About the Author
Kenneth Deahl is Research Leader (Acting) for the Vegetable Laboratory at the USDA’s Beltsville, MD, Agricultural Research Center. He received his Ph.D. from West Virginia University in Microbiology and Plant Pathology. During his career, he has explored certain fungal viruses, Colorado potato beetle resistance in wild potato species, and naturally occurring toxins in potatoes and tomatoes as insect resistance factors. Recently, he has done research work on different phases of late blight, including disease physiology, nature of host resistance, and epidemiology.
Life History of the Fungus
K. Deahl
USDA-ARS, BARC-West, Beltsville, Maryland
The life history of many of the fungi in the Oomycetes group has been shrouded in considerable controversy for nearly a century. Phytophthora infestans, the organism that causes the late blight disease of tomato and potato, is an ideal representative of this contentious reputation. This fungus not only possesses some of the "most sophisticated weaponry known among plant pathogens" (6), but it has great genetic flexibility and it shows unlimited variability and pliability. Hopefully, new information about the life history will help determine how P. infestans, by developing fungicide-resistant biotypes in the field, was capable of overcoming "the most efficient fungicide (metalaxyl) that has ever been produced" (5).
Regardless of this plasticity, the life history of P. infestans needs to be understood since such information is fundamental in the development of better control practices and in understanding how different control methods work. Part of the explanation of why P. infestans is such as successful pathogens comes from the finding that the disease cycle is actually two cycles: a very efficient and effective asexual cycle and a putatively successful sexual cycle. The asexual spore, the sporangium is a unique spore with the ability to fruit quickly on leaf and stem tissue. Depending on environmental conditions, regeneration time can be very rapid and the entire cycle repeated in 5 to 7 days. In addition, a single sporangium can undergo indirect germination and produce 6 to 12 zoospores that are mobile by the means of 2 flagella. Zoospores can move about by way of moisture on the foliage; sporangia depend on external help - wind, rain, or wind-blown rain for movement. These propagative cells are mainly responsible for the new infections which may take place through any part of the epidermis of leaves and stems, either through stomata or the intact (unbroken) cells. Foliar infections may occur through either the upper or lower surfaces of the leaf, but the undersurface seems to be more susceptible, perhaps due to the number of stomata. The sporangia are thin-walled and are thought to be very ephemeral, retaining their viability for 10 to 14 days only; however, there are conflicting findings about this area.
Tuber infections following an attack of late blight is by means of sporangia or zoospores which are produced on the diseased foliage and are subsequently washed or swim into the soil. The general infection of the tubers can take place through lenticels, or cracks in the periderm. Contact of tubers with blighted foliage at harvest is also responsible for infections. Healthy tubers can become infected from blighted ones in the soil or storage if sufficient moisture is available.
Several theories have been advanced to explain the yearly occurrence of late blight: (1) the persistence of mycelium in the soil; (2) mycelium within the affected tubers; (3) occurrences of oospores or resting spores which overwinter in the soil; (4) the sporulation of the pathogen on the parent tuber in the soil; (5) the development of sclerotia; (6) the persistence of latent infections within potato tissues.
However, in actuality, the biology of P. infestans in soils and the soil stages of the life cycle are not fully understood. Andrivon (2) presents an excellent review of the controversial information available on the ecology and epidemiology of P. infestans in the soil in which he points out the many unanswered questions and future research needed on these topics. The following areas are a few examples of these gaps in knowledge: Survival of asexual inoculum. Of the three possible sources of asexual inoculum, sporangia are thought to be the primary sources of survival in the soil, since mycelium is an unlikely candidate and zoospores are too short-lived to be of any significance in long-term survival of the fungus. However, there are a number of papers that would disagree with this point of view. Period of soil infectivity. Although soil type, moisture content, and pH affect the persistence of infectivity, 15 to 77 days has been reported as the range of time that soils contaminated with sporangia remain infective to potato tubers (1,3,7,8,10,11). Again, work is still needed to find evidence of the full extent and consequences of soil infectivity, as well as data on "suppressive soils".
