Characterization and Functional Analysis of Related to Chitin Metabolism in Walker (Lepidoptera: Pyralidae)

Overview

Journal Insects

Specialty Biology

Date 2021 Apr 30

PMID 33924270

Citations 6

Authors

Zuo-Min Shao

Jian-Hao Ding

De-Lei Jiang

Zhi-Xiang Liu

Yi-Jiangcheng Li

Jiao Wang

Jun Wang

Sheng Sheng

Fu-An Wu

Affiliations

Soon will be listed here.

Abstract

Walker () is a serious pest on mulberry. Due to the increasing pesticide resistance, the development of new and effective environmental methods to control is needed. Trehalase is an essential enzyme in trehalose hydrolysis and energy supply, and it has been considered a promising target for insect pest control. However, the specific function of in has not been reported. In this study, two trehalase genes ( and ) were identified from our previous transcriptome database. The functions of the in chitin metabolism were studied by injecting larvae with dsRNAs and trehalase inhibitor, Validamycin A. The open reading frames (ORFs) of GpTre1 and GpTre2 were 1,704 bp and 1,869 bp, which encoded 567 and 622 amino acid residues, respectively. Both of and were mainly expressed in the head and midgut. The highest expression levels of them were in 5th instar during different development stages. Moreover, knockdown both of and by the dsRNAs led to significantly decreased expression of chitin metabolism pathway-related genes, including , , , , , , , , and , and abnormal phenotypes. Furthermore, the trehalase inhibitor, Validamycin A, treatment increased the expressions of and , increased content of trehalose, and decreased the levels of glycogen and glucose. Additionally, the inhibitor caused a significantly increased cumulative mortality of larvae on the 2nd (16%) to 6th (41.3%) day, and decreased the rate of cumulative pupation (72.3%) compared with the control group (95.6%). After the activities of trehalase were suppressed, the expressions of 6 integument chitin metabolism-related genes decreased significantly at 24 h and increased at 48 h. The expressions of and , involved in chitin metabolism pathway of peritrophic membrane in the midgut, increased at 24 h and 48 h, and there were no changes to and . These results reveal that and play an essential role in the growth of by affecting chitin metabolism, and this provides useful information for insect pest control in the future.

Citing Articles

Knockdown of the Expression of Two Trehalase Genes with RNAi Disrupts the Trehalose and Chitin Metabolism Pathways in the Oriental Armyworm, .

Yang H, Wang Y, Zhang W, Zhang X, Wang S, Cui M Insects. 2024; 15(3).

PMID: 38535338 PMC: 10971163. DOI: 10.3390/insects15030142.

Validamycin Inhibits the Synthesis and Metabolism of Trehalose and Chitin in the Oriental Fruit Fly, (Hendel).

Li Y, Xu Y, Wu S, Wang B, Li Y, Liu Y Insects. 2023; 14(8).

PMID: 37623381 PMC: 10455558. DOI: 10.3390/insects14080671.

Knockdown of Two Trehalase Genes by RNA Interference Is Lethal to the White-Backed Planthopper (Horváth) (Hemiptera: Delphacidae).

Wang Z, Long G, Jin D, Yang H, Zhou C, Yang X Biomolecules. 2022; 12(11).

PMID: 36421713 PMC: 9687761. DOI: 10.3390/biom12111699.

The Effect of Ice-Nucleation-Active Bacteria on Metabolic Regulation in (Scopoli) (Lepidoptera: Pyralidae) Overwintering Larvae on the Qinghai-Tibet Plateau.

Shao H, Liu Y, Liu Y, Lai Y Insects. 2022; 13(10).

PMID: 36292857 PMC: 9604135. DOI: 10.3390/insects13100909.

Purification and Functional Characterization of a Soluble Trehalase in (Coleoptera: Curculionidae).

Wang Q, Fang K, Qi L, Wang X, Pan Y, Li Y Insects. 2022; 13(10).

PMID: 36292815 PMC: 9604388. DOI: 10.3390/insects13100867.

References

Zhao L, Yang M, Shen Q, Liu X, Shi Z, Wang S . Functional characterization of three trehalase genes regulating the chitin metabolism pathway in rice brown planthopper using RNA interference. Sci Rep. 2016; 6:27841. PMC: 4916506. DOI: 10.1038/srep27841. View

Zhang L, Qiu L, Yang H, Wang H, Zhou M, Wang S . Study on the Effect of Wing Bud Chitin Metabolism and Its Developmental Network Genes in the Brown Planthopper, , by Knockdown of Gene. Front Physiol. 2017; 8:750. PMC: 5627005. DOI: 10.3389/fphys.2017.00750. View

Bansal R, Mian M, Mittapalli O, Michel A . Molecular characterization and expression analysis of soluble trehalase gene in Aphis glycines, a migratory pest of soybean. Bull Entomol Res. 2013; 103(3):286-95. DOI: 10.1017/S0007485312000697. View

Bai L, Li L, Xu H, Minagawa K, Yu Y, Zhang Y . Functional analysis of the validamycin biosynthetic gene cluster and engineered production of validoxylamine A. Chem Biol. 2006; 13(4):387-97. PMC: 1474575. DOI: 10.1016/j.chembiol.2006.02.002. View

