Molecular characterization and RNA interference responses of the lethal giant larvae gene in Diabrotica virgifera virgifera adults.

European corn borer RNA interference lethal giant larvae target gene selection western corn rootworm

Journal

Archives of insect biochemistry and physiology
ISSN: 1520-6327
Titre abrégé: Arch Insect Biochem Physiol
Pays: United States
ID NLM: 8501752

Informations de publication

Date de publication:
Jun 2021
Historique:
revised: 15 03 2021
received: 05 01 2021
accepted: 17 03 2021
pubmed: 20 4 2021
medline: 4 6 2021
entrez: 19 4 2021
Statut: ppublish

Résumé

High specificity for silencing target genes and single-copy target genes that yield clear phenotypes are two important factors for the success of RNA interference (RNAi). The lethal giant larvae (Lgl) gene appears to be an ideal gene for RNAi because RNAi can effectively suppress its expression and results in molting defects and mortality in Tribolium castaneum. To investigate the suitability of this gene for RNAi in other insects, we identified and characterized DvLgl from the western corn rootworm, Diabrotica virgifera virgifera, a species exhibiting high RNAi efficiency. DvLgl was expressed in all developmental stages and tissues investigated. The deduced DvLgl protein showed high amino-acid sequence identities and similar domain architecture to Lgls from other insect species. Despite many similarities among insect Lgls, RNAi-mediated suppression of DvLgl failed to produce a phenotype in D. v. virgifera adults. The difference in developing phenotypes could be attributed greatly to the level of gene suppression and the insect developmental stages for RNAi. These results highlight the variability in RNAi response among insects and showcase the importance of screening multiple target genes when conducting RNAi studies. Our findings are expected to help the design of future RNAi studies and future investigations of Lgl in insects.

Identifiants

pubmed: 33871104
doi: 10.1002/arch.21787
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e21787

Subventions

Organisme : U.S. Department of Agriculture
ID : 2014-67013-21714

Informations de copyright

© 2021 Wiley Periodicals LLC.

