Insights into female sperm storage from the spermathecal fluid proteome of the honeybee Apis mellifera

Genome Biology

Volumn 10, Issue 6, 2009, Pages

  Baer, Boris ^a   Eubel, Holger ^a   Taylor, Nicolas L ^a   O'Toole, Nicholas ^a   Millar, A Harvey ^a  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ACONITATE HYDRATASE; ACYLTRANSFERASE; ALANINE AMINOTRANSFERASE; ALDEHYDE DEHYDROGENASE; ARGININE KINASE; ASPARTATE AMINOTRANSFERASE ISOENZYME 2; CARBONATE DEHYDRATASE; CITRATE SYNTHASE; ENOLASE; FRUCTOSE BISPHOSPHATE ALDOLASE; ISOCITRATE DEHYDROGENASE; MELITTIN; PEROXIREDOXIN; PEROXIREDOXIN 2; PROLINE DEHYDROGENASE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; PYRUVATE KINASE; SUPEROXIDE DISMUTASE; THIOREDOXIN 2; THIOREDOXIN REDUCTASE; INSECT PROTEIN; PROTEOME;

ANTIOXIDANT ACTIVITY; ARTICLE; CONTROLLED STUDY; ENERGY METABOLISM; FEMALE; HONEYBEE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEOMICS; SEMINAL PLASMA; SPERM PRESERVATION; ANIMAL; BEE; BODY FLUID; MALE; METABOLISM; POLYACRYLAMIDE GEL ELECTROPHORESIS; SEXUAL BEHAVIOR; SPERMATOZOON;

ANIMALIA; APIS MELLIFERA;

ANIMALS; BEES; BODY FLUIDS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FEMALE; INSECT PROTEINS; MALE; METABOLIC NETWORKS AND PATHWAYS; PROTEOME; SEXUAL BEHAVIOR, ANIMAL; SPERMATOZOA;

EID: 67650588722     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2009-10-6-r67     Document Type: Article

References (53)

