BackgroundThe yellow potato cyst nematode, Globodera rostochiensis, is a devastating plant pathogen of global economic importance. This biotrophic parasite secretes effectors from pharyngeal glands, some of which were acquired by horizontal gene transfer, to manipulate host processes and promote parasitism. G. rostochiensis is classified into pathotypes with different plant resistance-breaking phenotypes.ResultsWe generate a high quality genome assembly for G. rostochiensis pathotype Ro1, identify putative effectors and horizontal gene transfer events, map gene expression through the life cycle focusing on key parasitic transitions and sequence the genomes of eight populations including four additional pathotypes to identify variation. Horizontal gene transfer contributes 3.5 % of the predicted genes, of which approximately 8.5 % are deployed as effectors. Over one-third of all effector genes are clustered in 21 putative ‘effector islands’ in the genome. We identify a dorsal gland promoter element motif (termed DOG Box) present upstream in representatives from 26 out of 28 dorsal gland effector families, and predict a putative effector superset associated with this motif. We validate gland cell expression in two novel genes by in situ hybridisation and catalogue dorsal gland promoter element-containing effectors from available cyst nematode genomes. Comparison of effector diversity between pathotypes highlights correlation with plant resistance-breaking.ConclusionsThese G. rostochiensis genome resources will facilitate major advances in understanding nematode plant-parasitism. Dorsal gland promoter element-containing effectors are at the front line of the evolutionary arms race between plant and parasite and the ability to predict gland cell expression a priori promises rapid advances in understanding their roles and mechanisms of action.Electronic supplementary materialThe online version of this article (doi:10.1186/s13059-016-0985-1) contains supplementary material, which is available to authorized users.

Nonhost environmental reservoirs of pathogens play key roles in their evolutionary ecology and in particular in the evolution of pathogenicity. In light of recent reports of the plant pathogen Pseudomonas syringae in pristine waters outside agricultural regions and its dissemination via the water cycle, we have examined the genetic and phenotypic diversity, population structure, and biogeography of P. syringae from headwaters of rivers on three continents and their phylogenetic relationship to strains from crops. A collection of 236 strains from 11 sites in the United States, in France, and in New Zealand was characterized for genetic diversity based on housekeeping gene sequences and for phenotypic diversity based on measures of pathogenicity and ice nucleation activity. Phylogenetic analyses revealed several new genetic clades from water. The genetic structure of P. syringae populations was not influenced by geographic location or water chemistry, whereas the phenotypic structure was affected by these parameters. Comparison with strains from crops revealed that the metapopulation of P. syringae is structured into three genetic ecotypes: a crop-specific type, a water-specific type, and an abundant ecotype found in both habitats. Aggressiveness of strains was significantly and positively correlated with ice nucleation activity. Furthermore, the ubiquitous genotypes were the most aggressive, on average. The abundance and diversity in water relative to crops suggest that adaptation to the freshwater habitat has played a nonnegligible role in the evolutionary history of P. syringae. We discuss how adaptation to the water cycle is linked to the epidemiological success of this plant pathogen.

Quantitative resistance has gained interest in plant breeding for pathogen control in low-input cropping systems. Although quantitative resistance frequently has only a partial effect and is difficult to select, it is considered more durable than major resistance (R) genes. With the exponential development of molecular markers over the past 20 years, resistance QTL have been more accurately detected and better integrated into breeding strategies for resistant varieties with increased potential for durability. This review summarizes current knowledge on the genetic inheritance, molecular basis, and durability of quantitative resistance. Based on this knowledge, we discuss how strategies that combine major R genes and QTL in crops can maintain the effectiveness of plant resistance to pathogens. Combining resistance QTL with complementary modes of action appears to be an interesting strategy for breeding effective and potentially durable resistance. Combining quantitative resistance with major R genes has proven to be a valuable approach for extending the effectiveness of major genes. In the plant genomics era, improved tools and methods are becoming available to better integrate quantitative resistance into breeding strategies. Nevertheless, optimal combinations of resistance loci will still have to be identified to preserve resistance effectiveness over time for durable crop protection.

BackgroundIn gene-for-gene models of plant-pathogen interactions, the existence of fitness costs associated with unnecessary virulence factors still represents an issue, both in evolutionary biology and agricultural sciences. Measuring such costs experimentally has proven difficult, especially in pathogens not readily amenable to genetic transformation, since the creation of isogenic lines differing only by the presence or absence of avirulence genes cannot be achieved in many organisms. Here, we circumvented this difficulty by comparing fitness traits in groups of Phytophthora infestans isolates sharing the same multilocus fingerprint, but differing by their virulence/avirulence spectrum.ResultsFitness was assessed from calculations derived from the basic reproduction number, combining several life history traits (latent period, spore density and lesion growth rate) evaluated on leaflets of the potato cultivar Bintje, which is free of resistance genes. A statistically significant fitness cost was found in isolates virulent to the R10 resistance gene. That cost was due to a lower spore production in virulent isolates; however, the latent period was shorter in virulent isolates. Similar trends, although not statistically significant, were observed for the other genes tested.ConclusionThe data likely reflect the adaptive response of the pathogen to the cost associated with virulence. They suggest strong trade-offs between life history traits related to pathogenicity and adaptive biology of pathogens.

