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      Role of the Genetic Background in Resistance to Plant Viruses

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          Abstract

          In view of major economic problems caused by viruses, the development of genetically resistant crops is critical for breeders but remains limited by the evolution of resistance-breaking virus mutants. During the plant breeding process, the introgression of traits from Crop Wild Relatives results in a dramatic change of the genetic background that can alter the resistance efficiency or durability. Here, we conducted a meta-analysis on 19 Quantitative Trait Locus (QTL) studies of resistance to viruses in plants. Frequent epistatic effects between resistance genes indicate that a large part of the resistance phenotype, conferred by a given QTL, depends on the genetic background. We next reviewed the different resistance mechanisms in plants to survey at which stage the genetic background could impact resistance or durability. We propose that the genetic background may impair effector-triggered dominant resistances at several stages by tinkering the NB-LRR (Nucleotide Binding-Leucine-Rich Repeats) response pathway. In contrast, effects on recessive resistances by loss-of-susceptibility—such as eIF4E-based resistances—are more likely to rely on gene redundancy among the multigene family of host susceptibility factors. Finally, we show how the genetic background is likely to shape the evolution of resistance-breaking isolates and propose how to take this into account in order to breed plants with increased resistance durability to viruses.

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          Most cited references102

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          Development of broad virus resistance in non-transgenic cucumber using CRISPR/Cas9 technology.

          Genome editing in plants has been boosted tremendously by the development of CRISPR/Cas9 (Clustered Regularly Interspaced Short Palindromic Repeats) technology. This powerful tool allows substantial improvement in plant traits in addition to those provided by classical breeding. Here, we demonstrate the development of virus resistance in cucumber (Cucumis sativus L.) using Cas9/subgenomic RNA (sgRNA) technology to disrupt the function of the recessive eIF4E (eukaryotic translation initiation factor 4E) gene. Cas9/sgRNA constructs were targeted to the N' and C' termini of the eIF4E gene. Small deletions and single nucleotide polymorphisms (SNPs) were observed in the eIF4E gene targeted sites of transformed T1 generation cucumber plants, but not in putative off-target sites. Non-transgenic heterozygous eif4e mutant plants were selected for the production of non-transgenic homozygous T3 generation plants. Homozygous T3 progeny following Cas9/sgRNA that had been targeted to both eif4e sites exhibited immunity to Cucumber vein yellowing virus (Ipomovirus) infection and resistance to the potyviruses Zucchini yellow mosaic virus and Papaya ring spot mosaic virus-W. In contrast, heterozygous mutant and non-mutant plants were highly susceptible to these viruses. For the first time, virus resistance has been developed in cucumber, non-transgenically, not visibly affecting plant development and without long-term backcrossing, via a new technology that can be expected to be applicable to a wide range of crop plants.
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            Navigating complexity to breed disease-resistant crops

            Plant diseases are responsible for substantial crop losses each year and pose a threat to global food security and agricultural sustainability. Improving crop resistance to pathogens through breeding is an environmentally sound method for managing disease and minimizing these losses. However, it is challenging to breed varieties with resistance that is effective, stable and broad-spectrum. Recent advances in genetic and genomic technologies have contributed to a better understanding of the complexity of host-pathogen interactions and have identified some of the genes and mechanisms that underlie resistance. This new knowledge is benefiting crop improvement through better-informed breeding strategies that utilize diverse forms of resistance at different scales, from the genome of a single plant to the plant varieties deployed across a region.
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              Novel alleles of rice eIF4G generated by CRISPR/Cas9‐targeted mutagenesis confer resistance to Rice tungro spherical virus

              Summary Rice tungro disease (RTD) is a serious constraint in rice production across tropical Asia. RTD is caused by the interaction between Rice tungro spherical virus (RTSV) and Rice tungro bacilliform virus. RTSV resistance found in traditional cultivars has contributed to a reduction in the incidence of RTD in the field. Natural RTSV resistance is a recessive trait controlled by the translation initiation factor 4 gamma gene (eIF4G). The Y1059V1060V1061 residues of eIF4G are known to be associated with the reactions to RTSV. To develop new sources of resistance to RTD, mutations in eIF4G were generated using the CRISPR/Cas9 system in the RTSV‐susceptible variety IR64, widely grown across tropical Asia. The mutation rates ranged from 36.0% to 86.6%, depending on the target site, and the mutations were successfully transmitted to the next generations. Among various mutated eIF4G alleles examined, only those resulting in in‐frame mutations in SVLFPNLAGKS residues (mainly NL), adjacent to the YVV residues, conferred resistance. Furthermore, our data suggest that eIF4G is essential for normal development, as alleles resulting in truncated eIF4G could not be maintained in homozygous state. The final products with RTSV resistance and enhanced yield under glasshouse conditions were found to no longer contain the Cas9 sequence. Hence, the RTSV‐resistant plants with the novel eIF4G alleles represent a valuable material to develop more diverse RTSV‐resistant varieties.
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                Author and article information

                Journal
                Int J Mol Sci
                Int J Mol Sci
                ijms
                International Journal of Molecular Sciences
                MDPI
                1422-0067
                20 September 2018
                October 2018
                : 19
                : 10
                : 2856
                Affiliations
                [1 ]INRA-UR 1052, Génétique et Amélioration des Fruits et Légumes (GAFL), Domaine St Maurice, CS 60094, F-84143 Montfavet CEDEX, France; jean-luc.gallois@ 123456inra.fr
                [2 ]INRA, Unité Pathologie Végétale, 67 Allée des Chênes, Domaine Saint Maurice, CS 60094, F-84143 Montfavet CEDEX, France; benoit.moury@ 123456inra.fr
                [3 ]UMR 1332, Biologie du Fruit et Pathologie, INRA, Univ. Bordeaux, 71 Av. E. Bourlaux, CS 20032, 33882 Villenave d’Ornon CEDEX, France
                Author notes
                [* ]Correspondence: sylvie.german-retana@ 123456inra.fr ; Tel.: +33-5-571-22383
                Author information
                https://orcid.org/0000-0003-0451-1740
                Article
                ijms-19-02856
                10.3390/ijms19102856
                6213453
                30241370
                007bfdc2-71bf-4e29-83e1-cba7ff40eeab
                © 2018 by the authors.

                Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

                History
                : 24 July 2018
                : 11 September 2018
                Categories
                Review

                Molecular biology
                plant,virus,resistance,durability,genetic background,quantitative trait loci,epistasis
                Molecular biology
                plant, virus, resistance, durability, genetic background, quantitative trait loci, epistasis

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