Abstract
BackgroundCoding 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.ResultsBased 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.ConclusionNatural selection appears to favor the compactness of highly expressed genes in chicken genome. This observation can be explained by the selection of economy model.ReviewersThis article was reviewed by Dr. Gavin Huttley, Dr. Liran Carmel (nominated by Dr. Eugene V. Koonin) and Dr. Araxi Urrutia (nominated by Dr. Laurence D. Hurst).
Highlights
Coding sequence (CDS) length, gene size, and intron length vary within a genome and among genomes
We found that gene size, coding sequence (CDS) length, first intron length, average intron length, and total intron length are negatively correlated with expression level and expression breadth
CDS length, first intron length, average intron length and total intron length are negatively correlated with expression level Only genes with no evidence of multiple-splicing forms and genes with no obvious annotation errors were included in this study
Summary
Coding sequence (CDS) length, gene size, and intron length vary within a genome and among genomes. In this study the chicken was used as a model organism to elucidate the interaction between gene features and expression pattern upon selection pressure Gene characteristics such as gene size, coding sequence (CDS) length, intron density and intron length, exon density and exon length, as well as amino acid composition are determined by many factors. Urrutia et al [2] gathered expression data for > 10,000 human genes from public datasets obtained by different technologies (SAGE and high-density oligonucleotide chip arrays) and compared them with gene parameters They found that, even after controlling for regional effects, highly expressed genes coding the smaller proteins, have less intronic DNA and higher codon and amino acid biases. They argued that this correlation is more likely to be explained by the higher abundance of cis -regulatory elements in introns (especially first introns) in genes under strong selective constraints
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