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We performed a genome‐wide association study of pepper (Capsicum annuum) tolerance to potato virus Y (PVY). For 254 pepper accessions, we estimated the tolerance to PVY as the coefficient of regression of the fresh weight (or height) of PVY‐infected and mock‐inoculated plants against within‐plant virus load. Small (strongly negative) coefficients of regression indicate low tolerance because plant biomass or growth decreases sharply as virus load increases. The tolerance level varied largely, with some pepper accessions showing no symptoms or fairly mild mosaics, whereas about half (48%) of the accessions showed necrotic symptoms. We found two adjacent single‐nucleotide polymorphisms (SNPs) at one extremity of chromosome 9 that were significantly associated with tolerance to PVY. Similarly, in three biparental pepper progenies, we showed that the induction of necrosis on PVY systemic infection segregated as a monogenic trait determined by a locus on chromosome 9. Our results also demonstrate the existence of a negative correlation between resistance and tolerance among the cultivated pepper accessions at both the phenotypic and genetic levels. By comparing the distributions of the tolerance‐associated SNP alleles and previously identified PVY resistance‐associated SNP alleles, we showed that cultivated pepper accessions possess favourable alleles for both resistance and tolerance less frequently than expected under random associations, while the minority of wild pepper accessions frequently combined resistance and tolerance alleles. This divergent evolution of PVY resistance and tolerance could be related to pepper domestication or farmer's selection. Among a core‐collection of pepper accessions, phenotypic and genetic negative correlations were found between resistance and tolerance to PVY for the cultivated pepper accessions, but not for the wild pepper accessions.

Root knot nematodes are obligate phytoparasites that invade the roots of important crop plants causing severe economic losses. Arbuscular Mycorrhizal Fungi (AMF) are soil borne microorganisms that establish mutualistic associations with the roots of most plants. AMF have been frequently indicated to help their host to attenuate the damage caused by pathogens and predators. In this study, the effects of a commercial inoculum of AMF against Meloidogyne incognita on tomato and pepper were evaluated under controlled conditions. Mycorrhizal association decreased M. incognita development in pepper, and improved tolerance to nematode infection in tomato plants. Rapid plant mycorrhization is critical for delivering protective effects against biotic stress. A novel mycorrhization technique using AMF from the highly mycotrophic plant sorghum was applied to tomato. More rapid mycorrhization was achieved in tomato plants grown in soil containing mycorrhized roots of sorghum than in plants directly inoculated with the commercial AMF. Keywords. Crop pests, symbiosis, agricultural management.

KEY MESSAGE : The plant genetic background influences the efficiency of major resistance genes to root-knot nematodes in pepper and has to be considered in breeding strategies. Root-knot nematodes (RKNs), Meloidogyne spp., are extremely polyphagous plant parasites worldwide. Since the use of most chemical nematicides is being prohibited, genetic resistance is an efficient alternative way to protect crops against these pests. However, nematode populations proved able to breakdown plant resistance, and genetic resources in terms of resistance genes (R-genes) are limited. Sustainable management of these valuable resources is thus a key point of R-gene durability. In pepper, Me1 and Me3 are two dominant major R-genes, currently used in breeding programs to control M. arenaria, M. incognita and M. javanica, the three main RKN species. These two genes differ in the hypersensitive response induced by nematode infection. In this study, they were introgressed in either a susceptible or a partially resistant genetic background, in either homozygous or heterozygous allelic status. Challenging these genotypes with an avirulent M. incognita isolate demonstrated that (1) the efficiency of the R-genes in reducing the reproductive potential of RKNs is strongly affected by the plant genetic background, (2) the allelic status of the R-genes has no effect on nematode reproduction. These results highlight the primary importance of the choice of both the R-gene and the genetic background into which it is introgressed during the selection of new elite cultivars by plant breeders.

