The quasi-universality of nestedness in the structure of quantitative plant-parasite interactions

Understanding the relationships between host range and pathogenicity for parasites, and between the efficiency and scope of immunity for hosts are essential to implement efficient disease control strategies. In the case of plant parasites, most studies have focused on describing qualitative interactions and a variety of genetic and evolutionary models has been proposed in this context. Although plant quantitative resistance benefits from advantages in terms of durability, we presently lack models that account for quantitative interactions between plants and their parasites and the evolution of these interactions. Nestedness and modularity are important features to unravel the overall structure of host-parasite interaction matrices. Here, we analysed these two features on 32 matrices of quantitative pathogenicity trait data gathered from 15 plant-parasite pathosystems consisting of either annual or perennial plants along with fungi or oomycetes, bacteria, nematodes, insects and viruses. The performance of several nestedness and modularity algorithms was evaluated through a simulation approach, which helped interpretation of the results. We observed significant modularity in only six of the 32 matrices, with two or three modules detected. For three of these matrices, modules could be related to resistance quantitative trait loci present in the host. In contrast, we found high and significant nestedness in 30 of the 32 matrices. Nestedness was linked to other properties of plant-parasite interactions. First, pathogenicity trait values were explained in majority by a parasite strain effect and a plant accession effect, with no parasite-plant interaction term. Second, correlations between the efficiency and scope of the resistance of plant genotypes, and between the host range breadth and pathogenicity level of parasite strains were overall positive. This latter result questions the efficiency of strategies based on the deployment of several genetically-differentiated cultivars of a given crop species in the case of quantitative plant immunity

Adaptation of phytopathogenic fungi to genetically heterogeneous host populations – case study of the durum wheat – Zymoseptoria tritici pathosystem

Les variétés traditionnelles sont génétiquement hétérogènes et constituent une source de diversité contribuant à la productivité et à la stabilité des agroécosystèmes. En effet, la diversité végétale fournit des services écosystémiques, dont la réduction globale des pressions parasitaires. Pour une meilleure gestion des maladies, la compréhension des mécanismes d’interaction plante-pathogène est primordiale. Dans cette optique, j’ai étudié l’adaptation entre variétés traditionnelles tunisiennes de blé dur et populations fongiques de Zymoseptoria tritici responsable de la septoriose. Dans un premier temps, le génotypage de 14 variétés traditionnelles dites «populations», à l'aide de 9 microsatellites, a montré que la diversité génétique était aussi importante au sein des populations (45%) qu'entre les populations (54%). Cette diversité est structurée en sept groupes génétiques qui s'expliquent en partie par la combinaison « nom de variété » x « localité ». La caractérisation de 15 traits phénotypiques, dont la résistance à la septoriose, a révélé que ces populations étaient également diversifiées phénotypiquement. La résistance à la septoriose est de nature qualitative (résistance majeure) dans deux populations mais plus généralement de nature quantitative dans les autres populations. Une comparaison Pst-Fst a démontré une adaptation locale des variétés traditionnelles, soulignant des trajectoires de sélection intimement liées au territoire et pratiques des agriculteurs les cultivant. Parallèlement, un génotypage SNP à haute densité (puce TaBW35K) d’un panel de 127 individus provenant de quatre populations portant le même nom de variété ‘Mahmoudi’ a mis en évidence deux groupes génétiques partagés par les quatre populations. Ce panel d’individus a été phénotypé au champ et en conditions contrôlées pour sa résistance à une souche tunisienne de Z. tritici, ce qui a permis de conduire une analyse GWAS. Cette analyse a mis en évidence 6 loci associés à la résistance contre la septoriose sur les chromosomes 1B, 4A, 5B et 7A, dont un locus sur le chromosome 1B associé à une résistance majeure de type qualitative. La fréquence des allèles favorables à la résistance oscille entre 6 et 46% dans le panel et est variable d’une population à une autre. Côté agent pathogène, quatre populations de Z. tritici collectées sur le cultivar moderne majoritaire en Tunisie ‘Karim’ et une population collectée sur une des variétés traditionnelles ‘Mahmoudi’ ont été génotypées à l'aide de 12 microsatellites. La faible différenciation génétique entre ces populations fongiques suggère l’existence de flux de gènes importants entre localités. La population collectée sur ‘Mahmoudi’ est apparue comme étant moins diversifiée et ayant une fraction clonale plus importante que les populations collectées sur ‘Karim’, suggérant un effet significatif de l’hôte sur la diversité de Z. tritici. Des tests d'inoculations croisées ont révélé une agressivité supérieure des isolats collectés sur ‘Mahmoudi’ sur les lignées de la variété ‘Mahmoudi’ que des isolats collectés sur le cultivar ‘Karim’, interprétée comme une adaptation locale des populations pathogènes à leur hôte sympatrique. Cette adaptation a été particulièrement marquée par la période de latence des isolats, soulignant à nouveau l’importance de la résistance quantitative dans les processus adaptatifs mis en évidence. Les variétés traditionnelles tunisiennes de blé dur sont des cas concrets de populations hôtes hétérogènes limitant efficacement les épidémies de l’agent pathogène responsable de la septoriose. Les résultats obtenus suggèrent que la combinaison de gènes de résistance, principalement à effet quantitatif et occasionnellement à effet majeur, à des fréquences variables d’une variété à une autre, est la clé de la robustesse sanitaire de ces variétés. Les enseignements acquis au cours de cette étude pourront être mobilisés pour améliorer la gestion de la diversité cultivée dans d’autres environnements.Traditional varieties are heterogeneous and constitute a source of diversity, which contributes to the productivity and the stability of agroecosystems. Indeed, plant diversity provides services to a given ecosystem, including reducing disease pressure. Understanding the mechanisms underlying plant-pathogen interactions is fundamental to improve disease management. With this in mind, I studied the adaptation between traditional Tunisian durum wheat varieties and populations of Zymoseptoria tritici, the fungus responsible for Septoria Tritici Blotch (STB). Firstly, genotyping 14 traditional varieties, considered as populations, using 9 SSR, showed that genetic diversity is equally important within a population (45%) as it is between populations (54%). This diversity is structured in seven genetic groups that can be explained in part by the nested effect of the « variety name » and the « location ». 15 phenotypic traits, including resistance to STB, were characterized and showed that the populations were also phenotypically diverse. Resistance to STB is qualitative (major resistance) for two of the populations, but generally more quantitative for the other populations. A Pst-Fst comparison demonstrated a local adaptation of traditional varieties, underlining selection trajectories that are closely linked to the territory and the agricultural practices in place. Meanwhile, a high density SNP genotyping (TaBW35K array) of a panel of 127 individuals hailing from four populations all carrying the same variety name ‘Mahmoudi’ brought to light two genetic groups shared by the four populations. This panel of individuals was phenotyped for resistance to a Tunisian Z. tritici strain in a field trial and in controlled conditions. The resulting data was used in a GWAS analysis. This analysis led to the detection of 6 loci associated to STB resistance on chromosomes 1B, 4A, 5B and 7A, including a locus on chromosome 1B associated to a qualitative major resistance. The frequency of the resistant alleles oscillates between 6 and 46% and is variable between populations. On the fungus side, four populations of Z. tritici collected on modern cultivar ‘Karim’ widely cultivated in Tunisia and one population collected on traditional variety ‘Mahmoudi’ were genotyped using 12 SSR. A low level of genetic differentiation was identified between these fungal populations suggesting a significant gene flow between locations. The population collected on ‘Mahmoudi’ was less diversified and had a higher clonal fraction than the populations collected on ‘Karim’. This points towards host-effect on Z. tritici diversity. Cross-inoculation tests highlighted a higher aggressiveness of isolates collected on ‘Mahmoudi’ to ‘Mahmoudi’ lines than that of isolates collected on ‘Karim’, interpreted as a local adaptation of pathogen populations to their sympatric host. This adaptation was especially pronounced for the latency period of isolates, once again underlining the importance of quantitative resistance in the adaptive processes evidenced here. Traditional Tunisian durum wheat varieties are practical cases of heterogeneous host populations effectively limiting STB epidemics. Our results suggest that a combination of resistance genes, mainly quantitative and occasionally with a major effect, with variable frequencies from one variety to another, is key to the sanitary success of these varieties. Findings from this study can be utilized to improve our management of crop diversity in other environments

