Identification of Novel 5′ and 3′ Translation Enhancers in Umbravirus-Like Coat Protein-Deficient RNA Replicons

被引:8
作者
Liu, Jingyuan [1 ]
Simon, Anne E. [1 ]
机构
[1] Univ Maryland, Dept Cell Biol & Mol Genet, College Pk, MD 20742 USA
基金
美国国家科学基金会;
关键词
3 ' CITEs; noncanonical translation; RNA structure; eIF4G-binding structure; translation enhancer; CAP-INDEPENDENT TRANSLATION; ENATION-MOSAIC-VIRUS; T-SHAPED STRUCTURE; RIBOSOME-BINDING; ELEMENT; INITIATION; SUBUNIT; EIF4F; RECRUITMENT; COMPLEX;
D O I
10.1128/jvi.01736-21
中图分类号
Q93 [微生物学];
学科分类号
071005 ; 100705 ;
摘要
Translation of plant plus-strand RNA viral genomes that lack a 5' cap frequently requires the use of cap-independent translation enhancers (CITEs) located in or near the 3' untranslated region (UTR). 3'CITEs are grouped based on secondary structure and ability to interact with different translation initiation factors or ribosomal subunits, which assemble a complex at the 3' end that is nearly always transferred to the 5' end via a long-distance kissing-loop interaction between sequences in the 3'CITE and 5' hairpins. We report here the identification of a novel 3'CITE in coat protein-deficient RNA replicons that are related to umbraviruses. Umbra-like associated RNAs (uIaRNAs), such as citrus yellow vein-associated virus (CYVaV), are a new type of subviral RNA that do not encode movement proteins, coat proteins, or silencing suppressors but can independently replicate using their encoded RNA-dependent RNA polymerase. An extended hairpin structure containing multiple internal loops in the 3' UTR of CYVaV is strongly conserved in the most closely related ulaRNAs and structurally resembles an I-shaped structure (ISS) 3'CITE. However, unlike ISS, the CYVaV structure binds to eIF4G and no long-distance interaction is discernible between the CYVaV ISS-like structure and sequences at or near the 5' end. We also report that the similar to 30-nucleotide (nt) 5' terminal hairpin of CYVaV and related ulaRNAs can enhance translation of reporter constructs when associated with either the CYVaV 3'CITE or the 3'CITEs of umbravirus pea enation mosaic virus (PEMV2) and even independent of a 3'CITE. These findings introduce a new type of 3'CITE and provide the first information on translation of ulaRNAs. IMPORTANCE Umbra-like associated RNAs (ulaRNAs) are a recently discovered type of subviral RNA that use their encoded RNA-dependent RNA polymerase for replication but do not encode any coat proteins, movement proteins, or silencing suppressors yet can be found in plants in the absence of any discernible helper virus. We report the first analysis of their translation using class 2 uIaRNA citrus yellow vein-associated virus (CYVaV). CYVaV uses a novel eIF4G-binding I-shaped structure as its 3' cap-independent translation enhancer (3'CITE), which does not connect with the 5' end by a long-distance RNA:RNA interaction that is typical of 3'CITEs. uIaRNA 5' terminal hairpins can also enhance translation in association with cognate 3'CITEs or those of related ulaRNAs and, to a lesser extent, with 3'CITEs of umbraviruses, or even independent of a 3'CITE. These findings introduce a new type of 3'CITE and provide the first information on translation of ulaRNAs.
引用
收藏
页数:18
相关论文
共 54 条
[1]   Efficient Translation of Pelargonium line pattern virus RNAs Relies on a TED-Like 3′-Translational Enhancer that Communicates with the Corresponding 5′-Region through a Long-Distance RNA-RNA Interaction [J].
Blanco-Perez, Marta ;
Perez-Canamas, Miryam ;
Ruiz, Leticia ;
Hernandez, Carmen .
PLOS ONE, 2016, 11 (04)
[2]   Long-distance kissing loop interactions between a 3′ proximal Y-shaped structure and apical loops of 5′ hairpins enhance translation of Saguaro cactus virus [J].
Chattopadhyay, Maitreyi ;
Shi, Kerong ;
Yuan, Xuefeng ;
Simon, Anne E. .
VIROLOGY, 2011, 417 (01) :113-125
[3]   Multifaceted Regulation of Translational Readthrough by RNA Replication Elements in a Tombusvirus [J].
Cimino, Peter A. ;
Nicholson, Beth L. ;
Wu, Baodong ;
Xu, Wei ;
White, Andrew .
PLOS PATHOGENS, 2011, 7 (12)
[4]   An umbra-related virus found in babaco (Vasconcellea x heilbornii) [J].
Cornejo-Franco, Juan F. ;
Flores, Francisco ;
Mollov, Dimitre ;
Quito-Avila, Diego F. .
ARCHIVES OF VIROLOGY, 2021, 166 (08) :2321-2324
[5]   Transmission of the umbra-like Papaya virus Q in Ecuador and its association with meleira-related viruses from Brazil [J].
Cornejo-Franco, Juan F. ;
Alvarez-Quinto, Robert A. ;
Quito-Avila, Diego F. .
CROP PROTECTION, 2018, 110 :99-102
[6]   Recruitment of the 40S Ribosomal Subunit to the 3′-Untranslated Region (UTR) of a Viral mRNA, via the eIF4 Complex, Facilitates Cap-independent Translation [J].
Das Sharma, Sohani ;
Kraft, Jelena J. ;
Miller, W. Allen ;
Goss, Dixie J. .
JOURNAL OF BIOLOGICAL CHEMISTRY, 2015, 290 (18) :11268-11281
[7]   Concerted action of two 3′ cap-independent translation enhancers increases the competitive strength of translated viral genomes [J].
Du, Zhiyou ;
Alekhina, Olga M. ;
Vassilenko, Konstantin S. ;
Simon, Anne E. .
NUCLEIC ACIDS RESEARCH, 2017, 45 (16) :9558-9572
[8]  
Felker P, 2019, J PROF ASSOC CACTUS, V21, P1
[9]   Differential use of 3′CITEs by the subgenomic RNA of Pea enation mosaic virus 2 [J].
Gao, Feng ;
Simon, Anne E. .
VIROLOGY, 2017, 510 :194-204
[10]   Multiple Cis-acting elements modulate programmed-1 ribosomal frameshifting in Pea enation mosaic virus [J].
Gao, Feng ;
Simon, Anne E. .
NUCLEIC ACIDS RESEARCH, 2016, 44 (02) :878-895