The use of partially resistant cultivars should become an essential component of a sustainable management strategy of potato late blight, caused by Phytophthora infestans. It is therefore important to determine to what extent P. infestans populations can be selected for increased aggressiveness by potato cultivars with different levels of partial resistance. To this end, we sampled P. infestans populations from France and Morocco, chosen as locations where late blight occurs regularly but which differ in the distribution of potato cultivars. Cross-inoculation experiments were used to determine the aggressiveness of all populations to potato cvs. Bintje (prevalent in France but not grown in Morocco) and Désirée (popular in Morocco but cultivated to a very small extent in France). French populations were more aggressive on cv. Bintje than on cv. Désirée, irrespective of the site they were sampled from. Their aggressiveness increased between early and late samplings, suggesting that both cultivars selected for increased aggressiveness during epidemics. By contrast, Moroccan populations were more aggressive on Désirée, regarded as partially resistant in Europe, than on Bintje, highly susceptible under European conditions. These data indicate that P. infestans populations adapt to locally dominant cultivars, irrespective of their resistance levels, and can therefore overcome polygenic, partial resistance. This adaptive pattern may render partial resistance nondurable if not properly managed.

To understand why the Pvr4 resistance of pepper against Potyvirus spp. remained durable in field conditions while virulent Potato virus Y (PVY) variants could be selected in the laboratory, we studied the molecular mechanisms which generated these variants and the consequences on viral fitness. Using a reverse genetics approach with an infectious cDNA clone of PVY, we found that the region coding for the NIb protein (RNA-dependent RNA polymerase) of PVY was the avirulence factor corresponding to Pvr4 and that a single nonsynonymous nucleotide substitution in that region, an adenosine to guanosine substitution at position 8,424 of the PVY genome (A(8424)G), was sufficient for virulence. This substitution imposed a high competitiveness cost to the virus against an avirulent PVY variant in plants devoid of Pvr4. In addition, during serial passages in susceptible pepper plants, the only observed possibility of the virulent mutant to increase its fitness was through the G(8424)A reversion, strengthening the high durability potential of the Pvr4 resistance. This is in accordance with the fact that the NIb protein is one of the most constrained proteins expressed by the PVY genome and, more generally, by Potyvirus spp., and with a previously developed model predicting the durability of virus resistances as a function of the evolutionary constraint applied on corresponding avirulence factors.

The discovery of genetically distinct Erysiphe necator groups (A or B), with high phenotypic similarities, raises important questions about their coexistence. For plant pathogens, niche partitioning, allowing the coexistence on the same host (i.e. the same resource), might result from separation in space and/or time. We used a landscape genetic approach to study the geographic distribution of genetic groups of E. necator (distinguished by a SNP in the β-tubulin gene) at the spatial scale of the Languedoc-Roussillon region (southern France) and to assess the temporal succession of groups along the course of the 2007 epidemic. Spatial distribution revealed a high heterogeneity between vineyards: from 100% B to 100% A, with 62% and 38% of vineyards showing a majority of A and B isolates, respectively. Temporal isolation seems to be the major mechanism in the coexistence of the two genetic groups: all isolates collected towards the end of the epidemic belonged to group B, whatever the initial frequency of genetic groups. Our results confirm that both A or B isolates can lead to flag-shoot symptoms, and showed that group A isolates tend to disappear during the course of the epidemic, whereas group B isolates may be active during the entire epidemic and involved in further production of cleistothecia, when recombination takes place. For the first time, the relationship between the frequency of genetic groups and disease levels on leaves and clusters at the end of the epidemic was evaluated. We showed a strong relationship between the disease severity and the genetic composition of E. necator populations: the damage was more important when the epidemic was initiated by B isolates.

The variability of resistance durability in different potato genotypes harbouring the same resistance QTL but differing by their genetic background was explored. The indirect consequences of the resistance adaptation in terms of local (i.e. genotype-specific) adaptation and cross-virulence was also investigated. Following the virulence of the potato cyst nematode Globodera pallida in a long-term experimental evolution protocol, the results showed that nematode populations were able to adapt to the resistance of four potato genotypes carrying the QTL GpaV from Solanum vernei, and that the plant genetic background has an impact upon the durability of resistance. The pattern of local adaptation observed here indicates that divergent selection has occurred during the experimental evolution performed from the same initial nematode population, and revealed a trade-off between the adaptation to a resistant potato genotype and the adaptation to another resistant genotype differing in its genetic background. In terms of cross-virulence between potato genotypes derived from different resistance sources (S. sparsipilum and S. spegazzinii), this study shows that the adaptation to resistance QTL GpaV vrn does not necessarily allow the adaptation to collinear GpaV loci. The results presented here could be useful for predicting evolution of nematode populations in natural agro-ecosystems and identifying durable strategies for resistance deployment.