Selection for the compactness of highly expressed genes in Gallus gallus.
BACKGROUND
Coding sequence (CDS) length, gene size, and intron length vary within a genome and among genomes. Previous studies in diverse organisms, including human, D. Melanogaster, C. elegans, S. cerevisiae, and Arabidopsis thaliana, indicated that there are negative relationships between expression level and gene size, CDS length as well as intron length. Different models such as selection for economy model, genomic design model, and mutational bias hypotheses have been proposed to explain such observation. The debate of which model is a superior one to explain the observation has not been settled down. The chicken (Gallus gallus) is an important model organism that bridges the evolutionary gap between mammals and other vertebrates. As D. Melanogaster, chicken has a larger effective population size, selection for chicken genome is expected to be more effective in increasing protein synthesis efficiency. Therefore, in this study the chicken was used as a model organism to elucidate the interaction between gene features and expression pattern upon selection pressure.


RESULTS
Based on different technologies, we gathered expression data for nuclear protein coding, single-splicing genes from Gallus gallus genome and compared them with gene parameters. We found that gene size, CDS length, first intron length, average intron length, and total intron length are negatively correlated with expression level and expression breadth significantly. The tissue specificity is positively correlated with the first intron length but negatively correlated with the average intron length, and not correlated with the CDS length and protein domain numbers. Comparison analyses showed that ubiquitously expressed genes and narrowly expressed genes with the similar expression levels do not differ in compactness. Our data provided evidence that the genomic design model can not, at least in part, explain our observations. We grouped all somatic-tissue-specific genes (n = 1105), and compared the first intron length and the average intron length between highly expressed genes (top 5% expressed genes) and weakly expressed genes (bottom 5% expressed genes). We found that the first intron length and the average intron length in highly expressed genes are not different from that in weakly expressed genes. We also made a comparison between ubiquitously expressed genes and narrowly expressed somatic genes with similar expression levels. Our data demonstrated that ubiquitously expressed genes are less compact than narrowly expressed genes with the similar expression levels. Obviously, these observations can not be explained by mutational bias hypotheses either. We also found that the significant trend between genes' compactness and expression level could not be affected by local mutational biases. We argued that the selection of economy model is most likely one to explain the relationship between gene expression and gene characteristics in chicken genome.


CONCLUSIONS
Natural selection appears to favor the compactness of highly expressed genes in chicken genome. This observation can be explained by the selection of economy model.
Rao
You S
YS
Department of Biological Technology, Jiangxi Educational Institute, Nanchang, Jiangxi, China.
Wang
Zhang F
ZF
Chai
Xue W
XW
Wu
Guo Z
GZ
Zhou
Ming
M
Nie
Qing H
QH
Zhang
Xi Q
XQ
D000818:Animals; D002645:Chickens / Q000235:genetics*; D016678:Genome / Q000235:genetics; D007438:Introns / Q000235:genetics
PLoS One. 2008 Aug 29;3(8):e3093
18769727
Genome Res. 2003 Sep;13(9):1998-2004
12915492
Genetics. 2004 Jul;167(3):1293-304
15280243
PLoS One. 2009 Jul 27;4(7):e6356
19633720
Genome Res. 2006 Mar;16(3):347-54
16461636
Nat Genet. 2002 Aug;31(4):415-8
12134150
Genetics. 2000 Nov;156(3):1285-98
11063702
BMC Evol Biol. 2008 May 20;8:154
18492248
Bioinformatics. 2005 Mar 1;21(5):650-9
15388519
Trends Genet. 2008 Oct;24(10):481-4
18786740
Genetics. 2005 May;170(1):481-5
15781704
Nucleic Acids Res. 2006;34(20):5906-14
17062620
Genome Res. 2003 Oct;13(10):2260-4
12975314
Trends Genet. 2008 Aug;24(8):375-8
18586348
Trends Genet. 2003 Jul;19(7):362-5
12850439
Genome Res. 2006 Nov;16(11):1339-44
17065604
Biol Direct. 2009 Nov 21;4:45; discussion 45
19930585
Nat Struct Mol Biol. 2009 Nov;16(11):1128-33
19820712
Nature. 2004 Dec 9;432(7018):695-716
15592404
Genome Res. 2004 Aug;14(8):1530-6
15256508
Genome Biol. 2005;6(8):R67
16086849
J Evol Biol. 2007 May;20(3):1223-9
17465932
Hum Mol Genet. 2005 Sep 1;14(17):2533-46
16037065
J Biol. 2004;3(5):21
15588312
J Mol Evol. 2007 May;64(5):511-8
17460807
Mol Biol Evol. 2005 Jun;22(6):1475-81
15788745
Biochem Biophys Res Commun. 2007 Aug 31;360(3):586-92
17610841
J Biol. 2009;8(3):33
19371447
Curr Opin Genet Dev. 2001 Dec;11(6):652-9
11682309
Nature. 2004 Dec 9;432(7018):717-22
15592405
Genome Biol Evol. 2009 Sep 22;1:382-90
20333206
Trends Genet. 2004 May;20(5):248-53
15109779
PLoS Genet. 2005 Aug;1(2):e13
16110339
Genetica. 2002 May;115(1):81-91
12188050
Yi Chuan. 2007 Sep;29(9):1083-8
17855258
BMC Genomics. 2009 May 09;10:213
19426519
Science. 2003 May 30;300(5624):1393
12775832
Trends Genet. 2005 Apr;21(4):203-7
15797613
Genome Res. 2007 Jul;17(7):1045-50
17495009
Evolution. 2005 Jan;59(1):126-37
15792233
Mol Biol Evol. 2004 Jun;21(6):1014-23
15014158
Genome Res. 2000 Jan;10(1):137-47
10645958