Historical Contingencies Modulate the Adaptability of Rice Yellow Mottle Virus

Poulicard, Nils; Pinel‐Galzi, Agnès; Traoré, Oumar; Vignols, Florence; Ghesquière, Alain; Konaté, G.; Hébrard, Eugénie; Fargette, Denis

doi:10.1371/journal.ppat.1002482

Cited by 45 publications

(51 citation statements)

References 34 publications

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“…Emergence of new pathogen strains through genetic mutation and recombination may result to virulent strains which are capable for overcoming the resistance of commercial rice varieties used in crop production world-wide. The resistance breaking of cultivars carrying rymv1 resistant allele has been studied and genetic determinants established [40]. Multiple resistance-breaking was evident on resistant cultivars Gigante, Tog12387, Tog5438 and Tog5681 overcome by all strains except S4lv (Tz516), S4ug (Tz508) and S6c (Tz486) on cultivar Tog5681.…”

Section: Discussionmentioning

confidence: 99%

Pathogenic Variation and Occurrence of Multiple Resistance-Breaking <i>Rice yellow mottle virus</i> Strains in Tanzania

Hubert¹,

Lyimo²,

Luzi-Kihupi³

2017

AJPS

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Rice yellow mottle virus (RYMV) is a major biotic constraint for rice production in Africa. The resistance-breaking ability of Tanzanian RYMV strains and phylotypes (S4lm (Tz526), S4lv (Tz516), S4ug (Tz508), S5 (Tz429, Tz445), S6c (Tz486) and S6w (Tz539)) were tested by inoculating rice cultivars with RYMV1 resistant alleles (Gigante (rymv1-2), Tog12387 (rymv1-3), Tog5681 (rymv1-3), Tog5438 (rymv1-4), Tog5672 (rymv1-4+rymv2) and Tog5674 (rymv 1-5)) in a screen house. The results revealed multiple resistance-breaking strains and phylotypes on resistant cultivars Gigante, Tog12387, Tog5438 and Tog5681. However, the resistance breakdown was highly variable depending on the strain used, and disease severity ranged from 11% -75.3%. The virulence potential of RYMV phylotype S4lm (Tz526) was similar to phylotype S6w (Tz539). The impact of strains and phylotypes on yield and its components in rice cultivars revealed highly significant differences (P ≤ 0.001). The lowest percent plant height reduction (2.8%), number of tillers per plant (2.5%), 1000 grain weight (2.7%), spikelet sterility (3.5%) and yield (5%) was recorded in rice cultivar Gigante inoculated with RYMV phylotype S6c (Tz486). Phylotype S6c (Tz486) despite being less virulent compared to other strains, its virus titer in rice cultivar Gigante (1.833) was higher than S5 (Tz429, Tz445) inoculated on Tog5674 (0.171, 0.207) and S6w (Tz539) inoculated on Tog5681 (0.283). The resistant-breaking strain S5 (Tz445) multiplied in resistant rice cultivar Tog5674 without inducing visible symptoms but showed positive reaction to ELISA with low virus titer. The strain S5 overcame wide range of resistant alleles including rymv1-2, rymv1-3, rymv1-4 and rymv1-5 resistance, with exception of rymv1-4 + rymv2. The current results gave a new perspective for future identification of resistance-breaking mutations through sequencing of the RYMV genome in infected rice cultivars and mutagenesis of an infectious viral clone useful for future RYMV resistant breeding programs.How to cite this paper: Hubert, J., Lyimo, H

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Section: Discussionmentioning

confidence: 99%

Pathogenic Variation and Occurrence of Multiple Resistance-Breaking <i>Rice yellow mottle virus</i> Strains in Tanzania

Hubert¹,

Lyimo²,

Luzi-Kihupi³

2017

AJPS

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“…Indeed, in these pathosystems, infectivity depends on a direct physical interaction between a host factor (eIF4E or eIF4G) and a virus factor (most frequently, the genome-linked viral protein, or VPg) (7,8). The most exhaustive study is that of the interaction between rice recessive resistance alleles at the rymv1 locus (mainly alleles rymv1-2 and rymv1-3) and Rice yellow mottle virus (RYMV; genus Sobemovirus) (9)(10)(11). As in the MA model, cross-infectivity was rare since among the RYMV isolates that could adapt to plants carrying the resistance alleles, 89% (34/38) were able to infect only genotypes with rymv1-2 or only genotypes with rymv1-3 (11).…”

