Abstract in Spanish

About the Author

William E. Fry has been a plant pathologist on the faculty of Comell University since 1971, where his efforts have focused on late blight and on Phytophthora infestans. Epidemiological studies have included incorporation of host resistance into standard and forecast- assisted disease management. Hs lab has used field studies and a complex computer simulation model of the late blight disease to identify and evaluate approaches and to improving the efficiency of disease management. For the past 15 years his lab has investigated the genetics/population genetics of P. infestans and has been particularly interested in detecting migrations of this pathogen. He was chairman of the Department of Plant Pathology at Comell from 1981 to 1995, and is currently immediate (1996-1997) past president of the American Phytopathological Society.

Epidemiology

William E. Fry
Plant Pathology Department
Cornell University

The epidemiology of Phytophthora infestans and of potato has been investigated for the past 150 years. As result, we know much about the factors that influence this disease. There have been many research publications, reviews and books devoted to this topic. An introduction to this literature is found in recent reviews and books (2,8,17,19). Current concepts and explanations have evolved from the earlier studies. However, some of the earlier studies seem to retain their value for current application. Among these are the comprehensive studies of Crosier and Van der Zaag (6,27) which have utility not only for the basic information, but also for comparative purposes. Crosier’s study provided much basic information on the influence of abiotic factors (e.g., temperature and moisture) on the various stages of pathogenesis and pathogen development. Van der Zaag’s study provided additional information on these influences, but also on the factors influencing establishment from various sources of the pathogen.

A short discussion cannot be comprehensive over the entire subject of the epidemiology of P. infestans and potato late blight, therefore my focus is to evaluate the thesis that in the United States and Canada a new heterogeneous population of P. infestans implies a more diverse epidemiology of late blight. If central Mexico is the origin of new populations (25), this thesis cannot apply to Mexico. The discussion will follow the disease cycle in a seasonal agriculture: a) between season survival; b) establishment and resultant foliar and tuber disease; c) aerial dispersal. However, the concept of clonal lineages of P. infestans is crucial to evaluation of the thesis, so this concept is first evaluated.

Clonal lineages. Clonal lineages have been discussed by Anderson and Kohn (1), and a paraphrase of their definition of a clonal lineage is useful: ‘the asexual descendants of a given genotype differing from the originator only via mutation and mitotic recombination’. Clonal lineages are a useful concept for organisms with asexual reproduction and with very simple homogeneous population structures so that the individual lineages can be identified. Goodwin et al. have defined several clonal lineages of P. infestans in the United States and Canada (11,12,14-16). These lineages are based on diverse genetic markers: mating type (A1, A2); two (or three markers) for the Glucose-6-phosphate isomerase (Gpi) allozyme locus; two markers for the Peptidase (Pep) allozyme locus; and 25 markers identified by RFLP probe RG57. The most commonly occurring lineages in the United States and Canada during the last several years are identified in Table 1.

Table 1. Clonal lineages of Phytophthora infestans detected in the United States and Canada. US-1, UDS-6, US-7, and US-8 have been locally predominant, and US-8 has been nationally predominant since 1995

¹ MT is the mating type (A1 or A2).
² met refers to metalaxyl sensitivity: S = sensitive; R= resistant.
³ Spec refers to pathogenic specialization. Some isolates are primarily pathogens of potatoes (P), and others are pathogens of both potatoes and tomatoes (P-T). The US-1 clonal lineage contained a few individuals that were pathogenic on both potatoes and tomatoes, but most were pathogenic mainly on potatoes.
⁴ Dates refers to the time during which these lineages were common. The US-1 clonal lineage seems rare since 1993. The US-6 lineage has declined in frequency since 1993.

These clonal lineages have utility because certain epidemiological traits are associated with specific lineages. For example isolates of the US-1 lineage have been largely sensitive to metalaxyl, and metalaxyl retains its excellent activity in suppressing established epidemics caused by US-1. However, isolates in the US-6, US-7, and US-8 lineages are largely much less affected by metalaxyl, and the efficacy of metalaxyl in suppressing epidemics caused by these lineages is largely eliminated (16). Additionally, isolates in the US-6 and US-7 lineages are especially aggressive to tomatoes and knowledge that an isolate of either of these lineages is in an area is especially important for tomato growers.

While isolates within a lineage are more similar to each other than to isolates in other lineages, there is some diversity within lineages for specific traits. Diversity increases with the number of asexual generations, because this increases the opportunity for accumulation of mutations and mitotic recombination events. As illustration, both Goodwin et al, and Sujkowski et al. found greater diversity for pathotype in "older" lineages than in "younger" lineages (15,26).