Ge L, Zhao K, Huang L, Wu J . The effects of triazophos on the trehalose content, trehalase activity and their gene expression in the brown planthopper Nilaparvata lugens (Stål) (Hemiptera: Delphacidae). Pestic Biochem Physiol. 2011; 100(2):172-181. PMC: 3102831. DOI: 10.1016/j.pestbp.2011.03.007. View

Chen J, Tang B, Chen H, Yao Q, Huang X, Chen J . Different functions of the insect soluble and membrane-bound trehalase genes in chitin biosynthesis revealed by RNA interference. PLoS One. 2010; 5(4):e10133. PMC: 2853572. DOI: 10.1371/journal.pone.0010133. View

Tatun N, Singtripop T, Sakurai S . Dual control of midgut trehalase activity by 20-hydroxyecdysone and an inhibitory factor in the bamboo borer Omphisa fuscidentalis Hampson. J Insect Physiol. 2007; 54(2):351-7. DOI: 10.1016/j.jinsphys.2007.10.006. View

Gu J, Shao Y, Zhang C, Liu Z, Zhang Y . Characterization of putative soluble and membrane-bound trehalases in a hemipteran insect, Nilaparvata lugens. J Insect Physiol. 2009; 55(11):997-1002. DOI: 10.1016/j.jinsphys.2009.07.003. View

Shukla E, Thorat L, Nath B, Gaikwad S . Insect trehalase: physiological significance and potential applications. Glycobiology. 2014; 25(4):357-67. DOI: 10.1093/glycob/cwu125. View

10.

Shao Z, Li Y, Zhang X, Chu J, Ma J, Liu Z . Identification and Functional Study of Chitin Metabolism and Detoxification-Related Genes in Walker (Lepidoptera: Pyralidae) Based on Transcriptome Analysis. Int J Mol Sci. 2020; 21(5). PMC: 7084822. DOI: 10.3390/ijms21051904. View

11.

Marten A, Stothard A, Kalera K, Swarts B, Conway M . Validamycin A Delays Development and Prevents Flight in Aedes aegypti (Diptera: Culicidae). J Med Entomol. 2020; 57(4):1096-1103. PMC: 7334893. DOI: 10.1093/jme/tjaa004. View

12.

Su H, Gao Y, Liu Y, Li X, Liang Y, Dai X . Comparative transcriptome profiling reveals candidate genes related to insecticide resistance of . Bull Entomol Res. 2019; 110(1):57-67. DOI: 10.1017/S0007485319000257. View

13.

Gu Z, Li M, Xia S, Mao T, Lu Z, Chen J . Effects of sublethal phoxim exposure and lower food intake on nutrient metabolism in the midguts of Bombyx mori. Pestic Biochem Physiol. 2020; 167:104593. DOI: 10.1016/j.pestbp.2020.104593. View

14.

Tang B, Chen X, Liu Y, Tian H, Liu J, Hu J . Characterization and expression patterns of a membrane-bound trehalase from Spodoptera exigua. BMC Mol Biol. 2008; 9:51. PMC: 2424068. DOI: 10.1186/1471-2199-9-51. View

15.

Tang B, Wei P, Zhao L, Shi Z, Shen Q, Yang M . Knockdown of five trehalase genes using RNA interference regulates the gene expression of the chitin biosynthesis pathway in Tribolium castaneum. BMC Biotechnol. 2016; 16(1):67. PMC: 5011928. DOI: 10.1186/s12896-016-0297-2. View

16.

Chen X, Quan Y, Wang H, Luo H . Trehalase regulates neuroepithelial stem cell maintenance and differentiation in the Drosophila optic lobe. PLoS One. 2014; 9(7):e101433. PMC: 4086926. DOI: 10.1371/journal.pone.0101433. View

17.

Yang M, Zhao L, Shen Q, Xie G, Wang S, Tang B . Knockdown of two trehalose-6-phosphate synthases severely affects chitin metabolism gene expression in the brown planthopper Nilaparvata lugens. Pest Manag Sci. 2016; 73(1):206-216. DOI: 10.1002/ps.4287. View

18.

Liebl M, Nelius V, Kamp G, Ando O, Wegener G . Fate and effects of the trehalase inhibitor trehazolin in the migratory locust (Locusta migratoria). J Insect Physiol. 2009; 56(6):567-74. DOI: 10.1016/j.jinsphys.2009.11.021. View

19.

Li Y, Chen X, Wang S, Pan B, Wang S, Wang S . Evaluation of the Expression and Function of the and Genes in Ecdysis of . Front Physiol. 2019; 10:1371. PMC: 6839538. DOI: 10.3389/fphys.2019.01371. View

20.

Adhav A, Kokane S, Joshi R . Functional characterization of Helicoverpa armigera trehalase and investigation of physiological effects caused due to its inhibition by Validamycin A formulation. Int J Biol Macromol. 2018; 112:638-647. DOI: 10.1016/j.ijbiomac.2018.01.221. View