1. Birkhead TR Moller AP Sperm Competition and Sexual Selection New York: Academic Press 1998.
2. Eberhard WG Sexual Selection and Animal Genitalia Cambridge, Massachusetts: Harvard University Press 1985.
3. Eberhard WG Female Control: Sexual Selection by Cryptic Female Choice Princeton, New Jersey: Princeton University Press 1996.
4. Ruttner F Koeniger G The filling of the spermatheca of the honey bee queen active migration or passive transport of the spermatozoa. Z vergl Physiol 1971, 72:411-422. 10.1007/BF00300712
5. Klenk M Koeniger G Koeniger N Fasold H Proteins in spermathecal gland secretion and spermathecal fluid and the properties of a 29 kDa protein in queens of Apis mellifera. Apidologie 2004, 35:371-381. 10.1051/ apido:2004029
6. den Boer SP Boomsma JJ Baer B Seminal fluid enhances sperm viability in the leafcutter ant Atta colombica. Behav Ecol Sociobiol 2008, 62:1843-1849. 10.1007/s00265-008-0613-5
7. den Boer SP Boomsma JJ Baer B Honey bee males and queens use glandular secretions to enhance sperm viability before and after storage. J Insect Physiol 2009, 55:538-543. 10.1016/j.jinsphys.2009.01.012 19232404
8. Collins AM Williams V Evans JD Sperm storage and antioxidative enzyme expression in the honey bee, Apis mellifera. Insect Mol Biol 2004, 13:141-146. 10.1111/j.0962-1075.2004.00469.x 15056361
9. Verma LR An ionic basis for a possible mechanism of sperm survival in the spermatheca of the queen honey bee Apis mellifera. Comp Biochem Physiol 1973, 44:1325-1331. 10.1016/0300-9629(73)90272-7
10. Gessner B Transfer der Spermatozoen in die Spermatheca der Koenigin bei Apis mellifica carnica Frankfurt am Main: Johann Wolfgang Goethe Universität 1973.
11. Baer B Armitage SAO Boomsma JJ Sperm storage induces an immunity cost in ants. Nature 2006, 441:872-875. 10.1038/nature04698 16778889
12. Simmons LW Sperm Competition and Its Evolutionary Consequences in the Insects Oxford: Princeton University Press 2001.
13. Tozetto SDO Bitondi MMG Dallacqua RP Simoes ZLP Protein profiles of testes, seminal vesicles and accessory glands of honey bee pupae and their relation to the ecdysteroid titer. Apidologie 2007, 38:1-11. 10.1051/apido:2006045
14. Ram KR Wolfner MF Seminal influences: Drosophila Acps and the molecular interplay between males and females during reproduction. Integr Comp Biol 2007, 47:427-10. 1093/icb/icm046
15. Poiani A Complexity of seminal fluid: A review. Behav Ecol Sociobiol 2006, 60:289-310. 10.1007/s00265-006-0178-0
16. Baer B Bumblebees as model organisms to study male sexual selection in social insects. Behav Ecol Sociobiol 2003, 54:521-533. 10.1007/ s00265-003-0673-5
17. Findlay GD Yi X Maccoss MJ Swanson WJ Proteomics reveals novel Drosophila seminal fluid proteins transferred at mating. PLoS Biol 2008, 6:e178. 16709260 10.1371/journal.pbio.0060178 1779515
18. Pilch B Mann M Large-scale and high-confidence proteomic analysis of human seminal plasma. Genome Biol 2006, 7:R40. 1779515 16709260 10.1186/ gb-2006-7-5-r40
19. Baer B Heazlewood JL Taylor NL Eubel H Millar AH The seminal fluid proteome of the honeybee Apis mellifera. Proteomics 2009, 9:2085-2097. 10.1002/pmic.200800708 19322787
20. Collins AM Caperna TJ Williams V Garett WM D EJ Proteomic analyses of male contributions to honeybee sperm storage and mating. Insect Mol Biol 2006, 15:541-549. 1847503 17069630 10.1111/j.1365-2583.2006.00674.x
21. Colonello NA Hartfelder K She's my girl - male accessory gland products and their function in the reproductive biology of social bees. Apidologie 2005, 36:231-244. 10.1051/apido:2005012
22. Chen PS Stumm Zollinger E Aigaki T Balmer J Bienz M Bohlen P A male accessory gland peptide that regulates reproductive behavior of female Drosophila melanogaster. Cell 1988, 54:291-298. 10.1016/ 0092-8674(88)90192-4 3135120
23. Baer B Morgan ED Schmid-Hempel P A non-specific fatty acid within the bumblebee mating plug prevents females from remating. Proc Natl Acad Sci USA 2001, 98:3926-3928. 31155 11274412 10.1073/pnas.061027998
24. Baer B Maile R Schmid-Hempel P Morgan ED Jones GR Chemistry of a mating plug in bumblebees. J Chem Ecol 2000, 26:1869-1875. 10.1023/ A:1005596707591
25. Sauter A Brown MJF Baer B Schmid-Hempel P Males of social insects can prevent queens from multiple mating. Proc R Soc B 2001, 268:1449-1454. 1088762 11454287 10.1098/rspb.2001.1680