The clonal lineage concept in the United States and Canada has considerable utility as long as the population structure remains fairly simple. During the early 1990s, there were generally four lineages that were predominant but with temporal and spatial diversity. For example US-6 was common in the early 1990s, especially in the west. But after 1993, US-7 and US-8 became predominant – first in the eastern United States, but subsequently US-8 became dominant throughout most of the United States and Canada. The predominant lineages could be distinguished via analysis of the Gpi locus (13). Because most (but not all) epidemic populations were homogeneous for lineage, analysis of a few isolates from a field could provide indication of important epidemiologically important traits. With additional introduction of new strains or with significant sexual reproduction, the clonal lineage concept will be less useful, because it will be difficult to characterize a large number of new lineages, and because it will become more difficult to use simple technology to identify new strains.

Prior to the introduction of the US-6, US-7, and US-8 clonal lineages, populations of P. infestans were dominated by the US-1 clonal lineage (11,12), and this lineage was characterized by traits that are different from those in the US-6, US-7 and US-8 clonal lineages. The decline in frequency of the US-1 clonal lineage and the predominance of more lineages that differ from each other and from the US-1 lineage indicate that there is now greater genetic diversity in populations of P. infestans in the United States. With this phenomenon established, we can investigate the ways in which this diversity might influence the epidemiology of late blight.

Between-season survival. P.infestans survives between seasons in a variety of ways in the potato agro-ecosystem. It survives in stored tubers that will be used as seed, in infected potatoes that are stored between seasons and that will be discarded prior to or during the next season (some of these potatoes are discarded in piles [cull piles]), in infected tubers that are not harvested and survive the between season period in the soil producing "volunteer" potatoes the next season, and perhaps eventually in the United States and Canada as oospores resulting from mating between A1 and A2 strains. Will the greater diversity of P. infestans populations that now exist in Canada and the United States lead to greater diversity in between season survival?

It is now abundantly clear from observation and from experiment that the US-8 clonal lineage is especially aggressive against potato tubers and tubers are more likely to become infected when foliar disease is caused by US-8 rather than with the US-1 clonal lineage (10,21). Thus, tubers are more likely to be infected than previously and this includes seed tubers. Additionally, the resultant greater probability of tuber infections means that cull piles with infected tubers are more likely and that tubers left in the field after harvest are also more likely to be infected. This greater likelihood of tuber infections may translate to greater chance for inoculum to be available in potato production areas. However, it now seems clear that the probabilities will be different for different lineages. For example the US-8 lineage is more likely to kill sprouts than is the US-1 lineage (22). Differences among lineages seems likely to lead to greater diversity of epidemiology within the potato - late blight pathosystem. The epidemiological impact of the apparently competing (and compensating?) effects of greater probability of infection and greater probability of sprout mortality caused by US-8 relative to US-1 is currently unknown and should be investigated.

In addition to survival in infected potatoes, survival as oospores is possible in local regions in Canada and the United States. This survival mechanism is only recently possible north of Mexico, because both mating types have been only recently widely distributed north of Mexico. Although possible in several locations, the probability of oospore survival is not yet known. Despite the lack of certainty of occurrence, we need to understand factors that influence oospore survival and we need to develop quantitative understanding of the potential role of oospores in the epidemiology of late blight. It is now clear from observation and experiment that some crosses involving strains of P. infestans currently in Canada and the United States can yield viable oospores that germinate to yield viable recombinant progeny (28). Fortunately, it appears that most matings yield very few progeny. The viable oospores seem quite capable of surviving winter soil temperatures in most production regions. Using several diverse crosses between US-1, US-6, US-7, and US-8, Fay and Fry (9) determined that oospores survived termperatures from -20 C to 43C in laboratory tests. These data are similar to other studies with other Phytophthora species and to other P. infestans studies.

Thus, it seems likely that the new strains will create greater diversity of between-season survival. Survival can be as mycelium associated with living plant parts and eventually also via oospores.

