Haplotype structure and expression divergence at the Drosophila cellular immune gene eater.
The protein Eater plays an important role in microbial recognition and defensive phagocytosis in Drosophila melanogaster. We sequenced multiple alleles of the eater gene from an African and a North American population of D. melanogaster and found signatures of a partial selective sweep in North America that is localized around the second intron. This pattern is consistent with local adaptation to novel selective pressures during range expansion out of Africa. The North American sample is divided into two predominant haplotype groups, and the putatively selected haplotype is associated with a significantly higher gene expression level, suggesting that gene regulation is a possible target of selection. The eater alleles contain from 22 to 40 repeat units that are characterized by the presence of a cysteine-rich NIM motif. NIM repeats in the structural stalk of the protein exhibit concerted evolution as a function of physical location in the repeat array. Several NIM repeats within eater have previously been implicated in binding to microbial ligands, a function which in principle might subject them to special evolutionary pressures. However, we find no evidence of elevated positive selection on these pathogen-interacting units. Our study presents an instance where gene expression rather than protein structure is thought to drive the adaptive evolution of a pathogen recognition molecule in the immune system.
Juneja
Punita
P
Department of Entomology, Cornell University, Ithaca, New York, USA. pj46@cornell.edu
Lazzaro
Brian P
BP
D000220:Adaptation, Biological / Q000235:genetics / Q000276:immunology; D000818:Animals; D001483:Base Sequence; D016000:Cluster Analysis; D003198:Computer Simulation; D029721:Drosophila Proteins / Q000235:genetics* / Q000378:metabolism; D004331:Drosophila melanogaster / Q000235:genetics* / Q000276:immunology; D019143:Evolution, Molecular; D005786:Gene Expression Regulation / Q000235:genetics*; D014644:Genetic Variation; D005828:Genetics, Population; D006239:Haplotypes / Q000235:genetics*; D016013:Likelihood Functions; D008957:Models, Genetic; D008969:Molecular Sequence Data; D011956:Receptors, Cell Surface / Q000235:genetics* / Q000378:metabolism; D012641:Selection, Genetic; D016415:Sequence Alignment; D017422:Sequence Analysis, DNA; D014481:United States; D015030:Zimbabwe
D029721:Drosophila Proteins; D011956:Receptors, Cell Surface; C505820:eater protein, Drosophila
Genome Biol. 2008 Jan 21;9(1):R12
18208589
Genetics. 1997 Jul;146(3):1197-206
9215920
Curr Biol. 2007 Apr 3;17(7):649-54
17363253
Evolution. 2003 Aug;57(8):1829-36
14503624
Genes Immun. 2006 Mar;7(2):179-83
16222342
Nature. 2002 Oct 24;419(6909):832-7
12397357
Genetics. 2005 Apr;169(4):2013-22
15654108
PLoS Genet. 2006 Oct 13;2(10):e166
17040129
Science. 2000 Mar 24;287(5461):2185-95
10731132
Science. 2005 Jul 29;309(5735):764-7
16051794
Mol Biol Evol. 1989 Mar;6(2):198-212
2716519
Genome Res. 2009 May;19(5):804-14
19265028
Genetics. 1997 Oct;147(2):915-25
9335623
Science. 1976 Feb 13;191(4227):528-35
1251186
Nature. 1994 Sep 15;371(6494):215-20
8078581
Bioinformatics. 2009 Jun 1;25(11):1451-2
19346325
Nat Genet. 2007 Dec;39(12):1461-8
17987029
J Mol Evol. 2006 Dec;63(6):769-80
17103056
Genetics. 2000 Jul;155(3):1405-13
10880498
Genetics. 2007 Jun;176(2):1245-60
17435238
PLoS Pathog. 2008 Mar 14;4(3):e1000025
18369474
Mech Dev. 2008 Jul;125(7):617-30
18448314
Genetics. 2005 Apr;169(4):2023-34
15716507
J Mol Evol. 2004 Oct;59(4):498-506
15638461
PLoS Biol. 2007 Nov 6;5(11):e310
17988176
Genetics. 2006 Feb;172(2):1093-105
16322515
Genetics. 2005 Feb;169(2):709-22
15520267
PLoS Pathog. 2009 Apr;5(4):e1000385
19381251
Immunity. 2001 Dec;15(6):1027-38
11754822
Cell. 2005 Oct 21;123(2):335-46
16239149
Genetics. 1995 Jul;140(3):1019-32
7672574
Insect Mol Biol. 2005 Dec;14(6):599-605
16313560
Genesis. 2009 Nov;47(11):771-4
19830816
Mol Biol Evol. 1986 Sep;3(5):418-26
3444411
Proc Natl Acad Sci U S A. 1981 Nov;78(11):7052-5
6273906
Mol Biol Evol. 2008 Nov;25(11):2337-47
18703524
Proc Natl Acad Sci U S A. 1997 Jul 22;94(15):7725-9
9223255
Mol Biol Evol. 2008 Jun;25(6):1025-42
18199829
Genetics. 2006 Mar;172(3):1607-19
16299396
Mol Biol Evol. 2007 Aug;24(8):1596-9
17488738
Bioinformatics. 2002 Feb;18(2):337-8
11847089
Genes Dev. 1996 Jun 1;10(11):1411-21
8647437
J Biol Chem. 2008 Aug 22;283(34):23376-87
18524767
Trends Genet. 1988 Apr;4(4):106-11
3149056
Evolution. 2005 Nov;59(11):2312-23
16396172
Bioinformatics. 2004 Jan 22;20(2):289-90
14734327
Mol Biol Evol. 2004 Aug;21(8):1482-91
15014160
Genetics. 1988 Nov;120(3):831-40
3147214
Genet Res. 1974 Feb;23(1):23-35
4407212
Genetics. 1989 Nov;123(3):585-95
2513255
Genetics. 2006 Jan;172(1):287-92
16204221