Roselyne Corbière

Does selection by resistant hosts trigger local adaptation in plant-pathogen systems?

Understanding the consequences of selection by host resistance on pathogen population structure provides useful insights into the dynamics of host–parasite co‐evolution processes and is crucial for effective disease management through resistant cultivars. We tested general vs. local population adaptation to host cultivars, by characterizing a French collection of Phytophthora infestans (the causal organism of potato late blight) sampled during two consecutive years on cultivars exhibiting various levels of resistance. Local populations were structured by the host for virulence (qualitative pathogenicity) but also for aggressiveness (quantitative pathogenicity). All populations had a low genotypic diversity for amplified fragment length polymorphisms (AFLPs), and presumably consisted of a few closely related clonal lineages. No correlation was detected between pathogenicity traits and AFLP genotypes. The data support the hypothesis of general adaptation for aggressiveness, to which directional selection for virulence is superimposed when race‐specific resistance is introduced.

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.

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 (FST = 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.

Fitness costs associated with unnecessary virulence factors and life history traits: evolutionary insights from the potato late blight pathogen Phytophthora infestans

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.

Multiphasic approach for the identification of the different classification levels of Pseudomonas savastanoi pv. phaseolicola

The relationships between strains of Pseudomonas savastanoi pv. phaseolicola (P. sav. phaseolicola), P. syringae pv. tabaci (P. syr. tabaci) and P. syr. syringae which all cause disease on bean; the related species P. sav. glycinea and P. syr. actinidiae, and reference bacteria, were evaluated by studying the phenotypic and genetic diversity of a collection of 62 strains. All the P. sav. phaseolicola strains tested produced characteristic watersoaked lesions on bean pods. Other pathovars produced varying combinations of symptoms including necrotic lesions, with or without watersoaked centres and sunken tissue collapse of the lesion (P. syr. tabaci) and necrotic lesions with or without sunken collapse (P. syr. syringae). At the genomospecies level, all the strains of P. sav. phaseolicola, P. sav. glycinea and P. syr. tabaci, belonging to genomospecies 2, could be separated from P. syr. syringae strains (genomospecies 1) and P. syr. actinidiae strains (unknown genomospecies) by BOX-PCR and DNA/DNA hybridisation. To distinguish P. sav. phaseolicola, within genomospecies 2, from P. sav. glycinea and P. syr. tabaci, it was necessary to perform nutritional characterisations myo-inositol negative and p-hydroxy benzoate positive for P. sav. phaseolicola strains), PCR with specific primers designed from the tox region (positive for all of the P. sav. phaseolicola strains) and serotyping, as 71% of the P. sav. phaseolicola strains reacted as O-serogroup PHA1. Important intrapathovar variation was seen by genomic fingerprinting with REP and ERIC primers, as well as with RAPD primers (AE7 and AE10) and esterase profilings. While RAPD fingerprinting detected variability correlated with two race-associated evolutionary lines, REP, ERIC and esterase profiles revealed intrapathovar variation linked to some host origins, that separated the kudzu isolates, and the mungbean isolates, from the other P. sav. phaseolicola strains.

Resistance to late blight and soft rot in six potato progenies and glycoalkaloid contents in the tubers

Glycoalkaloids are anti-nutritional compounds commonly found in wildSolanum species used as resistance sources to major potato pathogens. It is therefore important for breeding purposes to know whether selecting for resistance using such species necessarily selects also for high glycoalkaloid contents in the tubers. To test this hypothesis, we used six partial progenies from crosses betweenSolanum tuberosum and accessions ofS. andigena, S. berthaultii, S. phureja, andS. vernei to investigate the possible correlation between resistance toPhytophthora infestans and/or toErwinia carotovora subsp.atroseptica and the concentration of glycoalkaloids in tubers. Concentrations of α-solanine and α-chaconine in the tubers segregated in each progeny, as did resistance to each pathogen. Some, but not all, clones from each progeny showed hypersensitive reactions to the isolate ofP. infestans used. Furthermore, clones within each progeny also differed for components of partial resistance toP. infestans, suggesting that all four wild species could be used as sources of both race-specific and partial resistance to late blight. With the exception of low, but statistically significant, correlations between concentration of α-solanine and two late blight resistance components (incubation period and spore production per unit lesion area) in progenies derived fromS. vernei, and despite a trend towards higher glycoalkaloid concentrations in the tubers of the clones most resistant to soft rot within progenies derived fromS. berthaultii andS. vernei, no consistent relationship between resistance to either disease and concentrations of α-solanine and/or α-chaconine was observed. These results indicate that neither race-specific nor partial resistance to late blight and soft rot in the accessions used as progenitors of resistance depend on high solanine or chaconine concentrations. These resistance sources could thus prove useful in breeding programs for improved behaviour againstP. infestans and/orE. carotovora.ResumenLos glicoalcaloides son compuestos antinutricionales que se encuentran presentes en las especies silvestres deSolanum usadas como fuentes de resistencia a los principales patógenos. Es por lo tanto importante con fines de mejoramiento, conocer si la selección hecha para obtener resistencia utilizando tales especies selecciona también necesariamente para contenidos altos de glicoalcaloides en los tubérculos. Para probar esta hipótesis, hemos utilizado seis progenies parciales provenientes de cruzamientos entreSolanum tuberosum y accesiones deS. andigena, S. berthaultii, S. phureja yS. vernei, con el objeto de investigar la existencia de una posible correlación entre la resistencia aPhytophthora infestans y/o aErwinia carotovora subsp.atroseptica y la concentración de glicoalcaloides en los tubérculos. Las concentraciones de α-solanina y α-chaconina en los tubérculos segregaron en cada progenie, asi como la resistencia a cada uno de los patógenos mencionados. Algunos, aunque no todos los clones en cada progenie mostraron reacciones de hipersensibilidad al aislamiento utilizado deP. infestans. Más aun, los clones dentro de cada progenie también mostraron diferencias en los componentes de la resistencia parcial aP. infestans, lo que sugiere que las cuatro especies de papa silvestre antes mencionadas pueden ser utilizadas como fuentes tanto para resistencia específica como para resistencia parcial aP. infestans. Con excepción de una reducida pero estadísticamente significativa correlación entre concentración de α-sblanina y dos componentes de resistencia al tizón tardío (periodo de incubación y producción de esporas por unidad de área de lesión) en progenies derivadas deS. vernei, y a pesar de una tendencia hacia altas concentraciones de glicoalcaloides en los tubérculos de los clones más resistentes a la pudrición blanda dentro de las progenies derivadas deS. berthaultii yS. vernei, no se ha observado una relación consistente en la resistencia a ambas enfermedades y la concentracios de α-solanina y/o α-chaconina. Estos resultados indican que ni la resistencia especifica, ni la resistencia parcial al tizón tardío y a la pudrición blanda en las accesiones utilizadas como progenitores de resistencia depende de la presencia de altas concentraciónes de solanina o de chaconina. Estas fuentes de resistencia pueden así ser de utilidad en los programas de mejoramiento para una mejor respuesta contraP. infestans y/oE. carotovora.

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.

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.

Abstract 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.