Evolution of a helper virus-derived, ribosome binding translational enhancer in an untranslated satellite RNA of Turnip crinkle virus

Guo, Ruifeng; Meškauskas, Arturas; Dinman, Jonathan D.; Simon, Anne

doi:10.1016/j.virol.2011.07.019

Cited by 5 publications

(4 citation statements)

References 34 publications

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“…In TCV but not satC, H5 along with H4a, H4b, Ψ 2 (a pseudoknot formed from sequences immediately 3′ of H5 and in the loop of H4b) and Ψ 3 (a pseudoknot between the loop of H4a and upstream adjacent sequence) fold into a T-shaped structure (TSS; McCormack et al ., 2008) that binds to ribosomes and serves as a cap-independent translation enhancer (Stupina et al ., 2008). This region in satC is not predicted to form a TSS and no longer binds efficiently to ribosomes due to six positional differences with the TCV parental sequence (Guo et al ., 2011). However, hairpins H5, H4a, H4b and pseudoknot Ψ 2 are important for satC accumulation (Zhang et al ., 2006c), and Ψ 3 appears to be important for satC fitness (Guo et al ., 2011).…”

Section: Introductionmentioning

confidence: 99%

“…This region in satC is not predicted to form a TSS and no longer binds efficiently to ribosomes due to six positional differences with the TCV parental sequence (Guo et al ., 2011). However, hairpins H5, H4a, H4b and pseudoknot Ψ 2 are important for satC accumulation (Zhang et al ., 2006c), and Ψ 3 appears to be important for satC fitness (Guo et al ., 2011). …”

Section: Introductionmentioning

confidence: 99%

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Rapid evolution of in vivo-selected sequences and structures replacing 20% of a subviral RNA

et al. 2015

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The 356 nt noncoding satellite RNA C (satC) of Turnip crinkle virus (TCV) is composed of 5′ sequences from a second TCV satRNA (satD) and 3′ sequences derived from TCV. SHAPE structure mapping revealed that 76 nt in the poorly-characterized satD-derived region form an extended hairpin (H2). Pools of satC in which H2 was replaced with 76, 38, or 19 random nt were co-inoculated with TCV helper virus onto plants and satC fitness assessed using in vivo functional selection (SELEX). The most functional progeny satCs, including one as fit as wild-type, contained a 38-39 nt H2 region that adopted a hairpin structure and exhibited an increased ratio of dimeric to monomeric molecules. Some progeny of satC with H2 deleted featured a duplication of 38 nt, partially rebuilding the deletion. Therefore, H2 can be replaced by a 38-39 nt hairpin, sufficient for overall structural stability of the 5′ end of satC.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Rapid evolution of in vivo-selected sequences and structures replacing 20% of a subviral RNA

et al. 2015

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“…Although satC contains the TCV region that harbors the TSS, six positional differences between satC and TCV in this region disrupt the TSS structure (Stupina et al, 2008), and satC is unable to bind to ribosomes (Guo et al, 2011;Stupina et al, 2008).…”

Section: Higher-order Structures: Carmovirus 3'citesmentioning

confidence: 99%

3′UTRs of carmoviruses

Simon

2015

Virus Research

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Carmovirus is a genus of small, single-stranded, positive-strand RNA viruses in the Tombusviridae. One member of the carmoviruses, Turnip crinkle virus (TCV), has been used extensively as a model for examining the structure and function of RNA elements in 3'UTR as well as in other regions of the virus. Using a variety of genetic, biochemical and computational methods, a structure for the TCV 3'UTR has emerged where secondary structures and tertiary interactions combine to adopt higher order 3-D structures including an internal, ribosome-binding tRNA-shaped configuration that functions as a 3' cap-independent translation enhancer (3'CITE). The TCV 3'CITE also serves as a scaffold for non-canonical interactions throughout the 3'UTR and extending into the upstream open reading frame, interactions that are significantly disrupted upon binding by the RNA-dependent RNA polymerase. Long-distance interactions that connect elements in the 3'UTR with both the 5' end and the internal ribosome recoding site suggest that 3'UTR of carmoviruses are intimately involved in multiple functions in the virus life cycle. Although carmoviruses share very similar genome organizations, lengths of 5' and 3'UTRs, and structural features at the 3' end, the similarity rapidly breaks down the further removed from the 3' terminus revealing different 3'CITEs and unique virus-specific structural features. This review summarizes 20 years of work dissecting the structure and function of the 3'UTR of TCV and other carmoviruses. The astonishing structural complexity of the 3'UTRs of these simple carmoviruses provides lessons that are likely applicable to many other plant and animal RNA viruses.

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“…The current model for the gRNA switching from a translated template to a replication template posits that the RNA-dependent RNA polymerase (RdRp) binds to an A-rich region upstream of H4a/Ψ 3 , leading to disruption of H4a/Ψ 3 that disassembles the TSS, resulting in a widespread conformational switch (Yuan et al ., 2009; Yuan et al ., 2012; Le et al ., 2017). SatC, despite having similar versions of all these hairpins and pseudoknots, is not predicted to form a TSS and does not bind ribosomes due to 6 single-nt differences with the TSS of TCV (Guo et al ., 2011). However, initiation of minus-strand synthesis by the RdRp requires that the 3’ end of satC toggles between pre-active and active structures (Zhang et al ., 2006a; Zhang et al ., 2006b).…”

Section: Introductionmentioning

confidence: 99%

SELEX and SHAPE reveal that sequence motifs and an extended hairpin in the 5’ portion of Turnip crinkle virus satellite RNA C mediate fitness in plants

et al. 2018

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Noncoding RNAs use their sequence and/or structure to mediate function(s). The 5' portion (166 nt) of the 356-nt noncoding satellite RNA C (satC) of Turnip crinkle virus (TCV) was previously modeled to contain a central region with two stem-loops (H6 and H7) and a large connecting hairpin (H2). We now report that in vivo functional selection (SELEX) experiments assessing sequence/structure requirements in H2, H6, and H7 reveal that H6 loop sequence motifs were recovered at nonrandom rates and only some residues are proposed to base-pair with accessible complementary sequences within the 5' central region. In vitro SHAPE of SELEX winners indicates that the central region is heavily base-paired, such that along with the lower stem and H2 region, one extensive hairpin exists composing the entire 5' region. As these SELEX winners are highly fit, these characteristics facilitate satRNA amplification in association with TCV in plants.

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Evolution of a helper virus-derived, ribosome binding translational enhancer in an untranslated satellite RNA of Turnip crinkle virus

Cited by 5 publications

References 34 publications

Rapid evolution of in vivo-selected sequences and structures replacing 20% of a subviral RNA

Rapid evolution of in vivo-selected sequences and structures replacing 20% of a subviral RNA

3′UTRs of carmoviruses

SELEX and SHAPE reveal that sequence motifs and an extended hairpin in the 5’ portion of Turnip crinkle virus satellite RNA C mediate fitness in plants

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