Codon Usage Heterogeneity in the Multipartite Prokaryote Genome. Selection-Based Coding Bias Associated with Gene Location, Expression Level, and Ancestry
López JL, Lozano MJ, Lagares A, Fabre ML, Draghi WO, Del Papa MF, Pistorio M, Becker A, Wibberg D, Schlüter A, Pühler A, et al. (2019)
mBio 10(3): e00505-19.
Zeitschriftenaufsatz
| Veröffentlicht | Englisch
Download
Autor*in
López, J. L.;
Lozano, M. J.;
Lagares, A.;
Fabre, M. L.;
Draghi, W. O.;
Del Papa, M. F.;
Pistorio, M.;
Becker, A.;
Wibberg, DanielUniBi;
Schlüter, AndreasUniBi ;
Pühler, AlfredUniBi ;
Blom, J.
Alle
Alle
Abstract / Bemerkung
Prokaryotes represent an ancestral lineage in the tree of life and constitute optimal resources for investigating the evolution of genomes in unicellular organisms. Many bacterial species possess multipartite genomes offering opportunities to study functional variations among replicons, how and where new genes integrate into a genome, and how genetic information within a lineage becomes encoded and evolves. To analyze these issues, we focused on the model soil bacterium Sinorhizobium meliloti , which harbors a chromosome, a chromid (pSymB), a megaplasmid (pSymA), and, in many strains, one or more accessory plasmids. The analysis of several genomes, together with 1.4 Mb of accessory plasmid DNA that we purified and sequenced, revealed clearly different functional profiles associated with each genomic entity. pSymA, in particular, exhibited remarkable interstrain variation and a high density of singletons (unique, exclusive genes) featuring functionalities and modal codon usages that were very similar to those of the plasmidome. All this evidence reinforces the idea of a close relationship between pSymA and the plasmidome. Correspondence analyses revealed that adaptation of codon usages to the translational machinery increased from plasmidome to pSymA to pSymB to chromosome, corresponding as such to the ancestry of each replicon in the lineage. We demonstrated that chromosomal core genes gradually adapted to the translational machinery, reminiscent of observations in several bacterial taxa for genes with high expression levels. Such findings indicate a previously undiscovered codon usage adaptation associated with the chromosomal core information that likely operates to improve bacterial fitness. We present a comprehensive model illustrating the central findings described here, discussed in the context of the changes occurring during the evolution of a multipartite prokaryote genome.
IMPORTANCE Bacterial genomes usually include many thousands of genes which are expressed with diverse spatial-temporal patterns and intensities. A well-known evidence is that highly expressed genes, such as the ribosomal and other translation-related proteins (RTRPs), have accommodated their codon usage to optimize translation efficiency and accuracy. Using a bioinformatic approach, we identify core-genes sets with different ancestries, and demonstrate that selection processes that optimize codon usage are not restricted to RTRPs but extended at a genome-wide scale. Such findings highlight, for the first time, a previously undiscovered adaptation strategy associated with the chromosomal-core information. Contrasted with the translationally more adapted genes, singletons (i.e., exclusive genes, including those of the plasmidome) appear as the gene pool with the less-ameliorated codon usage in the lineage. A comprehensive summary describing the inter- and intra-replicon heterogeneity of codon usages in a complex prokaryote genome is presented.
Erscheinungsjahr
2019
Zeitschriftentitel
mBio
Band
10
Ausgabe
3
Art.-Nr.
e00505-19
ISSN
2150-7511
eISSN
2150-7511
Page URI
https://pub.uni-bielefeld.de/record/2935899
Zitieren
López JL, Lozano MJ, Lagares A, et al. Codon Usage Heterogeneity in the Multipartite Prokaryote Genome. Selection-Based Coding Bias Associated with Gene Location, Expression Level, and Ancestry. mBio. 2019;10(3): e00505-19.
López, J. L., Lozano, M. J., Lagares, A., Fabre, M. L., Draghi, W. O., Del Papa, M. F., Pistorio, M., et al. (2019). Codon Usage Heterogeneity in the Multipartite Prokaryote Genome. Selection-Based Coding Bias Associated with Gene Location, Expression Level, and Ancestry. mBio, 10(3), e00505-19. doi:10.1128/mbio.00505-19
López, J. L., Lozano, M. J., Lagares, A., Fabre, M. L., Draghi, W. O., Del Papa, M. F., Pistorio, M., et al. 2019. “Codon Usage Heterogeneity in the Multipartite Prokaryote Genome. Selection-Based Coding Bias Associated with Gene Location, Expression Level, and Ancestry”. mBio 10 (3): e00505-19.
