Heterogeneity in the 3′-terminal untranslated region of tobacco mild green mosaic tobamoviruses from Nicotiana glauca resulting in variants with three or six pseudoknots

Bodaghi, Sohrab; Yassi, Martin Ngon A; Dodds, J. A.

doi:10.1099/0022-1317-81-3-577

Cited by 13 publications

(11 citation statements)

References 23 publications

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“…A second posibility is that TMGMV infects other, nonidentified hosts in the same region, in which an alanine at CP position 148 would be advantageous. The 3= UTR-length dimorphism has been reported in the TMGMV population infecting N. glauca in California (60,61), and it was shown that isolates with a long 3= UTR outcompeted those with a short one (61). In our isolate collection, however, the 3= UTR length was not associated with differential levels of virus multiplication in N. glauca, but in pepper, isolates having a short 3= UTR had an advantage.…”

Section: Discussionsupporting

confidence: 50%

Analysis of Fitness Trade-Offs in the Host Range Expansion of an RNA Virus, Tobacco Mild Green Mosaic Virus

Bera

Fraile

García‐Arenal

2018

J Virol

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The acquisition of new hosts provides a virus with more opportunities for transmission and survival but may be limited by across-host fitness trade-offs. Major causes of across-host trade-offs are antagonistic pleiotropy, that is, host differential phenotypic effects of mutations, a Genotype x Environment interaction, and epistasis, a Genotype x Genotype interaction. Here, we analyze if there are trade-offs, and what are the causes, associated with the acquisition by tobacco mild green mosaic virus (TMGMV) of a new host. For this, the multiplication of sympatric field isolates of TMGMV from its wild reservoir host Nicotiana glauca and from pepper crops was quantified in the original and the heterologous hosts. TMGMV isolates from N. glauca were adapted to their host, but pepper isolates were not adapted to pepper, and the acquisition of this new host was associated with a fitness penalty in the original host. Analyses of the collection of field isolates and of mutant genotypes derived from biologically active cDNA clones showed a role of mutations in the coat protein and the 3′ untranslated region in determining within-host virus fitness. Fitness depended on host-specific effects of these mutations, on the genetic background in which they occurred, and on higher-order interactions of the type Genotype x Genotype x Environment. These types of effects had been reported to generate across-host fitness trade-offs under experimental evolution. Our results show they may also operate in heterogeneous natural environments and could explain why pepper isolates were not adapted to pepper and their lower fitness in N. glauca.IMPORTANCE The acquisition of new hosts conditions virus epidemiology and emergence; hence it is important to understand the mechanisms behind host range expansion. Experimental evolution studies have identified antagonistic pleiotropy and epistasis as genetic mechanisms that limit host range expansion, but studies from virus field populations are few. Here, we compare the performance of isolates of tobacco mild green mosaic virus from its reservoir host, Nicotiana glauca, and its new host, pepper, showing that acquisition of a new host was not followed by adaptation to it but was associated with a fitness loss in the original host. Analysis of mutations determining host-specific virus multiplication identified antagonistic pleiotropy, epistasis, and host-specific epistasis as mechanisms generating across-host fitness trade-offs that may prevent adaptation to pepper and cause a loss of fitness in N. glauca. Thus, mechanisms determining trade-offs, identified under experimental evolution, could also operate in the heterogeneous environment in which natural plant virus populations occur.

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Section: Discussionsupporting

confidence: 50%

Analysis of Fitness Trade-Offs in the Host Range Expansion of an RNA Virus, Tobacco Mild Green Mosaic Virus

Bera

Fraile

García‐Arenal

2018

J Virol

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“…Of the three strains, U2 and U5 have been described from the United States, 8,9 and they differ in the size in their 3 0 untranslated regions (UTR). Strain TMGMV-U5 has a repeated sequence of 147-nucleotides in the 3´UTR compared with TMGMV-U2.…”

Section: Introductionmentioning

confidence: 99%

Host‐virus interaction between tobacco mild green mosaic virus strain U2 and tropical soda apple resulting in systemic hypersensitive necrosis and the host range, survival, spread, and molecular characterization of the virus