Description du sujet. Une approche système basée sur la co-conception et l’évaluation expérimentale in situ de prototypes de systèmes de culture (SDC) a été mise en œuvre dans le projet INRA « GeDuNem » pour une gestion durable des nématodes à galles (NG) dans les systèmes maraîchers sous abris. Objectifs. Il s’agissait (i) d’évaluer pendant quatre ans diverses stratégies de culture combinant résistances génétiques et pratiques culturales (rotations culturales incluant des plantes sensibles, résistantes et non-hôtes, gestion de l’interculture avec couvert végétal nématicide ou solarisation) pour réduire les populations de NG dans le sol et augmenter la durabilité des résistances variétales à ces bioagresseurs, (ii) d’étudier leur impact sur les communautés de nématodes rencontrées et (iii) d’évaluer l’acceptabilité des nouveaux SDC par les agriculteurs. Méthode. Trois prototypes de SDC, co-conçus entre acteurs de la recherche et ceux du développement, ont été comparés à des SDC appliqués classiquement en région méditerranéenne et évalués grâce à des dispositifs complémentaires : (i) expérimentations-système sur trois sites de producteurs du Sud de la France ; (ii) expérimentations analytiques pour approfondir les mécanismes d’action des leviers mobilisés ; (iii) enquêtes pour évaluer l’acceptabilité des prototypes par les agriculteurs. Résultats. Les trois SDC se sont révélés efficaces (90 % de réduction des NG, protection des Solanaceae à résistance partielle, pas d’effet négatif sur les nématodes non phytoparasites) et durables lorsque les conditions d’application et les équilibres biologiques du sol étaient favorables (nématofaune totale diversifiée et abondante). Leur degré d’acceptabilité dépendait du type d’exploitation et de la sensibilité des agriculteurs face à l’innovation. Conclusions. Ces nouveaux SDC doivent encore être améliorés, en interaction avec les producteurs, tant en termes d’efficacité, par l’introduction de nouveaux leviers agroécologiques, que de cout. Les recherches futures devront aussi s’ouvrir à la gestion plus globale de la santé des sols. Design and assessment of innovative Mediterranean vegetable cropping systems to manage root-knot nematodes Description of the subject. A system approach based on co-design and experimental field evaluation of cropping systems (CSs), combining technical and varietal innovations, has been implemented for sustainable management of root-knot nematodes (RKN) in Mediterranean sheltered vegetable systems. Objectives. Cropping systems combining genetic resistance and cultural practices (crop rotations including susceptible, resistant, and non-host plants; intercropping management with nematicidal cover crops or soil solarization) were assessed over a period of 4 years (i) to reduce RKN populations and increase the durability of varietal resistances, (ii) to study the impact of these systems on soil ecology (plant-parasitic and free-living nematode communities), and (iii) to evaluate their acceptability by farmers. Method. Three CS prototypes, resulting from a co-design process with research and development stakeholders, were compared with CSs conventionally implemented in the Mediterranean region. The three prototypes were also evaluated using complementary methods: (i) system experiments in three commercial farms in Southern France; (ii) analytical experiments to decipher the mechanisms of action for some [agroecological??] levers; (iii) surveys to evaluate the acceptability of the prototypes by farmers. Results. All three CSs were found to be effective (90% RKN decrease, protection of partially resistant Solanaceae, no negative effect on non-phytoparasitic nematodes) and sustainable, when application conditions and soil biological equilibrium were favorable (global soil nematofauna diversified and abundant). The acceptability of the three systems depended on the type of farm where they were implemented and the attitude of the farmers towards innovation. Conclusions. These three CSs still need to be improved, in terms of their efficiency, in consultation with participating farmers, by introducing new agroecological levers, as well as innovation costs. Future research will also need to open up to a more comprehensive management of soil health.

