[Show abstract][Hide abstract]ABSTRACT: The main objective of this paper was to test the ‘always more aggressive’ hypothesis, often advocated to explain lineage replacements in clonal populations of the potato late blight oomycete Phytophthora infestans. To this end, we analysed genotypic and pathogenicity data on 1274 French isolates of P. infestans collected over the period 2001-2008. Overall, the populations sampled showed limited genetic diversity, with four multilocus lineages (1_A1, 2_A1, 8_A1 and 13_A2) accounting for over 80% of the isolates collected. As in other West European countries, we observed drastic changes of these dominant clonal lineages along the course of the eight years, particularly with the appearance and propagation of the clone 13_A2. However, invasiveness of clones was not associated with higher aggressiveness; on the contrary, dominant clones had generally low or moderate aggressiveness relative to others present at the same time within the same populations. This finding challenges the link between invasive behavior and increased aggressiveness often assumed in this biotrophic pathogen, and could rather reflect the existence of a trade-off between intra-season and inter-season transmission. This would be consistent with the concept of inclusive fitness, which involves the abilities to both reproduce and survive.This article is protected by copyright. All rights reserved.
[Show abstract][Hide abstract]ABSTRACT: Sustainably managing plant resistance to epidemic pathogens implies controlling the genetic and demographic changes in pathogen populations faced with resistant hosts. Resistance management thus depends upon the dynamics of local adaptation, mainly driven by the balance between selection and gene flow. This dynamics is best investigated with populations from locally dominant hosts in islands with long histories of local selection. We used the unique case of the potato late blight pathosystem on Jersey, where a monoculture of potato cultivar 'Jersey Royal' has been in place for over a century. We also sampled populations from the coasts of Brittany and Normandy, as likely sources for gene flow. The isolation by distance pattern and the absence of genetic differentiation between Jersey and the closest French sites revealed gene flow at that spatial scale. Microsatellite allele frequencies revealed no evidence of recombination in the populations, but admixture of two genotypic clusters. No local adaptation in Jersey was detected from pathogenicity tests on Jersey Royal and on French cultivars. These data suggest that long-distance gene flow (∼ 50/100 km) prevents local adaptation in Jersey despite a century of local selection by a single host cultivar and emphasize the need for regional rather than local management of resistance gene deployment.
[Show abstract][Hide abstract]ABSTRACT: Quantitative resistance mediated by multiple genetic factors has been shown to increase the potential for durability of major resistance genes. This was demonstrated in the Leptosphaeria maculans/Brassica napus pathosystem in a five year recurrent selection field experiment on lines harboring the qualitative resistance gene Rlm6 combined or not with quantitative resistance. The quantitative resistance limited the size of the virulent isolate population. In this study we continued this recurrent selection experiment in the same way to examine whether the pathogen population could adapt and render the major gene ineffective in the longer term. The cultivars Eurol, with a susceptible background, and Darmor, with quantitative resistance, were used. We confirmed that the combination of qualitative and quantitative resistance is an effective approach for controlling the pathogen epidemics over time. This combination did not prevent isolates virulent against the major gene from amplifying in the long term but the quantitative resistance significantly delayed for five years the loss of effectiveness of the qualitative resistance and disease severity was maintained at a low level on the genotype with both types of resistance after the fungus population had adapted to the major gene. We also showed that diversity at the AvrLm6 virulence allele was comparable in isolates recovered after the recurrent selection on lines carrying either the major gene alone or in combination with quantitative resistance: a single repeat-induced point mutation and deletion events were observed in both situations. Breeding varieties which combine qualitative and quantitative resistance can effectively contribute to disease control by increasing the potential for durability of major resistance genes.
No preview · Article · Jan 2014 · Infection, genetics and evolution: journal of molecular epidemiology and evolutionary genetics in infectious diseases
[Show abstract][Hide abstract]ABSTRACT: The strict dependency of biotrophic pathogens upon living host tissue for multiplication and survival makes them particularly exposed to evolutionary trade-offs. Such trade-offs can occur both between life history traits directly involved in pathogenicity (e.g. fitness costs due to unnecessary virulence factors), or between traits involved in either pathogenicity (within-season fitness) or survival (between-season fitness). Both types of trade-offs should result in the limitation of maximum pathogenicity, and shape the invasive potential of pathogen genotypes. While strong theoretical developments have been made on evolutionary consequences, including recent work taking seasonality into account (i.e. periodic host absence and/or periodic sexual/asexual reproduction), experimental evidence to confirm theoretical predictions is still scarce. This paper will therefore attempt to illustrate the different kinds of trade-offs that can be measured, and their likely consequences, taking Phytophthora infestans (the cause of potato and tomato late blight) as a case study.
[Show abstract][Hide abstract]ABSTRACT: Outcomes of host-pathogen coevolution are influenced by migration rates of the interacting species. Reduced gene flow with increasing spatial distance between populations leads to spatial genetic structure, as predicted by the isolation by distance (IBD) model. In wind-dispersed plant-pathogenic fungi, a significant spatial genetic structure is theoretically expected if local spore dispersal is more frequent than long-distance dispersal, but this remains to be documented by empirical data. For 29 populations of the oilseed rape fungus Leptosphaeria maculans sampled from two French regions, genetic structure was determined using eight minisatellite markers. Gene diversity (H = 0.62-0.70) and haplotypic richness (R = 0.96-1) were high in all populations. No linkage disequilibrium was detected between loci, suggesting the prevalence of panmictic sexual reproduction. Analysis of molecular variance showed that > 97% of genetic diversity was observed within populations. Genetic differentiation was low among populations (F(st) < 0.05). Although direct methods previously revealed short-distance dispersal for L. maculans, our findings of no correlation between genetic and geographic distances among populations illustrate that the IBD model does not account for dispersal of the fungus at the spatial scale we examined. These results indicate high gene flow among French populations of L. maculans, suggesting high dispersal rates and/or large effective population sizes, two characteristics giving the pathogen high evolutionary potential against the deployment of resistant oilseed rape cultivars.