López, J. L., Lozano, M. J., Lagares, A., Fabre, M. L., Draghi, W. O., Del Papa, M. F., Pistorio, M., Becker, A., Wibberg, D., Schlüter, A., et al. (2019). Codon Usage Heterogeneity in the Multipartite Prokaryote Genome. Selection-Based Coding Bias Associated with Gene Location, Expression Level, and Ancestry. mBio 10:e00505-19.
López, J.L., et al., 2019. Codon Usage Heterogeneity in the Multipartite Prokaryote Genome. Selection-Based Coding Bias Associated with Gene Location, Expression Level, and Ancestry. mBio, 10(3): e00505-19.
J.L. López, et al., “Codon Usage Heterogeneity in the Multipartite Prokaryote Genome. Selection-Based Coding Bias Associated with Gene Location, Expression Level, and Ancestry”, mBio, vol. 10, 2019, : e00505-19.
López, J.L., Lozano, M.J., Lagares, A., Fabre, M.L., Draghi, W.O., Del Papa, M.F., Pistorio, M., Becker, A., Wibberg, D., Schlüter, A., Pühler, A., Blom, J., Goesmann, A., Lagares, A.: Codon Usage Heterogeneity in the Multipartite Prokaryote Genome. Selection-Based Coding Bias Associated with Gene Location, Expression Level, and Ancestry. mBio. 10, : e00505-19 (2019).
López, J. L., Lozano, M. J., Lagares, A., Fabre, M. L., Draghi, W. O., Del Papa, M. F., Pistorio, M., Becker, A., Wibberg, Daniel, Schlüter, Andreas, Pühler, Alfred, Blom, J., Goesmann, A., and Lagares, A. “Codon Usage Heterogeneity in the Multipartite Prokaryote Genome. Selection-Based Coding Bias Associated with Gene Location, Expression Level, and Ancestry”. mBio 10.3 (2019): e00505-19.
Alle Dateien verfügbar unter der/den folgenden Lizenz(en):
Copyright Statement:
Dieses Objekt ist durch das Urheberrecht und/oder verwandte Schutzrechte geschützt. [...]
Volltext(e)
Name
Access Level
Open Access
Zuletzt Hochgeladen
2019-06-03T12:02:25Z
MD5 Prüfsumme
4f7e43e149d4c789bad6d4284f4c2531
Daten bereitgestellt von European Bioinformatics Institute (EBI)
Zitationen in Europe PMC
Daten bereitgestellt von Europe PubMed Central.
60 References
Daten bereitgestellt von Europe PubMed Central.
The microbial pan-genome.
Medini D, Donati C, Tettelin H, Masignani V, Rappuoli R., Curr. Opin. Genet. Dev. 15(6), 2005
PMID: 16185861
Medini D, Donati C, Tettelin H, Masignani V, Rappuoli R., Curr. Opin. Genet. Dev. 15(6), 2005
PMID: 16185861
Origins of bacterial diversity through horizontal genetic transfer and adaptation to new ecological niches.
Wiedenbeck J, Cohan FM., FEMS Microbiol. Rev. 35(5), 2011
PMID: 21711367
Wiedenbeck J, Cohan FM., FEMS Microbiol. Rev. 35(5), 2011
PMID: 21711367
Examining bacterial species under the specter of gene transfer and exchange.
Ochman H, Lerat E, Daubin V., Proc. Natl. Acad. Sci. U.S.A. 102 Suppl 1(), 2005
PMID: 15851673
Ochman H, Lerat E, Daubin V., Proc. Natl. Acad. Sci. U.S.A. 102 Suppl 1(), 2005
PMID: 15851673
Plasmids in Rhizobia: the role of nonsymbiotic plasmids
Mercado-Blanco J, Toro N., 1996
Mercado-Blanco J, Toro N., 1996
Conjugal properties of the Sinorhizobium meliloti plasmid mobilome.
