Epigenetic effects of polymorphic Y chromosomes modulate chromatin components, immune response, and sexual conflict.
Genetic conflicts between sexes and generations provide a foundation for understanding the functional evolution of sex chromosomes and sexually dimorphic phenotypes. Y chromosomes of Drosophila contain multi-megabase stretches of satellite DNA repeats and a handful of protein-coding genes that are monomorphic within species. Nevertheless, polymorphic variation in heterochromatic Y chromosomes of Drosophila result in genome-wide gene expression variation. Here we show that such naturally occurring Y-linked regulatory variation (YRV) can be detected in somatic tissues and contributes to the epigenetic balance of heterochromatin/euchromatin at three distinct loci showing position-effect variegation (PEV). Moreover, polymorphic Y chromosomes differentially affect the expression of thousands of genes in XXY female genotypes in which Y-linked protein-coding genes are not transcribed. The data show a disproportionate influence of YRV on the variable expression of genes whose protein products localize to the nucleus, have nucleic-acid binding activity, and are involved in transcription, chromosome organization, and chromatin assembly. These include key components such as HP1, Trithorax-like (GAGA factor), Su(var)3-9, Brahma, MCM2, ORC2, and inner centromere protein. Furthermore, mitochondria-related genes, immune response genes, and transposable elements are also disproportionally affected by Y chromosome polymorphism. These functional clusterings may arise as a consequence of the involvement of Y-linked heterochromatin in the origin and resolution of genetic conflicts between males and females. Taken together, our results indicate that Y chromosome heterochromatin serves as a major source of epigenetic variation in natural populations that interacts with chromatin components to modulate the expression of biologically relevant phenotypic variation.
Lemos
Bernardo
B
Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA. blemos@oeb.harvard.edu
Branco
Alan T
AT
Hartl
Daniel L
DL
D000818:Animals; D002843:Chromatin / Q000502:physiology*; D004330:Drosophila / Q000235:genetics / Q000276:immunology / Q000502:physiology*; D044127:Epigenesis, Genetic; D005260:Female; D011110:Polymorphism, Genetic; D012726:Sexual Behavior, Animal; D014998:Y Chromosome
D002843:Chromatin
Annu Rev Genet. 1992;26:239-75
1482113
Genetics. 1997 Jul;146(3):891-902
9215895
Evolution. 2009 Dec;63(12):3124-35
19624721
Bioinformatics. 2003 May 1;19(7):891-2
12724301
Cell. 1997 Oct 31;91(3):311-23
9363940
J Cell Biol. 1998 Mar 23;140(6):1297-306
9508764
Annu Rev Entomol. 2007;52:171-92
16881818
Proc Natl Acad Sci U S A. 2001 May 8;98(10):5677-82
11320221
Proc Natl Acad Sci U S A. 2009 Oct 20;106(42):17829-34
19822756
EMBO Rep. 2002 Aug;3(8):747-52
12151333
J Exp Biol. 2004 Jul;207(Pt 16):2735-43
15235002
Gene. 2008 Feb 15;409(1-2):72-82
18182173
Genetics. 2010 Jan;184(1):295-307
19897751
Science. 2008 Jan 4;319(5859):42-3
18174425
Nucleic Acids Res. 2002 May 1;30(9):e36
11972351
Bioessays. 2008 May;30(5):409-11
18404685
J Biol Chem. 2007 Jul 20;282(29):20868-76
17526489
Mol Cell. 2000 Nov;6(5):1013-24
11106741
Science. 2008 Jan 4;319(5859):91-3
18174442
Trends Genet. 2009 Jun;25(6):270-7
19443075
Genetica. 2000;109(1-2):141-50
11293789
Heredity (Edinb). 2008 Jun;100(6):564-73
18414505
J Hered. 2010 Mar-Apr;101 Suppl 1:S94-9
20421329
Genome Biol. 2002;3(12):RESEARCH0071
12537560
Behav Genet. 2003 Jan;33(1):17-24
12645818
Genetics. 1999 Dec;153(4):1709-15
10581278
Science. 2007 Jun 15;316(5831):1625-8
17569867
Genetics. 2007 Mar;175(3):1241-50
17194772
Genetics. 1987 Mar;115(3):569-77
3569883
PLoS Genet. 2005 Jul;1(1):96-108
16103923
Genetics. 1991 Aug;128(4):785-97
1916244
J Cell Biol. 1967 Mar;32(3):663-75
6034483
Proc Natl Acad Sci U S A. 1998 May 26;95(11):6217-21
9600945
Bioessays. 1992 Sep;14(9):605-12
1365916
Genetics. 1989 Aug;122(4):793-800
2503420
Proc Natl Acad Sci U S A. 1989 Mar;86(6):1944-8
2494656
PLoS Genet. 2008 Dec;4(12):e1000313
19096519