Vitellogenin of the parasitoid wasp, Encarsia formosa (Hymenoptera: Aphelinidae): Gene organization and differential use by members of the genus

Insect Biochemistry and Molecular Biology

Volumn 34, Issue 9, 2004, Pages 951-961

  Donnell, David M ^a,b  

^a UNIVERSITY OF ARIZONA   (United States)

^b UNIVERSITY OF GEORGIA   (United States)

Author keywords

Aphelinidae; Egg provisioning; Encarsia; Parasitoids; Vitellin; Vitellogenin

Indexed keywords

APHELINIDAE; APIS; APIS MELLIFERA; ENCARSIA; ENCARSIA FORMOSA; ENCARSIA LUTEOLA; ENCARSIA PERGANDIELLA; ENCARSIA SOPHIA; HEXAPODA; HYMENOPTERA; INSECTA; PIMPLA; PIMPLA NIPPONICA; VESPIDAE;

EID: 11144219793     PISSN: 09651748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ibmb.2004.06.011     Document Type: Article

References (68)

1. Abdu, U., Davis, C., Khalaila, I., Sagi, A., 2002. The vitellogenin cDNA of Cherax quadricarinatus encodes a lipoprotein with calcium binding ability, and its expression is induced following the removal of the androgenic gland in a sexually plastic system. Gen. Comp. Endocrinol. 127 (3), 263-272.
2. Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Miller, W., Lipman, D.J., 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402.
3. Barr, P.J., 1991. Mammalian subtilisins: the long-sought dibasic processing endoproteases. Cell 66, 1-3.
4. Bownes, M., Hames, B.D., 1977. Accumulation and degradation of 3 major yolk proteins in Drosophila melanogaster. J. Exp. Zool. 200(1), 149-156.
5. Breathnach, R., Chambon, P., 1981. Organization and expression of eucaryotic split genes coding for proteins. Annu. Rev. Biochem. 50, 349-383.
6. Bucher, P., 1990. Weight matrix descriptions of four eukaryotic RNA polymerase II promoter elements derived from 502 unrelated promoter sequences. J. Mol. Biol. 212, 563-578.
7. Byrne, B.M., Gruber, M., Ab, G., 1989. The evolution of egg yolk proteins. Prog. Biophys. Mol. Biol. 53 (1), 33-69.
8. Chen, J.S., Cho, W.L., Raikhel, A.S., 1994. Analysis of mosquito vitellogenin cDNA. Similarity with vertebrate phosvitins and arthropod serum proteins. J. Mol. Biol. 237, 641-647.
9. Chen, J.S., Sappington, T.W., Raikhel, A.S., 1997. Extensive sequence conservation among insect, nematode, and vertebrate vitellogenins reveals ancient common ancestry. J. Mol. Evol. 44, 440-451.
10. Chen, T.T., Strahlendorf, P.W., Wyatt, G.R., 1978. Vitellin and vitellogenin from locusts (Loscusta migratoria) - properties and posttranslational modification in fat-body. J. Biol. Chem. 253 (15), 5325-5331.
11. Chinzei, Y., Miura, K., Kobayashi, L., Shinoda, T., Numata, H., 1992. Cyanoprotein - developmental stage, sex and diapause-dependent expression and synthesis regulation by juvenile hormone in the bean bug, Riptortus clavatus. Arch. Insect Biochem. Physiol. 21, 61-73.
12. Chomczynski, P., Sacchi, N., 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate phenol chloroform extraction. Anal. Biochem. 162 (1), 156-159.
13. Comas, D., Piulachs, M., Belles, X., 2000. Vitellogenin of Blatella germanica (L.) (Dictyoptera, Blatellidae): nucleotide sequence of the cDNA and analysis of the protein primary structure. Arch. Insect Biochem. Physiol. 45, 1-11.
14. Dhadialla, T.S., Raikhel, A.S., 1990. Biosynthesis of mosquito vitellogenin. J. Biol. Chem. 265 (17), 9924-9933.