Pistorio M, Giusti MA, Del Papa MF, Draghi WO, Lozano MJ, Tejerizo GT, Lagares A., FEMS Microbiol. Ecol. 65(3), 2008
PMID: 18537840
Pistorio M, Giusti MA, Del Papa MF, Draghi WO, Lozano MJ, Tejerizo GT, Lagares A., FEMS Microbiol. Ecol. 65(3), 2008
PMID: 18537840
Sequence analysis of the 144-kilobase accessory plasmid pSmeSM11a, isolated from a dominant Sinorhizobium meliloti strain identified during a long-term field release experiment.
Stiens M, Schneiker S, Keller M, Kuhn S, Puhler A, Schluter A., Appl. Environ. Microbiol. 72(5), 2006
PMID: 16672515
Stiens M, Schneiker S, Keller M, Kuhn S, Puhler A, Schluter A., Appl. Environ. Microbiol. 72(5), 2006
PMID: 16672515
Synonymous codon usage in Escherichia coli: selection for translational accuracy.
Stoletzki N, Eyre-Walker A., Mol. Biol. Evol. 24(2), 2006
PMID: 17101719
Stoletzki N, Eyre-Walker A., Mol. Biol. Evol. 24(2), 2006
PMID: 17101719
Forces that influence the evolution of codon bias.
Sharp PM, Emery LR, Zeng K., Philos. Trans. R. Soc. Lond., B, Biol. Sci. 365(1544), 2010
PMID: 20308095
Sharp PM, Emery LR, Zeng K., Philos. Trans. R. Soc. Lond., B, Biol. Sci. 365(1544), 2010
PMID: 20308095
Modal codon usage: assessing the typical codon usage of a genome.
Davis JJ, Olsen GJ., Mol. Biol. Evol. 27(4), 2009
PMID: 20018979
Davis JJ, Olsen GJ., Mol. Biol. Evol. 27(4), 2009
PMID: 20018979
Working of the genetic code
Grantham R., 1980
Grantham R., 1980
Codon catalog usage and the genome hypothesis.
Grantham R, Gautier C, Gouy M, Mercier R, Pave A., Nucleic Acids Res. 8(1), 1980
PMID: 6986610
Grantham R, Gautier C, Gouy M, Mercier R, Pave A., Nucleic Acids Res. 8(1), 1980
PMID: 6986610
Evidence for horizontal gene transfer in Escherichia coli speciation.
Medigue C, Rouxel T, Vigier P, Henaut A, Danchin A., J. Mol. Biol. 222(4), 1991
PMID: 1762151
Medigue C, Rouxel T, Vigier P, Henaut A, Danchin A., J. Mol. Biol. 222(4), 1991
PMID: 1762151
Codon catalog usage is a genome strategy modulated for gene expressivity.
Grantham R, Gautier C, Gouy M, Jacobzone M, Mercier R., Nucleic Acids Res. 9(1), 1981
PMID: 7208352
Grantham R, Gautier C, Gouy M, Jacobzone M, Mercier R., Nucleic Acids Res. 9(1), 1981
PMID: 7208352
Synonymous but not the same: the causes and consequences of codon bias.
Plotkin JB, Kudla G., Nat. Rev. Genet. 12(1), 2010
PMID: 21102527
Plotkin JB, Kudla G., Nat. Rev. Genet. 12(1), 2010
PMID: 21102527
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.
Ikemura T., J. Mol. Biol. 158(4), 1982
PMID: 6750137
Ikemura T., J. Mol. Biol. 158(4), 1982
PMID: 6750137
The source of laterally transferred genes in bacterial genomes.
Daubin V, Lerat E, Perriere G., Genome Biol. 4(9), 2003
PMID: 12952536
Daubin V, Lerat E, Perriere G., Genome Biol. 4(9), 2003
PMID: 12952536
Detecting alien genes in bacterial genomes.
Mrazek J, Karlin S., Ann. N. Y. Acad. Sci. 870(), 1999
PMID: 10415493
Mrazek J, Karlin S., Ann. N. Y. Acad. Sci. 870(), 1999
PMID: 10415493
Molecular archaeology of the Escherichia coli genome.
Lawrence JG, Ochman H., Proc. Natl. Acad. Sci. U.S.A. 95(16), 1998
PMID: 9689094
Lawrence JG, Ochman H., Proc. Natl. Acad. Sci. U.S.A. 95(16), 1998
PMID: 9689094
Similarity of genes horizontally acquired by Escherichia coli and Salmonella enterica is evidence of a supraspecies pangenome.
