Molecular characterization, expression pattern and RNAi-mediated silencing of vitellogenin receptor gene in almond moth, Cadra cautella.

Publisher: Blackwell Scientific For The Royal Entomological Society Country of Publication: England NLM ID: 9303579 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1365-2583 (Electronic) Linking ISSN: 09621075 NLM ISO Abbreviation: Insect Mol Biol Subsets: MEDLINE

Publication: Oxford : Blackwell Scientific For The Royal Entomological Society
Original Publication: Oxford : Published for the Royal Entomological Society by Blackwell Scientific Publications, c1992-

Gene Expression*; Egg Proteins/*genetics ; Insect Proteins/*genetics ; Moths/*genetics ; Receptors, Cell Surface/*genetics; Amino Acid Sequence ; Animals ; Egg Proteins/chemistry ; Egg Proteins/metabolism ; Female ; Gene Expression Profiling ; Insect Proteins/chemistry ; Insect Proteins/metabolism ; Larva/growth & development ; Larva/metabolism ; Male ; Moths/growth & development ; Moths/metabolism ; Phylogeny ; Pupa/growth & development ; Pupa/metabolism ; RNA Interference ; Receptors, Cell Surface/chemistry ; Receptors, Cell Surface/metabolism ; Sequence Alignment

The almond moth is an important pest of date fruits worldwide. The females produce several eggs; however, role of vitellogenin receptor (VgR) in oocyte development by mediating endocytosis of major yolk protein precursor Vg remains yet unexplored. To investigate the role of vitellogenin receptor (VgR) in reproduction, Cadra cautella vitellogenin receptor (CcVgR) transcript was obtained using rapid amplification of cDNA ends-polymerase chain reaction. Expression analysis of CcVgR was performed using reverse transcriptase and quantitative polymerase chain reaction (qPCR) in different developmental stages. RNA interference was performed by injecting CcVgR-based double-stranded (ds)RNA at different exposure times. The results revealed that CcVgR is 5421 bp long, encoded 1807 amino acid, belongs to low-density lipoprotein receptor superfamily and contains all conserved domains. Expression analysis confirmed that CcVgR is sex-specific and starts to express in female larvae on day 19. Additionally, RNA interference (RNAi) of CcVgR-based dsRNA inhibited CcVgR expression up to 83% after 72 h, reduced fecundity and hatchability, and confirmed involvement of CcVgR in C. cautella reproduction. This report provides a basis for gene silencing in this species, and proposes RNAi technology potential for pest management.
(© 2020 The Royal Entomological Society.)