Section: Figmentioning

confidence: 99%

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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“…The relevance of resistance-breaking costs in plant-virus coevolution and as modulators of the durability of crop resistance has led to efforts for their detection and quantification. Analyses of virus multiplication in susceptible hosts have provided evidence for resistancebreaking costs in various plant-virus systems (15)(16)(17)(18)(19)(20)(21).…”

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Mutations That Determine Resistance Breaking in a Plant RNA Virus Have Pleiotropic Effects on Its Fitness That Depend on the Host Environment and on the Type, Single or Mixed, of Infection

Moreno‐Pérez

García-Luque

Fraile

et al. 2016

J Virol

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Overcoming host resistance in gene-for-gene host-virus interactions is an important instance of host range expansion, which can be hindered by across-host fitness trade-offs. Trade-offs are generated by negative effects of host range mutations on the virus fitness in the original host, i.e., by antagonistic pleiotropy. It has been reported that different mutations in Pepper mild mottle virus (PMMoV) coat protein result in overcoming L-gene resistance in pepper. To analyze if resistance-breaking mutations in PMMoV result in antagonistic pleiotropy, all reported mutations determining the overcoming of L 3 and L 4 alleles were introduced in biologically active cDNA clones. Then, the parental and mutant virus genotypes were assayed in susceptible pepper genotypes with an L ؉ , L 1 , or L 2 allele, in single and in mixed infections. Resistance-breaking mutations had pleiotropic effects on the virus fitness that, according to the specific mutation, the host genotype, and the type of infection, single or mixed with other virus genotypes, were antagonistic or positive. Thus, resistance-breaking mutations can generate fitness trade-offs both across hosts and across types of infection, and the frequency of host range mutants will depend on the genetic structure of the host population and on the frequency of mixed infections by different virus genotypes. Also, resistance-breaking mutations variously affected virulence, which may further influence the evolution of host range expansion. Changes in virus host range affect virus ecology and epidemiology, condition virus emergence, and can compromise the success of strategies for the control of viral diseases (1-4). The acquisition of new hosts, that is, host range expansion, would provide a virus with more opportunities for transmission and survival. However, differential host-associated selection may result in across-host fitness trade-offs so that increasing the virus fitness in a new host will decrease its fitness in the original one, which will hinder host range expansion (4-6). The simplest mechanism generating across-hosts fitness trade-offs is antagonistic pleiotropy, in which mutations that increase fitness in one host are deleterious in another one (7). Evidence indicates that antagonistic pleiotropy is common in RNA viruses as a result of their small genomes, which are compacted with genetic information and encode few, multifunctional proteins (5,8).Host range evolution is particularly relevant for the sustainable use of genetic resistance to control viral diseases of crops. Disease control based on resistant cultivars is target specific and highly efficient but is not durable due to the appearance of new virus genotypes able to infect otherwise resistant host genotypes. The increase in frequency of resistance-breaking virus genotypes eventually renders resistance inefficient (9-11). Plant-virus interactions can often be explained by the gene-for-gene (GFG) model, under which direct or indirect recognition of viral proteins by those encoded by plant resistan...

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Historical Contingencies Modulate the Adaptability of Rice Yellow Mottle Virus

Cited by 45 publications

References 34 publications

Pathogenic Variation and Occurrence of Multiple Resistance-Breaking <i>Rice yellow mottle virus</i> Strains in Tanzania

Pathogenic Variation and Occurrence of Multiple Resistance-Breaking <i>Rice yellow mottle virus</i> Strains in Tanzania

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

Mutations That Determine Resistance Breaking in a Plant RNA Virus Have Pleiotropic Effects on Its Fitness That Depend on the Host Environment and on the Type, Single or Mixed, of Infection

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Historical Contingencies Modulate the Adaptability of Rice Yellow Mottle Virus

Cited by 45 publications

References 34 publications

Pathogenic Variation and Occurrence of Multiple Resistance-Breaking &lt;i&gt;Rice yellow mottle virus&lt;/i&gt; Strains in Tanzania

Pathogenic Variation and Occurrence of Multiple Resistance-Breaking &lt;i&gt;Rice yellow mottle virus&lt;/i&gt; Strains in Tanzania

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

Mutations That Determine Resistance Breaking in a Plant RNA Virus Have Pleiotropic Effects on Its Fitness That Depend on the Host Environment and on the Type, Single or Mixed, of Infection

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Pathogenic Variation and Occurrence of Multiple Resistance-Breaking <i>Rice yellow mottle virus</i> Strains in Tanzania

Pathogenic Variation and Occurrence of Multiple Resistance-Breaking <i>Rice yellow mottle virus</i> Strains in Tanzania