Abstract
In this present study, the cDNA of Bombus hypocrita vitellogenin (Vg) was cloned and sequenced. It is composed of 5,478 bp and contains an ORF of 1,772 amino acids within a putative signal peptide of 16 residues. The deduced amino acid sequence shows significant similarity with Bombus ignitus (95%) and Apis mellifera (52%) and a high number of conserved motifs. Close to the C terminus there is a GL/ICG motif followed by nine cysteines, and a DGXR motif is located 18 residues upstream from the GL/ICG motif. Moreover, we predicted the 3D structure of B. hypocrita Vg. Furthermore, the Vg mRNA of B. hypocrita was spatio-temporally analyzed in different castes (such as queen, worker and drone) from pupae to adult. The Vg mRNA was found in the white-eyed pupal (Pw) stage in queens, and the expression increased during the entire pupal development and attained its peak in the dark brown pupal stage. It also had a high expression in the adult fat body. In workers, the Vg expression was detected in the Pw stage, and its levels increased with age with the highest in 15 days. Afterward, it decreased progressively. Vg mRNA was also observed in drones, with a higher level of expression shown in only freshly molted adult drones.
Similar content being viewed by others
References
Alaux C, Savarit F, Jaisson P, Hefetz A (2004) Does the queen win it all, Queen-worker conflict over male production in the bumblebee Bombus terrestris. Naturwissenschaften 91:400–403
Barchuk AR, Bitondi MMG, Simoes ZLP (2002) Effects of juvenile hormone and ecdysone on the timing of vitellogenin appearance in hemolymph of queen and worker pupae of Apis mellifera. J Insect Sci 2(1):9
Bourke AFG (1994) Worker matricide in social bees and wasps. J Theor Biol 167:283–292
Chen JS, Sappington W, Raikhel AS (1997) Extensive sequence conservation among insect, nematode, and vertebrate vitellogenins reveals common ancestry. J Mol Evol 44:440–451
Comas D, Piulachs MD, Belles X (2000) Vitellogenin of Blattella germanica (L.) (Dictyoptera, Blattellidae): nucleotide sequence of the cDNA and analysis of the protein primary structure. Arch Insect Biochem Physiol 45:1–11
Dallacqua RP, Simes ZLP, Bitondi MMG (2007) Vitellogenin gene expression in stingless bee workers differing in egg-laying behavior. Insect Soc 54:70–76
Dogterom MH, Matteoni JA, Plowright RC (1998) Pollination of greenhouse tomatoes by the North American Bombus vosnesenskii (Hymenoptera: Apidae). J Econ Entomol 91(1):71–75
Donnell DM (2004) Vitellogenin of the parasitoid wasp, Encarsia formosa (Hymenoptera: Aphelinidae): gene organization and differential use by members of the genus. Insect Biochem Mol Biol 34(9):951–961
Duchateau MJ, Velthuis HHW (1988) Development and reproductive strategies in Bombus terrestris colonies. Behaviour 107:186–207
Engels W (1974) Occurrence and significance of vitellogenins in female castes of social Hymenoptera. Am Zool 14:1229–1237
Engels W, Kaatz H, Zillikens A, Simoes ZLP, Trube A, Braun R, Dittrich F (1990) Honey bee reproduction: vitellogenin and caste-specific regulation of fertility. In: Hoshi M, Yamashita O (eds) Advances in invertebrate reproduction, vol 5. Elsevier, Amsterdam, pp 495–502
Engelmann F (1979) Insect vitellogenin: identification, biosynthesis, and role in vitellogenesis. Adv Insect Physiol 14:49–108
Fluri P, Lüscher M, Wille H, Gerig L (1982) Changes in weight of the pharyngeal gland and haemolymph titres of juvenile hormone, protein and vitellogenin in worker honey bees. J Insect Physiol 28:61–68
Hartfelder K, Steinbrück G (1997) Germ cell cluster formation and cell death are alternatives in caste-specific differentiation of the larval honey bee ovary. Invertebr Reprod Dev 31:237–250
Hiremath S, Lehtoma K (1997a) Complete nucleotide sequence of the vitellogenin mRNA from the gypsy moth: novel arrangement of the subunit encoding regions. Insect Biochem Mol Biol 27:27–35
Hiremath S, Lehtoma K (1997b) Structure of the gypsy moth vitellogenin gene. Arch Insect Biochem Physiol 36:151–164
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
Kageyama Y, Kinoshita T, Umesono Y, Hatakeyama 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
Larrere M, Couillaud F (1993) Role of juvenile hormone biosynthesis in dominance status and reproduction of the bumblebee, Bombus terrestris. Behav Ecol Sociobiol 33:335–338
Lee JM, Hatakeyama M, Oishi K (2000a) A simple and rapid method for cloning insect vitellogenin cDNA. Insect Biochem Mol Biol 30:189–194
Lee JM, Nishimori Y, Hatakeyama M, Bae TW, Oishi K (2000b) Vitellogenin of the cicada Graptopsaltria nigrofuscata (Homoptera): analysis of its primary structure. Insect Biochem Mol Biol 30:1–7
Lee KY, Yoon HJ, Lee SB, Park IG, Jin BR (2009) Molecular cloning and characterization of a vitellogenin of the bumblebee Bombus hypocrita. Int J Indust Entomol 18(1):37–44
Li JL, Peng WJ, Wu J, An JD, Guo ZB, Tong YM, Huang JX (2006) Strawberry pollination by Bombus lucorum and Apis mellifera in glasshouses. Acta Entomol Sin 49(2):342–348
Li JL, Wu J, Cai WZ, Peng WJ, An JD, Huang JX (2008) Comparison of the colony development of two native bumblebee species Bombus hypocrita and Bombus lucorum as candidates for commercial pollination in China. J Apic Res 47(1):22–26
