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Chapter 10 : tRNA-Like Structures in Plant Viral RNAs

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Abstract:

This chapter summarizes the structural and functional mimicry of tRNA by plant viral tRNA-like structures, and emphasizes how studies on these structures were innovative in the domain of RNA folding and beneficial to the better understanding of canonical tRNA aminoacylation. It also discusses current ideas about the biological significance of these aminoacylatable structures as well as other viral RNA sequences mimicking tRNA, during the life cycles of their carrier viruses.

Citation: Florentz C, Giegé R. 1995. tRNA-Like Structures in Plant Viral RNAs , p 141-163. In tRNA. ASM Press, Washington, DC. doi: 10.1128/9781555818333.ch10

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Figures

Image of Figure 1.
Figure 1.

Secondary structure of a canonical tRNA, yeast tRNA (A), and of the 3′ ends of TYMV RNA (B), TMV RNA (C), and BMV RNA (D), encompassing the tRNA-like domains. Numbering of the tRNA-like structures starts at the 3′-end, at variance with the convention in nucleic acids. This is due to the lack of knowledge about the exact minimal length required for tRNA functions. The anticodon triplet of tRNA and the potential anticodon triplets of the tRNA-like structures are shaded. The strongest structural analogies with the tRNA cloverleaf appear for TYMV RNA, where stem and loops II to IV are analogous to the T, anticodon, and D stems and loops. Sequence homologies of this tRNA-like structure with yeast tRNAare boxed in both molecules. In contrast to canonical tRNAs, viral RNAs have no modified bases.

Citation: Florentz C, Giegé R. 1995. tRNA-Like Structures in Plant Viral RNAs , p 141-163. In tRNA. ASM Press, Washington, DC. doi: 10.1128/9781555818333.ch10
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Image of Figure 2.
Figure 2.

Folding pathway of the tRNA-like domain of TYMV RNA. (A) Experimental secondary structure of the 84 last nucleotides of the viral RNA, with long distance Watson-Crick interactions indicated ( ). (B) Schematic representation of an L folding emphasizing the 12-bp acceptor arm, including a pseudoknot. L1 and L2, two single-stranded regions crossing the acceptor arm helix, are part of the pseudoknot. (C) Artist′s view of the three-dimensional folding ( ). (D) Three-dimensional model, constructed by computer modeling ( ). Whereas the acceptor arm including the pseudoknot has been constructed de novo, the construction of the rest of the molecule was mainly based on the crystallographic structure of yeast tRNA( ).

Citation: Florentz C, Giegé R. 1995. tRNA-Like Structures in Plant Viral RNAs , p 141-163. In tRNA. ASM Press, Washington, DC. doi: 10.1128/9781555818333.ch10
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Image of Figure 3.
Figure 3.

Schematic three-dimensional foldings of tRNA-like domains of TMV RNA (A) and BMV RNA (B and C). Notice that the tRNA-like structure of TMV contains two pseudoknots ( ) and that of BMV presents a new type of pseudoknot involved in the formation of the acceptor arm. The folding in panel B corresponds to the proposed minimal sequence of 134 nucleotides required for aminoacylation of BMV RNA ( ); an alternative structure presented in panel C includes a hairpin (boxed) external to the minimal structure, which is important for the aminoacylation of this molecule ( ). Modeling has recently shown that hairpin loop C156-C169 (see Fig. 1D ) belongs to the actual BMV tRNA-like core in which it mimics the D-arm ( ). Potential anticodon sequences are shaded in the three models.

Citation: Florentz C, Giegé R. 1995. tRNA-Like Structures in Plant Viral RNAs , p 141-163. In tRNA. ASM Press, Washington, DC. doi: 10.1128/9781555818333.ch10
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Image of Figure 4.
Figure 4.

Pseudoknots. (A) Different schematic steps of formation of a pseudoknot. (B and C) Stereoscopic views of the modelized pseudoknot from the acceptor arm of the TYMV tRNA-like structure ( ). In panel B, the view is along the axis of the helix, the 3′-end CCA sequence being on top of the picture; in panel C, it is through the helical axis (CCA-end in front of the reader), highlighting the differential bulging out of loops L1 (left) and L2 (bottom). Notice that about two-thirds of the external surface of the pseudoknot helix perfectly mimics a classical RNA helix. (Adapted from references 102 and 37.)

Citation: Florentz C, Giegé R. 1995. tRNA-Like Structures in Plant Viral RNAs , p 141-163. In tRNA. ASM Press, Washington, DC. doi: 10.1128/9781555818333.ch10
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Image of Figure 5.
Figure 5.

Arrhenius plot of aminoacylation with yeast ValRS of various tRNAs from yeast and of the RNA of TYMV. Notice the biphasic dependence of the rate of aminoacylation of TYMV RNA. Aminoacylation conditions are as described by Giegé et al. ( ). ka is the valylation rate constant and T is the absolute temperature.

Citation: Florentz C, Giegé R. 1995. tRNA-Like Structures in Plant Viral RNAs , p 141-163. In tRNA. ASM Press, Washington, DC. doi: 10.1128/9781555818333.ch10
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Image of Figure 6.
Figure 6.