Al Antary, T.M., Al-Khawaldeh, M.M. and Ateyyat, M.A. (2015) Economic importance of date palm Phoenix dactylifera L. (Liliopsida: Arecales: Arecaceae) pests in Jordan Valley. Brazilian Journal of Biological Sciences, 2, 101-109.
Aldawood, A.S. (2013) Effect of covering dates fruit bunches on Ephestia cautella Walker (Lepidoptera: Pyralidae) infestation: population dynamics studies in the field. International Journal of Applied Agricultural Sciences, 5, 98-100.
Aldawood, A.S., Rasool, K.G., Alrukban, A.H., Soffan, A., Husain, M., Sutanto, K.D. et al. (2013) Effects of temperature on the development of Ephestia cautella (Walker) (Pyralidae: Lepidoptera): a case study for its possible control under storage conditions. Pakistan Journal of Zoology, 45, 1573-1578.
Al-Zadjali, T.S., Abd-Allah, F.F. and El-Haidari, H.S. (2006) Insect pests attacking date palms and dates in Sultanate of Oman. Egyptian Journal of Agricultural Research, 84, 51-59.
Amdam, G.V., Norberg, K., Hagen, A. and Omholt, S.W. (2003) Social exploitation of vitellogenin. Proceedings of the National Academy of Sciences, 100, 1799-1802.
Arbogast, R.T., Chini, S.R. and Kendra, P.E. (2005) Infestation of stored saw palmetto berries by Cadra cautella (Lepidoptera: Pyralidae) and the host paradox in stored-product insects. Florida Entomologist, 88, 314-321.
Bai, H., Qiao, H., Li, F., Fu, H., Jiang, S., Zhang, W. et al. (2016) Molecular and functional characterization of the vitellogenin receptor in oriental river prawn, Macrobrachium nipponense. Comparative Biochemistry and Physiology - Part A: Molecular & Integrative Physiology, 194, 45-55.
Baum, J.A., Bogaert, T., Clinton, W., Heck, G.R., Feldmann, P., Ilagan, O. et al. (2007) Control of coleopteran insect pests through RNA interference. Nature Biotechnology, 25, 1322-1326.
Bell, W.J. (1969) Continuous and rhythmic reproductive cycle observed in Periplaneta americana (L.). The Biological Bulletin, 137, 239-249.
Brown, M.S., Anderson, R.G. and Goldstein, J.L. (1983) Recycling receptors: the round-trip itinerary of migrant membrane proteins. Cell, 32, 663-667.
Bujo, H., Hermann, M., Kaderli, M.O., Jacobsen, L., Sugawara, S., Nimpf, J. et al. (1994) Chicken oocyte growth is mediated by an eight ligand binding repeat member of the LDL receptor family. The EMBO Journal, 13, 5165-5175.
Chen, M.E., Lewis, D.K., Keeley, L.L. and Pietrantonio, P.V. (2004) cDNA cloning and transcriptional regulation of the vitellogenin receptor from the imported fire ant, Solenopsis invicta Buren (Hymenoptera: Formicidae). Insect Molecular Biology, 13, 195-204.
Cline, L.D. and Highland, H.A. (1985) Survival, reproduction, and development of seven species of stored-product insects on the various food components of lightweight, high-density, prototype military rations. Journal of Economic Entomology, 78, 779-782.
Cong, L., Yang, W.J., Jiang, X.Z., Niu, J.Z., Shen, G.M., Ran, C. et al. (2015) The essential role of vitellogenin receptor in ovary development and vitellogenin uptake in Bactrocera dorsalis (Hendel). International Journal of Molecular Sciences, 16, 18368-18383.
Ferenz, H.J. (1993) Yolk protein accumulation in Locusta migratoria (R. & F.) (Orthoptera: Acrididae) oocytes. International Journal of Insect Morphology and Embryology, 22, 295-314.
Goldstein, J.L., Brown, M.S., Anderson, R.G., Russell, D.W. and Schneider, W.J. (1985) Receptor-mediated endocytosis: concepts emerging from the LDL receptor system. Annual Review of Cell and Developmental Biology, 1, 1-39.