Lopez-Vaamonde C, Koning JW, Jordan WC, Bourke AFG (2003) No evidence that reproductive bumblebee workers reduce the production of new queens. Anim Behav 66:577–584
Lopez-Vaamonde C, Koning JW, Brown RM, Jordan WC, Bourke AFG (2004) Social parasitism by male-producing reproductive workers in a eusocial insect. Nature 430:557–560
Martin D, Piulachs MD, Comas D, Belles X (1998) Isolation and sequence of a partial vitellogenin cDNA from the cockroach, Blattella germanica (L.) (Dictyoptera, Blattellidae), and characterization of the vitellogenin gene expression. Arch Insect Biochem Physiol 38(3):137–146
Meng Y, Liu C, Shiomi K, Nakagaki M, Banno Y, Kajiura Z (2006a) Genetic variations in the vitellogenin of Japanese populations of the wild silkworm, Bombyx mandaraina. J Insect Biotechnol Sericol 75:127–134
Meng Y, Liu C, Zhao A, Shiomi K, Nakagaki M, Banno Y, Kajiura Z (2006b) Vitellogenin gene organization of Antheraea yamamai and promoter activity analysis. Int J Wild Silkmoth Silk 11:29–40
Meng Y, Liu C, Shiomi K, Nakagaki M, Banno Y, Kajiura Z (2008) Purification and cDNA cloning of vitellogenin of the wild silkworm, Saturnia japonica (Lepidoptera: Saturniidae). J Insect Biotechnol Sericol 77:35–44
Michelette ER, Soares AEE (1993) Characterization of preimaginal development stages in Africanized honeybee workers (Apis mellifera L.). Apidologie 24:431–440
Nose Y, Lee JM, 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 27:1047–1056
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 10:1–6
Oldroyd BP, Smolenski AJ, Cornuet JM, Crozler RH (1994) Anarchy in the beehive. Nature 371:749
Page RE, Erickson EH (1988) Reproduction by worker honey bees (Apis mellifera L). Behav Ecol Sociobiol 23:117–126
Piulachs MD, Guidugli KR, Barchuk AR, Cruz J, Simoes ZLP, 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
Plettner E, Slessor KN, Winston ML, Robinson GE, Page RE (1993) Mandibular gland components and ovarian development as measures of caste differentiation in the honey bee (Apis mellifera L). J Insect Physiol 39:235–240
Rachinsky A, Hartfelder K (1990) Corpora allata activity, a prime regulating element for caste-specific juvenile hormone titre in honey bee larvae (Apis mellifera carnica). J Insect Physiol 36:189–194
Raikhel AS, Dhadialla T (1992) Accumulation of yolk proteins in insect oocytes. Annu Rev Entomol 37:217–251
Sappington TW, Raikhel AS (1998) Molecular characteristics of insect vitellogenin receptors. Insect Biochem Mol Biol 28:277–300
Schmidt-Capella IC, Hartfelder K (1998) Juvenile hormone effect on DNA synthesis and apoptosis in caste-specific differentiation of the larval honey bee (Apis mellifera L.) ovary. J Insect Physiol 44:385–391
Trenczek T, Zillikens A, Engels W (1989) Developmental patterns of vitellogenin hemolymph titre and rate of synthesis in adult drone honey bees (Apis mellifera). J Insect Physiol 35:475–481
Tufail M, Takeda M (2002) Vitellogenin of the cockroach, Leuco-phaea maderae: nucleotide sequence, structure and analysis of processing in the fat body and oocytes. Insect Biochem Mol Biol 32:1469–1476
Tufail M, Lee JM, 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
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
van Doorn A, Heringa J (1986) The ontogeny of a dominance hierarchy in colonies of the bumblebee Bombus terrestris (Hymenoptera, Apidae). Insectes Soc 33:3–25
van Honk CGJ, Hogeweg P (1981) The ontogeny of the social structure in a captive Bombus terrestris colony. Behav Ecol Sociobiol 9:111–119
Valle D, Lima Gomes JEP, Goldenberg S, Garca ES (1987) Rhodnius prolixus vitellogenesis: dependence upon the blood source. J Insect Physiol 33:249–254
Winston ML, Slessor KN (1998) Honey bee primer pheromones and colony organization: gaps in our knowledge. Apidologie 29:81–95
Ye GY, Dong SZ, Song QS, Shi M, Chen XX, Hu C (2008) Molecular cloning and developmental expression of the vitellogenin gene in the endoparasitoid, Pteromalus puparum. Insect Mol Biol 17(3):227–233
Yin CM, Zou BX, Yi SX, Stoffolano JG Jr (1990) Ecdysteroid activity during oogenesis in the black blowfly, Phormia regina (Meigen). J Insect Physiol 36:375–382
Acknowledgments
We would like to thank Prof. Paul Schmid-Hempel and Michele C. Hamilton for their help in revising this paper, and Jiandong An, Shudong Luo, Haiyan Shi and Wenfeng Chen for help and advice in the lab. The work was financially supported by grants from the Chinese National Natural Science Foundation for Young Scholars (No. 30700606, No. 30800805), International joint research project (No. 2009DFA32600), the R&D Special Fund for Public Welfare Industry (agriculture) (No. nyhyzx07-041) and China Application of Advances in Agricultural Science and Technology Projects (No. 2006GB23260392).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by G. Heldmaier.
Rights and permissions
About this article
Cite this article
Li, J., Huang, J., Cai, W. et al. The vitellogenin of the bumblebee, Bombus hypocrita: studies on structural analysis of the cDNA and expression of the mRNA. J Comp Physiol B 180, 161–170 (2010). https://doi.org/10.1007/s00360-009-0434-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00360-009-0434-5