Karberg KA, Olsen GJ, Davis JJ., Proc. Natl. Acad. Sci. U.S.A. 108(50), 2011
PMID: 22128332
Karberg KA, Olsen GJ, Davis JJ., Proc. Natl. Acad. Sci. U.S.A. 108(50), 2011
PMID: 22128332
Plasmids are vectors for redundant chromosomal genes in the Bacillus cereus group.
Zheng J, Guan Z, Cao S, Peng D, Ruan L, Jiang D, Sun M., BMC Genomics 16(), 2015
PMID: 25608745
Zheng J, Guan Z, Cao S, Peng D, Ruan L, Jiang D, Sun M., BMC Genomics 16(), 2015
PMID: 25608745
Rhizobial extrachromosomal replicon variability, stability and expression in natural niches.
Lopez-Guerrero MG, Ormeno-Orrillo E, Acosta JL, Mendoza-Vargas A, Rogel MA, Ramirez MA, Rosenblueth M, Martinez-Romero J, Martinez-Romero E., Plasmid 68(3), 2012
PMID: 22813963
Lopez-Guerrero MG, Ormeno-Orrillo E, Acosta JL, Mendoza-Vargas A, Rogel MA, Ramirez MA, Rosenblueth M, Martinez-Romero J, Martinez-Romero E., Plasmid 68(3), 2012
PMID: 22813963
The complete sequence of the 1,683-kb pSymB megaplasmid from the N2-fixing endosymbiont Sinorhizobium meliloti.
Finan TM, Weidner S, Wong K, Buhrmester J, Chain P, Vorholter FJ, Hernandez-Lucas I, Becker A, Cowie A, Gouzy J, Golding B, Puhler A., Proc. Natl. Acad. Sci. U.S.A. 98(17), 2001
PMID: 11481431
Finan TM, Weidner S, Wong K, Buhrmester J, Chain P, Vorholter FJ, Hernandez-Lucas I, Becker A, Cowie A, Gouzy J, Golding B, Puhler A., Proc. Natl. Acad. Sci. U.S.A. 98(17), 2001
PMID: 11481431
The composite genome of the legume symbiont Sinorhizobium meliloti.
Galibert F, Finan TM, Long SR, Puhler A, Abola P, Ampe F, Barloy-Hubler F, Barnett MJ, Becker A, Boistard P, Bothe G, Boutry M, Bowser L, Buhrmester J, Cadieu E, Capela D, Chain P, Cowie A, Davis RW, Dreano S, Federspiel NA, Fisher RF, Gloux S, Godrie T, Goffeau A, Golding B, Gouzy J, Gurjal M, Hernandez-Lucas I, Hong A, Huizar L, Hyman RW, Jones T, Kahn D, Kahn ML, Kalman S, Keating DH, Kiss E, Komp C, Lelaure V, Masuy D, Palm C, Peck MC, Pohl TM, Portetelle D, Purnelle B, Ramsperger U, Surzycki R, Thebault P, Vandenbol M, Vorholter FJ, Weidner S, Wells DH, Wong K, Yeh KC, Batut J., Science 293(5530), 2001
PMID: 11474104
Galibert F, Finan TM, Long SR, Puhler A, Abola P, Ampe F, Barloy-Hubler F, Barnett MJ, Becker A, Boistard P, Bothe G, Boutry M, Bowser L, Buhrmester J, Cadieu E, Capela D, Chain P, Cowie A, Davis RW, Dreano S, Federspiel NA, Fisher RF, Gloux S, Godrie T, Goffeau A, Golding B, Gouzy J, Gurjal M, Hernandez-Lucas I, Hong A, Huizar L, Hyman RW, Jones T, Kahn D, Kahn ML, Kalman S, Keating DH, Kiss E, Komp C, Lelaure V, Masuy D, Palm C, Peck MC, Pohl TM, Portetelle D, Purnelle B, Ramsperger U, Surzycki R, Thebault P, Vandenbol M, Vorholter FJ, Weidner S, Wells DH, Wong K, Yeh KC, Batut J., Science 293(5530), 2001
PMID: 11474104
Nucleotide sequence and predicted functions of the entire Sinorhizobium meliloti pSymA megaplasmid.