Establishment/foliar and tuber disease. One of the outstanding questions in the epidemiology of potato late blight concerns the probability of infected seed tubers giving rise to foliar infections in the subsequent crop. Whereas it is quite clear that infected seed tubers are responsible for long distance dispersal of P. infestans, the probability of success seems very low. Van der Zaag (27) summarized seventy-five years of research on this topic and demonstrated that in the vast majority of cases successful establishment of P. infestans in a crop from infected seed tubers occurred at a rate ranging from 0 to 1-2% of the infected tubers giving rise to foliar infections. Studies in the 1980s provided similar findings (7). However, all of these studies were presumably done with the US-1 clonal lineage, and it is currently unknown whether the greater tuber pathogenicity of US-8 would alter the success rate of establishment. It is even conceivable that the greater tuber pathogenicity might lower the rate of successful field establishment. In controlled tests, emergence of shoots from tubers infected with US-8 was less likely than from tubers infected with US-1 (22). Another source of initial inoculum for late blight is infected tubers in piles of cull potatoes(4,27). The cull pile may have survived the winter from the previous season, or the cull pile may have been created during the spring when the potato storage was cleaned. Sometimes piles of infected cull potatoes occur in unexpected places such as in piles of rocks dumped from the harvesting process or from "rock picking." The greater pathogenicity of US-8 relative to US-1 seems to have heightened the importance of cull piles as sources of P. infestans now relative to just a few years ago in the United States and this source has received much deserved publicity in cooperative extension education programs throughout the United States and Canada. (3). Quantification of the greater probability would be helpful to disease management.

Heightened pathogenicity of the US-8 clonal lineage relative to the US-1 clonal lineage appears also to have contributed to the successful establishment of this lineage in potato fields. Studies in several locations conclude that US-8 has greater pathogenicity to potatoes than does US-1 (20,23). Other new strains might have similar heightened pathogenicity (P. Hamm, personal communication).

The heightened pathogenicity might increased the "establishment rate" of new lineages in at least two ways. The first is via "stem infections." Stem infections seem from observation by persons throughout the United States and Canada to be associated with the new lineages. Van der Zaag demonstrated that under conditions marginal for P. infestans germination, successful infections of axils were more likely than of leaf blades (27). Comparisons between US-8 and US-1 to determine if US-8 can infect axils more rapidly than US-1 seem warranted. A second mechanism by which US-8 might establish more readily than US-1 is if it can grow more rapidly. Simulation experiments with a complex computer simulator of the late blight disease (5) indicated that suppression of epidemics by US-8 would require more frequent applications of protectant fungicide than were required to suppress epidemics caused by US-1 to the same level (M. Kato, E. S. G. Mizubuti, W. E. Fry, unpublished results).

The facts that there are now a diversity of clonal lineages throughout the United States and Canada, and that these lineages have detectable foliar and tuber pathogenicity differences provides additional evidence that the epidemiology of late blight in the United States and Canada will be more diverse in the future than it was prior to the introduction of the new strains.

The basic responses of the recently introduced lineages to temperature, moisture and other abiotic factors need to be determined. Preliminary studies at Cornell have indicated that germination of US-7 and US-8 differ from US-1 in response to temperature (E. S. G. Mizubuti, unpublished). The US-1 clonal lineage responded similarly as described by Crosier (6) in 1934, who was presumably also working with US-1. Surprisingly, the US-7 and US-8 clonal lineages did not germinate so well at temperatures from 15 to 20 C as did the US-1 clonal lineage. Thus it seems that diversity in response to at least some abiotic factors will also lead to greater diversity in the epidemiology of late blight.

In some other respects, the recently introduced clonal lineages appear similar to US-1. In a series of field tests, US-1 and "new" lineages ranked potato cultivars in the same order (18). This is good news because it means that although the resistances might be associated with higher levels of disease caused by new lineages, cultivars that previously were regarded as less susceptible, will still be relatively less susceptible. Thus adjustment of management intensity to complement previously determined host resistance will likely be reasonably accurate. Similarly, the sensitivities of new lineages to mancozeb and chlorothalonil seem to be the same as that of US-1 (20).

Dispersal. The aerial transport of P. infestans deserves considerably more investigation than it has received. Van der Zaag (27) demonstrated that sporangia could be transported by at least 11 km through the air. Crosier and Minogue demonstrated that sporangia could survive several hours in unsaturated atmospheres at a variety of temperatures (6,24). Survival was shortened by decreasing moisture and by increasing temperature. However, these studies were done with old clonal lineages, and the recently introduced lineages might differ in their responses.

Anecdotal stories of new lineages of P. infestans being carried from one location to another warrant investigation. Growers have indicated that sporangia of the new lineages can be carried on ground spray equipment, because the first late blight they have seen has been in the wheel rows of the sprayer that came from an affected field into a previously unaffected field. Some growers in Maine indicated that they could identify the path of a moose that wandered through a "hot spot" and beyond. The path became the next hot spot of late blight. Other growers in northeastern US have indicated that deer paths through potato fields similarly have been detectable. If these observations reflect different survival abilities of the new lineages relative to the old lineages, the differences need to be quantified and incorporated into management considerations.