Charudattan,

Hiebert,

Pettersen

et al. 2023

Pest Management Science

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BackgroundTobacco mild green mosaic virus strain U2 (TMGMV‐U2) is a registered active ingredient in a bioherbicide to control tropical soda apple (TSA), Solanum viarum, an invasive weed. As required for registration, we developed empirical data on the host‐virus interaction and the virus's host range, survival, spread, and genomic sequence.ResultsTMGMV‐U2 killed TSA plants by causing systemic hypersensitive necrosis (SHN). It elicited local lesions in inoculated leaves which was followed by the plant's wilting and death. It moved from inoculated terminal leaves through the vasculature to roots and then to newly developed leaves. Phloem death was implicated in wilting and plant death. The SHN response was attenuated in plants grown at constant 32 °C. TMGMV‐U2 titer in TSA was low compared to a systemically susceptible tobacco. The virus remained infective for up to 6 mo in infected dead TSA tissues and in soil in which infected plants had grown. Susceptible tobacco and pepper plants grown in soil that previously had infected dead TSA or in soil amended with the virus remained asymptomatic and virus‐free. A susceptible pepper crop grown in a field block following two consecutive crops of TMGMV‐U2‐infected susceptible tobacco grew disease‐free and virus‐free and without yield loss. Purified TMGMV‐U2 was infective for 1 yr when stored at ‐20 °C or 5 °C and for 1 mo at room temperature. No virus spread was found in the field. Genomic analyses confirmed the registered isolate to be a U2 strain and free of satellite TMV. The TMGMV‐U2‐susceptible species preponderantly belonged to the Solanaceae. A few hosts that were killed belonged to this family. Several new hosts to TMGMV‐U2 were found. These data enabled registration of TMGMV‐U2.ConclusionTMGMV‐U2 can be used safely as a bioherbicide without risks to nontarget plants and the environment.This article is protected by copyright. All rights reserved.

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“…It illustrates the high flexibility in the make-up of 39 ends among these virus genera, which is presumably due to recombination events in doubly infected plant hosts. This suggestion is supported by the occurrence of frequent duplications of UPDs and parts of the TLS in several tobamoviruses (Gultyaev et al, 1994;Bodaghi et al, 2000;Ruiz del Pino et al, 2003). In view of the observations summarized in Figs 5 and 7, it might not be surprising if some day a pomo-or furovirus would be detected with an RNA that has a histidylatable TLS on its 39 end rather than the common valylatable TLS.…”

Section: Discussionmentioning

confidence: 80%

Nemesia ring necrosis virus: a new tymovirus with a genomic RNA having a histidylatable tobamovirus-like 3′ end

Koenig¹,

Barends

Gultyaev

et al. 2005

Journal of General Virology

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The complete nucleotide sequence of the genomic RNA of the new virus Nemesia ring necrosis virus (NeRNV), which is widespread in various ornamental plant species belonging to the Scrophulariaceae and Verbenaceae, has been determined. Based on its gene content, the folding properties of its 59-untranslated region and in vitro translation experiments, NeRNV RNA is a typical tymovirus RNA. Its 39 end, however, differs greatly from those of the valine-specific tymoviral RNAs that have been analysed previously. It can be folded into an upstream pseudoknot domain and a histidine-specific tRNA-like structure, a combination that, so far, has been found only in tobamoviral RNAs. The identity elements found in NeRNV RNA for recognition by yeast histidyl-tRNA synthetase are more similar to those of yeast tRNA His than the ones found in tobacco mosaic virus RNA. As a result NeRNV RNA can be charged with histidine even more efficiently than tobacco mosaic virus RNA.

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Heterogeneity in the 3′-terminal untranslated region of tobacco mild green mosaic tobamoviruses from Nicotiana glauca resulting in variants with three or six pseudoknots

Cited by 13 publications

References 23 publications

Analysis of Fitness Trade-Offs in the Host Range Expansion of an RNA Virus, Tobacco Mild Green Mosaic Virus

Analysis of Fitness Trade-Offs in the Host Range Expansion of an RNA Virus, Tobacco Mild Green Mosaic Virus

Host‐virus interaction between tobacco mild green mosaic virus strain U2 and tropical soda apple resulting in systemic hypersensitive necrosis and the host range, survival, spread, and molecular characterization of the virus

Nemesia ring necrosis virus: a new tymovirus with a genomic RNA having a histidylatable tobamovirus-like 3′ end

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