15. Donnell, D.M., Hunter, M.S., 2002. Developmental rates of two congeneric parasitoids, Encarsia formosa and E. pergandiella (Hymenoptera: Aphelinidae), utilizing different egg provisioning strategies. J. Insect Physiol. 48, 487-493.
16. Ferkovich, S.M., Dillard, C.R., 1986. A study of uptake of radiolabled host proteins and protein synthesis during development of eggs of the endoparasitoid, Microplitis croceipes (Cresson) (Braconidae). Insect Biochem. 16 (2), 337-345.
17. Fisher, R.C., 1971. Aspects of the physiology of endoparasitic Hymenoptera. Biol. Rev. 46, 243-278.
18. Flanders, S.E., 1942. Oosorption and ovulation in relation to oviposition in the parasitic Hymenoptera. Ann. Entomol. Soc. Am. 35, 251-266.
19. Fourney, R.M., Pratt, G.F., Harnish, D.G., Wyatt, G.R., White, B.N., 1982. Structure and synthesis of vitellogenin and vitellin from Calliphora erythrocephala. Insect Biochem. 12 (3), 311-321.
20. Gerber-Huber, S., Nardelli, D., Haefliger, J.A., Cooper, D.N., Givel, F., Germond, J.E., Engel, J., Green, N.M., Wahli, W., 1987. Precursor-product relationship between vitellogenin and the yolk proteins as derived from the complete sequence of a Xenopus vitellogenin gene. Nucleic Acids Res. 15 (12), 4737-4760.
21. Gerling, D., 1966. Studies with whitefly parasites of Southern California. I. Encarsia pergandiella Howard (Hymenoptera: Aphelinidae). Can. Entomol. 98, 707-724.
22. Hagedorn, H.H., Kunkel, J.G., 1979. Vitellogenin and vitellin in insects. Annu. Rev. Entomol. 24, 475-505.
23. Hagedorn, H.H., Maddison, D.R., Tu, Z., 1998. The evolution of vitellogenins, cyclorrhaphan yolk proteins and related molecules. Adv. Insect Physiol. 27, 235-284.
24. Harnish, D., White, B., 1982. An evolutionary model for the insect vitellins. J. Mol. Evol. 18, 405-413.
25. Hirai, M., Watanabe, D., Kiyota, A., Chinzei, Y., 1998. Nucleotide sequence of vitellogenin mRNA in the bean bug, Riptortus clavatus: analysis of processing in the fat body and ovary. Insect Biochem. Mol. Biol. 28, 537-547.
26. Hiremath, S., Lehtoma, K., 1997. Structure of the gypsy moth vitellogenin gene. Arch. Insect Biochem. Physiol. 36, 151-164.
27. Hunter, M.S., Kelly, S.E., 1998. Hyperparasitism by an exotic autoparasitoid: secondary host selection and the window of vulnerability of conspecific and native heterospecific hosts. Entomol. Exp. Appl. 89 (3), 249-259.
28. Hunter, M.S., Woolley, J.B., 2001. Evolution and behavioral ecology of heteronomous aphelinid parasitoids. Annu. Rev. Entomol. 46, 251-290.
29. Ivanova-Kasas, O.M., 1972. Polyembryony in insects. In: Counce, S.J., Waddington, C.H. (Eds.), Developmental Systems: Insects, vol. 1. Academic Press, New York, pp. 243-271.
30. Kageyama, Y., Kinoshita, T., Umesono, Y., Hatekeyama, M., Oishi, K., 1994. Cloning of cDNA for vitellogenin of Athalia rosae (Hymenoptera) and characterization of the vitellogenin gene expression. Insect Biochem. Mol. Biol. 24, 599-605.
31. King, P.E., Ratcliffe, N.A., Fordy, M.R., 1971. Oogenesis in a braconid, Apanteles glomeratus (L.) possessing an hydropic type of egg. Z. Zellforsch. Mik. Ana. 119, 43-57.
32. Kunkel, J.G., Nordin, J.H., 1985. Yolk proteins. In: Kerkut, G.A., Gilbert, L.I. (Eds.), Comprehensive Insect Physiology, Biochemistry and Pharmacology, vol. 1. Pergamon Press, New York, pp. 83-111.