Resistance of the Wheat Cultivar ‘Renan’ to Septoria Leaf Blotch Explained by a Combination of Strain Specific and Strain Non-Specific QTL Mapped on an Ultra-Dense Genetic Map

International audienceQuantitative resistance is considered more durable than qualitative resistance as it does not involve major resistance genes that can be easily overcome by pathogen populations, but rather a combination of genes with a lower individual effect. This durability means that quantitative resistance could be an interesting tool for breeding crops that would not systematically require phytosanitary products. Quantitative resistance has yet to reveal all of its intricacies. Here, we delve into the case of the wheat/Septoria tritici blotch (STB) pathosystem. Using a population resulting from a cross between French cultivar Renan, generally resistant to STB, and Chinese Spring, a cultivar susceptible to the disease, we built an ultra-dense genetic map that carries 148,820 single nucleotide polymorphism (SNP) markers. Phenotyping the interaction was done with two different Zymoseptoria tritici strains with contrasted pathogenicities on Renan. A linkage analysis led to the detection of three quantitative trait loci (QTL) related to resistance in Renan. These QTL, on chromosomes 7B, 1D, and 5D, present with an interesting diversity as that on 7B was detected with both fungal strains, while those on 1D and 5D were strain-specific. The resistance on 7B was located in the region of Stb8 and the resistance on 1D colocalized with Stb19. However, the resistance on 5D was new, so further designated Stb20q. Several wall-associated kinases (WAK), nucleotide-binding and leucine-rich repeats (NB-LRR) type, and kinase domain carrying genes were present in the QTL regions, and some of them were expressed during the infection. These results advocate for a role of Stb genes in quantitative resistance and for resistance in the wheat/STB pathosystem being as a whole quantitative and polygenic

Life story of Tunisian durum wheat landraces revealed by their genetic and phenotypic diversity

Durum wheat (Triticum turgidum L. subsp. durum) landraces represent a prominent genetic resource for Mediterranean farming systems and breeding programs. Fourteen landraces sampled in Tunisia were genotyped with 9 microsatellite markers and characterized with 15 morphological descriptors, including resistance to the fungal disease Septoria tritici blotch (STB). The genetic diversity, nearly was as important within landraces populations (45%) than between populations (54%). It was structured in seven genetic groups and was only partly explained by the variety name or the locality of origin. Populations were also greatly diversified phenotypically (Shannon-Weaver H'=0.54) with traits related to spike and awn colours being the most diversified. Resistance to STB was either qualitative in two populations or with varying degrees of quantitative resistance in the others. A Pst-Fst comparison indicate a local adaptation of the populations. Overall, the genetic structure of Tunisian durum wheat landraces revealed a complex selection trajectory and seed exchanges between farmers

Une structure emboîtée universelle pour les interactions quantitatives entre les plantes et leurs parasites ?

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Many different recipes but one flavor: A universal nested structure of quantitative interactions between plant genotypes and their parasites, including viruses

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