Hagedorn, H.H. and Judson, C.L. (1972) Purification and site of synthesis of Aedes aegypti yolk proteins. Journal of Experimental Zoology, 182, 367-377.
Hiramatsu, N., Chapman, R.W., Lindzey, J.K., Haynes, M.R. and Sullivan, C.V. (2004) Molecular characterization and expression of vitellogenin receptor from white perch (Morone americana). Biology of Reproduction, 70, 1720-1730.
Husain, M., Alwaneen, W.S., Mehmood, K., Rasool, K.G., Tufail, M. and Aldawood, A.S. (2017) Biological traits of Cadra cautella (Lepidoptera: Pyralidae) reared on Khodari date fruits under different temperature regimes. Journal of Economic Entomology, 110, 1923-1928.
Husain, M., Tufail, M., Mehmood, K., Rasool, K.G. and Aldawood, A.S. (2019) Transcriptome analysis of the almond moth, Cadra cautella, female abdominal tissues and identification of reproduction control genes. BMC Genomics., 20, 883.
Kola, V.S.R., Renuka, P., Padmakumari, A.P., Mangrauthia, S.K., Balachandran, S.M., Ravindra Babu, V. et al. (2016) Silencing of CYP6 and APN genes affects the growth and development of rice yellow stem borer, Scirpophaga incertulas. Frontiers in Physiology, 7, 20.
Lin, Y., Meng, Y., Wang, Y.X., Luo, J., Katsuma, S., Yang, C.W. et al. (2013) Vitellogenin receptor mutation leads to the oogenesis mutant phenotype “scanty vitellin” of the silkworm, Bombyx mori. Journal of Biological Chemistry, 288, 13345-13355.
Lin, Y., Zhao, P., Hou, Y., Li, J., Gong, D., Sun, Q. et al. (2005) Vitellogenin and vitellogenin receptor gene of the silkworm, Bombyx mori. Dongwu Xue bao. Acta Zoologica Sinica, 51, 117-125.
Liu, C.L., Kajiura, Z., Shiomi, K., Takei, R. and Nakagaki, M. (2001) Purification and cDNA sequencing of vitellogenin of the wild silkworm, Antheraea pernyi. Journal of Insect Biotechnology, 70, 95-104.
Liu, L., Wang, Y., Li, Y., Lin, Y., Hou, Y., Zhang, Y. et al. (2016) LBD1 of vitellogenin receptor specifically binds to the female-specific storage protein SP1 via LBR1 and LBR3. PLoS One, 11, e0162317.
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.
Lu, K., Shu, Y., Zhou, J., Zhang, X., Zhang, X., Chen, M. et al. (2015) Molecular characterization and RNA interference analysis of vitellogenin receptor from Nilaparvata lugens (Stål). Journal of Insect Physiology, 73, 20-29.
Mankin, R.W., Hagstrum, D.W., Nansen, C. and Meikle, W.G. (2014) Almond moth oviposition patterns in continuous layers of peanuts. The Journal of Stored Products Research, 59, 48-54.
Mehmood, K., Tufail, M., Husain, M., Rasool, K.G., Aldawood, A., 2018. Molecular characterization, expression profiling of vitellogenin gene, and reproductive ability disruption by RNAi in red palm weevil, Rhynchophorus ferrugineus (Olivier). PhD Thesis, King Saud University.
Mitchell, R.D., Perez De Leon, A. and Sonenshine, D.E. (2019) Vitellogenin receptor as a target for tick control: a mini-review. Frontiers in Physiology, 10, 618.
Mohammed, A.M., Diab, M.R., Abdelsattar, M. and Sayed, M.S. (2017) Characterization and RNAi-mediated knockdown of Chitin Synthase A in the potato tuber moth, Phthorimaea operculella. Scientific Reports, 7, 9502.
Moriyama, M., Hosokawa, T., Tanahashi, M., Nikoh, N. and Fukatsu, T. (2016) Suppression of bedbug's reproduction by RNA interference of vitellogenin. PLoS One, 11, e0153984.
Mukherjee, S., Ghosh, R.N. and Maxfield, F.R. (1997) Endocytosis. Physiological Reviews, 77, 759-803.
Nelson, C.M., Ihle, K.E., Fondrk, M.K., Page, R.E., Jr. and Amdam, G.V. (2007) The gene vitellogenin has multiple coordinating effects on social organization. PLoS Biology, 5, e62.
