Eur. J. Entomol. 109 (1): 7-14, 2012 | DOI: 10.14411/eje.2012.002

Proteomic approach to understanding the maternal effect in the flesh fly, Sarcophaga bullata (Diptera: Sarcophagidae)

Aiqing LI, Liangliang WANG, Min LIANG, Qiugen ZHOU, Guobao WANG, Fanfan HOU
Key Lab for Organ Failure Research, Ministry of Education of China, Nanfang Hospital, Southern Medical University, 1838 North Guangzhou Avenue, Guangzhou, 510515, P.R. China; e-mail: ffhou@public.guangzhou.gd.cn

Progeny of the flesh fly Sarcophaga bullata exposed to short day length show a maternal effect that prevents the expression of pupal diapause. Although ecological aspects of this effect are well studied, not enough is known about the molecular mechanisms underlying this maternal effect. In this study, two-dimensional electrophoresis was performed to detect differences of the abundance of certain proteins in the ovaries of this fly kept under long day and short day conditions for 2 days after eclosion. Eleven proteins that were abundant and showed significant changes were selected for mass spectrometric identification. Ovary proteins that increased in abundance under short-day conditions were similar to twinstar CG4254-PA, muscle protein 20-like protein, GA13413-PA, gene analogous to small peritrophins (Gasp CG10287-PA) and Ribosomal protein LP1 CG4087-PA. Ovary proteins that decreased in abundance under short-day conditions were similar to the ATP synthase beta subunit, fk506-binding protein and storage protein-binding protein. The 2-D proteome maps included 2 additional unknown proteins that were more abundant and 1 that was less abundant in the ovaries of 2-day old short-day females. Twinstar CG4254-PA, muscle protein 20-like protein and GA13413-PA harbour an actin-binding domain. That the 3 actin-binding proteins increase in abundance suggests that it is likely that an alteration in the actin cytoskeleton is involved in this maternal effect in the flesh fly.

Keywords: Diptera, Sarcophagidae, Sarcophaga bullata, maternal effect, short-day history, proteomic, actin-binding, diapause

