Phytophthora infestans's 10-year truce with Holland: a long-term analysis of potato late-blight epidemics in the Netherlands

A sequence of 47 potato late-blight ( Phytophthora infestans ) epidemics in the Netherlands, from 1950 to 1996, was analysed using agronomic and meteorological variables. The intensity of annual epidemics was characterized by an index of disease intensity (DI, 0 = absence of late blight; 4 = severe epidemic). Three periods were identified, with average DIs of 2·9, 0 and 2, respectively. Period I (1950–68) had relatively regular epidemics; period II (1969–78) was virtually blight free; and period III (1979–96) showed large variations in disease intensity. Disease-enhancing factors were number of days with precipitation, and number of hours with temperatures between 10 and 27°C and relative humidity >90% during the growing season. Limiting factors were number of hours with temperatures >27°C, and amount of global radiation. Linear discriminant analysis of DI using the blight status of the previous year and meteorological variables correctly classified up to 40 years out of 47 (87·0%), with five out of the six incorrectly classified years falling in period III. Blight status of the previous year and number of days with precipitation were important discriminating variables.     

Late Blight Forecasting in Norway 1957–19801

A regular late-blight warning service was established in Norway in 1957, run by the Plant Protection Service. The service was revised in 1965 and from that year the warnings were distributed by the Norwegian Institute of Meteorology. The criteria for warnings are described. A regression analysis of the relationship between warnings and intensity of late-blight epidemics in 1957–1980 showed no significant differences between locations, but significant differences in the relationship between years and periods. The weather in the years 1973 to 1978 caused unfavourable conditions for late blight in all parts of the country. In 1979 and 1980 the weather changed and favourable climate to late blight occurred in most regions of the country, but the progress of epidemics in 1979 was slower than expected due to reduced inoculum potential. In 1980 a more normal progress of epidemics was observed, which indicated a reestablishment of the inoculum potential in the autumn of 1979.     

Development of potato late blight epidemics: disease foci, disease gradients, and infection sources

ABSTRACT Natural potato late blight epidemics were studied to assess the relative impact of various inoculum sources of Phytophthora infestans in Southern Flevoland (the Netherlands) from 1994 through 1996. Disease surveys were combined with characterization of isolates for mating type and DNA fingerprint pattern using probe RG57. Seventy-four percent of the commercial potato fields with early foci were clearly associated with nearby infested refuse piles. Characterization of isolates from refuse piles and fields confirmed the association. Infected seed tubers, volunteer plants, and infested allotment gardens appeared to be of minor importance for late blight development in potato fields. Several foci in refuse piles, potato fields, and allotment gardens contained more than one genotype. Due to favorable weather in August 1994, infested organic potato fields became major inoculum sources, resulting in the spread of P. infestans to adjacent conventional potato fields. Analyses of disease gradients, both at the field and regional levels, confirmed the role of the organic fields as mid-season infection sources. The mean slope of field gradients downwind of refuse piles (point sources) was significantly steeper (100-fold difference) than the mean slope of field gradients downwind of organic fields (area sources). The genotypic composition of the P. infestans populations along the gradient and of the source populations in the organic potato crops did not differ significantly. Analysis of the region gradient revealed genotype-specific disease gradients. Control measures are recommended.     

Spatial Analysis of Phytophthora infestans Genotypes and Late Blight Severity on Tomato and Potato in the Del Fuerte Valley Using Geostatistics and Geographic Information Systems

ABSTRACT Genetic structure of Phytophthora infestans, the causal agent of potato and tomato late blight, was analyzed spatially in a mixed potato and tomato production area in the Del Fuerte Valley, Sinaloa, Mexico. Isolates of P. infestans were characterized by mating type, allozyme analysis at the glucose-6-phosphate isomerase and peptidase loci, restriction fragment length polymorphism with probe RG57, metalaxyl sensitivity, and aggressiveness to tomato and potato. Spatial patterns of P. infestans genotypes were analyzed by geographical information systems and geo-statistics during the seasons of 1994-95, 1995-96, and 1996-97. Spatial analysis of the genetic structure of P. infestans indicates that geographic substructuring of this pathogen occurs in this area. Maps displaying the probabilities of occurrence of mating types and genotypes of P. infestans, and of disease severity at a regional scale, were presented. Some genotypes that exhibited differences in epidemiologically important features such as metalaxyl sensitivity and aggressiveness to tomato and potato had a restricted spread and were localized in isolated areas. Analysis of late blight severity showed recurring patterns, such as the earliest onset of the disease in the area where both potato and tomato were growing, strengthening the hypothesis that infected potato tubers are the main source of primary inoculum. The information that geostatistical analysis provides might help improve management programs for late blight in the Del Fuerte Valley.     