Barnett MJ, Fisher RF, Jones T, Komp C, Abola AP, Barloy-Hubler F, Bowser L, Capela D, Galibert F, Gouzy J, Gurjal M, Hong A, Huizar L, Hyman RW, Kahn D, Kahn ML, Kalman S, Keating DH, Palm C, Peck MC, Surzycki R, Wells DH, Yeh KC, Davis RW, Federspiel NA, Long SR., Proc. Natl. Acad. Sci. U.S.A. 98(17), 2001
PMID: 11481432
Barnett MJ, Fisher RF, Jones T, Komp C, Abola AP, Barloy-Hubler F, Bowser L, Capela D, Galibert F, Gouzy J, Gurjal M, Hong A, Huizar L, Hyman RW, Kahn D, Kahn ML, Kalman S, Keating DH, Palm C, Peck MC, Surzycki R, Wells DH, Yeh KC, Davis RW, Federspiel NA, Long SR., Proc. Natl. Acad. Sci. U.S.A. 98(17), 2001
PMID: 11481432
Introducing the bacterial 'chromid': not a chromosome, not a plasmid.
Harrison PW, Lower RP, Kim NK, Young JP., Trends Microbiol. 18(4), 2010
PMID: 20080407
Harrison PW, Lower RP, Kim NK, Young JP., Trends Microbiol. 18(4), 2010
PMID: 20080407
Variation in the strength of selected codon usage bias among bacteria.
Sharp PM, Bailes E, Grocock RJ, Peden JF, Sockett RE., Nucleic Acids Res. 33(4), 2005
PMID: 15728743
Sharp PM, Bailes E, Grocock RJ, Peden JF, Sockett RE., Nucleic Acids Res. 33(4), 2005
PMID: 15728743
The strength of translational selection for codon usage varies in the three replicons of Sinorhizobium meliloti.
Peixoto L, Zavala A, Romero H, Musto H., Gene 320(), 2003
PMID: 14597394
Peixoto L, Zavala A, Romero H, Musto H., Gene 320(), 2003
PMID: 14597394
Solving the riddle of codon usage preferences: a test for translational selection.
dos Reis M, Savva R, Wernisch L., Nucleic Acids Res. 32(17), 2004
PMID: 15448185
dos Reis M, Savva R, Wernisch L., Nucleic Acids Res. 32(17), 2004
PMID: 15448185
A role for tRNA modifications in genome structure and codon usage.
Novoa EM, Pavon-Eternod M, Pan T, Ribas de Pouplana L., Cell 149(1), 2012
PMID: 22464330
Novoa EM, Pavon-Eternod M, Pan T, Ribas de Pouplana L., Cell 149(1), 2012
PMID: 22464330
The codon Adaptation Index--a measure of directional synonymous codon usage bias, and its potential applications.
Sharp PM, Li WH., Nucleic Acids Res. 15(3), 1987
PMID: 3547335
Sharp PM, Li WH., Nucleic Acids Res. 15(3), 1987
PMID: 3547335
Replicon-dependent bacterial genome evolution: the case of Sinorhizobium meliloti.
Galardini M, Pini F, Bazzicalupo M, Biondi EG, Mengoni A., Genome Biol Evol 5(3), 2013
PMID: 23431003
Galardini M, Pini F, Bazzicalupo M, Biondi EG, Mengoni A., Genome Biol Evol 5(3), 2013
PMID: 23431003
Robustness encoded across essential and accessory replicons of the ecologically versatile bacterium Sinorhizobium meliloti.
diCenzo GC, Benedict AB, Fondi M, Walker GC, Finan TM, Mengoni A, Griffitts JS., PLoS Genet. 14(4), 2018
PMID: 29672509
diCenzo GC, Benedict AB, Fondi M, Walker GC, Finan TM, Mengoni A, Griffitts JS., PLoS Genet. 14(4), 2018
PMID: 29672509
The complete replicons of 16 Ensifer meliloti strains offer insights into intra- and inter-replicon gene transfer, transposon-associated loci, and repeat elements.
