Context-dependent codon bias and messenger RNA longevity in the yeast transcriptome.

Context-dependent codon bias and its relationship with messenger RNA (mRNA) longevity was examined in 4,648 mRNA transcripts of the Saccharomyces cerevisiae transcriptome for which mRNA half-lives have been empirically determined. Surprisingly, rare codon usage (codons used <13 times per 1,000 codons in the genome) increased with mRNA half-life. However, it is shown that this pattern was not due to preference for rare codon use within codon families containing both rare and nonrare codons. Rather, the pattern was due to an increase in the frequency of amino acids encoded solely by rare codons, and a decrease in the frequency of amino acids never encoded by rare codons, with mRNA half-life. When standardized by open reading frame length, the use of consecutive rare codons was also positively correlated with mRNA half-life. There was negative correlation between the usage of synonymous A|T dinucleotides spanning codon boundaries and mRNA half-life, despite the fact that the frequency of AT dinucleotide usage overall, and AT dinucleotide usage at other codon position contexts (e.g., 1-2, 2-3, or 3|1 total), was not correlated with mRNA half-life. The use of A|T dinucleotides at synonymous dicodon boundaries could potentially allow for more efficient 3'-5' degradation by endonucleolytic cleavage.

[1]  A. E. Hirsh,et al.  Noise Minimization in Eukaryotic Gene Expression , 2004, PLoS biology.

[2]  J. Parsch,et al.  Pleiotropic Effect of Disrupting a Conserved Sequence Involved in a Long-Range Compensatory Interaction in the Drosophila Adh Gene , 2004, Genetics.

[3]  J. Duan,et al.  Mammalian Mutation Pressure, Synonymous Codon Choice, and mRNA Degradation , 2003, Journal of Molecular Evolution.

[4]  C. Burge,et al.  Widespread selection for local RNA secondary structure in coding regions of bacterial genes. , 2003, Genome research.

[5]  Hiroshi Akashi,et al.  Translational selection and yeast proteome evolution. , 2003, Genetics.

[6]  Michael Zuker,et al.  Mfold web server for nucleic acid folding and hybridization prediction , 2003, Nucleic Acids Res..

[7]  Simon Kasif,et al.  On the normalization of RNA equilibrium free energy to the length of the sequence. , 2003, Nucleic acids research.

[8]  Mads Kærn,et al.  Noise in eukaryotic gene expression , 2003, Nature.

[9]  John D. Storey,et al.  Genome-wide analysis of mRNA translation profiles in Saccharomyces cerevisiae , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[10]  R. Parker,et al.  mRNA decay enzymes: Decappers conserved between yeast and mammals , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[11]  John D. Storey,et al.  Precision and functional specificity in mRNA decay , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[12]  L. Isaksson,et al.  Influences on translation initiation and early elongation by the messenger RNA region flanking the initiation codon at the 3' side. , 2002, Gene.

[13]  Alexei Fedorov,et al.  Regularities of context-dependent codon bias in eukaryotic genes. , 2002, Nucleic acids research.

[14]  Ivan Ivanov,et al.  Missing Codon Pairs in the Genome of Escherichia Coli , 2002, Bioinform..

[15]  H. Akashi,et al.  Gene expression and molecular evolution. , 2001, Current opinion in genetics & development.

[16]  W. Stephan,et al.  The relationship between third-codon position nucleotide content, codon bias, mRNA secondary structure and gene expression in the drosophilid alcohol dehydrogenase genes Adh and Adhr. , 2001, Genetics.

[17]  S. Peltz,et al.  Regulated ARE-mediated mRNA decay in Saccharomyces cerevisiae. , 2001, Molecular cell.

[18]  Patrick O. Brown,et al.  Global and Specific Translational Regulation in the Genomic Response of Saccharomyces cerevisiae to a Rapid Transfer from a Fermentable to a Nonfermentable Carbon Source , 2001, Molecular and Cellular Biology.

[19]  W. Tate,et al.  Codon bias at the 3'-side of the initiation codon is correlated with translation initiation efficiency in Escherichia coli. , 2001, Gene.

[20]  H. Beug,et al.  Isolation of translationally controlled mRNAs by differential screening , 2000, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[21]  A. Krogh,et al.  No evidence that mRNAs have lower folding free energies than random sequences with the same dinucleotide distribution. , 1999, Nucleic acids research.

[22]  P. Brown,et al.  Identification of eukaryotic mRNAs that are translated at reduced cap binding complex eIF4F concentrations using a cDNA microarray. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[23]  M. Schummer,et al.  Messenger RNA translation state: the second dimension of high-throughput expression screening. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[24]  C. Squires,et al.  Enhancement of translation by the downstream box does not involve base pairing of mRNA with the penultimate stem sequence of 16S rRNA. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[25]  K. Struhl.  Fundamentally Different Logic of Gene Regulation in Eukaryotes and Prokaryotes , 1999, Cell.

[26]  M. Kreitman,et al.  The Nonrandom Location of Synonymous Codons Suggests That Reading Frame-Independent Forces Have Patterned Codon Preferences , 1999, Journal of Molecular Evolution.