Phytophthora infestans in a subtropical region: survival on tomato debris, temporal dynamics of airborne sporangia and alternative hosts

Little is known about inoculum dynamics of late blight caused by Phytophthora infestans in tropical/subtropical areas, particularly in Brazil. The objectives of the present study were to assess (i) the survival of the pathogen on stems, leaflets and tomato fruits, either buried or not in soil; (ii) the pathogenicity of P . infestans to mostly solanaceous plant species commonly found in Brazil that could act as inoculum reservoir; and (iii) the temporal dynamics of airborne sporangia. Phytophthora infestans survived in tomato plant parts for less than 36 days under greenhouse and field conditions. In greenhouse tests, pathogen structures were detected earlier on crop debris kept in dry than in wet soil conditions. Isolates of two clonal lineages of P. infestans , US-1 from tomato, and BR-1 from potato, were inoculated on 43 plant species. In addition to potato and tomato, Petunia  ×  hybrida and Nicotiana benthamiana were susceptible to the pathogen. Airborne inoculum was monitored with Rotorod and Burkard spore traps as well as with tomato and potato trap plants. Sporangia were sampled in most weeks throughout 2004 and in the first two weeks of 2005. Under tropical/subtropical conditions, airborne inoculum is abundant and is more important to late blight epidemics than inoculum from crop debris or alternative hosts.     

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.     

Host diversity can reduce potato late blight severity for focal and general patterns of primary inoculum

ABSTRACT The use of host diversity as a tool for management of potato late blight has not been viewed as promising in the past. But the increasing importance of late blight internationally has brought new consideration to all potential management tools. We studied the effect of host diversity on epidemics of potato late blight in Oregon, where there was little outside inoculum. The experimental system consisted of susceptible potato cv. Red LaSoda and a highly resistant breeding selection, inoculated with local isolates of US-8 Phytophthora infestans. Potatoes were grown in single-genotype plots and also in a mixture of 10 susceptible and 26 resistant potato plants. Half of the plots received inoculation evenly throughout the plot (general inoculation) and half received an equal quantity of inoculum in only one corner of the plot (focal inoculation). The area under the disease progress curve (AUDPC) was greater in single genotype stands of susceptible cv. Red LaSoda inoculated throughout the plot than with stands inoculated in one focus. The host-diversity effect on foliar late blight was significant in both years of the investigation; the AUDPC was reduced by an average of 37% in 1997 and 36% in 1998, compared with the mean disease level for the potato genotypes grown separately. Though the evidence for influence of inoculum pattern on host-diversity effects was weak (P = 0.15), in both years there was a trend toward greater host-diversity effects for general inoculation. Statistical significance of host-diversity effects on tuber yield and blight were found only in one of the two years. In that year, tuber yield from both the resistant and susceptible cultivar was increased in mixtures compared with single genotype stands and tuber blight was decreased in mixtures for susceptible cv. Red LaSoda.     

Influence of host diversity on development of epidemics: an evaluation and elaboration of mixture theory

ABSTRACT A spatiotemporal/integro-difference equation model was developed and utilized to study the progress of epidemics in spatially heterogeneous mixtures of susceptible and resistant host plants. The effects of different scales and patterns of host genotypes on the development of focal and general epidemics were investigated using potato late blight as a case study. Two different radial Laplace kernels and a two-dimensional Gaussian kernel were used for modeling the dispersal of spores. An analytical expression for the apparent infection rate, r, in general epidemics was tested by comparison with dynamic simulations. A genotype connectivity parameter, q, was introduced into the formula for r. This parameter quantifies the probability of pathogen inoculum produced on a certain host genotype unit reaching the same or another unit of the same genotype. The analytical expression for the apparent infection rate provided accurate predictions of realized r in the simulations of general epidemics. The relationship between r and the radial velocity of focus expansion, c, in focal epidemics, was linear in accordance with theory for homogeneous genotype mixtures. The findings suggest that genotype mixtures that are effective in reducing general epidemics of Phytophthora infestans will likewise curtail focal epidemics and vice versa.     