Nelson M, Guhlin J, Epstein B, Tiffin P, Sadowsky MJ., Microb Genom 4(5), 2018
PMID: 29671722
Nelson M, Guhlin J, Epstein B, Tiffin P, Sadowsky MJ., Microb Genom 4(5), 2018
PMID: 29671722
Codon usage bias in prokaryotic pyrimidine-ending codons is associated with the degeneracy of the encoded amino acids.
Wald N, Alroy M, Botzman M, Margalit H., Nucleic Acids Res. 40(15), 2012
PMID: 22581775
Wald N, Alroy M, Botzman M, Margalit H., Nucleic Acids Res. 40(15), 2012
PMID: 22581775
Studies of codon usage and tRNA genes of 18 unicellular organisms and quantification of Bacillus subtilis tRNAs: gene expression level and species-specific diversity of codon usage based on multivariate analysis.
Kanaya S, Yamada Y, Kudo Y, Ikemura T., Gene 238(1), 1999
PMID: 10570992
Kanaya S, Yamada Y, Kudo Y, Ikemura T., Gene 238(1), 1999
PMID: 10570992
General trends in selectively driven codon usage biases in the domain archaea.
Iriarte A, Jara E, Leyton L, Diana L, Musto H., J. Mol. Evol. 79(3-4), 2014
PMID: 25239794
Iriarte A, Jara E, Leyton L, Diana L, Musto H., J. Mol. Evol. 79(3-4), 2014
PMID: 25239794
Evolution of optimal codon choices in the family Enterobacteriaceae.
Iriarte A, Baraibar JD, Romero H, Castro-Sowinski S, Musto H., Microbiology (Reading, Engl.) 159(Pt 3), 2013
PMID: 23288542
Iriarte A, Baraibar JD, Romero H, Castro-Sowinski S, Musto H., Microbiology (Reading, Engl.) 159(Pt 3), 2013
PMID: 23288542
DNA sequence homology in Rhizobium meliloti plasmids.
Jouanin L, De Lajudie P, Bazetoux S, Huguet T., Mol. Gen. Genet. 182(2), 1981
PMID: 6270502
Jouanin L, De Lajudie P, Bazetoux S, Huguet T., Mol. Gen. Genet. 182(2), 1981
PMID: 6270502
GenDB--an open source genome annotation system for prokaryote genomes.
Meyer F, Goesmann A, McHardy AC, Bartels D, Bekel T, Clausen J, Kalinowski J, Linke B, Rupp O, Giegerich R, Puhler A., Nucleic Acids Res. 31(8), 2003
PMID: 12682369
Meyer F, Goesmann A, McHardy AC, Bartels D, Bekel T, Clausen J, Kalinowski J, Linke B, Rupp O, Giegerich R, Puhler A., Nucleic Acids Res. 31(8), 2003
PMID: 12682369
WebMGA: a customizable web server for fast metagenomic sequence analysis.
Wu S, Zhu Z, Fu L, Niu B, Li W., BMC Genomics 12(), 2011
PMID: 21899761
Wu S, Zhu Z, Fu L, Niu B, Li W., BMC Genomics 12(), 2011
PMID: 21899761
FactoMineR: an R package for multivariate analysis
Lê S, Josse J, Husson F., 2008
Lê S, Josse J, Husson F., 2008
Package `pheatmap’
Kolde R., 2012
Kolde R., 2012
ggplot2: elegant graphics for data analysis by Wickham, H
Wilkinson L., 2011
Wilkinson L., 2011
EDGAR: a software framework for the comparative analysis of prokaryotic genomes.
Blom J, Albaum SP, Doppmeier D, Puhler A, Vorholter FJ, Zakrzewski M, Goesmann A., BMC Bioinformatics 10(), 2009
PMID: 19457249
Blom J, Albaum SP, Doppmeier D, Puhler A, Vorholter FJ, Zakrzewski M, Goesmann A., BMC Bioinformatics 10(), 2009
PMID: 19457249
PHYLIP (Phylogeny Inference Package) version 3.6
Felsenstein J., 2005
Felsenstein J., 2005
FigTree v1. 3.1
Rambaut A, Drummond A., 2009
Rambaut A, Drummond A., 2009
MUSCLE: multiple sequence alignment with high accuracy and high throughput.
Edgar RC., Nucleic Acids Res. 32(5), 2004
PMID: 15034147
Edgar RC., Nucleic Acids Res. 32(5), 2004
PMID: 15034147
Modelling the efficiency of codon-tRNA interactions based on codon usage bias.