26. Pamilo P Life span of queens in the ant Formica exsecta. Insect Soc 1991, 38:111-120. 10.1007/BF01240961
27. Keller L Genoud M Extraordinary lifespans in ants: A test of evolutionary theories of ageing. Nature 1997, 389:958-960. 10.1038/40130
28. Baer B Dijkstra MB Mueller UG Nash DR Boomsma JJ Sperm length evolution in the fungus growing ants. Behav Ecol 2009, 20:38-45. 10.1093/beheco/ arn112
29. Baer B Sexual selection in Apis bees. Apidologie 2005, 36:187-200. 10.1051/apido:2005013
30. Boomsma JJ Baer B Heinze J The evolution of male traits in social insects. Annu Rev Entomol 2005, 50:395-420. 10.1146/ annurev.ento.50.071803.130416 15822204
31. Weber NA Gardening Ants: The Attines Philadelphia: The American Philosophical Society 1972.
32. Shannon P Markiel A Ozier O Baliga NS Wang JT Ramage D Amin N Schwikowski B Ideker T Cytoscape: A software environment for integrated models of biomolecular interaction networks. Genome Res 2003, 13:2498-2504. 403769 14597658 10.1101/gr.1239303
33. Baer B Schmid-Hempel P Sperm influences female hibernation success, survival and fitness in the bumblebee Bombus terrestris. Proc R Soc B 2005, 272:319-323. 1634972 15705558 10.1098/rspb.2004.2958
34. Weinstock GM Robinson GE Gibbs RA Worley KC Evans JD Maleszka R Robertson HM Weaver DB Beye M Bork P Elsik CG Hartfelder K Hunt GJ Zdobnov EM Amdam GV Bitondi MMG Collins AM Cristino AS Lattorff HMG Lobo CH Moritz RFA Nunes FMF Page RE Simoes ZLP Wheeler D Carninci P Fukuda S Hayashizaki Y Kai C Kawai J et al Insights into social insects from the genome of the honeybee Apis mellifera. Nature 2006, 443:931-949. 2048586 17073008 10.1038/nature05260
35. Chan QWT Howes CG Foster LJ Quantitative comparison of caste differences in honeybee hemolymph. Mol Cell Proteomics 2006 5 2252 2262 10.1074/ mcp.M600197-MCP200 16920818
36. Kyoto Encyclopedia of Genes and Genomes http://www.genome.jp/kegg/
37. Kanehisa M Araki M Goto S Hattori M Hirakawa M Itoh M Katayama T Kawashima S Okuda S Tokimatsu T Yamanishi Y KEGG for linking genomes to life and the environment. Nucleic Acids Res 2008, 36:D480-D484. 2238879 18077471 10.1093/nar/gkm882
38. Cytoscape http://www.cytoscape.org
39. Lensky Y Schindler H Motility and reversible inactivation of honeybee spermatozoa in vivo and in vitro. Ann Abeille 1967, 10:5-16. 10.1051/ apido:19670101
40. Huss M Holme P Currency and commodity metabolites: Their identification and relation to the modularity of metabolic networks. IET Syst Biol 2007, 1:280-285. 10.1049/iet-syb:20060077 17907676
41. Prokupek A Hoffmann F Eyun SI Moriyama E Zhou M Harshman L An evolutionary expressed sequence tag analysis of Drosophila spermathecal genes. Evolution 2008, 62:2936-2947. 10.1111/j.1558-5646.2008.00493.x 18752616
42. Allen AK Spradling AC The Sf1-related nuclear hormone receptor Hr39 regulates Drosophila female reproductive tract development and function. Development 2008, 135:311-321. 10.1242/dev.015156 18077584
43. FlyAtlas: The Drosophila Gene Expression Atlas http://www.flyatlas.org
44. Chintapalli VR Wang J Dow JAT Using FlyAtlas to identify better Drosophila melanogaster models of human disease. Nat Genet 2007, 39:715-720. 10.1038/ng2049 17534367
45. Stevens TH Forgac M Structure, function and regulation of the vacuolar (H+)-ATPase. Annu Rev Cell Dev Biol 1997, 13:779-808. 10.1146/ annurev.cellbio.13.1.779 9442887
46. Nelson N Harvey WR Vacuolar and plasma membrane proton-adenosinetriphosphatases. Physiol Rev 1999, 79:361-385. 10221984
47. Verma LR Shuel RW Respiratory metabolism of the semen of the honeybee, Apis mellifera. J Insect Physiol 1973, 19:97-103. 10.1016/ 0022-1910(73)90225-4
48. Gessner B Ruttner F Transfer of spermatozoa into the spermatheca of the honey bee queen. Apidologie 1977, 8:1-18. 10.1051/apido:19770101
49. Kunieda T Fujiyuki T Kucharski R Foret S Ament SA Toth AL Ohashi K Takeuchi H Kamikouchi A Kage E Morioka M Beye M Kubo T Robinson GE Maleszka R Carbohydrate metabolism genes and pathways in insects: Insights from the honey bee genome. Insect Mol Biol 2006, 15:563-576. 1847477 17069632 10.1111/j.1365-2583.2006.00677.x
50. BeeBase: Hymenoptera Genome Database http://www.beebase.org
51. Kegg FTP Site ftp://ftp.genome.jp/pub/kegg/ligand/enzyme/enzyme
52. TargetP 1.1 Server http://www.cbs.dtu.dk/services/TargetP/
53. Psort Site http://psort.ims.u-tokyo.ac.jp/