Populations of Phytophthora infestans in Israel Underwent Three Major Genetic Changes During 1983 to 2000

ABSTRACT In this survey, 799 isolates of Phytophthora infestans collected from potato crops in Israel during 1983 to 2000 were analyzed for mating type and sensitivity to metalaxyl, and 324 were analyzed for race structure. The A(2) mating type, first recorded in 1983, fully dominated the pathogen population from 1983 until 1991 (9 years). It was thereafter replaced by the A(1) mating type, which dominated the population during 1993 to 2000. Metalaxyl-resistant isolates were first recorded in 1982. During 1983 to 1991, the majority of the isolates were resistant. Isolates with intermediate sensitivity (I) to this fungicide were first observed in 1993, when both A(1) and A(2) mating types occurred in the population. The proportion of I isolates gradually increased, reaching 39 to 41% in 1997 to 1998, and then declined to approximately 15% in 1999 to 2000. Pathogenicity to nine potato differential cultivars was determined for 80 potato isolates collected in 1983 to 1991, to 11 potato differentials in 173 isolates collected in 1993 to 1998, and in 71 potato isolates collected in 1999 to 2000. The first population was composed of 5 races with race 1,3,4,7,8,10 predominating (76%), the second population was composed of 19 races with race 1,3,4,7,8,10,11 predominating (63%), and the third population exhibited 42 (34 new) races with no single predominating race. RG-57 DNA fingerprinting and allozymes loci assays of 23 isolates revealed that isolates collected during 1984 to 1986 belonged to the PO-57 lineage, whereas those collected during 1997 to 1999 belonged to the RFO-39 lineage. Among isolates collected during 1993 to 1995, two unreported DNA fingerprinting patterns were found. Severe late blight epidemics occurred in tomato crops during 1998 to 2000. Of 35 tomato isolates, 28 were A(1) and only 7 were A(2). Of these tomato isolates, 94% were sensitive to metalaxyl. Almost every isolate had a different race structure on the 11 potato differentials. When inoculated onto three tomato differential cultivars, tomato isolates showed a virulence much more enhanced than potato isolates. The data suggest the Israeli population of P. infestans has passed through three major genetic changes during the past 18 years: in 1983, 1993, and 1999. The recent change included host specialization to tomato.     

Phytophthora infestans: populations,pathogenicity and phenylamides

Isolates of Phytophthora infestans (Mont) de Bary (the potato and tomato late blight pathogen) resistant to phenylamides appeared in Europe and North America in the late 1970s and early 1990s respectively. Concurrent, but coincidentally, with both these events there were radical structural shifts in the pathogen populations as immigrant genotypes from Mexico displaced the indigenous populations. Both A1 and A2 mating type isolates are now present in blighted crops, permitting alternative inoculum via germinating sexually produced oospores to influence dynamics of late blight populations. Studies of inheritance of ploidy, host-specific pathogenicity, mating type and resistance to antibiotics and phenylamide fungicides have provided insight into mechanisms of variation in this potent pathogen.     

Multi‐scale modelling of infection pressure from Phytophthora infestans*

Management of potato late blight could benefit from prediction of the risk posed to potato fields from external inoculum sources of Phytophthora infestans. Influx of inoculum depends on a complex interplay of population biological, atmospheric and spore survival processes, and is difficult to predict. This research aims at building tools for such prediction. BLIGHTSPACE is a spatio‐temporal model (parameterized for potato late blight) that has been developed and utilized to study the progress of epidemics in individual fields and networks of fields. A quasi‐Gaussian plume model was developed to provide long‐range transport of spores within BLIGHTSPACE. Numerical results compared favorably with experimental data. A further submodel for the survival of spores during long‐range transportation has been added. Integration of these three submodels will create an experimental arena for comparing control options for potato late blight.     

Development of natural late blight epidemics in pure and mixed plots of potato cultivars with different levels of partial resistance

Late blight, caused by Phytophthora infestans , is the most severe disease of potato worldwide. Controlling late blight epidemics is difficult, and resistance of host cultivars is either not effective enough, or too easily overcome by the pathogen to be used alone. In field trials conducted for 3 years under natural epidemics, late blight severity was significantly lower in a susceptible cultivar growing in rows alternating with partially resistant cultivars (mixtures) than in unmixed plots of the susceptible cultivar alone. Partially resistant cultivars behaved similarly in unmixed and mixed plots. Mixtures of cultivars reduced disease progress rates and sometimes delayed disease onset over unmixed plots, but did so significantly only for the slowest epidemic. This suggests that reduction of area under the disease progress curve (AUDPC) in mixtures resulted from the cumulative action of minor effects. Disease distribution was focal in all plots at all dates, as shown by Morisita's index values significantly exceeding 1. Significant yield increases for the susceptible cultivar, and occasionally for the partially resistant ones, were observed in mixed-cultivar plots compared with single-cultivar plots. These results show that cultivar mixtures can significantly reduce natural, polycyclic epidemics in broadleaved plants attacked by pathogens causing rapidly expanding lesions.     