In the pepper Capsicum annuum CM334, which is used by breeders as a source of resistance to Phytophthora spp. and potyviruses, a resistance gene entirely suppresses reproduction of the root-knot nematode (Meloidogyne spp.). The current study compared the histological responses of this resistant line and a susceptible cultivar to infection with the three most damaging root-knot nematodes: M. arenaria, M. incognita, or M. javanica. Resistance of CM334 to root-knot nematodes was associated with unidentified factors that limited nematode penetration and with post-penetration biochemical responses, including the hypersensitive response, which apparently blocked nematode migration and thereby prevented juvenile development and reproduction. High-performance liquid chromatography analysis suggested that phenolic compounds, especially chlorogenic acid, may be involved in CM334 resistance. The response to infection in the resistant line varied with root-knot nematode species and was correlated with nematode behavior and pathogenicity in the susceptible cultivar: nematode species that quickly reached the vascular cylinder and initiated feeding sites in the susceptible cultivar were quickly recognized in CM334 and stopped in the epidermis or cortex. After comparing our data with those from other resistant pepper lines, we suggest that timing of the resistance response and the mechanism of resistance vary with plant genotype, resistance gene, and root-knot nematode species.

The root-knot nematode (Meloidogyne spp.) is a major plant pathogen, affecting several solanaceous crops worldwide. In Capsicum annuum, resistance to this pathogen is controlled by several independent dominant genes--the Me genes. Six Me genes have previously been shown to be stable at high temperature in three highly resistant and genetically distant accessions: PI 322719, PI 201234, and CM334 (Criollo de Morelos 334). Some genes (Me4, Mech1, and Mech2) are specific to certain Meloidogyne species or populations, whereas others (Me1, Me3, and Me7) are effective against a wide range of Meloidogyne species, including M. arenaria, M. javanica, and M. incognita, the most common species in Mediterranean and tropical areas. These genes direct different response patterns in root cells depending on the pepper line and nematode species. Allelism tests and fine mapping using the BSA-AFLP approach showed these genes to be different but linked, with a recombination frequency of 0.02-0.18. Three of the PCR-based markers identified in several genetic backgrounds were common to the six Me genes. Comparative mapping with CarthaGene software indicated that these six genes clustered in a single genomic region within a 28 cM interval. Four markers were used to anchor this cluster on the P9 chromosome on an intraspecific reference map for peppers. Other disease resistance factors have earlier been mapped in the vicinity of this cluster. This genomic area is colinear to chromosome T12 of tomato and chromosome XII of potato. Four other nematode resistance genes have earlier been identified in this area, suggesting that these nematode resistance genes are located in orthologous genomic regions in Solanaceae.

Root-knot nematodes (RKNs, Meloidogyne spp.) are major plant pathogens of vegetables in most production areas, including the Solanaceous crops tomato and pepper. Due to the banning of chemical nematicides, current control strategies are mainly based on the deployment of resistance genes (R-genes), i.e., Mi(s) in tomato, Me(s) in pepper. These genes are effective against a wide range of RKN species, including M. arenaria, M. incognita and M. javanica, the most common species in temperate and tropical areas. However, the recent emergence of virulent populations able to overcome the resistance conferred by some of these R-genes may constitute a severe limitation to their use in the field. Research has been conducted to evaluate the durability of the Mi(s) and Me(s) R-genes, by comparing the reproduction of several laboratory-selected and wild virulent M. incognita isolates on both susceptible and resistant tomatoes and peppers. We first showed that the Me1 R-gene in pepper behaves as a robust R-gene controlling avirulent and virulent Me3 or Mi-1 isolates. We also confirm that virulence is highly specific to a determined R-gene on which selection has occurred, thus allowing the alternance of R-genes in the rotation as an effective mean to improve soil health. Another significant experimental result is the observation that a reproductive fitness cost is associated to nematode virulence. The adaptative significance of trade-offs between selected characters and fitness-related traits suggests that, although the resistance can be broken, it might prove durable in some conditions if the virulent nematodes are counterselected in susceptible plants, which has important consequences for the management of plant resistance in the field.