Conclusions

This consideration of the impact of new lineages on the epidemiology of late blight in Canada and the United States indicates that there is now greater diversity within the population of there was P. infestans in Canada and the United States than prior to the 1990s. The new lineages differ from old lineage(s) in some but not all epidemiologically important aspects. The occurrence of several lineages implies that there will be some diversity in the epidemiology of the disease.

The implications to plant pathologists are that the differences need to be identified, quantified and incorporated into management recommendations. The investigations recommended by the Epidemiology working group at the North American Potato Late Blight Workshop need to be initiated as quickly as possible so that the damage caused by new lineages can be limited through knowledgeable actions.

References

1. Anderson, J. B., and Kohn, L. M. 1995. Clonality in solborne, plant-pathogenic fungi. Annu. Rev. Phytoopathol. 33:369-391.

2. Andrivon, D. 1995. Biology, ecology, and epidemiology of the potato late blight pathogen Phytophthora infestans in soil. Phytopathology 85:1053-1056.

3. Anonymous. 1996. Breaking down cull piles. Crop Protection Manager November 1996:7-9.

4. Bonde, R., and Schultz, E. S. 1943. Potato refuse piles as a factor in the dissemination of late blight. Bull. 416 Maine Agr. Exp. Stn., Orono: 229-246.

5. Bruhn, J. A., and Fry, W. E. .1981. Analysis of potato late blight epidemiology via simulation modeling. Phytopathology 71:612-616.

6. Crosier, W. 1934. Studies in the biology of Phytophthora infestans (Mont) de Bary. Cornell University Agricultural Experiment Station, Ithaca, NY(Memoir 155).

7. Doster, M. A., and Fry, W. E. 1987. Influence of host resistance on the initial appearance of foliar late blight of potato from infected seed tubers. Phytopathology 77:1614.

8. Erwin, D. C., and Ribeiro, O. K. 1996. Phytophthora Diseases Worldwide. American Phytopathological Society, St. Paul, MN.

9. Fay, J. C., and Fry, W. E. 1996. Effects of hot and cold temperatures on the survival of oospores produced by United States strains of Phytophthora infestans. (Abstr.) Phytopathology 86:S121.

10. Fry, W. E., and Goodwin, S. B. 1997. Resurgence of the Irish Potato Famine Fungus. Bioscience: (in press).

11. Goodwin, S. B., Cohen, B. A., Deahl, K. L., and Fry, W. E. .1994. Migration from northern Mexico was the probable cause of recent genetic changes in populations of Phytophthora infestans in the United States and Canada. Phytopathology 84:553-558.

12. Goodwin, S. B., Cohen, B. A., and Fry, W. E. 1994. Panglobal distribution of a single clonal lineage of the Irish potato famine fungus. Proc. Nat'l. Acad. Sci USA 91:11591-11595.

13. Goodwin, S. B., Schneider, R. E., and Fry, W. E. 1995. Use of cellulose-acetate electrophoresis provides rapid identification of allozyme genotypes of Phytophthora infestans. Plant Dis.79:1181-1185.

14. Goodwin, S. B., Sujkowski, L. S., Dyer, A. T., Fry, B. A., and Fry, W. E. .1995. Direct detection of gene flow and probable sexual reproduction of Phytophthora infestans in northern North America. Phytopathology 85:473-479.

15. Goodwin, S. B., Sujkowski, L. S., and Fry, W. E. 1995. Rapid evolution of pathogenicity within clonal lineages of the potato late blight disease fungus. Phytopathology 85:669-676.

16. Goodwin, S. B., Sujkowski, L. S., and Fry, W. E. 1996. Widespread distribution and probable origin of resistance to metalaxyl in clonal genotypes of Phytophthora infestans in the United States and western Canada. Phytopathology 86(7):793-800.

17. Harrison, J. G. 1992. Effects of the aerial environment on late blight of potato foliage -- a review. Plant Pathol. 41:384-416.

18. Inglis, D. A., Johnson, D. A., Legard, D. E., Fry, W. E., and Hamm, P. B. 1996. Relative resistances of potato clones in response to new and old populations of Phytophthora infestans. Plant Dis. 80:575-578.

19. Ingram, D. S., and Williams, P. H. 1991. Phytophthora infestans, The Cause of Late Blight of Potato. London, Academic Press.

20. Kato, M., and Fry, W. E. .1995. Fitness components and tolerance to mancozeb among genotypes of Phytophthora infestans in the United States. Phytopathology 85:1131.

