Publications
2003
Yang H, Jossinet F, Leontis N, Chen L, Westbrook J, Berman H, Westhof E
Tools for the automatic identification and classification of RNA base pairs Journal Article
In: Nucleic Acids Res, vol. 31, no. 13, pp. 3450-3460, 2003, ISBN: 12824344, (1362-4962 Journal Article).
Abstract | Links | BibTeX | Tags: Algorithms Base Pairing Base Sequence Computer Graphics Data Interpretation, Molecular Nucleic Acid Conformation RNA/*chemistry/classification *Software Support, Non-P.H.S. Support, Non-U.S. Gov't Support, Nucleic Acid Internet Models, P.H.S., Statistical Databases, U.S. Gov't, Unité ARN, WESTHOF
@article{,
title = {Tools for the automatic identification and classification of RNA base pairs},
author = {H Yang and F Jossinet and N Leontis and L Chen and J Westbrook and H Berman and E Westhof},
url = {http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=12824344},
isbn = {12824344},
year = {2003},
date = {2003-01-01},
journal = {Nucleic Acids Res},
volume = {31},
number = {13},
pages = {3450-3460},
abstract = {Three programs have been developed to aid in the classification and visualization of RNA structure. BPViewer provides a web interface for displaying three-dimensional (3D) coordinates of individual base pairs or base pair collections. A web server, RNAview, automatically identifies and classifies the types of base pairs that are formed in nucleic acid structures by various combinations of the three edges, Watson-Crick, Hoogsteen and the Sugar edge. RNAView produces two-dimensional (2D) diagrams of secondary and tertiary structure in either Postscript, VRML or RNAML formats. The application RNAMLview can be used to rearrange various parts of the RNAView 2D diagram to generate a standard representation (like the cloverleaf structure of tRNAs) or any layout desired by the user. A 2D diagram can be rapidly reformatted using RNAMLview since all the parts of RNA (like helices and single strands) are dynamically linked while moving the selected parts. With the base pair annotation and the 2D graphic display, RNA motifs are rapidly identified and classified. A survey has been carried out for 41 unique structures selected from the NDB database. The statistics for the occurrence of each edge and of each of the 12 bp families are given for the combinations of the four bases: A, G, U and C. The program also allows for visualization of the base pair interactions by using a symbolic convention previously proposed for base pairs. The web servers for BPViewer and RNAview are available at http://ndbserver.rutgers.edu/services/. The application RNAMLview can also be downloaded from this site. The 2D diagrams produced by RNAview are available for RNA structures in the Nucleic Acid Database (NDB) at http://ndbserver.rutgers.edu/atlas/.},
note = {1362-4962
Journal Article},
keywords = {Algorithms Base Pairing Base Sequence Computer Graphics Data Interpretation, Molecular Nucleic Acid Conformation RNA/*chemistry/classification *Software Support, Non-P.H.S. Support, Non-U.S. Gov't Support, Nucleic Acid Internet Models, P.H.S., Statistical Databases, U.S. Gov't, Unité ARN, WESTHOF},
pubstate = {published},
tppubtype = {article}
}
Tsai H Y, Masquida B, Biswas R, Westhof E, Gopalan V
Molecular modeling of the three-dimensional structure of the bacterial RNase P holoenzyme Journal Article
In: J Mol Biol, vol. 325, no. 4, pp. 661-675, 2003, ISBN: 12507471, (0022-2836 Journal Article).
Abstract | Links | BibTeX | Tags: Amino Acid Sequence Base Sequence Catalytic Domain Computer Simulation Cysteine/chemistry DNA Footprinting DNA, Bacterial/chemistry/genetics/metabolism RNA, Bacterial/genetics Edetic Acid Endoribonucleases/*chemistry/genetics/metabolism Escherichia coli/*enzymology/genetics Evolution, Catalytic/*chemistry/genetics/metabolism Ribonuclease P Support, Molecular Ferrous Compounds Holoenzymes/chemistry/genetics/metabolism Hydroxyl Radical/chemistry Models, Molecular Molecular Sequence Data Mutagenesis, Non-P.H.S. Support, P.H.S., Site-Directed Nucleic Acid Conformation Protein Subunits RNA, U.S. Gov't, Unité ARN, WESTHOF
@article{,
title = {Molecular modeling of the three-dimensional structure of the bacterial RNase P holoenzyme},
author = {H Y Tsai and B Masquida and R Biswas and E Westhof and V Gopalan},
url = {http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=12507471},
isbn = {12507471},
year = {2003},
date = {2003-01-01},
journal = {J Mol Biol},
volume = {325},
number = {4},
pages = {661-675},
abstract = {Bacterial ribonuclease P (RNase P), an enzyme involved in tRNA maturation, consists of a catalytic RNA subunit and a protein cofactor. Comparative phylogenetic analysis and molecular modeling have been employed to derive secondary and tertiary structure models of the RNA subunits from Escherichia coli (type A) and Bacillus subtilis (type B) RNase P. The tertiary structure of the protein subunit of B.subtilis and Staphylococcus aureus RNase P has recently been determined. However, an understanding of the structure of the RNase P holoenzyme (i.e. the ribonucleoprotein complex) is lacking. We have now used an EDTA-Fe-based footprinting approach to generate information about RNA-protein contact sites in E.coli RNase P. The footprinting data, together with results from other biochemical and biophysical studies, have furnished distance constraints, which in turn have enabled us to build three-dimensional models of both type A and B versions of the bacterial RNase P holoenzyme in the absence and presence of its precursor tRNA substrate. These models are consistent with results from previous studies and provide both structural and mechanistic insights into the functioning of this unique catalytic RNP complex.},
note = {0022-2836
Journal Article},
keywords = {Amino Acid Sequence Base Sequence Catalytic Domain Computer Simulation Cysteine/chemistry DNA Footprinting DNA, Bacterial/chemistry/genetics/metabolism RNA, Bacterial/genetics Edetic Acid Endoribonucleases/*chemistry/genetics/metabolism Escherichia coli/*enzymology/genetics Evolution, Catalytic/*chemistry/genetics/metabolism Ribonuclease P Support, Molecular Ferrous Compounds Holoenzymes/chemistry/genetics/metabolism Hydroxyl Radical/chemistry Models, Molecular Molecular Sequence Data Mutagenesis, Non-P.H.S. Support, P.H.S., Site-Directed Nucleic Acid Conformation Protein Subunits RNA, U.S. Gov't, Unité ARN, WESTHOF},
pubstate = {published},
tppubtype = {article}
}
2002
Waugh A, Gendron P, Altman R, Brown J W, Case D, Gautheret D, Harvey S C, Leontis N, Westbrook J, Westhof E, Zuker M, Major F
RNAML: a standard syntax for exchanging RNA information Journal Article
In: RNA, vol. 8, no. 6, pp. 707-717, 2002, ISBN: 12088144, (1355-8382 Journal Article).
Abstract | Links | BibTeX | Tags: *Databases, Non-P.H.S. Support, Non-U.S. Gov't Support, Nucleic Acid *Nucleic Acid Conformation Programming Languages RNA/*chemistry Support, P.H.S., U.S. Gov't, Unité ARN, WESTHOF
@article{,
title = {RNAML: a standard syntax for exchanging RNA information},
author = {A Waugh and P Gendron and R Altman and J W Brown and D Case and D Gautheret and S C Harvey and N Leontis and J Westbrook and E Westhof and M Zuker and F Major},
url = {http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=12088144},
isbn = {12088144},
year = {2002},
date = {2002-01-01},
journal = {RNA},
volume = {8},
number = {6},
pages = {707-717},
abstract = {Analyzing a single data set using multiple RNA informatics programs often requires a file format conversion between each pair of programs, significantly hampering productivity. To facilitate the interoperation of these programs, we propose a syntax to exchange basic RNA molecular information. This RNAML syntax allows for the storage and the exchange of information about RNA sequence and secondary and tertiary structures. The syntax permits the description of higher level information about the data including, but not restricted to, base pairs, base triples, and pseudoknots. A class-oriented approach allows us to represent data common to a given set of RNA molecules, such as a sequence alignment and a consensus secondary structure. Documentation about experiments and computations, as well as references to journals and external databases, are included in the syntax. The chief challenge in creating such a syntax was to determine the appropriate scope of usage and to ensure extensibility as new needs will arise. The syntax complies with the eXtensible Markup Language (XML) recommendations, a widely accepted standard for syntax specifications. In addition to the various generic packages that exist to read and interpret XML formats, an XML processor was developed and put in the open-source MC-Core library for nucleic acid and protein structure computer manipulation.},
note = {1355-8382
Journal Article},
keywords = {*Databases, Non-P.H.S. Support, Non-U.S. Gov't Support, Nucleic Acid *Nucleic Acid Conformation Programming Languages RNA/*chemistry Support, P.H.S., U.S. Gov't, Unité ARN, WESTHOF},
pubstate = {published},
tppubtype = {article}
}
Serra M J, Baird J D, Dale T, Fey B L, Retatagos K, Westhof E
Effects of magnesium ions on the stabilization of RNA oligomers of defined structures Journal Article
In: RNA, vol. 8, no. 3, pp. 307-323, 2002, ISBN: 12003491, (1355-8382 Journal Article).
Abstract | Links | BibTeX | Tags: Base Pairing Heat Hydrogen Bonding Magnesium/*pharmacology Models, Molecular Nucleic Acid Conformation RNA/*metabolism RNA Stability/*drug effects Support, Non-P.H.S. Support, Non-U.S. Gov't Support, P.H.S. Thermodynamics, U.S. Gov't, Unité ARN, WESTHOF
@article{,
title = {Effects of magnesium ions on the stabilization of RNA oligomers of defined structures},
author = {M J Serra and J D Baird and T Dale and B L Fey and K Retatagos and E Westhof},
url = {http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=12003491},
isbn = {12003491},
year = {2002},
date = {2002-01-01},
journal = {RNA},
volume = {8},
number = {3},
pages = {307-323},
abstract = {Optical melting was used to determine the stabilities of 11 small RNA oligomers of defined secondary structure as a function of magnesium ion concentration. The oligomers included helices composed of Watson-Crick base pairs, GA tandem base pairs, GU tandem base pairs, and loop E motifs (both eubacterial and eukaryotic). The effect of magnesium ion concentration on stability was interpreted in terms of two simple models. The first assumes an uptake of metal ion upon duplex formation. The second assumes nonspecific electrostatic attraction of metal ions to the RNA oligomer. For all oligomers, except the eubacterial loop E, the data could best be interpreted as nonspecific binding of metal ions to the RNAs. The effect of magnesium ions on the stability of the eubacterial loop E was distinct from that seen with the other oligomers in two ways. First, the extent of stabilization by magnesium ions (as measured by either change in melting temperature or free energy) was three times greater than that observed for the other helical oligomers. Second, the presence of magnesium ions produces a doubling of the enthalpy for the melting transition. These results indicate that magnesium ion stabilizes the eubacterial loop E sequence by chelating the RNA specifically. Further, these results on a rather small system shed light on the large enthalpy changes observed upon thermal unfolding of large RNAs like group I introns. It is suggested that parts of those large enthalpy changes observed in the folding of RNAs may be assigned to variations in the hydration states and types of coordinating atoms in some specifically bound magnesium ions and to an increase in the observed cooperativity of the folding transition due to the binding of those magnesium ions coupling the two stems together. Brownian dynamic simulations, carried out to visualize the metal ion binding sites, reveal rather delocalized ionic densities in all oligomers, except for the eubacterial loop E, in which precisely located ion densities were previously calculated.},
note = {1355-8382
Journal Article},
keywords = {Base Pairing Heat Hydrogen Bonding Magnesium/*pharmacology Models, Molecular Nucleic Acid Conformation RNA/*metabolism RNA Stability/*drug effects Support, Non-P.H.S. Support, Non-U.S. Gov't Support, P.H.S. Thermodynamics, U.S. Gov't, Unité ARN, WESTHOF},
pubstate = {published},
tppubtype = {article}
}
Leontis N B, Stombaugh J, Westhof E
The non-Watson-Crick base pairs and their associated isostericity matrices Journal Article
In: Nucleic Acids Res, vol. 30, no. 16, pp. 3497-3531, 2002, ISBN: 12177293, (1362-4962 Journal Article).
Abstract | Links | BibTeX | Tags: Algorithms *Base Pairing Base Sequence Hydrogen Bonding Models, Molecular RNA/*chemistry/classification/genetics Sequence Homology Support, Non-P.H.S. Support, P.H.S. Terminology, U.S. Gov't, Unité ARN, WESTHOF
@article{,
title = {The non-Watson-Crick base pairs and their associated isostericity matrices},
author = {N B Leontis and J Stombaugh and E Westhof},
url = {http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=12177293},
isbn = {12177293},
year = {2002},
date = {2002-01-01},
journal = {Nucleic Acids Res},
volume = {30},
number = {16},
pages = {3497-3531},
abstract = {RNA molecules exhibit complex structures in which a large fraction of the bases engage in non-Watson-Crick base pairing, forming motifs that mediate long-range RNA-RNA interactions and create binding sites for proteins and small molecule ligands. The rapidly growing number of three-dimensional RNA structures at atomic resolution requires that databases contain the annotation of such base pairs. An unambiguous and descriptive nomenclature was proposed recently in which RNA base pairs were classified by the base edges participating in the interaction (Watson-Crick, Hoogsteen/CH or sugar edge) and the orientation of the glycosidic bonds relative to the hydrogen bonds (cis or trans). Twelve basic geometric families were identified and all 12 have been observed in crystal structures. For each base pairing family, we present here the 4 x 4 'isostericity matrices' summarizing the geometric relationships between the 16 pairwise combinations of the four standard bases, A, C, G and U. Whenever available, a representative example of each observed base pair from X-ray crystal structures (3.0 A resolution or better) is provided or, otherwise, theoretically plausible models. This format makes apparent the recurrent geometric patterns that are observed and helps identify isosteric pairs that co-vary or interchange in sequences of homologous molecules while maintaining conserved three-dimensional motifs.},
note = {1362-4962
Journal Article},
keywords = {Algorithms *Base Pairing Base Sequence Hydrogen Bonding Models, Molecular RNA/*chemistry/classification/genetics Sequence Homology Support, Non-P.H.S. Support, P.H.S. Terminology, U.S. Gov't, Unité ARN, WESTHOF},
pubstate = {published},
tppubtype = {article}
}
Leontis N B, Stombaugh J, Westhof E
Motif prediction in ribosomal RNAs Lessons and prospects for automated motif prediction in homologous RNA molecules Journal Article
In: Biochimie, vol. 84, no. 9, pp. 961-973, 2002, ISBN: 12458088, (0300-9084 Journal Article).
Abstract | Links | BibTeX | Tags: Bacterial/*chemistry/genetics RNA, Base Pairing Base Sequence Catalytic Domain Conserved Sequence Databases, Factual Models, Molecular *Nucleic Acid Conformation RNA, Non-P.H.S. Support, P.H.S., Ribosomal/*chemistry/genetics Sequence Alignment Support, U.S. Gov't, Unité ARN, WESTHOF
@article{,
title = {Motif prediction in ribosomal RNAs Lessons and prospects for automated motif prediction in homologous RNA molecules},
author = {N B Leontis and J Stombaugh and E Westhof},
url = {http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=12458088},
isbn = {12458088},
year = {2002},
date = {2002-01-01},
journal = {Biochimie},
volume = {84},
number = {9},
pages = {961-973},
abstract = {The traditional way to infer RNA secondary structure involves an iterative process of alignment and evaluation of covariation statistics between all positions possibly involved in basepairing. Watson-Crick basepairs typically show covariations that score well when examples of two or more possible basepairs occur. This is not necessarily the case for non-Watson-Crick basepairing geometries. For example, for sheared (trans Hoogsteen/Sugar edge) pairs, one base is highly conserved (always A or mostly A with some C or U), while the other can vary (G or A and sometimes C and U as well). RNA motifs consist of ordered, stacked arrays of non-Watson-Crick basepairs that in the secondary structure representation form hairpin or internal loops, multi-stem junctions, and even pseudoknots. Although RNA motifs occur recurrently and contribute in a modular fashion to RNA architecture, it is usually not apparent which bases interact and whether it is by edge-to-edge H-bonding or solely by stacking interactions. Using a modular sequence-analysis approach, recurrent motifs related to the sarcin-ricin loop of 23S RNA and to loop E from 5S RNA were predicted in universally conserved regions of the large ribosomal RNAs (16S- and 23S-like) before the publication of high-resolution, atomic-level structures of representative examples of 16S and 23S rRNA molecules in their native contexts. This provides the opportunity to evaluate the predictive power of motif-level sequence analysis, with the goal of automating the process for predicting RNA motifs in genomic sequences. The process of inferring structure from sequence by constructing accurate alignments is a circular one. The crucial link that allows a productive iteration of motif modeling and realignment is the comparison of the sequence variations for each putative pair with the corresponding isostericity matrix to determine which basepairs are consistent both with the sequence and the geometrical data.},
note = {0300-9084
Journal Article},
keywords = {Bacterial/*chemistry/genetics RNA, Base Pairing Base Sequence Catalytic Domain Conserved Sequence Databases, Factual Models, Molecular *Nucleic Acid Conformation RNA, Non-P.H.S. Support, P.H.S., Ribosomal/*chemistry/genetics Sequence Alignment Support, U.S. Gov't, Unité ARN, WESTHOF},
pubstate = {published},
tppubtype = {article}
}
1999
Perreau V M, Keith G, Holmes W M, Przykorska A, Santos M A, Tuite M F
The Candida albicans CUG-decoding ser-tRNA has an atypical anticodon stem-loop structure Journal Article
In: J Mol Biol, vol. 293, no. 5, pp. 1039-1053, 1999, ISBN: 10547284, (0022-2836 Journal Article).
Abstract | Links | BibTeX | Tags: Anticodon/*chemistry/*genetics/metabolism Base Sequence Candida albicans/*genetics Evolution, Fungal/chemistry/genetics/metabolism RNA, Molecular Genetic Code/genetics Imidazoles/metabolism Lead/metabolism Methylation Mutation/genetics *Nucleic Acid Conformation Nucleosides/genetics/metabolism RNA, Non-P.H.S. Support, Non-U.S. Gov't Support, P.H.S. tRNA Methyltransferases/metabolism, Ser/*chemistry/*genetics/metabolism Ribonucleases/metabolism Saccharomyces cerevisiae/genetics Solutions Support, Transfer, U.S. Gov't, Unité ARN
@article{,
title = {The Candida albicans CUG-decoding ser-tRNA has an atypical anticodon stem-loop structure},
author = {V M Perreau and G Keith and W M Holmes and A Przykorska and M A Santos and M F Tuite},
url = {http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=10547284},
isbn = {10547284},
year = {1999},
date = {1999-01-01},
journal = {J Mol Biol},
volume = {293},
number = {5},
pages = {1039-1053},
abstract = {In many Candida species, the leucine CUG codon is decoded by a tRNA with two unusual properties: it is a ser-tRNA and, uniquely, has guanosine at position 33 (G33). Using a combination of enzymatic (V1 RNase, RnI nuclease) and chemical (Pb(2+), imidazole) probing of the native Candida albicans ser-tRNACAG, we demonstrate that the overall tertiary structure of this tRNA resembles that of a ser-tRNA rather than a leu-tRNA, except within the anticodon arm where there is considerable disruption of the anticodon stem. Using non-modified in vitro transcripts of the C. albicans ser-tRNACAG carrying G, C, U or A at position 33, we demonstrate that it is specifically a G residue at this position that induces the atypical anticodon stem structure. Further quantitative evidence for an unusual structure in the anticodon arm of the G33-tRNA is provided by the observed change in kinetics of methylation of the G at position 37, by purified Escherichia coli m(1)G37 methyltransferase. We conclude that the anticodon arm distortion, induced by a guanosine base at position 33 in the anticodon loop of this novel tRNA, results in reduced decoding ability which has facilitated the evolution of this tRNA without extinction of the species encoding it.},
note = {0022-2836
Journal Article},
keywords = {Anticodon/*chemistry/*genetics/metabolism Base Sequence Candida albicans/*genetics Evolution, Fungal/chemistry/genetics/metabolism RNA, Molecular Genetic Code/genetics Imidazoles/metabolism Lead/metabolism Methylation Mutation/genetics *Nucleic Acid Conformation Nucleosides/genetics/metabolism RNA, Non-P.H.S. Support, Non-U.S. Gov't Support, P.H.S. tRNA Methyltransferases/metabolism, Ser/*chemistry/*genetics/metabolism Ribonucleases/metabolism Saccharomyces cerevisiae/genetics Solutions Support, Transfer, U.S. Gov't, Unité ARN},
pubstate = {published},
tppubtype = {article}
}
1992
Dreher T W, Tsai C H, Florentz C, Giege R
Specific valylation of turnip yellow mosaic virus RNA by wheat germ valyl-tRNA synthetase determined by three anticodon loop nucleotides Journal Article
In: Biochemistry, vol. 31, no. 38, pp. 9183-9189, 1992, ISBN: 1390705, (0006-2960 Journal Article).