Oié, M., Takahashi, S.Y. and Ishizaki, H. (1975) Vitellogenin in the eggs of the cockroach, Blattella germanica: purification and characterization. Development, Growth & Differentiation, 17, 237-246.
Perazzolo, L.M., Coward, K., Davail, B., Normand, E., Tyler, C.R., Pakdel, F. et al. (1999) Expression and localization of messenger ribonucleic acid for the vitellogenin receptor in ovarian follicles throughout oogenesis in the rainbow trout, Oncorhynchus mykiss. Biology of Reproduction., 60, 1057-1068.
Qian, C., Fu, W.W., Wei, G.Q., Wang, L., Liu, Q.N., Dai, L.S. et al. (2015) Identification and expression analysis of vitellogenin receptor from the wild silkworm, Bombyx mandarina. Archives of Insect Biochemistry and Physiology, 89, 181-192.
Raikhel, A.S. and Dhadialla, T.S. (1992) Accumulation of yolk proteins in insect oocytes. Annual Review of Entomology, 37, 217-251.
Raza, A., Malik, H.J., Shafiq, M., Amin, I., Scheffler, J.A., Scheffler, B.E. et al. (2016) RNA interference based approach to down regulate osmoregulators of whitefly (Bemisia tabaci): potential technology for control of whitefly. PLoS One, 11, e0153883.
Rostom, Z.M. (1993) Survey of some granivorous and non-granivorous insects and mites of stores in Saudi Arabia. The Journal of Stored Products Research, 29, 27-31.
Sappington, T.W. and Raikhel, A.S. (1998) Molecular characteristics of insect vitellogenins and vitellogenin receptors. Insect Biochemistry and Molecular Biology, 28, 277-300.
SAS Institute (2009) In: Using JMP Student Edition for Windows and Macintosh: The User's Guide to Statistics with JMP, Vol. Student edition. SAS Institute, Cary, North Carolina.
Schneider, W.J. (1996) Vitellogenin receptors: oocyte-specific members of the low-density lipoprotein receptor supergene family. International Review of Cytology, 166, 103-137.
Schonbaum, C.P., Lee, S. and Mahowald, A.P. (1995) The Drosophila yolkless gene encodes a vitellogenin receptor belonging to the low density lipoprotein receptor superfamily. Proceedings of the National Academy of Sciences, 92, 1485-1489.
Seehuus, S.C., Norberg, K., Gimsa, U., Krekling, T. and Amdam, G.V. (2006) Reproductive protein protects functionally sterile honey bee workers from oxidative stress. Proceedings of the National Academy of Sciences, 103, 962-967.
Shu, Y., Zhou, J., Tang, W., Lu, K., Zhou, Q. and Zhang, G. (2009) Molecular characterization and expression pattern of Spodoptera litura (Lepidoptera: Noctuidae) vitellogenin, and its response to lead stress. Journal of Insect Physiology, 55, 608-616.
Shu, Y.H., Wang, J.W., Lu, K., Zhou, J.L., Zhou, Q. and Zhang, G.R. (2011) The first vitellogenin receptor from a Lepidopteran insect: molecular characterization, expression patterns and RNA interference analysis. Insect Molecular Biology, 20, 61-73.
Shukla, J.N., Kalsi, M., Sethi, A., Narva, K.E., Fishilevich, E., Singh, S. et al. (2016) Reduced stability and intracellular transport of dsRNA contribute to poor RNAi response in lepidopteran insects. RNA Biology, 13, 656-669.
Soffan, A., Antony, B., Abdelazim, M., Shukla, P., Witjaksono, W., Aldosari, S.A. et al. (2016) Silencing the olfactory co-receptor rferorco reduces the response to pheromones in the red palm weevil, Rhynchophorus ferrugineus. PlLoS One, 11, e0162203.
Springer, T.A. (1998) An extracellular β-propeller module predicted in lipoprotein and scavenger receptors, tyrosine kinases, epidermal growth factor precursor, and extracellular matrix components. Journal of Molecular Biology, 283, 837-862.
Subramanyam, B. and Hagstrum, D.W. (1993) Predicting development times of six stored-product moth species (Lepidoptera: Pyralidae) in relation to temperature, relative humidity, and diet. European Journal of Entomology, 90, 51-64.