Sabi R, Tuller T., DNA Res. 21(5), 2014
PMID: 24906480
Sabi R, Tuller T., DNA Res. 21(5), 2014
PMID: 24906480
Quantitative proteomic analysis of the Hfq-regulon in Sinorhizobium meliloti 2011.
Sobrero P, Schluter JP, Lanner U, Schlosser A, Becker A, Valverde C., PLoS ONE 7(10), 2012
PMID: 23119037
Sobrero P, Schluter JP, Lanner U, Schlosser A, Becker A, Valverde C., PLoS ONE 7(10), 2012
PMID: 23119037
A straightforward and highly efficient precipitation/on-pellet digestion procedure coupled with a long gradient nano-LC separation and Orbitrap mass spectrometry for label-free expression profiling of the swine heart mitochondrial proteome.
Duan X, Young R, Straubinger RM, Page B, Cao J, Wang H, Yu H, Canty JM, Qu J., J. Proteome Res. 8(6), 2009
PMID: 19290621
Duan X, Young R, Straubinger RM, Page B, Cao J, Wang H, Yu H, Canty JM, Qu J., J. Proteome Res. 8(6), 2009
PMID: 19290621
Regulation of Polyhydroxybutyrate Accumulation in Sinorhizobium meliloti by the Trans-Encoded Small RNA MmgR.
Lagares A Jr, Borella GC, Linne U, Becker A, Valverde C., J. Bacteriol. 199(8), 2017
PMID: 28167519
Lagares A Jr, Borella GC, Linne U, Becker A, Valverde C., J. Bacteriol. 199(8), 2017
PMID: 28167519
Qupe--a Rich Internet Application to take a step forward in the analysis of mass spectrometry-based quantitative proteomics experiments.
Albaum SP, Neuweger H, Franzel B, Lange S, Mertens D, Trotschel C, Wolters D, Kalinowski J, Nattkemper TW, Goesmann A., Bioinformatics 25(23), 2009
PMID: 19808875
Albaum SP, Neuweger H, Franzel B, Lange S, Mertens D, Trotschel C, Wolters D, Kalinowski J, Nattkemper TW, Goesmann A., Bioinformatics 25(23), 2009
PMID: 19808875
A correlation algorithm for the automated quantitative analysis of shotgun proteomics data.
MacCoss MJ, Wu CC, Liu H, Sadygov R, Yates JR 3rd., Anal. Chem. 75(24), 2003
PMID: 14670053
MacCoss MJ, Wu CC, Liu H, Sadygov R, Yates JR 3rd., Anal. Chem. 75(24), 2003
PMID: 14670053
Absolute quantification of proteins by LCMSE: a virtue of parallel MS acquisition.
Silva JC, Gorenstein MV, Li GZ, Vissers JP, Geromanos SJ., Mol. Cell Proteomics 5(1), 2005
PMID: 16219938
Silva JC, Gorenstein MV, Li GZ, Vissers JP, Geromanos SJ., Mol. Cell Proteomics 5(1), 2005
PMID: 16219938
Codon usage in yeast: cluster analysis clearly differentiates highly and lowly expressed genes.
Sharp PM, Tuohy TM, Mosurski KR., Nucleic Acids Res. 14(13), 1986
PMID: 3526280
Sharp PM, Tuohy TM, Mosurski KR., Nucleic Acids Res. 14(13), 1986
PMID: 3526280
phytools: an R package for phylogenetic comparative biology (and other things)
Revell LJ., 2011
Revell LJ., 2011
APE: Analyses of Phylogenetics and Evolution in R language.
Paradis E, Claude J, Strimmer K., Bioinformatics 20(2), 2004
PMID: 14734327
Paradis E, Claude J, Strimmer K., Bioinformatics 20(2), 2004
PMID: 14734327
dendextend: an R package for visualizing, adjusting and comparing trees of hierarchical clustering.
Galili T., Bioinformatics 31(22), 2015
PMID: 26209431
Galili T., Bioinformatics 31(22), 2015
PMID: 26209431
Export
Markieren/ Markierung löschen
Markierte Publikationen
Web of Science
Dieser Datensatz im Web of Science®Quellen
PMID: 31138741
PubMed | Europe PMC
Suchen in