Références

Almagor, L., Ufimtsev, I. S., Ayer, A., Li, J., & Weis, W. I. (2019). Structural insights into the aPKC regulatory switch mechanism of the human cell polarity protein lethal giant larvae 2. Proceedings of the National Academy of Sciences of the United States of America, 116, 10804-10812. https://doi.org/10.1073/pnas.1821514116
Baum, J. A., Bogaert, T., Clinton, W., Heck, G. R., Feldmann, P., Ilagan, O., Johnson, S., Plaetinck, G., Munyikwa, T., Pleau, M., Vaughn, T., & Robrets, J. (2007). Control of coleopteran insect pests through RNA interference. Nature Biotechnology, 25, 1322-1326. https://doi.org/10.1038/nbt1359
Betschinger, J., Eisenhaber, F., & Knoblich, J. A. (2005). Phosphorylation-induced autoinhibition regulates the cytoskeletal protein lethal (2) giant larvae. Current Biology, 3, 276-282. https://doi.org/10.1016/j.cub.2005.01.012
Bona, A. C. D., Chitolina, R. F., Fermino, M. L., de Castro Poncio, L., Weiss, A., Lima, J. B. P., Paldi, N., Bernardes, E. S., Henen, J., & Maori, E. (2016). Larval application of sodium channel homologous dsRNA restores pyrethroid insecticide susceptibility in a resistant adult mosquito population. Parasites Vectors, 9, 397. https://doi.org/10.1186/s13071-016-1634-y
Borel, B. (2017). When the pesticides run out. Nature, 543, 302-304.
Bustin, S. A., Benes, V., Garson, J. A., Hellemans, J., Huggett, J., Kubista, M., Mueller, R., Nolan, T., Pfaffl, M. W., Shipley, G. L., Vandersompele, J., & Wittwer, C. T. (2009). The MIQE guidelines: Minimum information for publication of quantitative real-time PCR experiments. Clinical Chemistry, 55, 611-622. https://doi.org/10.1373/clinchem.2008.112797
Calleja, M., Mortata, G., & Casanova, J. (2016). Tumorigenic properties of Drosophila epithelial cells mutant for lethal giant larvae. Developmental Dynamics, 245, 834-843. https://doi.org/10.1002/DVDY.24420
Cao, M., Gatehouse, J. A., & Fitches, E. C. (2018). A systematic study of RNAi effects and dsRNA stability in Tribolium castaneum and Acyrthosiphon pisum, following injection and ingestion of analogous dsRNAs. International Journal of Molecular Science, 19, 1079. https://doi.org/10.3390/ijms19041079
Cao, Y., Shi, Y., Qiao, H., Yang, Y., Liu, J., Shi, Y., Lin, J., Zhu, G., & Jin, Y. (2014). Distribution of lethal giant larvae (Lgl) protein in the tegument and negative impact of siRNA-based gene silencing on worm surface structure and egg hatching in Schistosoma japonicum. Parasitology Research, 113, 1-9. https://doi.org/10.1007/s00436-013-3620-z
Chou, K.-C., & Shen, H.-B. (2007). Euk-mPLoc: A fusion classifier for large-scale eukaryotic protein subcellular location prediction by incorporating multiple sites. Journal of Proteome Research, 6, 1728-1734. https://doi.org/10.1021/pr060635i
Cooper, A. M. W., Silver, K., Zhang, J., Park, Y., & Zhu, K. Y. (2019). Molecular mechanisms influencing efficiency of RNA interference in insects. Pest Management Science, 75, 18-28. https://doi.org/10.1002/ps.5126
Cooper, A. M. W., Song, H., Shi, X., Yu, Z., Lorenzen, M., Silver, K., Zhang, J., & Zhu, K. Y. (2020). Molecular characterizations of double-stranded RNA degrading nuclease genes from Ostrinia nubilalis. Insects, 11, 652. https://doi.org/10.3390/insects11100652
Cooper, A. M. W., Song, H., Shi, X., Yu, Z., Lorenzen, M., Silver, K., Zhang, J., & Zhu, K. Y. (2021). Characterization, expression patterns, and transcriptional responses of major core RNA interference pathway genes from Ostrinia nubilalis. Journal of Insect Physiology, 129, 104181. https://doi.org/10.1016/j.jinsphys.2020.104181
Cooper, A. M. W., Song, H., Yu, Z., Biondi, M., Bai, J., Shi, X., Ren, Z., Werasekara, S. M., Hua, D. H., Silver, K., Zhang, J., & Zhu, K. Y. (2021). Comparison of strategies for enhancing RNAi interference efficiency in Ostrinia nubilalis. Pest Management Science, 77(2), 635-645. https://doi.org/10.1002/ps.6114
