A Single Amino Acid Change in Viral Genome-Associated Protein of Potato Virus Y Correlates with Resistance Breaking in ‘Virgin A Mutant’ Tobacco

Masuta, Chikara; Nishimura, Mitsuyo; Morishita, Hiroshi; Hataya, Tatsuji

doi:10.1094/phyto.1999.89.2.118

Cited by 70 publications

(39 citation statements)

References 20 publications

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“…Similar cross-infectivity effects are also expected between tobacco (Nicotiana tabacum) and pepper resistance genes. Indeed, it was shown previously that the VPg of PVY was also the pathogenicity factor corresponding to the va gene in tobacco (40,41). Sequence comparisons indicated that the S101G and D119G substitutions in the VPg of PVY SON41p allowed the breakdown of the va 2 resistance allele in tobacco.…”

Section: Discussionmentioning

confidence: 93%

Interaction Patterns betweenPotato Virus Yand eIF4E-Mediated Recessive Resistance in the Solanaceae

Moury¹,

Janzac

Ruellan³

et al. 2014

J Virol

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The structural pattern of infectivity matrices, which contains infection data resulting from inoculations of a set of hosts by a set of parasites, is a key parameter for our understanding of biological interactions and their evolution. This pattern determines the evolution of parasite pathogenicity and host resistance, the spatiotemporal distribution of host and parasite genotypes, and the efficiency of disease control strategies. Two major patterns have been proposed for plant-virus genotype infectivity matrices. In the gene-for-gene model, infectivity matrices show a nested pattern, where the host ranges of specialist virus genotypes are subsets of the host ranges of less specialized viruses. In contrast, in the matching-allele (MA) model, each virus genotype is specialized to infect one (or a small set of) host genotype(s). The corresponding infectivity matrix shows a modular pattern where infection is frequent for plants and viruses belonging to the same module but rare for those belonging to different modules. We analyzed the structure of infectivity matrices between Potato virus Y (PVY) and plant genotypes in the family Solanaceae carrying different eukaryotic initiation factor 4E (eIF4E)-coding alleles conferring recessive resistance. Whereas this system corresponds mechanistically to an MA model, the expected modular pattern was rejected based on our experimental data. This was mostly because PVY mutations involved in adaptation to a particular plant genotype displayed frequent pleiotropic effects, conferring simultaneously an adaptation to additional plant genotypes with different eIF4E alleles. Such effects should be taken into account for the design of strategies of sustainable control of PVY through plant varietal mixtures or rotations. IMPORTANCEThe interaction pattern between host and virus genotypes has important consequences on their respective evolution and on issues regarding the application of disease control strategies. We found that the structure of the interaction between Potato virus Y (PVY) variants and host plants in the family Solanaceae departs significantly from the current model of interaction considered for these organisms because of frequent pleiotropic effects of virus mutations. These mutational effects allow the virus to expand rapidly its range of host plant genotypes, make it very difficult to predict the effects of mutations in PVY infectivity factors, and raise concerns about strategies of sustainable management of plant genetic resistance to viruses. T he interaction pattern between host and parasite genotypes has important consequences on their respective evolution and on issues regarding the application of disease control strategies. This pattern determines to a large extent the maintenance of genetic diversity in host and parasite populations (1), the structure of these populations in space and time (2, 3), and the evolution of parasite pathogenicity and host resistance (4).Different models of host-parasite interaction and coevolution have been proposed (3, 5) (F...