[Show abstract][Hide abstract]ABSTRACT: Specific resistance genes are an effective means of disease control when the pathogen population is mainly avirulent on the cultivated varieties carrying the corresponding resistance gene. Development of new races of Leptosphaeria maculans (Desmaz.) Ces. & de Not., the species responsible for the most damaging symptoms of blackleg disease of canola (Brassica napus L.), increases the risk that host genetic resistance may be rapidly overcome. This study aims to elucidate the race structure of L. maculans by determining, under controlled conditions, the frequency of avirulence alleles at eleven avirulence loci in pathogen populations collected from nine locations across western Canada. The avirulence allele at AvrLm6 was present in all isolates tested (63) from three locations. At eight locations >88% of the isolates (423) carried the avirulence allele at AvrLm2, but only 37% at another location. For all other avirulence genes (AvrLm1, AvrLm3, AvrLm4, AvrLm7, AvrLm9, AvrLmLepR1, AvrLmLepR2 and AvrLmLepR3), avirulence allele frequency varied from 0 to 99% depending on the loci and the location (300-600 isolates). Knowledge of avirulence allele frequency and the race structure of L. maculans in canola producing regions of western Canada will be crucial to develop strategies to maintain the efficacy of resistance genes.
[Show abstract][Hide abstract]ABSTRACT: Although sexual reproduction implies a cost, it represents an evolutionary advantage for the adaptation and survival of facultative sexual pathogens. Understanding the maintenance of sex in pathogens requires to analyse how host resistance will impact their sexual reproduction through the alteration of their life-history traits. We explored this experimentally using potato (Solanum tuberosum) and one of its pathogens, the heterothallic oomycete Phytophthora infestans. Sexual reproduction was highest on hosts favouring asexual multiplication of the pathogen, suggesting similar nutritional requirements for both sexual and asexual sporulation. Sexual reproduction was also highest on hosts decreasing the latent period, probably because of a trade-off between growth and reproduction. Distinguishing host effects on each pathogenic trait remains however uneasy, as most life-history traits linked to pathogenicity were not independent of each other. We argue that sexual reproduction of P. infestans is an adaptation to survive when the host is susceptible and rapidly destroyed.
Full-text · Article · Oct 2010 · Journal of Evolutionary Biology
[Show abstract][Hide abstract]ABSTRACT: It has frequently been hypothesized that quantitative resistance increases the durability of qualitative (R-gene mediated) resistance but supporting experimental evidence is rare. To test this hypothesis, near-isogenic lines with/without the R-gene Rlm6 introduced into two Brassica napus cultivars differing in quantitative resistance to Leptosphaeria maculans were used in a 5-yr field experiment. Recurrent selection of natural fungal populations was done annually on each of the four plant genotypes, using crop residues from each genotype to inoculate separately the four series of field trials for five consecutive cropping seasons. Severity of phoma stem canker was measured on each genotype and frequencies of avirulence alleles in L. maculans populations were estimated. Recurrent selection of virulent isolates by Rlm6 in a susceptible background rendered the resistance ineffective by the third cropping season. By contrast, the resistance was still effective after 5 yr of selection by the genotype combining this gene with quantitative resistance. No significant variation in the performance of quantitative resistance alone was noted over the course of the experiment. We conclude that quantitative resistance can increase the durability of Rlm6. We recommend combining quantitative resistance with R-gene mediated resistance to enhance disease control and crop production.
[Show abstract][Hide abstract]ABSTRACT: The influence of competitive effects between two isolates, of the number of infection sites on cotyledons and of host polygenic resistance on the systemic growth of Leptosphaeria maculans, the cause of phoma stem canker in oilseed rape (Brassica napus), were investigated. Controlled-condition experiments were conducted with two oilseed rape doubled haploid lines, one susceptible and the other with a high level of polygenic resistance, inoculated via wounded cotyledons with conidial suspensions obtained from two isolates. Expression of cankers in plants was enhanced by exposing inoculated plants to low temperature (6°C) followed by warm temperature (20°C). The fungus was detected by PCR amplifications of three minisatellite markers in all stems with visible canker symptoms and also in the stems of 14 of the 59 plants without visible cankers on the hypocotyls. Disease severity increased with the number of infection sites on cotyledons: in one of the three replicate experiments, the mean external necrosis length on the hypocotyl ranged from 6·47 to 35·3 mm for one and eight infections sites on cotyledons, respectively. The probability of an isolate reaching the hypocotyl from inoculated cotyledons decreased with increasing competing inoculum load on cotyledons: for instance, for isolate A290v it decreased from 1 when inoculated alone to 0·28 when coinoculated with six drops of competing isolate P27d. Polygenic resistance significantly reduced disease incidence and severity. For instance, in one of the three replicate experiments, disease incidence ranged from more than 74% in susceptible plants to 16% in resistant ones, while mean external necrosis length was up to 35·3 and 6·5 mm on susceptible and on resistant plants, respectively. This study offers new possibilities for assessing levels of polygenic resistance to stem canker in B. napus and studying the aggressiveness of L. maculans isolates.