Cooper, A. M. W., Yu, Z., Biondi, M., Song, H., Silver, K., Zhang, J., & Zhu, K. Y. (2020). Stability of double-stranded RNA in gut contents and hemolymph of Ostrinia nubilalis larvae. Pesticide Biochemistry Physiology, 169, 104672. https://doi.org/10.1016/j.pestbp.2020.104672
Davis-Vogel, C., Van Allen, B., Van Hemert, J. L., Sethi, A., Nelson, M. E., & Sashital, D. G. (2018). Identification and comparison of key RNA interference machinery from western corn rootworm, fall armyworm, and southern green stink bug. PLOS One, 2018(13):e0203160. https://doi.org/10.1371/journal.pone.0203160
Gray, M. E., Sappington, T. W., Miller, N. J., Moeser, J., & Bohn, M. O. (2009). Adaptation and invasiveness of western corn rootworm: Intensifying research on a worsening pest. Annual Review of Entomology, 54, 303-321. https://doi.org/10.1146/annurev.ento.54.110807.090434
Guan, R., Hu, S., Li, H., Shi, Z., & Miao, X. (2018). The in vivo dsRNA cleavage has sequence preference in insects. Frontiers in Physiology, 9, 1768. https://doi.org/10.3389/fphys.2018.01768
Guan, R. B., Li, H. C., & Miao, X. X. (2018). Prediction of effective RNA interference targets and pathway-related genes in lepidopteran insects by RNA sequencing analysis. Insect Science, 3, 356-367. https://doi.org/10.1111/1744-7917.12437
Hattendorf, D. A., Andreeva, A., Gangar, A., Brennwald, P. J., & Weis, W. I. (2007). Structure of the yeast polarity protein Sro7 reveals a SNARE regulatory mechanism. Nature, 444, 567-571. https://doi.org/10.1038/nature05635
Head, G., Carroll, M., Evans, S., Rule, D. M., Willse, A., Clark, T., Storer, N. P., Flannagan, R. D., Samuel, L. W., & Meinke, L. J. (2017). Evaluation of SmartStax and SmartStax Pro maize against western corn rootworm and northern corn rootworm: Efficacy and resistance management. Pest Management Science, 73, 1883-1899. https://doi.org/10.1002/ps.4554
Horton, P., Park, K.-J., Obayashi, T., Fujta, N., Harada, H., Adams-Collier, C. J., & Nakai, K. (2007). WoLF PSORT: Protein localization predictor. Nucleic Acids Research, 35, W585-W587. https://doi.org/10.1093/nar/gkm259
Khajuria, C., Ivashuta, S., Wiggins, E., Flagel, L., Moar, W., Pleau, M., Miller, K., Zhang, Y., Ramaseshadri, P., Jiang, C., Hodge, T., Jensen, P., Chen, M., Gowda, A., McCulty, B., Vazquez, C., Bolognesi, R., Haas, J., Head, G., & Clark, T. (2018). Development and characterization of the first dsRNA-resistant insect population from western corn rootworm, Diabrotica virgifera virgifera LeConte. PLOS One, 13, e0197059. https://doi.org/10.1371/journal.pone.0197059
Klämbt, C., & Schmidt, O. (1986). Developmental expression and tissue distribution of the lethal (2) giant larvae protein of Drosophila melanogaster. The EMBO Journal, 5, 2955-2961.
Kozlowski, L. P. (2016). IPC - Isoelectric point calculator. Biology Direct, 11, 55. https://doi.org/10.1186/s13062-016-0159-9
Kumar, S., Stecher, G., & Tamura, K. (2016). MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 3, 1870-1874. https://doi.org/10.1093/molbev/msw054
Lee, Y. S., Nakahara, K., Pham, J. W., Kim, K., He, Z., Sontheimer, E. J., & Carthew, R. W. (2004). Distinct roles for Drosophila Dicer-1 and Dicer-2 in the siRNA/miRNA silencing pathways. Cell, 117, 69-81. https://doi.org/10.1016/S0092-8674(04)00261-2
Lin, W.-Z., Fang, J.-A., Xiao, X., & Chou, K.-C. (2013). iLoc-Animal: A multi-label learning classifier for predicting subcellular localization of animal proteins. Molecular BioSystems, 9, 634-644. https://doi.org/10.1039/c3mb25466f
Musch, A., Cohen, D., Yeaman, C., Nelson, W. J., Rodriguez-Boulan, E., & Brennwald, P. J. (2002). Mammalian homolog of Drosophila tumor suppressor lethal (2) giant larvae interacts with basolaterial exocytic machinery in Madin-Darby canine kidney cells. Molecular Biology of the Cell, 13, 158-168. https://doi.org/10.1091/mbc.01-10-0496