Phenotypic and genetic variation in Finnish potato-late blight populations, 1997–2000

This study was conducted on potato late blight samples collected for monitoring early attacks in Finland from 1997 to 2000. Most of the 1726 Phytophthora infestans isolates were collected soon after the onset of the epidemics. Most of the isolates were tested for mating type as well as metalaxyl and propamocarb hydrochloride (HCl) sensitivity, while virulence on potato R-gene differentials and mitochondrial DNA (mtDNA) haplotype were determined for a subset of the isolates. In half of the fields from which more than one isolate was tested, both mating types were detected, indicating strong potential for sexual reproduction. The mating types coexisted more often in organic fields or gardens than in conventional fields. The proportion of A1 mating type decreased from approximately 80% (1997 and 1998) to 22% by the year 2000. Simultaneously, the proportion of isolates resistant to metalaxyl decreased from approximately 40% to 16%. Resistance to metalaxyl was confined to the IIa mtDNA haplotype and clearly associated with the A1 mating type, as resistance was 10 times more common among A1 isolates than among A2 isolates. Resistance to metalaxyl therefore probably derives from common descent from an isolate with the IIa haplotype. Most of the regional variation in metalaxyl sensitivity was also linked to mating type, as both metalaxyl resistance and the A1 mating type were most common in the north and south-west of Finland. In contrast to metalaxyl, only three propamocarb-HCl-insensitive isolates were found, but propamocarb-HCl sensitivity decreased significantly during the study.     

Can weed hosts increase aggressiveness of Phytophthora infestans on potato?

Potato late blight, caused by Phytophthora infestans, is a major disease in potato production throughout the world. In southern Sweden, hairy nightshade (Solanum physalifolium), an alternative non-crop host to the pathogen, is an increasing weed problem. Single-lesion leaves infected by P. infestans were collected from potato and hairy nightshade to determine phenotypic and genotypic population differentiation of P. infestans between the two hosts. Genotypic variation was estimated using microsatellites as markers. The results showed no genotypic differentiation in the samples between the two hosts. Aggressiveness tests were performed using the sampled isolates to cross-inoculate potato and hairy nightshade. The proportion of infected leaves, latency period, lesion growth rate, and sporulation capacity were measured. For isolates from hairy nightshade, the odds of infection were higher on both hosts combined. When tested on potato leaves, isolates from hairy nightshade showed a significantly shorter latency period and higher sporulation capacity compared with isolates from potato. This indicates that an alternative host can filter populations of P. infestans toward a higher aggressiveness, which could lead to increasing problems in controlling potato late blight.     

Stability of partial resistance in potato cultivars exposed to aggressive strains of Phytophthora infestans

Potato cultivars were evaluated for their resistance responses to aggressive strains of Phytophthora infestans in field and laboratory experiments. Analysis of variance revealed differential cultivar-by-isolate interactions for both foliar and tuber blight resistance. Differential responses occur as revealed by specific susceptibilities of cultivars to certain pathogen genotypes and changing rank order. In general, severity of late blight epidemics as observed in the haulms did not correlate well with foliar blight resistance ratings as presented in the National List of Recommended Potato Varieties. No significant correlation was found between tuber blight incidence under field conditions and the tuber blight rating in the National List. Also, there was no relation between the field and laboratory tuber blight resistance assessments. A significant association was demonstrated between late blight infection in the foliage and tuber blight incidence under field conditions. The presence of differential interaction, independent of R-gene-based resistance, indicates some adaptation of P. infestans to partial resistance and consequently adverse effects on the stability and durability of partial resistance to potato late blight.     

Prediction studies supported by computer on potato late blight in central Anatolia in Turkey*

Prediction of potato late blight epidemics, caused by Phytophthora infestans (Mont) de Bary, was studied in three different villages of Bolu Province having large potato growing areas with the Winstel and Ullrich Schrodter models in the years 2002–05. During these years, a late blight outbreak was observed only in 2005 with the disease being less apparent in the other years. The Ullrich Schrodter model was found to poorly predict potato late blight epidemics in 2005. The Winstel model gave first warnings too early but correctly predicted late infections. Both the A1 and A2 mating types were found in Central Anatolia for the first time, in Bolu province.     