[27]  David W. Digby,et al.  mRNAs have greater negative folding free energies than shuffled or codon choice randomized sequences. , 1999, Nucleic acids research.

[28]  A. Moreira,et al.  Degradation of hammerhead ribozymes by human ribonucleases , 1998, Molecular and General Genetics MGG.

[29]  A. Gingras,et al.  The mRNA 5' cap-binding protein eIF4E and control of cell growth. , 1998, Current opinion in cell biology.

[30]  Etsuko N. Moriyama,et al.  Codon Usage Bias and tRNA Abundance in Drosophila , 1997, Journal of Molecular Evolution.

[31]  O. Berg,et al.  Codon bias in Escherichia coli: the influence of codon context on mutation and selection. , 1997, Nucleic acids research.

[32]  J. Parsch,et al.  Site-directed mutations reveal long-range compensatory interactions in the Adh gene of Drosophila melanogaster. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[33]  S. Karlin,et al.  What drives codon choices in human genes? , 1996, Journal of molecular biology.

[34]  L. Kuo,et al.  Cleavage of Oligoribonucleotides by the 2′,5′-Oligoadenylate- dependent Ribonuclease L (*) , 1996, The Journal of Biological Chemistry.

[35]  G. Caponigro,et al.  Mechanisms and control of mRNA turnover in Saccharomyces cerevisiae. , 1996, Microbiological reviews.

[36]  R. Schneider,et al.  Rapid degradation of AU-rich element (ARE) mRNAs is activated by ribosome transit and blocked by secondary structure at any position 5' to the ARE , 1995, Molecular and cellular biology.

[37]  R Parker,et al.  Turnover mechanisms of the stable yeast PGK1 mRNA , 1995, Molecular and cellular biology.

[38]  R Parker,et al.  Deadenylation of the unstable mRNA encoded by the yeast MFA2 gene leads to decapping followed by 5'-->3' digestion of the transcript. , 1994, Genes & development.

[39]  G. Caponigro,et al.  A small segment of the MAT alpha 1 transcript promotes mRNA decay in Saccharomyces cerevisiae: a stimulatory role for rare codons , 1993, Molecular and cellular biology.

[40]  A. Sachs,et al.  Messenger RNA degradation in eukaryotes , 1993, Cell.

[41]  R Parker,et al.  A turnover pathway for both stable and unstable mRNAs in yeast: evidence for a requirement for deadenylation. , 1993, Genes & development.

[42]  M. Bulmer.  The selection-mutation-drift theory of synonymous codon usage. , 1991, Genetics.

[43]  R Parker,et al.  Identification and comparison of stable and unstable mRNAs in Saccharomyces cerevisiae , 1990, Molecular and cellular biology.

[44]  F. Wright.  The 'effective number of codons' used in a gene. , 1990, Gene.

[45]  R. Kastelein,et al.  Codon replacement in the PGK1 gene of Saccharomyces cerevisiae: experimental approach to study the role of biased codon usage in gene expression , 1987, Molecular and cellular biology.

[46]  Paul M. Sharp,et al.  Codon usage in yeast: cluster analysis clearly differentiates highly and lowly expressed genes , 1986, Nucleic Acids Res..

[47]  E. G. Shpaer.  Constraints on codon context in Escherichia coli genes. Their possible role in modulating the efficiency of translation. , 1986, Journal of molecular biology.

[48]  M Yarus,et al.  Sense codons are found in specific contexts. , 1985, Journal of molecular biology.

[49]  T. Ikemura.  Correlation between the abundance of yeast transfer RNAs and the occurrence of the respective codons in protein genes. Differences in synonymous codon choice patterns of yeast and Escherichia coli with reference to the abundance of isoaccepting transfer RNAs. , 1982, Journal of molecular biology.

[50]  W. Fiers,et al.  Preferential codon usage in prokaryotic genes: the optimal codon-anticodon interaction energy and the selective codon usage in efficiently expressed genes. , 1982, Gene.

[51]  T. Ikemura.  Correlation between the abundance of Escherichia coli transfer RNAs and the occurrence of the respective codons in its protein genes: a proposal for a synonymous codon choice that is optimal for the E. coli translational system. , 1981, Journal of molecular biology.

[52]  R Nussinov,et al.  Eukaryotic dinucleotide preference rules and their implications for degenerate codon usage. , 1981, Journal of molecular biology.

[53]  T. Ikemura.  Correlation between the abundance of Escherichia coli transfer RNAs and the occurrence of the respective codons in its protein genes. , 1981, Journal of molecular biology.

[54]  R. Parker,et al.  Mechanisms and control of mRNA decapping in Saccharomyces cerevisiae. , 2000, Annual review of biochemistry.

[55]  D. Morris.  Growth control of translation in mammalian cells. , 1995, Progress in nucleic acid research and molecular biology.

[56]  J A Koziol,et al.  Evolution of the genome and the genetic code: selection at the dinucleotide level by methylation and polyribonucleotide cleavage. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[57]  Jeffrey W. Smith,et al.  Stochastic Gene Expression in a Single Cell , 2022 .