Recovery from Cucurbit leaf crumple virus (Family Geminiviridae, Genus Begomovirus) Infection Is an Adaptive Antiviral Response Associated with Changes in Viral Small RNAs

Hagen, Charles; Rojas, María R.; Kon, Tatsuya; Gilbertson, R. L.

doi:10.1094/phyto-98-9-1029

Cited by 57 publications

(39 citation statements)

References 47 publications

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“…These results are very similar to those reported for ASBVd and CLCV (Hagen et al, 2008;Markarian et al, 2004). Because BPMV siRNAs continued to accumulate even though PTGS was suppressed, SMV HC-Pro must promote synergism by suppressing PTGS at a step downstream of the production of siRNA from viral dsRNAs by Dicer-like enzymes.…”

Section: Discussionsupporting

confidence: 87%

“…The opposite phenomenon has been observed with Avocado sunblotch viroid (ASBVd) and Cucurbit leaf crumple virus (CLCV) where accumulation of siRNAs was correlated with levels of viroid or virus genomic DNAs in infected tissues (Hagen et al, 2008;Markarian et al, 2004), but the accumulation of BPMV-derived siRNAs during recovery and mixed infections with SMV has not been investigated.…”

mentioning

confidence: 98%

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Soybean mosaic virus Infection and Helper Component-protease Enhance Accumulation of Bean pod mottle virus-Specific siRNAs

Lim¹,

Jang²,

Bae³

et al. 2011

The Plant Pathology Journal

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Soybean plants infected with Bean pod mottle virus (BPMV) develop acute symptoms that usually decrease in severity over time. In other plant-virus interactions, this type of symptom recovery has been associated with degradation of viral RNAs by RNA silencing, which is accompanied by the accumulation of virus-derived small interfering RNAs (siRNAs). In this study, changes in the accumulation of BPMV siRNAs were investigated in soybean plants infected with BPMV alone, or infected with both BPMV and Soybean mosaic virus (SMV) and in transgenic soybean plants expressing SMV helper component-protease (HC-Pro). In many potyviruses, HC-Pro is a potent suppressor of RNA silencing. In plants infected with BPMV alone, accumulation of siRNAs was positively correlated with symptom severity and accumulation of BPMV genomic RNAs. Plants infected with both BPMV and SMV and BPMV-infected transgenic soybean plants expressing SMV HC-Pro exhibited severe symptoms characteristic of BPMV-SMV synergism, and showed enhanced accumulation of BPMV RNAs and siRNAs compared to plants infected with BPMV alone and nontransgenic plants. Likewise, SMV HC-Pro enhanced the accumulation of siRNAs produced from a silenced green fluorescent protein gene in transient expression assays, while the P19 silencing suppressor of Tomato bushy stunt virus did not. Consistent with the modes of action of HC-Pro in other systems, which have shown that HC-Pro suppresses RNA silencing by preventing the unwinding of duplex siRNAs and inhibiting siRNA methylation, these studies showed that SMV HC-Pro interfered with the activities of RNA-induced silencing complexes, but not the activities of Dicer-like enzymes in antiviral defenses.

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Section: Discussionsupporting

confidence: 87%

mentioning

confidence: 98%

Soybean mosaic virus Infection and Helper Component-protease Enhance Accumulation of Bean pod mottle virus-Specific siRNAs

Lim¹,

Jang²,

Bae³

et al. 2011

The Plant Pathology Journal

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“…5B). The recovery phenotype in plants infected with begomoviruses is a type of defense response and is associated with reduced levels of viral DNA (55,56). Results of DNA gel blot hybridization analyses indicated that viral DNA levels were similar and relatively high for all three genotypes at 21 dpi, when infected plants showed severe leaf curl symptoms (Fig.…”

Section: Toldev Is Associated With Tolcd In Peru Andmentioning

confidence: 95%

Characterization of a New World Monopartite Begomovirus Causing Leaf Curl Disease of Tomato in Ecuador and Peru Reveals a New Direction in Geminivirus Evolution

Melgarejo

Kon

Rojas

et al. 2013

J Virol

145

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All characterized whitefly-transmitted geminiviruses (begomoviruses) with origins in the New World (NW) have bipartite genomes composed of a DNA-A and DNA-B component. Recently, an NW begomovirus lacking a DNA-B component was associated with tomato leaf curl disease (ToLCD) in Peru, and it was named Tomato leaf deformation virus (ToLDeV). Here, we show that isolates of ToLDeV associated with ToLCD in Ecuador and Peru have a single, genetically diverse genomic DNA that is most closely related to DNA-A components of NW bipartite begomoviruses. Agroinoculation of multimeric clones of the genomic DNA of three ToLDeV genotypes (two variants and a strain) resulted in the development of tomato leaf curl symptoms indistinguishable from those of ToLCD in Ecuador and Peru. Biological properties of these ToLDeV genotypes were similar to those of Old World (OW) monopartite tomato-infecting begomoviruses, including lack of sap transmissibility, phloem limitation, a resistance phenotype in tomato germplasm with the Ty-1 gene, and functional properties of the V1 (capsid protein) and C4 genes. Differences in symptom phenotypes induced by the ToLDeV genotypes in tomato and Nicotiana benthamiana plants were associated with a highly divergent left intergenic region and C4 gene. Together, these results establish that ToLDeV is an emergent NW monopartite begomovirus that is causing ToLCD in Ecuador and Peru. This is the first report of an indigenous NW monopartite begomovirus, and evidence is presented that it emerged from the DNA-A component of a NW bipartite progenitor via convergent evolution and recombination.