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Section: Discussionmentioning

confidence: 93%

Interaction Patterns betweenPotato Virus Yand eIF4E-Mediated Recessive Resistance in the Solanaceae

Moury¹,

Janzac

Ruellan³

et al. 2014

J Virol

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“…Such an alternative adaptation process has been described for the acquisition of virulence for other plant viruses such as Rice yellow mottle sobemovirus and Beet necrotic yellow vein furovirus in the presence of Rymv1-2 (in rice genotypes) and Rz1 (in beet genotypes) resistance genes, respectively (Pinel-Galzi et al 2007;Acosta-Leal et al 2010). The central part of the VPg has already been associated to a va resistance breaking phenotype for Tobacco vein mottling potyvirus (Nicolas et al 1997) and PVY (Masuta et al 1999), but amino acids substitutions observed under our experimental conditions did not correspond to those previously proposed (i.e. K/E 105 or R/E 105 ) as genetic determinants for overcoming the PVY-resistance gene va.…”

Section: Q E R F E V R R K M V E D D E I E T Q a L S H T S I Hmentioning

confidence: 98%

Effect of passage of a Potato virus Y isolate on a line of tobacco containing the recessive resistance gene va 2 on the development of isolates capable of overcoming alleles 0 and 2

Lacroix

Glais²,

Verrier³

et al. 2011

Eur J Plant Pathol

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Control strategies developed for plant viral diseases through breeding programs can be impaired by adaptive response of pathogens. A few years after the deployment in France of improved tobacco genotypes introgressed with alleles of the Potato virus Y (PVY) recessive resistance gene va, necrotic symptoms associated with PVY infection have been reported on these cultivars. Due to the lack of efficient alternative methods to control PVY, the va resistance sources have to be managed according to viral parameters, such as the dynamic of emergence of virulent variants. The effects of va alleles on the evolution of PVY was tested in experimental conditions using a PVY infectious clone and two couples of resistant tobacco near isogenic lines BVA/Bva 0 and FVA/Fva 2 both allelic for the va gene. Infection efficiencies data showed that a single passage on Fva 2 line led to the selection of virulent viral populations able to overcome both va 0 and va 2 alleles. Sequence analyses of va 2 derived PVY variants revealed that the acquisition of the capacity to overcome va 2 resistance is associated with single point mutations at two different nucleotide positions in the central part of the VPg. The described PVY adaptation process to overcome resistance mediated by different va alleles should be considered for the future development of durable and integrated strategies of management of PVY infections in tobacco crops.

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“…Plants were scored for symptoms, and viral concentrations were determined either by ELISA or by RNA gel blot analysis. Tissue prints were prepared as essentially described by Masuta et al (1999). Immature G. max seeds were cut in half and pressed onto a nitrocellulose membrane.…”

Section: Viral Inoculation and Detectionmentioning

confidence: 99%

Patterning of Virus-Infected Glycine max Seed Coat Is Associated with Suppression of Endogenous Silencing of Chalcone Synthase Genes

et al. 2004

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Most commercial Glycine max (soybean) varieties have yellow seeds because of loss of pigmentation in the seed coat. It has been suggested that inhibition of seed coat pigmentation in yellow G. max may be controlled by homology-dependent silencing of chalcone synthase (CHS) genes. Our analysis of CHS mRNA and short-interfering RNAs provide clear evidence that the inhibition of seed coat pigmentation in yellow G. max results from posttranscriptional rather than transcriptional silencing of the CHS genes. Furthermore, we show that mottling symptoms present on the seed coat of G. max plants infected with some viruses can be caused by suppression of CHS posttranscriptional gene silencing (PTGS) by a viral silencing suppressor protein. These results demonstrate that naturally occurring PTGS plays a key role in expression of a distinctive phenotype in plants and present a simple clear example of the elucidation of the molecular mechanism for viral symptom induction.

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A Single Amino Acid Change in Viral Genome-Associated Protein of Potato Virus Y Correlates with Resistance Breaking in ‘Virgin A Mutant’ Tobacco

Cited by 70 publications

References 20 publications

Interaction Patterns betweenPotato Virus Yand eIF4E-Mediated Recessive Resistance in the Solanaceae

Interaction Patterns betweenPotato Virus Yand eIF4E-Mediated Recessive Resistance in the Solanaceae

Effect of passage of a Potato virus Y isolate on a line of tobacco containing the recessive resistance gene va 2 on the development of isolates capable of overcoming alleles 0 and 2

Patterning of Virus-Infected Glycine max Seed Coat Is Associated with Suppression of Endogenous Silencing of Chalcone Synthase Genes

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