The emergence of virulent root-knot nematode populations, able to overcome the resistance conferred by some of the resistance genes (R-genes) in Solanaceous crops, i.e., Mi (s) in tomato, Me (s) in pepper, may constitute a severe limitation to their use in the field. Research has been conducted to evaluate the durability of these R-genes, by comparing the reproduction of several laboratory-selected and wild virulent Meloidogyne incognita isolates, on both susceptible and resistant tomatoes and peppers. We first show that the Me1 R-gene in pepper behaves as a robust R-gene controlling avirulent and virulent Me3, Me7 or Mi-1 isolates. Although the reproductive potential of the virulent isolates was highly variable on susceptible and resistant plants, we also confirm that virulence is highly specific to a determined R-gene on which selection has occurred. Another significant experimental result is the observation that a reproductive fitness cost is associated with nematode virulence against Mi-1 in tomato and Me3 and Me7 in pepper. The adaptative significance of trade-offs between selected characters and fitness-related traits, suggests that, although the resistance can be broken, it may be preserved in some conditions if the virulent nematodes are counter-selected in susceptible plants. All these results have important consequences for the management of plant resistance in the field.

The PM687 line of Capsicum annuum L. has a single dominant gene, Me-3, that confers heat-stable resistance to root-knot nematodes (RKN). Me-3 was mapped using doubled-haploid (DH) lines and F-2 progeny from a cross between the susceptible cultivar 'Yolo Wonder' ('YW') and the highly resistant line 'PM687'. Bulked-segregant analysis with DNA pools, from susceptible or resistant DH lines, was performed to identify RAPD and AFLP markers linked to Me-3. There was no polymorphism between bulks of ten DH lines using over 800 RADP primers (4,000 amplified fragments analysed). Using 512 AFLP primers (74,000 amplified fragments analysed), and bulked DNA templates from 20 resistant and 20 susceptible plants, we identified eight repulsion-phase and four coupling-phase markers linked to Me-3. Analysed in 103 DH progeny, they defined a 56.1-cM interval containing the target gene. The nearest were located 0.5, 1.0, 1.5 and 3.0 centimorgans (cM) on both sides of the gene. Analysis of the F-2 progeny (162 plants) with the nearest coupling-phase marker confirmed its close position. Another resistance gene to RKN, present in 'PM687' (Me-4), was shown to be linked to Me-3, 10 cM from it. In order to localize Me-3 and Me-4 on our reference intraspecific pepper linkage map, two AFLP markers were mapped. The Me-3 nearest marker was 10,1 cM from a RAPD marker named Q04_0.3 and 2.7 cM from a RFLP marker named CT135. We investigated map-position orthologies between Me-3 and two other nematode resistance genes, the tomato Mi-3 and the potato Gpa(2) genes, which mapped in the telomeric region of the short arm of the tomato and potato chromosome 12 (or XII for potato).

With the banning of most chemical nematicides, the control of root-knot nematodes (RKNs) in vegetable crops is now based essentially on the deployment of single, major resistance genes (R-genes). However, these genes are rare and their efficacy is threatened by the capacity of RKNs to adapt. In pepper, several dominant R-genes are effective against RKNs, and their efficacy and durability have been shown to be greater in a partially resistant genetic background. However, the genetic determinants of this partial resistance were unknown. Here, a quantitative trait loci (QTL) analysis was performed on the F2:3 population from the cross between Yolo Wonder, an accession considered partially resistant or resistant, depending on the RKN species, and Doux Long des Landes, a susceptible cultivar. A genetic linkage map was constructed from 130 F2 individuals, and the 130 F3 families were tested for resistance to the three main RKN species, Meloidogyne incognita, M. arenaria, and M. javanica. For the first time in the pepper-RKN pathosystem, four major QTLs were identified and mapped to two clusters. The cluster on chromosome P1 includes three tightly linked QTLs with specific effects against individual RKN species. The fourth QTL, providing specific resistance to M. javanica, mapped to pepper chromosome P9, which is known to carry multiple NBS-LRR repeats, together with major R-genes for resistance to nematodes and other pathogens. The newly discovered cluster on chromosome P1 has a broad spectrum of action with major additive effects on resistance. These data highlight the role of host QTLs involved in plant-RKN interactions and provide innovative potential for the breeding of new pepper cultivars or rootstocks combining quantitative resistance and major R-genes, to increase both the efficacy and durability of RKN control by resistance genes.