P. infestans is a heterothallic organism with two known mating types, A1 and A2. When mycelium of the two mating types interact, sexual propagation, by means of oospore formation, may take place. The oospore is the primary focus of the sexual cycle. Oospores are large, thick-walled spores which is thought to enable the fungus to survive for many years in plant debris or soil outside the living host plant. This occurs when blighted potato plants containing oospores remain in the field, decompose, and oospores are liberated. Reports from the Netherlands have shown that oospore formation occurs under Dutch climatic conditions and that the oospores, after the exposure to natural weather conditions in soil, gave rise to new pathogenic isolates (4). This occurred when mixtures of leaves containing oospores and sandy soil samples were exposed to natural weather conditions in the open field and after fixed periods soil samples were tested for infectivity. Results indicate that after eight months, the soil still contained infectious material. DNA fingerprints of the isolates obtained revealed that the infections were caused by sexual progeny originating from oospores. Also, it has been shown that oospores can germinate and infect tubers and stolons of newly planted potatoes, as well as stems and leaves which come in contact with the soil. Pittis and Shattock (9) demonstrated that oospores from several A1 and A2 matings of P. infestans produced isolates which survived for 8 months in soil. These workers reported that oospores were produced in potato stems after combined inoculations with zoospores of A1 and A2 isolates. Moreover, they found that oospores produced in vitro were capable of infecting potato shoots. However, since oospore formation is unknown for most potato production areas of the world, there have been only a few studies on the sexual cycle and the conditions that favor sexual reproduction of P. infestans in nature. Nevertheless, the recent appearance of the A2 mating type in many countries implies the possibility of sexual reproduction and raises the question of whether natural mating of the A1 and A2 types could lead to greater genetic diversity than existed when only the A1 mating type was present. Although extensive monitoring of genotypes representing "old" and "new" populations occurring in the U.S. and Canada during the past decade has not thus far indicated that recombinant types have arisen, the possibility still exists. Therefore, in order to quantify the epidemic impact of oospores as overwintering spores or as inoculum sources, the conditions for survival and germination must be explored and probed in greater detail. Detailed information on the sexual cycle and the production, survival, germination, and infectivity of the oospore is imperative for the development of future disease control and management strategies.
LITERATURE CITED
1. Andrivon, D. 1994. Dynamics of the survival and infectivity to potato tubers of sporangia of Phytophthora infestans in three different soils. Soil Biol. Biochem. 26:945-952.
2. Andrivon, D. 1995. Biology, ecology, and epidemiology of the potato late blight pathogen Phytophthora infestans in soil. Phytopathology 85:1053-1056.
3. Bogulavskaya, N. V., and Fillipov, A. 1977. Survival rates of Phytophthora infestans (Mont.) de Bary in different soils. (In Russian) Mikol. Fitopatol. 11:239-241.
4. Drenth, A., Janssen, E. M., and Govers, F. 1995. Formation and survival of oospores of Phytophthora infestans under natural conditions. Plant Pathol. 44:86-94.
5. Erwin, D. C., and Ribeiro, O. K. 1996. Phytophthora Diseases Worldwide. American Phytopathological Society Pres, St. Paul, MN.
6. Gregory, P. H. 1983. Some major epidemics caused by Phytophthora. Pages 271-278 in: Phytophthora: Its Biology, Taxonomy, Ecology, and Pathology. D.C. Erwin, S. Bartnicki-Garcia, and P.H. Tsao, eds. American Phytopathological Society, St. Paul, Minn. 392 pp.
7. Lacey, J. 1965. The infectivity of soils containing Phytophthora infestans. Ann. Appl. Biol. 56:363-380.
8. Murphy, P. A. 1922. The bionomics of conidia of Phytophthora infestans. Sci. Proc. R. Dublin Soc. 16:442-466.
9. Pittis, J. E., and Shattock, R. C. 1994. Viability, germination and infection potential of oospores of Phytophthora infestans. Plant Pathol. 43:387-396.
10. Sato, N. 1980. Sources of inoculum and sites of infection of potato tubers by Phytophthora infestans in soil. Ann. Phytopathol. Soc. Jpn. 46:231-240.
11. Zan, K. 1962. Activity of Phytophthora infestans in soil in relation to tuber infection. Trans. Br. Mycol. Soc. 45:205-221.
Historia de Vida
La historia de muchos hongos del grupo de los Oomycetes ha estado bajo una cosiderable contraversia por cerca de una centuria. Phytopthora infestans, el organismo que causa la enfermedad del tizon tardio de la papa y tomate, es un representativo ideal de una continua reputacion. Este hongo no solamente posee algunas de "los armamentos mas sofisticados conocido entre los patogenos de las plantas" pero tambien tiene la mayor flexibilidad genetica y demuestra una ilimitada variabilidad y docilidad. Felismente, una nueva informacion acerca de la historia de vida de este patogeno va ayudar a determinar como P. infestans, va desarrollando biotipos de campo con resistencia a los fungicidas, que fueron capaces de romper la accion de los mas eficientes fungicidas (metalaxyl)que han sido producidos por siempre".
