A Trade-Off Between Sporangia Size and Number Exists in the Potato Late Blight Pathogen Phytophthora infestans, and Is Not Altered by Biotic and Abiotic Factors.

The negative relationship between offspring size and number is a classic example of trade-off between life-history traits, reported many times in animal and plant species. Here, we wanted to ascertain whether such a trade-off occurred in the oomycete Phytophthora infestans, and whether it was impacted by biotic and abiotic factors. We thus conducted three infection experiments under controlled conditions and measured the number and the size of sporangia (asexual propagules) produced on potato by different P. infestans isolates. In all experiments, we observed a negative relationship between sporangia size and number, demonstrating the existence of a trade-off. Moreover, although the potato host cultivar, temperature and host of origin (tomato or potato) all affected sporangia number, sporangia size or both, none of these biotic and abiotic factors did change the trade-off. Therefore, the trade-off between sporangia size and number could maintain the polyphenism for these traits in P. infestans populations, and favors the coexistence of distinct reproductive strategies within this species. Our results emphasize the relevance to focus on the relationship between offspring size and number in other fungal plant pathogens, as well as to study the impact of offspring size on fitness-linked traits (virulence and disease lesion development) in these organisms.

Local adaptation to temperature in populations and clonal lineages of the Irish potato famine pathogen Phytophthora infestans.

Environmental factors such as temperature strongly impact microbial communities. In the current context of global warming, it is therefore crucial to understand the effects of these factors on human, animal, or plant pathogens. Here, we used a common-garden experiment to analyze the thermal responses of three life-history traits (latent period, lesion growth, spore number) in isolates of the potato late blight pathogen Phytophthora infestans from different climatic zones. We also used a fitness index (FI) aggregating these traits into a single parameter. The experiments revealed patterns of local adaptation to temperature for several traits and for the FI, both between populations and within clonal lineages. Local adaptation to temperature could result from selection for increased survival between epidemics, when isolates are exposed to more extreme climatic conditions than during epidemics. We also showed different thermal responses among two clonal lineages sympatric in western Europe, with lower performances of lineage 13_A2 compared to 6_A1, especially at low temperatures. These data therefore stress the importance of thermal adaptation in a widespread, invasive pathogen, where adaptation is usually considered almost exclusively with respect to host plants. This must now be taken into account to explain, and possibly predict, the global distribution of specific lineages and their epidemic potential.

And the nasty ones lose in the end: foliar pathogenicity trades off with asexual transmission in the Irish famine pathogen Phytophthora infestans.

A trade-off between pathogenicity and transmission is often postulated to explain the persistence of pathogens over time. If demonstrated, it would help to predict the evolution of pathogenicity across cropping seasons, and to develop sustainable control strategies from this prediction. Unfortunately, experimental demonstration of such trade-offs in agricultural plant pathogens remains elusive. We measured asexual transmission of Phytophthora infestans isolates differing in pathogenicity in two sets of artificial infection experiments under controlled, semi-outdoor conditions. Higher foliar pathogenicity decreased mean daughter tuber weight, increased infection severity in daughter tubers, and increased stem mortality before emergence. The most pathogenic isolates thus suffer a double penalty for asexual transmission: a lower survival probability within small and severely infected tubers; and a lower infection probability of neighbouring healthy plants due to fewer infected stems produced by surviving tubers. Moderate tuber resistance favoured transmission of the least pathogenic isolates, while high levels of resistance almost abolished transmission of all isolates. These data demonstrate a trade-off between foliar pathogenicity and asexual transmission over seasons in P. infestans, which should stabilise pathogenicity over time in the potato late blight pathosystem and possibly favour clone replacement by less pathogenic lineages after demographic bottlenecks.

Long-distance gene flow outweighs a century of local selection and prevents local adaptation in the Irish famine pathogen Phytophthora infestans.

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.

Absence of isolation by distance patterns at the regional scale in the fungal plant pathogen Leptosphaeria maculans.

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.

Quantitative resistance increases the durability of qualitative resistance to Leptosphaeria maculans in Brassica napus.

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.