Valylation of yeast tRNA (A and C) and of TYMV tRNA-like structure (B) by yeast ValRS as a function of increasing ammonium sulfate concentrations. Valylation initial rates were normalized with values obtained for the tRNA or the tRNA-like structure in the absence of ammonium sulfate. Aminoacylation conditions are as described by Florentz et al. ( ). In panel C, the reaction medium contained an additional 500 mM NaCl.

Citation: Florentz C, Giegé R. 1995. tRNA-Like Structures in Plant Viral RNAs , p 141-163. In tRNA. ASM Press, Washington, DC. doi: 10.1128/9781555818333.ch10
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Image of Figure 7.
Figure 7.

Protection of tRNA-like molecules and tRNAs against nuclease digestion and /or chemical modification by complex formation with their cognate aminoacyl-tRNA synthetase. Protected residues are dotted. TYMV tRNA-like structure (A1 ) and yeast tRNA (A2), protected by yeast ValRS ( ); TMV (strain U2) tRNA-like structure (B), protected by yeast HisRS ( ); and BMV tRNA-like structure (C1) and yeast tRNA (C2), protected by yeast TyrRS ( ). Involvement of the CCA-end could not been tested in Al, A2, B, and C2.

Citation: Florentz C, Giegé R. 1995. tRNA-Like Structures in Plant Viral RNAs , p 141-163. In tRNA. ASM Press, Washington, DC. doi: 10.1128/9781555818333.ch10
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Image of Figure 8.
Figure 8.

Nucleotides within tRNA-like structure of BMV RNA (A) and TYMV RNA (B) important for specific aminoacylation by TyrRS ( ) and ValRS ( ), respectively. Nucleotides that are required for aminoacylation by wheat germ enzymes are boxed in heavy lines, and nucleotides in the TYMV tRNA-like structure required for valylation by yeast ValRS are circled. The requirement of the two 3′-nucleotides of the anticodon loop for aminoacylation by yeast ValRS has not been tested. The boxed hairpin in panel A can be removed from the BMV structure without affecting tyrosylation.

Citation: Florentz C, Giegé R. 1995. tRNA-Like Structures in Plant Viral RNAs , p 141-163. In tRNA. ASM Press, Washington, DC. doi: 10.1128/9781555818333.ch10
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Image of Figure 9.
Figure 9.

Comparison of regions within BMV tRNA-like structure important for adenylation (A), tyrosylation (B), and replication (C) ( ). See also reference 40b for a discussion on structure-function aspects.

Citation: Florentz C, Giegé R. 1995. tRNA-Like Structures in Plant Viral RNAs , p 141-163. In tRNA. ASM Press, Washington, DC. doi: 10.1128/9781555818333.ch10
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Tables

Generic image for table
Table 1

Summary of published work establishing that plant viral RNAs are substrates in tRNA specific processes

(+) indicates a reactivity with viral RNA, (—) indicates no reactivity.

For a classification of viruses, see Francki et al. ( ).

RNA from the TMV cowpea strain is valylatable.

TYMV RNA can be efficiently mischarged by yeast histidyl-tRNA synthetase Rudinger et al.; reference 149).

Citation: Florentz C, Giegé R. 1995. tRNA-Like Structures in Plant Viral RNAs , p 141-163. In tRNA. ASM Press, Washington, DC. doi: 10.1128/9781555818333.ch10
Generic image for table
Table 2

Aminoacylation of various classical and tRNA-like substrates

Aminoacylation conditions and numerical data for K and values are from Giege et al. ( ). Efficiency of valylation is estimated by the ration k/K, normalized to 1 for cognate tRNA.

Citation: Florentz C, Giegé R. 1995. tRNA-Like Structures in Plant Viral RNAs , p 141-163. In tRNA. ASM Press, Washington, DC. doi: 10.1128/9781555818333.ch10
Generic image for table
Table 3

Kinetic parameters of valylation of wild-type and mutated TYMV tRNA-like transcripts (264 nucleotides) with wheat germ ValRS

Mutations affect the anticodon nucleotides CS7, A56, C55 as well as the nucleotides of the 3′ side of the anticodon loop, AS4 and C53. Names of mutants reflect their sequence. Calculated losses in efficiency for double or triple mutants correspond to the products of measured losses in efficiency of the corresponding single mutants. Adapted from Dreher et al. ( ).

Citation: Florentz C, Giegé R. 1995. tRNA-Like Structures in Plant Viral RNAs , p 141-163. In tRNA. ASM Press, Washington, DC. doi: 10.1128/9781555818333.ch10
Generic image for table
Table 4

Kinetic parameters of histidinylation of TYMV transcripts of different sequence and length

Data are adapted from Rudinger et al. ( ).

Citation: Florentz C, Giegé R. 1995. tRNA-Like Structures in Plant Viral RNAs , p 141-163. In tRNA. ASM Press, Washington, DC. doi: 10.1128/9781555818333.ch10

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