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“…Moreover, both silencing routes may be used to knock down host genes with the help of geminivirus vectors (virus-induced gene silencing [VIGS]) (12,13,20,43,45,51). In this context, the analysis of the methylation status of geminivirus episomal or integrated DNA has revealed important insights (4,11,28,60,62,65).…”

mentioning

confidence: 99%

“…(iii) Transgenes which were expressed under the control of geminivirus promoters were silenced, and their cytosines methylated, if the plants were superinfected with the corresponding virus, and in complement, an increased level of C-methylation was observed for the replicated DNA (4,65). (iv) Recovery of plants was accompanied by elevated C-methylation of geminivirus DNA (28,60,62). (v) Geminivirus suppressors of silencing changed the global methylation profile of plants (11).…”

mentioning

confidence: 99%

Conformation-Selective Methylation of Geminivirus DNA

Paprotka

Deuschle

Metzler

et al. 2011

J Virol

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Geminiviruses with small circular single-stranded DNA genomes replicate in plant cell nuclei by using various double-stranded DNA (dsDNA) intermediates: distinct open circular and covalently closed circular as well as heterogeneous linear DNA. Their DNA may be methylated partially at cytosine residues, as detected previously by bisulfite sequencing and subsequent PCR. In order to determine the methylation patterns of the circular molecules, the DNAs of tomato yellow leaf curl Sardinia virus (TYLCSV) and Abutilon mosaic virus were investigated utilizing bisulfite treatment followed by rolling circle amplification. Shotgun sequencing of the products yielded a randomly distributed 50% rate of C maintenance after the bisulfite reaction for both viruses. However, controls with unmethylated single-stranded bacteriophage DNA resulted in the same level of C maintenance. Only one short DNA stretch within the C2/C3 promoter of TYLCSV showed hyperprotection of C, with the protection rate exceeding the threshold of the mean value plus 1 standard deviation. Similarly, the use of methylation-sensitive restriction enzymes suggested that geminiviruses escape silencing by methylation very efficiently, by either a rolling circle or recombination-dependent replication mode. In contrast, attempts to detect methylated bases positively by using methylcytosine-specific antibodies detected methylated DNA only in heterogeneous linear dsDNA, and methylation-dependent restriction enzymes revealed that the viral heterogeneous linear dsDNA was methylated preferentially.Methylation of DNA is commonly investigated using methylation-sensitive restriction enzymes and bisulfite sequencing, which converts unmethylated cytosines into uracil. The products are usually amplified by PCR and sequenced after bacterial cloning (14, 23). The critical steps in various protocols are the complete conversion of unmethylated cytosines to uracil (26, 78) and the design of appropriate primers for the converted DNA (reviewed in references 58 and 85). Several bioinformatic tools have been developed to analyze the results (9, 46-48, 66, 71), including recent improvements for the analysis of plant DNA cytosine methylation (27,35).Eukaryotes methylate cytosine at C 5 by methyltransferases, which differ between plants, fungi, and mammals (reviewed in reference 25). In mammals, symmetric CpG sites are usually preferred, whereas nearly every cytosine residue in plant DNA can be methylated (reviewed in reference 5). As a result, only 2 to 8% of mammalian DNA is methylated, compared to up to 50% of DNA in higher plants (reviewed in reference 84). The methylation status is highly dynamic. In plants, demethylation is mediated by DNA glycosylases and strand cleavage (84), a mechanism which would inactivate single-stranded DNA (ssDNA). In addition to C-methylation, N 6 -adenine methylation is well known for bacteria but rarely described for plants (19,74).The circular ssDNA-containing geminiviruses (reviewed in reference 37) are important plant pathogens causing severe damag...

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Recovery from Cucurbit leaf crumple virus (Family Geminiviridae, Genus Begomovirus) Infection Is an Adaptive Antiviral Response Associated with Changes in Viral Small RNAs

Cited by 57 publications

References 47 publications

Soybean mosaic virus Infection and Helper Component-protease Enhance Accumulation of Bean pod mottle virus-Specific siRNAs

Soybean mosaic virus Infection and Helper Component-protease Enhance Accumulation of Bean pod mottle virus-Specific siRNAs

Characterization of a New World Monopartite Begomovirus Causing Leaf Curl Disease of Tomato in Ecuador and Peru Reveals a New Direction in Geminivirus Evolution

Conformation-Selective Methylation of Geminivirus DNA

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