Examining Phenotypic Traits Contributing to the Spread in Northern European Potato Crops of EU_41_A2, a New Clonal Lineage of Phytophthora infestans.

Until recently, genotypes of Phytophthora infestans were regionally distributed in Europe, with populations in western Europe being dominated by clonal lineages and those in northern Europe being genetically diverse because of frequent sexual reproduction. However, since 2013 a new clonal lineage (EU_41_A2) has successfully established itself and expanded in the sexually recombining P. infestans populations of northern Europe. The objective of this study was to study phenotypic traits of the new clonal lineage of P. infestans, which may explain its successful establishment and expansion within sexually recombining populations. Fungicide sensitivity, aggressiveness, and virulence profiles of isolates of EU_41_A2 were analyzed and compared with those of the local sexual populations from Denmark, Norway, and Estonia. None of the phenotypic data obtained from the isolates collected from Denmark, Estonia, and Norway independently explained the invasive success of EU_41_A2 within sexual Nordic populations. Therefore, we hypothesize that the expansion of this new genotype could result from a combination of fitness traits and more favorable environmental conditions that have emerged in response to climate change.

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.

The coexistence of generalist and specialist clonal lineages in natural populations of the Irish Famine pathogen Phytophthora infestans explains local adaptation to potato and tomato.

Phytophthora infestans, causing late blight on Solanaceae, is a serious threat to potato and tomato crops worldwide. P. infestans populations sampled on either potato or tomato differ in genotypes and pathogenicity, suggesting niche exclusion in the field. We hypothesized that such niche separation can reflect differential host exploitation by different P. infestans genotypes. We thus compared genotypes and phenotypes in 21 isolates sampled on potato (n = 11) or tomato (n = 10). Typing at 12 microsatellite loci assigned potato isolates to the 13_A2, 6_A1 and 1_A1 lineages, and tomato isolates to the 23_A1, 2_A1 and unclassified multilocus genotypes. Cross-inoculations on potato and tomato leaflets showed that all isolates were pathogenic on both hosts. However, tomato isolates performed much better on tomato than did potato isolates, which performed better on potato than did tomato isolates, thus revealing a clear pattern of local adaptation. Potato isolates were significantly fitter on potato than on tomato, and are best described as potato specialists; tomato isolates appear to be generalists, with similar pathogenicity on both hosts. Niche separation in the field may thus result mainly from the large fitness gap on tomato between generalists and unadapted potato specialists, while the small, but significant fitness difference on potato between both types of isolates may prevent population invasion by generalists. Extreme specialization to potato seems very costly relative to performance loss on the alternative host. This study therefore shows that local adaptation and niche separation, commonly expected to involve and generate specialists, can occur with generalists.

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.

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.

Microsatellite markers reveal two admixed genetic groups and an ongoing displacement within the French population of the invasive plant pathogen Phytophthora infestans.

Potato late blight is an example of a re-emerging disease of plants. Phytophthora infestans was first introduced into Europe during the 19th century, where it caused the Irish potato famine. During the 20th century several additional introduction events have been suspected, especially in the mid-70s due to the import of large quantities of potato needed after the shortage caused by drought in 1976. Here, we investigate the genetic population structure of Phytophthora infestans, at the first stages of a recent invasion process in France. A total of 220 isolates was collected from 20 commercial fields of the potato susceptible cultivar Bintje, during two consecutive years (2004 and 2005). Clustering analyses based on eight recently developed microsatellite markers reveal that French P. infestans populations are made of two differentiated genetic clusters of isolates (F(ST) = 0.19). This result suggests multiple introductions of P. infestans into France, either through the introduction of a composite population of isolates or through the successive introduction of isolates having differentiated genetic backgrounds. Both clusters identified have a strong clonal structure and are similar regarding genetic diversity and mating type composition. The maintenance of differentiation between the two genetic clusters should result from the low or non-existent contribution of sexual reproduction in French P. infestans populations.

Adaptation of Phytophthora infestans to Partial Resistance in Potato: Evidence from French and Moroccan Populations.

ABSTRACT 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.