A network of interactions among seminal proteins underlies the long-term postmating response in Drosophila.
Despite the importance of seminal proteins in fertility and their capacity to alter mated females' physiology, the molecular pathways and networks through which they act have not been well characterized. Drosophila seminal fluid includes proteins that fall into biochemical classes conserved from insects to mammals, making it an excellent model with which to address this question. Drosophila seminal fluid also contains a "sex peptide" (SP, Acp70A) that plays a major role in regulating egg production and mating behavior in females for several days after mating. This long-term postmating response (LTR) initially requires the association of SP with sperm. The LTR also requires members of the conserved seminal protein classes (two lectins, a protease, and a cysteine-rich secretory protein). Here, we show that these seminal proteins function interdependently, regulating a three-step cascade (first, at the level of seminal protein transfer to the female; second, at the level of stability; and third, at the level of localization within females), leading to the normal localization of SP to sperm-storage organs. This localization is, in turn, necessary for successful induction of the LTR. The requirements for manifestation of the LTR in Drosophila establish the paradigm that multiple seminal proteins can exert their actions through a multistep, multicomponent network of interactions.
Ram
K Ravi
KR
Department of Molecular Biology and Genetics, Biotechnology Building, Cornell University, Ithaca, NY 14853, USA.
Wolfner
Mariana F
MF
D000818:Animals; D015153:Blotting, Western; D003433:Crosses, Genetic; D004330:Drosophila / Q000502:physiology*; D029721:Drosophila Proteins / Q000378:metabolism*; D005260:Female; D005455:Fluorescent Antibody Technique; D008297:Male; D008954:Models, Biological; D010455:Peptides / Q000378:metabolism*; D011485:Protein Binding; D029589:Seminal Plasma Proteins / Q000378:metabolism*; D012726:Sexual Behavior, Animal / Q000502:physiology*; D013094:Spermatozoa / Q000378:metabolism*; D036341:Intercellular Signaling Peptides and Proteins
D029721:Drosophila Proteins; D010455:Peptides; D029589:Seminal Plasma Proteins; C056736:SP protein, Drosophila; D036341:Intercellular Signaling Peptides and Proteins
Proc Natl Acad Sci U S A. 2003 Aug 19;100(17):9929-33
12897240
Insect Biochem Mol Biol. 2005 Sep;35(9):1059-71
15979005
Proc Natl Acad Sci U S A. 2006 Dec 5;103(49):18674-9
17116868
Genetics. 2005 Jan;169(1):243-57
15466425
PLoS Biol. 2008 Jul 29;6(7):e178
18666829
Soc Reprod Fertil Suppl. 2007;65:353-6
17644975
Arch Insect Biochem Physiol. 1996;32(3-4):363-74
8756302
Genetics. 1999 Oct;153(2):845-57
10511562
Genetics. 1995 Jan;139(1):189-201
7705622
Nature. 2008 Jan 3;451(7174):33-7
18066048
Cell. 1985 Nov;43(1):97-104
3935320
Anim Behav. 1967 Apr-Jul;15(2):239-50
6030948
Neuron. 2009 Feb 26;61(4):519-26
19249273
PLoS Genet. 2007 Dec;3(12):e238
18085830
Insect Biochem Mol Biol. 1999 Dec;29(12):1043-52
10612039
Neuron. 1999 Mar;22(3):451-61
10197526
Prostate. 2000 Oct 1;45(2):132-9
11027412
Genetics. 2000 Dec;156(4):1879-88
11102381
Curr Biol. 2005 Feb 8;15(3):207-13
15694303
Genetics. 2007 Jun;176(2):1245-60
17435238
Genetics. 2007 Nov;177(3):1321-35
18039869
J Ultrastruct Mol Struct Res. 1988 Aug;100(2):173-82
3147297
Proc Natl Acad Sci U S A. 2004 Sep 14;101(37):13542-7
15345744
Dev Biol. 1995 Oct;171(2):694-702
7556947
Neuron. 2009 Feb 26;61(4):511-8
19249272
Mol Biol Evol. 2008 Mar;25(3):497-506
18056920
Eur J Biochem. 1994 Feb 15;220(1):45-53
7509746
PLoS Biol. 2008 Jul 29;6(7):e179
18666830
Proc Natl Acad Sci U S A. 2003 Aug 19;100(17):9923-8
12893873
Cell Mol Life Sci. 2003 Aug;60(8):1689-704
14504657
Peptides. 2004 Sep;25(9):1477-90
15374649
Proc Natl Acad Sci U S A. 2000 Nov 21;97(24):12953-5
11087851
Integr Comp Biol. 2007 Sep;47(3):427-45
21672851
Neuron. 1991 Oct;7(4):557-63
1931051
Insect Biochem Mol Biol. 2008 Mar;38(3):320-30
18252246
Mol Cell Endocrinol. 2006 May 16;250(1-2):157-62
16423450
Cells Tissues Organs. 2001;168(1-2):105-12
11114592
Proc Natl Acad Sci U S A. 2001 Jun 19;98(13):7375-9
11404480
J Mol Evol. 2006 Jun;62(6):793-802
16752217
Genetics. 2005 Sep;171(1):131-43
15944345
J Biol Chem. 2008 Feb 8;283(6):3031-3041
18056261