Tufail, M. and Takeda, M. (2002) Vitellogenin of the cockroach, Leucophaea maderae: nucleotide sequence, structure and analysis of processing in the fat body and oocytes. Insect Biochemistry and Molecular Biology, 32, 1469-1476.
Tufail, M. and Takeda, M. (2005) Molecular cloning, characterization and regulation of the cockroach vitellogenin receptor during oogenesis. Insect Biochemistry and Molecular Biology, 14, 389-401.
Tufail, M. and Takeda, M. (2007) Molecular cloning and developmental expression pattern of the vitellogenin receptor from the cockroach, Leucophaea maderae. Insect Biochemistry and Molecular Biology, 37, 235-245.
Tufail, M. and Takeda, M. (2008) Molecular characteristics of insect vitellogenins. Journal of Insect Physiology, 54, 1447-1458.
Tufail, M. and Takeda, M. (2009) Insect vitellogenin/lipophorin receptors: molecular structures, role in oogenesis, and regulatory mechanisms. Journal of Insect Physiology, 55, 88-104.
Tufail, M., Elmogy, M., Ali Fouda, M.M., Elgendy, A.M., Bembenek, J., Trang, L.T.D. et al. (2009) Molecular cloning, characterization, expression pattern and cellular distribution of an ovarian lipophorin receptor in the cockroach, Leucophaea maderae. Insect Molecular Biology, 18, 281-294.
Tufail, M., Hatakeyama, M. and Takeda, M. (2001) Molecular evidence for two vitellogenin genes and processing of vitellogenins in the American cockroach, Periplaneta americana. Archives of Insect Biochemistry and Physiology, 48, 72-80.
Tufail, M., Nagaba, Y., Elgendy, A.M. and Takeda, M. (2014) Regulation of vitellogenin genes in insects. Entomological Science, 17, 269-282.
Upadhyay, S.K., Singh, H., Dixit, S., Mendu, V. and Verma, P.C. (2016) Molecular characterization of vitellogenin and vitellogenin receptor of Bemisia tabaci. PLoS One, 11, e0155306.
Veerana, M., Kubera, A. and Ngernsiri, L. (2014) Analysis of the vitellogenin gene of rice moth, Corcyra cephalonica Stainton. Archives of Insect Biochemistry and Physiology, 87, 126-147.
Xiao, H.J., Fu, X.W., Liu, Y.Q. and Wu, K.M. (2016) Synchronous vitellogenin expression and sexual maturation during migration are negatively correlated with juvenile hormone levels in Mythimna separata. Scientific Reports, 6, 33309.
Xu, Y., Zhu, B., Liu, Q., Wei, G., Chen, L., Yu, S.L. et al. (2012) Prokaryotic expression of vitellogenin receptor gene of Actias selene Hubner. African Journal of Agricultural Research, 7, 3166-3174.
Yao, Q., Xu, S., Dong, Y., Que, Y., Quan, L. and Chen, B. (2018) Characterization of vitellogenin and vitellogenin receptor of Conopomorpha sinensis Bradley and their responses to sublethal concentrations of insecticide. Frontiers in Physiology, 9, 1250.
Zhang, W., Ma, L., Xiao, H., Xie, B., Smagghe, G., Guo, Y. et al. (2016) Molecular characterization and function analysis of the vitellogenin receptor from the cotton bollworm, Helicoverpa armigera (Hübner) (Lepidoptera, Noctuidae). PLoS One, 11, e0155785.
Zhong, R., Ding, T.B., Niu, J.Z., Xia, W.K., Liao, C.Y., Dou, W. et al. (2015) Molecular characterization of vitellogenin and its receptor genes from citrus red mite, Panonychus citri (McGregor). International Journal of Molecular Sciences, 16, 4759-4773.

Keywords: Cadra cautella; RNA interference; dates; expression; vitellogenin receptor

0 (Egg Proteins)
0 (Insect Proteins)
0 (Receptors, Cell Surface)
0 (vitellogenin receptor)

Date Created: 20200506 Date Completed: 20201229 Latest Revision: 20201229

20250114

10.1111/imb.12646

32368832