Evolution of plant eukaryotic initiation factor 4E (eIF4E) and potyvirus genome-linked protein (VPg): A game of mirrors impacting resistance spectrum and durability

Moury, Benoît; Charron, Carine; Janzac, Bérenger; Simon, Vincent; Gallois, Jean‐Luc; Palloix, Alain; Caranta, Carole

doi:10.1016/j.meegid.2013.11.024

Cited by 55 publications

(62 citation statements)

References 65 publications

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“…The C. annuum plants with genotype pvr2 3 or pvr2 4 showed the same behaviors toward all PVY variants. This is in accordance with the fact that they possess very similar eIF4E sequences, differing by a single amino acid substitution (7,12), and suggests that they are redundant in terms of interaction specificity with PVY. In total, the PVY variants were able to infect plants belonging to 1 to 5 plant genotypes (3.25 on average) carrying resistance genes or alleles (i.e., excluding the reference susceptibility plant genotypes), of a total of 10, if we consider only cases where 100% of plants were infected.…”

Section: Infectivity Of Pvy Variants Insupporting

confidence: 85%

“…The pepper accessions had different alleles at the pvr2 locus encoding eIF4E: Yolo Wonder was the susceptible reference carrying the pvr2 ϩ allele, whereas Yolo Y, Florida VR2, HD285, PI322719, SC81, Maroc1, Serrano Vera Cruz, PI195301, and Chile de Arbol carried alleles pvr2 1 to pvr2 9 , respectively (7). These 10 alleles correspond to highly similar copies of an eIF4E which differ by a small number of amino acid substitutions (7,12). The S. habrochaites accessions carried different alleles at the pot-1 locus orthologous to the pepper pvr2 locus: PI247087 carried the pot-1 recessive resistance allele, whereas PI134417 was the susceptible reference (pot-1 ϩ ) (13).…”

Section: Methodsmentioning

confidence: 99%

“…The nucleotide sequences of the VPg-coding regions of PVY populations that infected plants carrying resistance genes or of susceptible control plants were determined as described previously (12,14) from a total of four (when available) infected plants per virus-plant genotype combination.…”

Section: Methodsmentioning

confidence: 99%

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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: Infectivity Of Pvy Variants Insupporting

confidence: 85%

Section: Methodsmentioning

confidence: 99%

See 1 more Smart Citation

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

Moury¹,

Janzac

Ruellan³

et al. 2014

J Virol

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“…Plants and many of their RNA viruses have co-evolved and a significant portion of this evolution appears to center on the use of eIF4F and eIFiso4F subunits by viruses for replication. Interestingly, neither Arabidopsis eIF4E1b nor eIF4E1c are recognized as virus resistance genes in contrast to dozens of examples for eIF4E and eIFiso4E (Robaglia and Caranta, 2006;Charron et al, 2008;Moury et al, 2013). Likely, other plants have multiple eIF4E/eIFiso4E genes, some of which may have evolutionary advantages for specific functions during stress or development.…”

Section: The Cast Of Cap-binding Proteins: Eif4e Eifiso4e and 4ehpmentioning

confidence: 99%

“…This suggests that it is not the protein synthesis activity per se that confers virus resistance, but some other aspect that has yet to be discovered. There is interest in using these genes to engineer better virus resistance for economically important crops (Wang and Krishnaswamy, 2012;Moury et al, 2013;Kim et al, 2014a) and it is likely that virus/ host co-evolution has shaped the roles of these initiation factors in plants (Moury et al, 2013).…”

Section: The Cast Of Cap-binding Proteins: Eif4e Eifiso4e and 4ehpmentioning

confidence: 99%

Mechanism of Cytoplasmic mRNA Translation

Browning

Bailey‐Serres

2015

The Arabidopsis Book

187

220

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Protein synthesis is a fundamental process in gene expression that depends upon the abundance and accessibility of the mRNA transcript as well as the activity of many protein and RNA-protein complexes. Here we focus on the intricate mechanics of mRNA translation in the cytoplasm of higher plants. This chapter includes an inventory of the plant translational apparatus and a detailed review of the translational processes of initiation, elongation, and termination. The majority of mechanistic studies of cytoplasmic translation have been carried out in yeast and mammalian systems. The factors and mechanisms of translation are for the most part conserved across eukaryotes; however, some distinctions are known to exist in plants. A comprehensive understanding of the complex translational apparatus and its regulation in plants is warranted, as the modulation of protein production is critical to development, environmental plasticity and biomass yield in diverse ecosystems and agricultural settings.

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