Evolution of chromosome organization driven by selection for reduced gene expression noise
- PMID: 17660811
- DOI: 10.1038/ng2071
Evolution of chromosome organization driven by selection for reduced gene expression noise
Abstract
The distribution of genes on eukaryotic chromosomes is nonrandom, but the reasons behind this are not well understood. The commonly observed clustering of essential genes is a case in point. Here we model and test a new hypothesis. Essential proteins are unusual in that random fluctuations in abundance (noise) can be highly deleterious. We hypothesize that persistently open chromatin domains are sinks for essential genes, as they enable reduced noise by avoidance of transcriptional bursting associated with chromatin remodeling. Simulation of the model captures clustering and correctly predicts that (i) essential gene clusters are associated with low nucleosome occupancy (ii) noise-sensitive nonessential genes cluster with essential genes (iii) nonessential genes of similar knockout fitness are physically linked (iv) genes in domains rich in essential genes have low noise (v) essential genes are rare subtelomerically and (vi) essential gene clusters are preferentially conserved. We conclude that different noise characteristics of different genomic domains favors nonrandom gene positioning. This has implications for gene therapy and understanding transgenic phenotypes.
Similar articles
-
The impact of nucleosome positioning on the organization of replication origins in eukaryotes.Biochem Biophys Res Commun. 2009 Jul 31;385(3):363-8. doi: 10.1016/j.bbrc.2009.05.072. Epub 2009 May 20. Biochem Biophys Res Commun. 2009. PMID: 19463783
-
Transcriptional coupling of neighboring genes and gene expression noise: evidence that gene orientation and noncoding transcripts are modulators of noise.Genome Biol Evol. 2011;3:320-31. doi: 10.1093/gbe/evr025. Epub 2011 Mar 14. Genome Biol Evol. 2011. PMID: 21402863 Free PMC article.
-
Evidence for co-evolution of gene order and recombination rate.Nat Genet. 2003 Mar;33(3):392-5. doi: 10.1038/ng1111. Epub 2003 Feb 10. Nat Genet. 2003. PMID: 12577060
-
Coexpression, coregulation, and cofunctionality of neighboring genes in eukaryotic genomes.Genomics. 2008 Mar;91(3):243-8. doi: 10.1016/j.ygeno.2007.11.002. Epub 2007 Dec 21. Genomics. 2008. PMID: 18082363 Review.
-
Gene Positioning Effects on Expression in Eukaryotes.Annu Rev Genet. 2015;49:627-46. doi: 10.1146/annurev-genet-112414-055008. Epub 2015 Oct 2. Annu Rev Genet. 2015. PMID: 26436457 Review.
Cited by
-
Predictive features of gene expression variation reveal mechanistic link with differential expression.Mol Syst Biol. 2020 Aug;16(8):e9539. doi: 10.15252/msb.20209539. Mol Syst Biol. 2020. PMID: 32767663 Free PMC article.
-
The genomic landscape and evolutionary resolution of antagonistic pleiotropy in yeast.Cell Rep. 2012 Nov 29;2(5):1399-410. doi: 10.1016/j.celrep.2012.09.017. Epub 2012 Oct 25. Cell Rep. 2012. PMID: 23103169 Free PMC article.
-
Systematic identification of balanced transposition polymorphisms in Saccharomyces cerevisiae.PLoS Genet. 2009 Jun;5(6):e1000502. doi: 10.1371/journal.pgen.1000502. Epub 2009 Jun 5. PLoS Genet. 2009. PMID: 19503594 Free PMC article.
-
An Individual-Based Diploid Model Predicts Limited Conditions Under Which Stochastic Gene Expression Becomes Advantageous.Front Genet. 2015 Nov 24;6:336. doi: 10.3389/fgene.2015.00336. eCollection 2015. Front Genet. 2015. PMID: 26635872 Free PMC article.
-
Independent regulation of gene expression level and noise by histone modifications.PLoS Comput Biol. 2017 Jun 30;13(6):e1005585. doi: 10.1371/journal.pcbi.1005585. eCollection 2017 Jun. PLoS Comput Biol. 2017. PMID: 28665997 Free PMC article.
Publication types
MeSH terms
Grants and funding
LinkOut - more resources
Full Text Sources
Molecular Biology Databases