Qi, H.-S., Liu, S.-M., Li, S., & Wei, Z.-J. (2013). Molecular expression of the scribble complex genes, Dlg, Scrib and Lgl, in silkworm, Bombyx mori. Genes, 4, 264-274. https://doi.org/10.3390/genes4020264
Silver, K., Cooper, A. M. W., & Zhu, K. Y. (2021). Strategies for enhancing efficiency of RNA interference in insects. Pest Management Science, https://doi.org/10.1002/ps.6277
Terenius, O., Papanicolaou, A., Garbutt, J. S., Eleftherianos, I., Huvenne, H., Kanginakudru, S., Albrechtsen, M., An, C., Aymeric, J.-L., Barthel, A., Bebas, P., Bitra, K., Bravo, A., Chevalier, F., Collinge, D. P., Crava, C. M., de Maagd, R. A., Duvic, B., Erlandson, M., … Smagghe, G. (2011). RNA interference in Lepidoptera: An overview of successful and unsucessful studies and implications for experimental design. Journal of Insect Physiology, 57, 231-245. https://doi.org/10.1016/j.jinsphys.2010.11.006
Ulrich, J., Dao, V. A., Majumdar, U., Schmitt-Engel, C., Schwirz, J., Schultheis, D., Ströhlein, N., Troelenberg, N., Grossmann, D., Richter, T., Dönitz, J., Gerischer, L., Leboulle, G., Vilcinskas, A., Stanke, M., & Bucher, G. (2015). Large scale RNAi screen in Tribolium reveals novel target genes for pest control and the proteasome as prime target. BioMed Central Genomics, 16, 674. https://doi.org/10.1186/s12864-015-1880-y
Wang, Y., Zhang, H., Li, H., & Miao, X. (2011). Second-generation sequencing supply an effective way to screen RNAi targets in large scale for potential application in pest insect control. Public Library of Science One, 6, e18644. https://doi.org/10.1371/journal.pone.0018644
Xiao, D., Liang, X., Gao, X., Yao, J., & Zhu, K. Y. (2014). The lethal giant larvae gene in Tribolium castaneum: Molecular properties and roles in larval and pupal development as revealed by RNA interference. International Journal of Molecular Science, 15, 6880-6896. https://doi.org/10.3390/ijms15046880
Ye, C., An, X., Jiang, Y.-D., Ding, B.-Y., Shang, F., Christiaens, O., Taning, C. N. T., Smagghe, G., Niu, J., & Wang, J.-J. (2019). Induction of RNAi core machinery's gene expression by exogenous dsRNA and the effects of pre-exposure to dsRNA on the gene silencing efficiency in the pea aphid (Acyrthosiphon pisum). Frontiers in Physiology, 9, 1906. https://doi.org/10.3389/fphys.2018.01906
Zhu, K. Y., & Palli, S. R. (2020). Mechanisms, applications, and challenges of insect RNA interference. Annual Review of Entomology, 65, 293-331. https://doi.org/10.1146/annurev-ento-011019-025224

Auteurs

Anastasia M W Cooper (AMW)

Department of Entomology, Kansas State University, Manhattan, Kansas, USA.

Huifang Song (H)

Department of Entomology, Kansas State University, Manhattan, Kansas, USA.
Institute of Applied Biology, Shanxi University, Taiyuan, Shanxi, China.

Xuekai Shi (X)

Department of Entomology, Kansas State University, Manhattan, Kansas, USA.
Institute of Applied Biology, Shanxi University, Taiyuan, Shanxi, China.

Zhitao Yu (Z)

Department of Entomology, Kansas State University, Manhattan, Kansas, USA.

Young Ho Kim (YH)

Department of Entomology, Kansas State University, Manhattan, Kansas, USA.
Department of Applied Biology, Kyungpook National University, Sangju, Gyeongbuk, South Korea.

Kristopher Silver (K)

Department of Entomology, Kansas State University, Manhattan, Kansas, USA.

Jianzhen Zhang (J)

Department of Entomology, Kansas State University, Manhattan, Kansas, USA.
Institute of Applied Biology, Shanxi University, Taiyuan, Shanxi, China.

Kun Yan Zhu (KY)

Department of Entomology, Kansas State University, Manhattan, Kansas, USA.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH