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Secondary structure and domain architecture of the 23S and 5S rRNAs.

Petrov AS, Bernier CR, Hershkovits E, Xue Y, Waterbury CC, Hsiao C, Stepanov VG, Gaucher EA, Grover MA, Harvey SC, Hud NV, Wartell RM, Fox GE, Williams LD - Nucleic Acids Res. (2013)

Bottom Line: We partitioned the 23S rRNA into domains through analysis of molecular interactions, calculations of 2D folding propensities and compactness.The best domain model for the 23S rRNA contains seven domains, not six as previously ascribed.Domain 0 forms the core of the 23S rRNA, to which the other six domains are rooted.

View Article: PubMed Central - PubMed

Affiliation: School of Chemistry and Biochemistry, Georgia Institute of Technology, Atlanta, GA 30332, USA, Center for Ribosomal Origins and Evolution, Georgia Institute of Technology, Atlanta, GA 30332, USA, School of Chemical and Biomolecular Engineering, Georgia Institute of Technology, Atlanta, GA 30332, USA, Department of Biology and Biochemistry, University of Houston, Houston, TX 77204, USA and School of Biology, Georgia Institute of Technology, Atlanta, GA 30332, USA.

ABSTRACT
We present a de novo re-determination of the secondary (2°) structure and domain architecture of the 23S and 5S rRNAs, using 3D structures, determined by X-ray diffraction, as input. In the traditional 2° structure, the center of the 23S rRNA is an extended single strand, which in 3D is seen to be compact and double helical. Accurately assigning nucleotides to helices compels a revision of the 23S rRNA 2° structure. Unlike the traditional 2° structure, the revised 2° structure of the 23S rRNA shows architectural similarity with the 16S rRNA. The revised 2° structure also reveals a clear relationship with the 3D structure and is generalizable to rRNAs of other species from all three domains of life. The 2° structure revision required us to reconsider the domain architecture. We partitioned the 23S rRNA into domains through analysis of molecular interactions, calculations of 2D folding propensities and compactness. The best domain model for the 23S rRNA contains seven domains, not six as previously ascribed. Domain 0 forms the core of the 23S rRNA, to which the other six domains are rooted. Editable 2° structures mapped with various data are provided (http://apollo.chemistry.gatech.edu/RibosomeGallery).

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The mapping of all base pairing interactions onto 2° structure3D. Nucleotides that are base paired in the 3D structure of the ribosome are connected by lines in the 2° structure here. The 5S rRNA is placed in proximity to Helix 39 to reflect their relative locations in 3D space. The interactions between 23S and 5S rRNAa are illustrated in Supplementary Figure S4. Domain 0 is stabilized by many base-pairing interactions. The coloring scheme of the domains is the same as in Figure 5. The most frequent subtypes of base pair interactions [cWW, tWW, tSS and cSS, defined by Leontis (26)] are illustrated in Supplementary Figure S6.
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gkt513-F6: The mapping of all base pairing interactions onto 2° structure3D. Nucleotides that are base paired in the 3D structure of the ribosome are connected by lines in the 2° structure here. The 5S rRNA is placed in proximity to Helix 39 to reflect their relative locations in 3D space. The interactions between 23S and 5S rRNAa are illustrated in Supplementary Figure S4. Domain 0 is stabilized by many base-pairing interactions. The coloring scheme of the domains is the same as in Figure 5. The most frequent subtypes of base pair interactions [cWW, tWW, tSS and cSS, defined by Leontis (26)] are illustrated in Supplementary Figure S6.

Mentions: The allocation of RNA–RNA interactions between secondary and tertiary interactions differs between 2° structure3D and Structurephylo. Twenty-one tertiary interactions in 2° structurephylo are converted to secondary interactions in 2° structure3D. This difference can be seen in the projections of all base-pairing interactions onto 2° structure3D (Figure 6) and 2° structurephylo (Figure 2). The short lines in Figures 2 and 6 that connect two opposing stands in a helix represent secondary interactions. Longer lines depict tertiary interactions. Eight base-pairing interactions of Helix 26a (residues 1262–1270 are paired with residues 2010–2017, with residue 1266 forming a triple base pair) are tertiary interactions in 2° structurephylo and secondary interactions in 2° structure3D. Eight base-pairing interactions in Helix 1 (residues 1–8 are paired with 2895–2902) and 5 base-pairing interactions in Helix 2 (residues 26–30 are paired with 510–514) are represented as tertiary interactions in 2° structurephylo, but as secondary interactions in 2° structurephylo.Figure 6.


Secondary structure and domain architecture of the 23S and 5S rRNAs.

Petrov AS, Bernier CR, Hershkovits E, Xue Y, Waterbury CC, Hsiao C, Stepanov VG, Gaucher EA, Grover MA, Harvey SC, Hud NV, Wartell RM, Fox GE, Williams LD - Nucleic Acids Res. (2013)

The mapping of all base pairing interactions onto 2° structure3D. Nucleotides that are base paired in the 3D structure of the ribosome are connected by lines in the 2° structure here. The 5S rRNA is placed in proximity to Helix 39 to reflect their relative locations in 3D space. The interactions between 23S and 5S rRNAa are illustrated in Supplementary Figure S4. Domain 0 is stabilized by many base-pairing interactions. The coloring scheme of the domains is the same as in Figure 5. The most frequent subtypes of base pair interactions [cWW, tWW, tSS and cSS, defined by Leontis (26)] are illustrated in Supplementary Figure S6.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3753638&req=5

gkt513-F6: The mapping of all base pairing interactions onto 2° structure3D. Nucleotides that are base paired in the 3D structure of the ribosome are connected by lines in the 2° structure here. The 5S rRNA is placed in proximity to Helix 39 to reflect their relative locations in 3D space. The interactions between 23S and 5S rRNAa are illustrated in Supplementary Figure S4. Domain 0 is stabilized by many base-pairing interactions. The coloring scheme of the domains is the same as in Figure 5. The most frequent subtypes of base pair interactions [cWW, tWW, tSS and cSS, defined by Leontis (26)] are illustrated in Supplementary Figure S6.
Mentions: The allocation of RNA–RNA interactions between secondary and tertiary interactions differs between 2° structure3D and Structurephylo. Twenty-one tertiary interactions in 2° structurephylo are converted to secondary interactions in 2° structure3D. This difference can be seen in the projections of all base-pairing interactions onto 2° structure3D (Figure 6) and 2° structurephylo (Figure 2). The short lines in Figures 2 and 6 that connect two opposing stands in a helix represent secondary interactions. Longer lines depict tertiary interactions. Eight base-pairing interactions of Helix 26a (residues 1262–1270 are paired with residues 2010–2017, with residue 1266 forming a triple base pair) are tertiary interactions in 2° structurephylo and secondary interactions in 2° structure3D. Eight base-pairing interactions in Helix 1 (residues 1–8 are paired with 2895–2902) and 5 base-pairing interactions in Helix 2 (residues 26–30 are paired with 510–514) are represented as tertiary interactions in 2° structurephylo, but as secondary interactions in 2° structurephylo.Figure 6.

Bottom Line: We partitioned the 23S rRNA into domains through analysis of molecular interactions, calculations of 2D folding propensities and compactness.The best domain model for the 23S rRNA contains seven domains, not six as previously ascribed.Domain 0 forms the core of the 23S rRNA, to which the other six domains are rooted.

View Article: PubMed Central - PubMed

Affiliation: School of Chemistry and Biochemistry, Georgia Institute of Technology, Atlanta, GA 30332, USA, Center for Ribosomal Origins and Evolution, Georgia Institute of Technology, Atlanta, GA 30332, USA, School of Chemical and Biomolecular Engineering, Georgia Institute of Technology, Atlanta, GA 30332, USA, Department of Biology and Biochemistry, University of Houston, Houston, TX 77204, USA and School of Biology, Georgia Institute of Technology, Atlanta, GA 30332, USA.

ABSTRACT
We present a de novo re-determination of the secondary (2°) structure and domain architecture of the 23S and 5S rRNAs, using 3D structures, determined by X-ray diffraction, as input. In the traditional 2° structure, the center of the 23S rRNA is an extended single strand, which in 3D is seen to be compact and double helical. Accurately assigning nucleotides to helices compels a revision of the 23S rRNA 2° structure. Unlike the traditional 2° structure, the revised 2° structure of the 23S rRNA shows architectural similarity with the 16S rRNA. The revised 2° structure also reveals a clear relationship with the 3D structure and is generalizable to rRNAs of other species from all three domains of life. The 2° structure revision required us to reconsider the domain architecture. We partitioned the 23S rRNA into domains through analysis of molecular interactions, calculations of 2D folding propensities and compactness. The best domain model for the 23S rRNA contains seven domains, not six as previously ascribed. Domain 0 forms the core of the 23S rRNA, to which the other six domains are rooted. Editable 2° structures mapped with various data are provided (http://apollo.chemistry.gatech.edu/RibosomeGallery).

Show MeSH