21. Lambert, D. H., and Currier, A. I. 1997. Differences in tuber rot development for North American clones of Phytophthora infestans. Am. Potato J. (in press).

22. Marshall, K. D., and Stevenson, W. R. 1996. Transmission of Phytophthora infestans from infected seed potato tubers to developing sprouts. Am. Potato J. 73:370-371.

23. Miller, J. S., Johnson, D. A., and Hamm, P. B. 1995. Aggressiveness of Phytophthora infestans isolates in the Pacific Northwest. Phytopathology 85: (Abstr. in press).

24. Minogue, K. P., and Fry, W. E. 1981. Effect of temperature, relative humidity and rehydration rate on germination of dried sporangia of Phytophthora infestans. Phytopathology 71:1181-1184.

25. Niederhauser, J. S. 1991. Phytophthora infestans: The Mexican Connection . Pages 25-45 in: Phytophthora. Cambridge University Press, Cambridge.

26. Sujkowski, L. S., Goodwin, S. B., and Fry, W. E. 1996. Changes in specific virulence in Polish populations of Phytophthora infestans: 1985-1991. European Journal of Plant Pathology 102:555-561.

27. van der Zaag, D. E. 1956. Overwintering en epidemiologie van Phytophthora infestans, tevens enige nieuwe bestrijdingsmogelijkheden." Tijdschrift over Plantenziekten 62:89-156.

28. Yun Lee, T. and Fry, W. E. 1994. Genetic Control of Aggressiveness to tomato in Phytophthora infestans. (Abstr.) Phytopathology 84:1372.

Epidemilogia

W. E. Fry

La tesis para esta presentacion es muy nuevo, las poblaciones heterogeneas de Phytophthora infestans en los Estados Unidos y Canada esta creando un problema nuevo y una epidemiologia muy heterogenea del tizon tardio. Poblaciones de P.infestans en muchas localidades de los Estados Unidos y del Canada actualmente estan compuestos de un pequeno numero de linajes de clones. El linaje clon US-8 ha estado ampliamente distribuido y de importancia epidemiologica. Estos linajes estan definidos en base a tipo de apareamiento, isomeros de Glucosa-6 fosfato(Gpi) y genotipos de pectidasa (Pep) y impresiones de DNA (determinado con el probador RG57). Analices de Gpi con electroforesis de acetato de celulosa ha probado ser un metodo rapido y corto para una primera evluacion del linaje. La diversidad dentro de un lineaje clonal para factores especificos de compatibilidad, sensibilidad a metalaxil, adaptacion de hospedero, agresividad, y reaccion a factores abioticos son mucho menores que la diversidad entre lineajes- permitiendo importantes abances de predicciones epidemiologicas del conocimiento del lineaje. Sin embargo, existe ahora muchos lineajes a traves de los EEUU y Canada, comparado con los anos anteriores a 1980, donde la poblacione de los EEUU y Canada estuvieron dominados por el lineaje clonal de US-1. Hay muy pocas localidades de los EEUU y Canada donde las poblaciones ahora son muy diversas donde reproduccion sexual o la introduccion de diversidad de lineajes es postulado. El concepto de linaje es muy utilizado solamente cuando largas poblaciones son dominados por un numero pequeno de linajes.

Comparaciones iniciales indican que algunos de los nuevos linajes difieren en importantes caracteristicas del linaje clonal US-1. Podria haber tambien diversidad entre los "nuevos" linajes clonales. Por ejemplo US-8 se ha estado caracterizando ser un patogeno mas agresivo en tuberculos y en las hojas de las papas que US-1. Sin embargo, US-1 y los nuevos linajes estan en el rango de una resistencia relativa. Esto parece ser que algunos nuevos linajes responden diferentemente a algunos factores abioticos comparado con US-1. Por ejemplo la germinacion de un esporangio de US-8 fue significativamente menos que la germinacion de US-1 a 20 C pero no a 10 o 15 C.

Diferencias de patogenecidad entre los 'viejos" y los "nuevos" linajes pueden tener implicaciones significativas en manejo de emfermedades. Por ejemplo "viejos" linajes fueron notoriamente ineficientes en iniciar una epidemia partiendo de tuberculos de papa infectadas utilizadas como semilla. La mayor agresividad de algunos "nuevos" linajes y su diferente respuesta a los factores abioticos pueden exigir alteraciones en las predicciones de enfermedades, y las fechas de aplicacion de fungicidas comunes. Esto presagia que las prediciones acerca de la influencia de factores epidemiologicos van ha necesitar de incluir una amplia respuesta del patogeno, y esto va ha ser menos preciso que el anterior