Referente a su plasticidad, la historia de vida de P. infestans necesita ser entendido debido a que esta informacion es fundamental para el desarrollo de mejores practicas de control y entender como estas diferentes practicas de control trabajan. Parte de la explicacion de el porque P. infestans es un patogeno de mucho exito es debido a que el ciclo de vida de esta enfermedad actualemnte tiene dos cyclos: Un ciclo asexual muy eficiente y un ciclo sexual putativo muy existoso. La espora asexual, el esporangio es una espora unica con la habilidad de fructificar rapidamente en el tejido de las hojas y tallos. Dependiendo de las condiciones medioambientales, el tiempo de regeneracion este patogeno puede ser muy rapido con un ciclo de vida que se repite solo de 5 a 7 dias. Ademas de esto, un simple esporangio puede permitir un germinacion inderecta y producir de 6 a 12 zoosporas que son moviles a traves de dos flagelos que tiene. Las zoosporas pueden moverse en un medio acuoso en las hojas; el movimiento de un esporangio depende de la ayuda externa como viento, lluvia o combinacion de ambos. Estas celulas propagativas son mayormente responsables para una nueva infeccion que puede ser atraves de cualquier parte de la epidermis de las hojas o tallos, a traves de estomas o de celulas intactas (no rotas). Infecciones de las hojas puede ocurrir por el haz y enves, pero parece ser que el enves de las hojas son mas suceptibles debido posiblemente al numero de estomas. Los esporangios son de una pared muy fina y paresen ser muy efimeros, reteniendo su biavilidad solamente por 10 a 14 dias, sin embargo, esto esta aun en discusion.
La infeccion de los tuberculos despues de un ataque del tizon tardio es por intermedio de esporangios o zoosporas los cuales son producidos en las hojas enfermas que son subsequentemente lavados al suelo donde estos puden movilizarse. Una infeccion general de los tuberculos pude ser atraves de los lenticelos, o de hendiduras del peridermo. Tuberculos en contacto con las hojas despues de la cosecha son tambien responsables de la infeccion. Teberculos sanos pueden ser infectados a traves de tuberculos infectados o particulas de suelo adherida al tuberculo siempre y cuando exista sufieciente humedad disponible en los silos.
P. infestans es un organismo heterotalico con dos tipos de apareamiento, A and A. Cuando el micelio de estos dos tipos de apareaminento interactuan, la propagacion sexual puede ocurrir formando una oospora. La oospora es el primer foco del ciclo sexual. Las oosporas son largos, de pared gruesa que permite que el hongo sobreviva por muchos anos en los residuos de la planta o en el suelo fuera del huesped. Esto ocurre cuando las plantas de papa enfermas conteniendo oosporas permanecen en el suelo, estos residuos se descomponen, y liberan oosporas. Reportes de Holanda han demostrado que la formacion de oosporas ocurre bajo condiciones climaticas de ese pais y las oosporas, despues de ser expuextas a las condiciones naturales del medio ambiente en el suelo, da lugar a la formacion de nuevos aislamientos patogenicos. Esto ocurre cuando mezclas de las hojas conteniendo oosporas y muestras de suelo arenoso son expuestos a condiciones naturales del medio ambiente en un campo abierto y despues de periodos fijos de que las muestras de suelo fueron recolectadas para su infectividad. Estudios del DNA de las muestras obtenidas revelaron que las infecciones fueron cusadas por una progenie sexual originada de oosporas. Tambien, esto ha demostrado que las oosporas pueden germinar y infectar tuberculos y estolones de nuevas plantaciones de papa, asi como tambien a los tallos y hojas que han estado en contacto con el suelo. Sin embargo, desde que la formacion de oosporas no es conocido por la mayoria de las areas productoras de papa en el mundo, solamente ha existido unos pocos estudios del ciclo sexual y de las condiciones que facvorecen la reproducion sexual en condiciones naturales de P. infestans. Sin embargo, el hallasgo reciente de tipos de apareamiento A en muchos paises implica la posibilidad de una reproducion sexual. Para poder cuantificar el impacto de una epidemia causada por oosporas que invernan como fuente de inoculo, las condiciones de sobrevivencia y germinacion debe ser explorados y probados con mucho detalle. Una informacion detallada del ciclo sexual, de la produccion, sobrevivencia, germinacion, y infectividad de las oosporas es un proceso imperativo para desallorrar estrategias de control y manejo.