33. Laemmli, U.K., 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
34. Le Ralec, A., 1995. Egg contents in relation to host-feeding in some parasitic Hymenoptera. Entomophaga 40 (1), 87-93.
35. Lee, J.M., Hatakeyama, M., Oishi, K., 2000a. A simple and rapid method for cloning insect vitellogenin cDNAs. Insect Biochem. Mol. Biol. 30(3), 189-194.
36. Lee, J.M., Nishimori, Y., Hatakeyama, M., Bae, T., Oishi, K., 2000b. Vitellogenin of the cicada Graptosaltria nigrofuscata (Homoptera): analysis of its primary structure. Insect Biochem. Mol. Biol. 30, 1-7.
37. Lewis, D.K., Campbell, J.Q., Sowa, S.M., Chen, M., Vinson, S.B., Keeley, L.L., 2001. Characterization of vitellogenin in the red imported fire ant, Solenopsis invicta (Hymenoptera: Apocrita: Formicidae). J. Insect Physiol. 47, 543-551.
38. Martinez, T., Wheeler, D., 1991. Identification of vitellogenin in the ant, Camponotus festinatus. changes in hemolymph proteins and fat body development in workers. Arch. Insect Biochem. Physiol. 17, 143-155.
39. Miller, S.J., Myers, E., 1999. The FAKtory DNA Sequence Fragment Assembly System. TR99-03. Department of Computer Science, University of Arizona, Tucson, AZ, USA.
40. Mouchel, N., Trichet, V., Naimi, B.Y., Le Pennee, J., Wolff, J., 1997. Structure of a fish (Oncorhynchits mykiss) vitellogenin gene and its evolutionary implication. Gene 197, 147-152.
41. Nardelli, D., Gerber-Huber, S., van het Schip, F.D., Gruber, M., Ab, G., Wahli, W., 1987. Vertebrate and nematode genes coding for yolk proteins are derived from a common ancestor. Biochemistry 26, 6397-6402.
42. Nielsen, H., Engelbrecht, J., Brunak, S., von Heijne, G., 1997. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng. 10 (1), 1-6.
43. Nose, Y., Lee, J.M., Ueno, T., Hatakeyama, M., Oishi, K., 1997. Cloning of cDNA for vitellogenin of the parasitoid wasp, Pimpla nipponica (Hymenoptera: Apocrita: Ichneumonidae): vitellogenin primary structure and evolutionary considerations. Insect Biochem. Mol. Biol. 27 (12), 1047-1056.
44. Piulachs, M.D., Guidugli, K.R., Barchuk, A.R., Cruz, J., Simoes, Z.L.P., Belles, X., 2003. The vitellogenin of the honey bee, Apis mellifera: structural analysis of the cDNA and expression studies. Insect Biochem. Mol. Biol. 33, 459-465.
45. Quicke, D.L.J., 1997. Parasitic Wasps. Cambridge University Press, London.
46. Raikhel, A.S., Dhadialla, T.S., 1992. Accumulation of yolk proteins in insect oocytes. Annu. Rev. Entomol. 37, 217-251.
47. Romans, P., Zu, Z., Ke, Z., Hagedorn, H.H., 1995. Analysis of a vitellogenin gene of the mosquito, Aedes aegypti and comparisons to vitellogenins from other organisms. Insect Biochem. Mol. Biol. 25, 939-958.
48. Sappington, T.W., 2002. The major yolk proteins of higher Diptera are homologs of a class of minor yolk proteins in Lepidoptera. J. Mol. Evol. 55, 470-475.
49. Sappington, T.W., Oishi, K., Raikhel, A.S., 2002. Structural characteristics of insect vitellogenins. In: Adiyodi, K.G., Adiyodi, R.G. (Eds.), Reproductive Biology of Invertebrates, vol. 12, Part A, pp. 69-101.
50. Sappington, T.W., Raikhel, A.S., 1998. Molecular characteristics of insect vitellogenins and vitellogenin receptors. Insect Biochem. Mol. Biol. 28, 277-300.
51. Sharrock, W.J., Rosenwasser, T.A., Gould, J., Knott, J., Hussey, D., Gordon, J.I., Banaszak, L., 1992. Sequence of lamprey vitellogenin. Implications for the lipovitellin crystal structure. J. Mol. Biol. 226 (3), 903-907.