Efficacy of the R2 resistance gene as a component for the durable management of potato late blight in France

Many race-specific resistance genes to potato late blight are overcome in France, but the disease appears later on genotypes carrying the R2 gene. This study examined whether R2 could contribute to durable late-blight control in France, and analysed the conditions of its performance. Plants grown from tubers of different physiological ages showed no difference in R2 expression in field and climate-chamber experiments, demonstrating that the delay in epidemic onset provided by R2 was not the result of gene inactivation in old plants. Among isolates collected at one site, those virulent on R2 were classified into three AFLP profiles. AFLP-VII comprised exclusively isolates virulent to R2 , whereas AFLP-IV and AFLP-V included both virulent and avirulent isolates. No significant aggressiveness differences were observed between virulent and avirulent isolates from AFLP-V; however, isolates from AFLP-VII were significantly less aggressive than virulent isolates from AFLP-V. These results indicate that: (i) the delayed onset of epidemics on R2 cultivars is the result of the breakdown of R2 by virulent isolates; (ii) aggressiveness of isolates virulent to R2 depends primarily on the genetic background of the pathogen where the mutation to virulence occurs; and (iii) this mutation does not lead per se to lower pathogenic fitness. It is suggested that R2 is unlikely to make a lasting contribution to late-blight control in France, and that diversification strategies such as cultivar mixtures might not considerably increase its durability.     

Variation in populations of Phytophthora infestans in Finland and Norway: mating type, metalaxyl resistance and virulence phenotype

Phytophthora infestans was isolated from potato leaves and tubers collected from different parts of Finland in 1990–96 and Norway in 1993–96. Isolates were assessed for mating type, resistance to metalaxyl and virulence phenotype. In Finland 15% of 200 isolates tested and in Norway 25% of 642 tested were A2 mating type. Differences in the A1/A2 ratio were evident among regions and A2 was not found in northern areas. In Finland the frequency of metalaxyl-resistant isolates, among 1834 tested, decreased from 59% in 1990–95 to 2% in 1996. In Norway 59% of 491 isolates tested were resistant to metalaxyl in 1996. Among 269 Finnish and 105 Norwegian isolates, all known virulence genes were found in both countries and race 1.3.4.7.10.11 was the most common (resistance gene R9 was not included in the differential set). Oospores were observed in potato leaves from three locations in the southern part of Norway. The implications of the 'new' populations in the Nordic countries are discussed.     

Resistance to acylalanines in Phytophthora infestans in The Netherlands1

In The Netherlands in 1980 a severe late-blight epidemic involving metalaxyl-resistant strains of Phytophthora infestans did considerable damage to the potato crop. As a consequence metalaxyl or metalaxyl-containing products were withdrawn from the Dutch fungicide market for the control of potato late blight. In 1981 the majority of the P. infestans isolates obtained from various parts of the country were sensitive to metalaxyl. In three areas where metalaxyl mixtures were used on a relatively large scale metalaxyl-resistant strains dominated the population. Incidental use of metalaxyl mixtures in 1982 and 1983 showed adequate late-blight control and, when in 1984 an early and in some areas severe epidemic developed, a metalaxyl/mancozeb mixture was reintroduced for curative application in combination with conventional fungicides. Although disease control was adequate, resistant strains were present in a small number of fields. Whether resistant strains will increase in frequency and threaten the usefulness of mixtures of acylalanines will heavily depend on how well potato farmers adopt strategies involving a limited use of mixtures of acylalanines in a spray schedule with conventional late-blight fungicides.     

Development of a species-specific and sensitive detection assay for Phytophthora infestans and its application for monitoring of inoculum in tubers and soil

A specific and sensitive PCR assay for the detection of Phytophthora infestans , the cause of late blight of potato, in soil and plant tissues was developed. A P. infestans -specific primer pair (INF FW2 and INF REV) was designed by comparing the aligned sequences of rDNA internal transcribed spacer regions of most of the known Phytophthora species. PCR amplification of P. infestans DNA with primers INF FW2 and INF REV generated a 613 bp product, and species specificity was demonstrated against DNA from nine other Phytophthora species and seven potato-blemish pathogens. In a single-round PCR assay, 0·5 pg pure P. infestans DNA was detectable. Sensitivity was increased to 5 fg DNA in a nested PCR assay using Peronsporales-specific-primers in the first round. As few as two sporangia or four zoospores of P. infestans could be detected using the nested assay. Procedures are described for detection of P. infestans in leaves, stem and seed potato tubers before expression of symptoms. A soil assay in which 10 oospores per 0·5 g soil were detectable was developed and validated using samples of field soil. The PCR assay was used to examine the long-term survival of sexual (oospores) and asexual (sporangia and mycelium) inoculum of P. infestans in leaf material buried in a replicated experiment under natural field conditions. Oospores were consistently detected using the PCR assay up to 24 months (total length of the study) after burial in soil, whereas the sporangial inoculum was detected for only 12 months after burial. Sporangial inoculum was shown to be nonviable using a baiting assay, whereas leaf material containing oospores remained viable up to 24 months after burial.