Abstract | Links | BibTeX | Tags: Anticodon/genetics/*metabolism Bacteriophage T7/enzymology Base Sequence DNA-Directed RNA Polymerases/metabolism Kinetics Molecular Sequence Data Mosaic Viruses/genetics/*metabolism Nucleic Acid Conformation RNA, FLORENTZ, Genetic Triticum/*enzymology Valine-tRNA Ligase/*metabolism Variation (Genetics), Non-P.H.S. Support, Non-U.S. Gov't Support, P.H.S. Transcription, Transfer/chemistry/metabolism RNA, U.S. Gov't, Unité ARN, Viral/chemistry/genetics/*metabolism Seeds/enzymology Support
@article{,
title = {Specific valylation of turnip yellow mosaic virus RNA by wheat germ valyl-tRNA synthetase determined by three anticodon loop nucleotides},
author = {T W Dreher and C H Tsai and C Florentz and R Giege},
url = {http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=1390705},
isbn = {1390705},
year = {1992},
date = {1992-01-01},
journal = {Biochemistry},
volume = {31},
number = {38},
pages = {9183-9189},
abstract = {The valylation by wheat germ valyl-tRNA synthetase of anticodon loop mutants of turnip yellow mosaic virus RNA has been studied. RNA substrates 264 nucleotides long were made by T7 RNA polymerase from cDNA encompassing the 3' tRNA-like region of genomic RNA. Substitution singly, or in combination, of three nucleotides in the anticodon loop resulted in very poor valylation (Vmax/KM less than 10(-3) relative to wild type). These nucleotides thus represent the major valine identity determinants recognized by wheat germ valyl-tRNA synthetase; their relative contribution to valine identity, in descending order, was as follows: the middle nucleotide of the anticodon (A56 in TYMV RNA), the 3' anticodon nucleotide (C55), and the 3'-most anticodon loop nucleotide (C53). Substitutions in the wobble position (C57) had no significant effect on valylation kinetics, while substitutions of the discriminator base (A4) resulted in small decreases in Vmax/Km. Mutations in the major identity nucleotides resulted in large increases in KM, suggesting that wheat germ valyl-tRNA synthetase has a lowered affinity for variant substrates with low valine identity. Comparison with other studies using valyl-tRNA synthetases from Escherichia coli and yeast indicates that the anticodon has been phylogenetically conserved as the dominant valine identity region, while the identity contribution of the discriminator base has been less conserved. The mechanism by which anticodon mutations are discriminated also appears to vary, being affinity-based for the wheat germ enzyme, and kinetically-based for the yeast enzyme [Florentz et al. (1991) Eur. J. Biochem. 195, 229-234].},
note = {0006-2960
Journal Article},
keywords = {Anticodon/genetics/*metabolism Bacteriophage T7/enzymology Base Sequence DNA-Directed RNA Polymerases/metabolism Kinetics Molecular Sequence Data Mosaic Viruses/genetics/*metabolism Nucleic Acid Conformation RNA, FLORENTZ, Genetic Triticum/*enzymology Valine-tRNA Ligase/*metabolism Variation (Genetics), Non-P.H.S. Support, Non-U.S. Gov't Support, P.H.S. Transcription, Transfer/chemistry/metabolism RNA, U.S. Gov't, Unité ARN, Viral/chemistry/genetics/*metabolism Seeds/enzymology Support},
pubstate = {published},
tppubtype = {article}
}