52. Spieth, J., Denison, K., Zucker, E., Blumenthal, T., 1985. The nucleotide sequence of a nematode vitellogenin gene. Nucleic Acids Res. 13 (19), 7129-7138.
53. Spieth, J., Nettleton, M., Zucker-Aprison, E., Lea, K., Blumenthal, T., 1991. Vitellogenin motifs conserved in nematodes and vertebrates. J. Mol. Evol. 32, 429-438.
54. Telfer, W.H., 2002. Insect yolk proteins: a progress report. In: Adiyodi, K.G., Adiyodi, R.G. (Eds.), Reproductive Biology of Invertebrates, vol. 12, Part A, pp. 29-67.
55. Thompson, J.D., Higgins, D.G., Gibson, T.J., 1994. ClustalW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673-4680.
56. Trewitt, P.M., Heilmann, L.J., Degrugillier, S.S., Kumaran, A.K., 1992. The boll weevil vitellogenin gene: nucleotide sequence, structure, and evolutionary relationship to nematode and vertebrate vitellogenin genes. J. Mol. Evol. 34, 418-492.
57. Tsang, W.S., Quackenbush, L.S., Chow, B.K., Tiu, S.H., He, J.G., Chan, S.M., 2003. Organization of the shrimp vitellogenin gene: evidence of multiple genes and tissue specific expression by the ovary and hepatopancreas. Gene 303 (1-2), 99-109.
58. Tsutsui, N., Kawazoe, I., Ohira, T., Jasmani, S., Yang, W.J., Wilder, M.N., Aida, K., 2000. Molecular characterization of a cDNA encoding vitellogenin and its expression in the hepatopancreas and ovary during vitellogenesis in the kuruma prawn, Penaeus japonicus. Zool. Sci. 17, 651-660.
59. Tufail, M., Takeda, M., 2002. Vitellogenin of the cockroach, Leucophaea maderae: nucleotide sequence, structure and analysis of processing in the fat body and oocytes. Insect Biochem. Mol. Biol. 32, 1469-1476.
60. Tufail, M., Lee, J.M., Hatakeyama, M., Oishi, K., Takeda, M., 2000. Cloning of vitellogenin cDNA of the American cockroach, Periplaneta americana (Dictyoptera), and its structural and expression analyses. Arch. Insect Biochem. Physiol. 45, 37-46.
61. Tufail, M., Hatakeyama, M., Takeda, M., 2001. Molecular evidence for two vitellogenin genes and processing of vitellogenins in the American cockroach, Periplaneta americana. Arch. Insect Biochem. Physiol. 48, 72-80.
62. Wahli, W., 1988. Evolution and expression of vitellogenin genes. Trends Genet. 4 (8), 227-232.
63. Wang, X., Cole, K.D., Law, J.H., 1988. cDNA cloning and deduced amino acid sequence of microvitellogenin, a female specific hemolymph and egg protein from the tobacco hornworm, Manduca sexta. J. Biol. Chem. 263 (18), 8851-8855.
64. Wheeler, D.E., Buck, N.A., 1995. Storage proteins in ants during development and colony founding. J. Insect Physiol. 41, 885-894.
65. Wheeler, D.E., Kawooya, J.K., 1990. Purification and characterization of honey bee vitellogenin. Arch. Insect Biochem. Physiol. 14, 253-267.
66. Wheeler, D., Liebig, J., Holldobler, B., 1999. Atypical vitellins in ponerine ants (Formicidae: Hymenoptera). J. Insect Physiol. 45, 287-293.
67. Yano, K., Sakurai, M.T., Watabe, S., Izumi, S., Tomino, S., 1994a. Structure and expression of mRNA for vitellogenin in Bombyx mori. Biochim. Biophys. Acta 1218 (1), 1-10.
68. Yano, K., Sakurai, M.T., Izumi, S., Tomino, S., 1994b. Vitellogenin gene of the silkworm, Bombyx mori: structure and sex-dependent expression. FEBS Lett. 356 (2-3), 207-211.