Received: May 25, 2011; Accepted: July 27, 2011; Published: January 3, 2012

Download citation

References

  1. ALEKSEEV V.R. & LAMPERT W. 2001: Maternal control of resting-egg production in Daphnia. Nature 414: 899-901 Go to original source...
  2. BAMBURG J.R. 1999: Proteins of the ADF/Cofilin family: essential regulators of actin dynamics. Annu. Rev. Cell. Dev. Biol. 15: 185-230 Go to original source...
  3. BARRY M.K., TRIPLETT A.A. & CHRISTENSEN A.C. 1999: A peritrophin-like protein expressed in the embryonic tracheae of Drosophila melanogaster. Insect Biochem. Mol. Biol. 29: 319-327 Go to original source...
  4. BLAIR A., TOMLINSON A., PHAM H., GUNSALUS K.C., GOLDBERG M.L. & LASKI F.A. 2006: Twinstar, the Drosophila homolog of cofilin/ADF, is required for planar cell polarity patterning. Development 133: 1789-1797 Go to original source...
  5. BURMESTER T. & SCHELLER K. 1999: Ligands and receptors: common theme in insect storage protein transport. Naturwissenschaften 86: 468-474 Go to original source...
  6. CARR S., AEBERSOLD R., BALDWIN M., BURLINGAME A., CLAUSER K. & NESVIZHSKII A. 2004: The need for guidelines in publication of peptide and protein identification data: Working group on publication guidelines for peptide and protein identification data. Mol. Cell. Proteom. 3: 531-533 Go to original source...
  7. COLINET H., NGUYEN T.T.A., CLOUTIER C., MICHAUD D. & HANCE T. 2007: Proteomic profiling of a parasitic wasp exposed to constant and fluctuating cold exposure. Insect Biochem. Mol. Biol. 37: 1177-1188 Go to original source...
  8. DENLINGER D.L. 1972: Induction and termination of pupal diapause in Sarcophaga (Diptera: Sarcophagidae). Biol. Bull. Woods Hole 142: 11-24 Go to original source...
  9. DENLINGER D.L. 1998: Maternal control of fly diapause. In Mousseau T.A. & Fox C.W. (eds): Maternal Effects as Adaptations. Oxford Univ. Press, New York, pp. 275-87
  10. DENLINGER D.L. 2002: Regulation of diapause. Annu. Rev. Entomol. 47: 93-122 Go to original source...
  11. HENRICH V.C. & DENLINGER D.L. 1982: A maternal effect that eliminates pupal diapause in progeny of the flesh fly, Sarcophaga bullata. J. Insect Physiol. 28: 881-884 Go to original source...
  12. HYMAN L.E. & WORMINGTON W.M. 1988: Translational inactivation of ribosomal protein mRNAs during Xenopus oocyte maturation. Genes Dev. 2: 598-605 Go to original source...
  13. IVANOV M.F. & REZNIK S.Y. 2008: Photoperiodic regulation of the diapause of the progeny in Trichogramma embryophagum Htg. (Hymenoptera, Trichogrammatidae): Dynamics of sensitivity to photoperiod at the immature stages of maternal females. Entomol. Rev. 88: 261-268 Go to original source...
  14. JOPLIN K.H., YOCUM G.D. & DENLINGER D.L. 1990: Diapause specific proteins expressed by the brain during the pupal diapause of the flesh fly, Sarcophaga crassipalpis. J. Insect Physiol. 36: 775-783 Go to original source...
  15. KAYUKAWA T. & ISHIKAWA Y. 2009: Chaperonin contributes to cold hardiness of the onion maggot Delia antique through repression of depolymerization of actin at low termperatures. PLoS ONE 4: e8277 Go to original source...
  16. KIM M. & DENLINGER D.L. 2009: Decreases in expression of beta-tubulin and microtubule abundance in flight muscles during diapause in adults of Culex pipiens. Insect Mol. Biol. 18: 295-302 Go to original source...
  17. KIM M., ROBICH R.M., RINEHART J.P. & DENLINGER D.L. 2006: Upregulation of two actin genes and redistribution of actin during diapause and cold stress in the northern house mosquito, Culex pipiens. J. Insect Physiol. 52: 1226-1233 Go to original source...
  18. KUANG X.J., XU J., XIA Q.W., HE H.M. & XUE F.S. 2011: Inheritance of the photoperiodic response controlling imaginal summer diapause in the cabbage beetle, Colaphellus bowringi. J. Insect Physiol. 57: 614-619 Go to original source...
  19. LI A.Q. & DENLINGER D.L. 2008: Rapid cold hardening elicits changes in brain protein proTles of the flesh fly, Sarcophaga crassipalpis. Insect Mol. Biol. 17: 565-572 Go to original source...
  20. LI A.Q., POPOVA-BUTLER A., DEAN D.H. & DENLINGER D.L. 2007: Proteomics of the flesh fly reveals an abundance of upregulated heat shock proteins during pupal diapause. J. Insect Physiol. 53: 385-391 Go to original source...
