Abstract
The origin and importance of exon-intron architecture comprises one of the remaining mysteries of gene evolution. Several studies have investigated the variations of intron length, GC content, ordinal position in a gene and divergence. However, there is little study about the structural variation of exons and introns. We investigated the length, GC content, ordinal position and divergence in both exons and introns of 13 eukaryotic genomes, representing plant and animal. Our analyses revealed that three basic patterns of exon-intron variation were present in nearly all analyzed genomes (P < 0.001 in most cases): an ordinal reduction of length and divergence in both exon and intron, a co-variation between exon and its flanking introns in their length, GC content and divergence, and a decrease of average exon (or intron) length, GC content and divergence as the total exon numbers of a gene increased. In addition, we observed that the shorter introns had either low or high GC content, and the GC content of long introns was intermediate. Although the factors contributing to these patterns have not been identified, our results provide three important clues: common factor(s) exist and may shape both exons and introns; the ordinal reduction patterns may reflect a time-orderly evolution; and the larger first and last exons may be splicing-required. These clues provide a framework for elucidating mechanisms involved in the organization of eukaryotic genomes and particularly in building exon-intron structures.
MeSH Terms
Animals
Base Composition
Evolution, Molecular
Exons
Genetic Variation
Genome
Humans
Introns
Plants
Sequence Alignment
Sequence Analysis, DNA
Species Specificity
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Zhu Liucun
State Key Laboratory of Pharmaceutical Biotechnology, Department of Biology, Nanjing University, Nanjing 210093, PR China. zhuliucun@gmail.com
Zhang Ying
Zhang Wen
Yang Sihai
Chen Jian-Qun
Tian Dacheng
References (31)
31 references, click to expand
-
Patterns and rates of intron divergence between humans and chimpanzees.
Genome Biol. 2007;8(2):R21
PMID: 17309804
-
So much "junk" DNA in our genome.
Brookhaven Symp Biol. 1972;23:366-70
PMID: 5065367
-
An isochore map of human chromosomes.
Genome Res. 2006 Apr;16(4):536-41
PMID: 16597586
-
Architectural limits on split genes.
Proc Natl Acad Sci U S A. 1996 Dec 24;93(26):15081-5
PMID: 8986767
-
On the abundance and distribution of transposable elements in the genome of Drosophila melanogaster.
Mol Biol Evol. 2002 Jun;19(6):926-37
PMID: 12032249
-
Evidence for DNA loss as a determinant of genome size.
Science. 2000 Feb 11;287(5455):1060-2
PMID: 10669421
-
Dynamics and function of intron sequences of the wingless gene during the evolution of the Drosophila genus.
Evol Dev. 2004 Sep-Oct;6(5):325-35
PMID: 15330865
-
Intron-exon structures of eukaryotic model organisms.
Nucleic Acids Res. 1999 Aug 1;27(15):3219-28
PMID: 10454621
-
First exons and introns--a survey of GC content and gene structure in the human genome.
In Silico Biol. 2006;6(3):237-42
PMID: 16922687
-
Proceedings of the SMBE Tri-National Young Investigators' Workshop 2005. Investigating the intron recognition mechanism in eukaryotes.
Mol Biol Evol. 2006 May;23(5):901-10
PMID: 16371412
-
The neoselectionist theory of genome evolution.
Proc Natl Acad Sci U S A. 2007 May 15;104(20):8385-90
PMID: 17494746
-
Distribution and characterization of regulatory elements in the human genome.
Genome Res. 2002 Dec;12(12):1827-36
PMID: 12466286
-
Analysis of evolution of exon-intron structure of eukaryotic genes.
Brief Bioinform. 2005 Jun;6(2):118-34
PMID: 15975222
-
Why genes in pieces?
Nature. 1978 Feb 9;271(5645):501
PMID: 622185
-
Patterns of intron sequence evolution in Drosophila are dependent upon length and GC content.
Genome Biol. 2005;6(8):R67
PMID: 16086849
-
Why do genes have introns? Recombination might add a new piece to the puzzle.
Trends Genet. 2001 Apr;17(4):172-5
PMID: 11275306
-
Preferential loss and gain of introns in 3' portions of genes suggests a reverse-transcription mechanism of intron insertion.
Gene. 2004 Aug 18;338(1):85-91
PMID: 15302409
-
Selfish DNA and the origin of introns.
Nature. 1985 May 23-29;315(6017):283-4
PMID: 2987701
-
The small nucleolar RNAs.
Annu Rev Biochem. 1995;64:897-934
PMID: 7574504
-
Analysis of conserved noncoding DNA in Drosophila reveals similar constraints in intergenic and intronic sequences.
Genome Res. 2001 Aug;11(8):1335-45
PMID: 11483574
-
Group II intron retroelements: function and diversity.
Cytogenet Genome Res. 2005;110(1-4):589-97
PMID: 16093712
-
Heterologous introns can enhance expression of transgenes in mice.
Proc Natl Acad Sci U S A. 1991 Jan 15;88(2):478-82
PMID: 1988947
-
What controls the length of noncoding DNA?
Curr Opin Genet Dev. 2001 Dec;11(6):652-9
PMID: 11682309
-
Human-mouse alignments with BLASTZ.
Genome Res. 2003 Jan;13(1):103-7
PMID: 12529312
-
Intron requirement for expression of the human purine nucleoside phosphorylase gene.
Nucleic Acids Res. 1992 Jun 25;20(12):3191-8
PMID: 1620616
-
Alternative splicing and RNA selection pressure--evolutionary consequences for eukaryotic genomes.
Nat Rev Genet. 2006 Jul;7(7):499-509
PMID: 16770337
-
Intron size and exon evolution in Drosophila.
Genetics. 2005 May;170(1):481-5
PMID: 15781704
-
The architecture of pre-mRNAs affects mechanisms of splice-site pairing.
Proc Natl Acad Sci U S A. 2005 Nov 8;102(45):16176-81
PMID: 16260721
-
Selective constraints on intron evolution in Drosophila.
Genetics. 2003 Dec;165(4):1843-51
PMID: 14704170
-
The evolution of controlled multitasked gene networks: the role of introns and other noncoding RNAs in the development of complex organisms.
Mol Biol Evol. 2001 Sep;18(9):1611-30
PMID: 11504843
-
Distributions of exons and introns in the human genome.
In Silico Biol. 2004;4(4):387-93
PMID: 15217358