Wang, H.J., Wang, S.G. et al. (2017) Suppressing the activity of trehalase with validamycin disrupts the trehalose and chitin biosynthesis pathways in the rice brown planthopper, Nilaparvata lugens. Pesticide Biochemistry and Physiology, 137, 81-90.
Tetreau, G., Cao, X., Chen, Y.R., Muthukrishnan, S., Jiang, H., Blissard, G.W. et al. (2015) Overview of chitin metabolism enzymes in Manduca sexta: Identification, domain organization, phylogenetic analysis and gene expression. Insect Biochemistry and Molecular Biology, 62, 114-126.
Tamura, K., Stecher, G., Peterson, D., Filipski, A. and Kumar, S. (2013) MEGA 6: Molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 30, 2725-2729.
Wang, Z., Yang, H., Zhou, C., Yang, W.J., Jin, D.Q. and Long, G.Y. (2019) Molecular cloning, expression, and functional analysis of the chitin synthase 1 gene and its two alternative splicing variants in the white-backed planthopper, Sogatella furcifera (Hemiptera: Delphacidae). Scientific Reports, 9, 1087.
Wang, L., Tang, N., Gao, X.L., Chang, Z.X. and Zhang, L.O. (2017) Genome sequence of a rice pest, the white-backed planthopper (Sogatella furcifera). GigaScience, 6, 1-9.
Whitten, M.M.A., Facey, P.D., DelSol, R., Fernández-Martínez, L.T., Evans, M.C., Mitchell, J.J. et al. (2016) Symbiont-mediated RNA interference in insects. Proceedings of the Royal Society B: Biological Sciences, 283, 20160042.
Wu, J.J., Mu, L.L., Chen, Z.C., Fu, K.Y., Guo, W.C., Li, C. et al. (2019a) Disruption of ecdysis in Leptinotarsa decemlineata by knockdown of chitin deacetylase 1. Journal of Asia-Pacific Entomology, 22, 443-452.
Wu, J.J., Chen, Z.C., Wang, Y.W., Fu, K.Y., Guo, W.C. and Li, G.Q. (2019b) Silencing chitin deacetylase 2 impairs larval-pupal and pupal-adult molts in Leptinotarsa decemlineata. Insect Molecular Biology, 28, 52-64.
Xi, Y., Pan, P.L., Ye, Y.X., Yu, B., Xu, H.J. and Zhang, C.X. (2015) Chitinase-like gene family in the brown planthopper, Nilaparvata lugens. Insect Molecular Biology, 24, 29-40.
Xi, Y., Pan, Y.X., Ye, B. and Zhang, C.X. (2014) Chitin deacetylase family genes in the brown planthopper, Nilaparvata lugens (Hemiptera: Delphacidae). Insect Molecular Biology, 23, 695-705.
Yang, W.J., Xu, K.K., Yan, X. and Li, C. (2019) Knockdown of β-N-acetylglucosaminidase 2 impairs molting and wing development in Lasioderma serricorne (Fabricius). Insects, 10, 396.
Yang, M.L., Wang, Y.L., Jiang, F., Song, T.Q., Wang, H.M., Zhang, J. et al. (2016) miR-71 and miR-263 jointly regulate target genes chitin synthase and chitinase to control Locust Molting. PLoS Genetics, 12, e1006257.
Yu, J.L., An, Z.F. and Liu, X.D. (2014) Wingless gene cloning and its role in manipulating the wing dimorphism in the white-backed planthopper, Sogatella furcifera. BMC Molecular Biology, 15, 1-9.
Yu, H.Z., Huang, Y.L., Lu, Z.J., Zhang, Q., Su, H.N., Du, Y.M. et al. (2021) Inhibition of trehalase affects the trehalose and chitin metabolism pathways in Diaphorina citri (Hemiptera: Psyllidae). Insect Science, 28, 718-734.
Zhu, C., Yang, H., Wang, Z., Long, G.Y. and Jin, D.C. (2018) Comparative transcriptome analysis of Sogatella furcifera (Horváth) exposed to different insecticides. Scientific Reports, 8, 8773.
Zhu, K.Y., Merzendorfer, H., Zhang, W.Q., Zhang, J.Z. and Muthukrishnan, S. (2016) Biosynthesis, turnover, and functions of chitin in insects. Annual Review of Entomology, 61, 177-196.
Zhu, B., Shan, J.P., Li, R., Liang, P. and Guo, X.W. (2019) Identification and RNAi-based function analysis of chitinase family genes in diamondback moth, Plutella xylostella. Pest Management Science, 75, 1951-1961.
Zhu, Q., Deng, Y, Vanka, P., Brown, S.J., Muthukrishnan, S. and Kramer, K.J. (2004) Computational identification of novel chitinase-like proteins in the Drosophila melanogaster genome. Bioinformatics, 20, 161-169.
Zhu, Q., Arakane, Y., Beeman, R.W., Kramer, K.J. and Muthukrishnan, S. (2008) Functional specialization among insect chitinase family genes revealed by RNA interference. Proceedings of the National Academy of Sciences USA, 105, 6650-6655.
Zhang, D., Chen, J., Yao, Q., Pan, Z., Chen, J. and Zhang, W. (2012) Functional analysis of two chitinase genes during the pupation and eclosion stages of the beet armyworm Spodoptera exigua by RNA interference. Archives of Insect Biochemistry and Physiology, 79, 220-234.
Zhang, J., Zhang, X., Arakane, Y., Muthukrishnan, S., Kramer, K.J., Ma, E. et al. (2011) Comparative genomic analysis of chitinase and chitinase-like genes in the African malaria mosquito (Anopheles gambiae). PLoS ONE, 6, e19899.
Zhang, T.T., Liu, W.W., Li, D.Q., Gao, L., Ma, E.B., Zhu, K.Y. et al. (2018) LmCht5-1 promotes pro-nymphal molting during locust embryonic development. Insect Biochemistry and Molecular Biology, 101, 124-130.
Zhang, L., Qiu, L.Y., Yang, H.L., Wang, H.J., Zhou, M., Wang, S.G. et al. (2017) Study on the effect of Wing bud chitin metabolism and its developmental network genes in the brown planthopper, Nilaparvata lugens, by knockdown of TRE gene. Frontiers in Physiology, 8, 750.
Zhao, X., Situ, G., He, K., Xiao, H., Su, C. and Li, F. (2018) Functional analysis of eight chitinase genes in rice stem borer and their potential application in pest control. Insect Molecular Biology, 27, 835-846.
Zhao, L.N., Yang, M.M., Shen, Q.D., Shi, Z.K., Wang, S.G. and Tang, B. (2016) Functional characterization of three trehalase genes regulating the chitin metabolism pathway in rice brown planthopper using RNA interference. Scientific Reports, 6, 27841.
Zhou, G.H., Wen, J.J., Cai, D.J., Lin, P., Xu, D.L. and Zhang, S.G. (2008) Southern rice black-streaked dwarf virus: a new proposed Fijivirus species in the family Reoviridae. Chinese Science Bulletin, 53, 3677-3685.