  21. LI A.Q., BENOIT J.B., LOPEZ-MARTINEZ G., ELNITSKY M.A., LEE R.E. & DENLINGER D.L. 2009a: Distinct contractile and cytoskeletal protein patterns in the Antarctic midge are elicited by desiccation and rehydration. Proteomics 9: 2788-2797 Go to original source...
  22. LI A.Q., MICHAUD M.R. & DENLINGER D.L. 2009b: Rapid elevation of Inos and decreases in abundance of other proteins at pupal diapause termination in the flesh fly Sarcophaga crassipalpis. Biochim. Biophys. Acta 1794: 663-668 Go to original source...
  23. LI A.Q., CHOI Y.S., DZIEMA H., CAO R., CHO H.Y., JUNG Y.Y. & OBREITAN K. 2010: Proteomic profiling of the epileptic dentate gyrus. Brain. Pathol. 20: 1077-1089 Go to original source...
  24. MAZUMDER B., SAMPATH P., SESHADRI V., MAITRA R.K., DICORLETO P.E. & FOX P.L. 2003: Regulated release of L13a from the 60S ribosomal subunit as a mechanism of transcriptspecific translational control. Cell 115: 187-198 Go to original source...
  25. MCWATTERS H.G. & SAUNDERS D.S. 1997: Inheritance of the photoperiodic response controlling larval diapause in the blow fly, Calliphora vicina. J. Insect Physiol. 43: 709-717 Go to original source...
  26. MOON W. & HAZELRIGG T. 2004: The Drosophila microtubuleassociated protein mini spindles is required for cytoplasmic microtubules in oogenesis. Curr. Biol. 14: 1957-1961 Go to original source...
  27. MOUSSEAU T.A. & FOX C.W. 1998: The adaptive significance of maternal effects. Trends Ecol. Evol. 13: 403-407 Go to original source...
  28. PERROT-APPLANAT M., CIBERT C., GERAUD G., RENOIR J.M. & BAULIEU E.E. 1995: The 59 kDa FK506-binding protein, a 90 kDa heat shock protein binding immunophilin (FKBP59-HBI), is associated with the nucleus, the cytoskeleton and mitotic apparatus. J. Cell Sci. 108: 2037-2051
  29. QIAN S., HONGO S. & JACOBS-LORENA M. 1988: Antisense ribosomal protein gene expression specifically disrupts oogenesis in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 85: 9601-9605 Go to original source...
  30. RASANEN K. & KRUUK L.E. 2007: Maternal effects and evolution at ecological time-scales. Funct. Ecol. 21: 408-421 Go to original source...
  31. RING R.A. 1967: Maternal induction of diapause in the larva of Lucilia caesar L. (Diptera: Calliphoridae). J. Exp. Biol. 46: 123-126
  32. ROCKEY S.J., MILLER B.B. & DENLINGER D.L. 1989: A diapause maternal effect in the flesh fly, Sarcophaga bullata: transfer of information from mother to progeny. J. Insect Physiol. 35: 553-558 Go to original source...
  33. SAUNDERS D.S. 1965: Larval diapause of maternal origin: induction of diapause in Nasonia vitripennis (Walk.). J. Exp. Biol. 42: 495-508
  34. SAUNDERS D.S. 1987: Maternal influence on the incidence and duration of larval diapause in Calliphora vicina. Physiol. Entomol. 12: 331-338 Go to original source...
  35. SCHNEIDERMAN H.A. & HOROWITZ J. 1958: The induction and termination of facultative diapause in the chalcid wasps Mormoniella vitripennis (Walker) and Trineptis klugii (Ratzeburg). J. Exp. Biol. 35: 520-551
  36. SHINTANI Y. 2009: Artificial selection for responsiveness to photoperiodic change alters the response to stationary photoperiods in maternal induction of egg diapause in the rice leaf bug Trigonotylus caelestialium. J. Insect Physiol. 55: 818-824 Go to original source...
  37. SINARS C.R., CHEUNG-FLYNN J., RIMERMAN R.A., SCAMMELL J.G., SMITH D.F. & CLARDY J. 2003: Structure of the large FK506 binding protein FKBP51, an Hsp90-binding protein and a component of steroid receptor complexes. Proc. Natl. Acad. Sci. USA 100: 868-873 Go to original source...
  38. VINOGRADOVA E.B. & ZINOVJEVA K.B. 1972: Maternal induction of larval diapause in the blowfly, Calliphora vicina. J. Insect Physiol. 18: 2401-2409 Go to original source...
  39. WEBB M.L.Z. & DENLINGER D.L. 1998: GABA and picrotoxin alter expression of a maternal effect that influences pupal diapause in the flesh fly, Sarcophaga bullata. Physiol. Entomol. 23: 184-191 Go to original source...
  40. YAMASHITA O. 1996: Diapause hormone of the silkworm, Bombyx mori, structure, gene expression and function. J. Insect Physiol. 42: 669-679 Go to original source...