Tizón tardío o mildew de la Papa (Phytophthora infestans)

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Condición fitosanitaria: Presente

Grupo de cultivos: Hortícola

Especie hospedante: Papa (Solanum tuberosum)

Rango de hospedantes: A menudo se asocia con sus dos hospedantes más comunes, la papa y el tomate. Sin embargo, P. infestans tiene un amplio rango de hospedantes que incluye muchos miembros de las Solanaceae, como por ejemplo Solanum muricatum (Huo et al., 2023). Las solanáceas ornamentales también pueden ser hospedantes, como por ejemplo Petunia spp., Calibrachoa spp., así como las especies silvestres Solanum dulcamara, Solanum sarrachoides, etc.

Epidemiología: policíclica, aguda.

Etiología: Pseudohongo. Hemibiotrófico

Agente causal: Phytophthora infestans (Mont.) de Bary

Taxonomía: Eukaryota > Stramenopiles > Oomycetes > Peronosporales > Phytophthora

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En Argentina, Lucca et al. genotipificaron aislamientos argentinos de P. infestans mediante PCR con una reacción multiplexada de 12 marcadores moleculares microsatélites (SSR) siguiendo la metodología propuesta por Li et al. (2013), que se complementó con el muestreo en campo con tarjetas FTA. Estos estudios determinaron que desde 2007, la población argentina del patógeno está dominada por la línea clonal EU_2_A1, diferente a la reportada a finales de los 90 (Forbes et al., 1998).

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Antecedentes

La enfermedad apareció por primera vez en los EE. UU. en 1843, cerca de los puertos de Nueva York, Filadelfia y los estados circundantes. La enfermedad se informó ampliamente por primera vez en el continente europeo dos años más tarde en Bélgica en 1845, después de lo cual se extendió por toda Europa y luego a Irlanda (Cox y Large, 1960; Bourke 1964; Zadoks, 2008; Ristaino et al., 2020). El linaje clonal que causó la hambruna de la papa en Irlanda (conocida mundialmente como «Gran hambruna irlandesa«) se denominó FAM-1, se secuenció el genoma y se documentó su ascendencia compartida con P. andina, una especie hermana de América del Sur (Martin et al., 2013). La ascendencia compartida de P. andina y el linaje de la hambruna sugieren que ambas especies pueden haber sido simpátricas en América del Sur (Martin et al., 2016).

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Sintomatología

Se caracteriza por la presencia de manchas oscuras, que se inician por lo general en el borde o ápice de los folíolos. Si las condiciones ambientales son favorables para el desarrollo de la enfermedad, es posible observar en el envés de las hojas la presencia de una felpilla blanco grisáceo (signo de la enfermedad) constituida por micelio y zoosporangios del patógeno. En estas condiciones, las manchas progresan rápidamente, afectan los pecíolos y se produce defoliación (principalmente de las hojas inferiores).
En los tallos se observan manchas oscuras y alargadas. Al confluir éstas, el tallo queda totalmente ennegrecido, adquiere consistencia vítrea y se quiebra con facilidad.

El patógeno puede infectar a los tubérculos a través de yemas, lenticelas o heridas y también puede penetrar directamente la cutícula a través de apresorios (Resjö et al., 2017). Las zoosporas se enquistan y forman tubos germinativos que se hinchan hasta convertirse en apresorios (Grenville-Briggs et al., 2005). Se forma una clavija de infección y el patógeno infecta la planta por penetración directa a través de las células epidérmicas o de los estomas. La corteza de los tubérculos afectados toma una coloración castaño azulado, que pude abarcar parte o la totalidad de la superficie. Luego la infección se interna en el parénquima amiláceo, el que toma un color castaño muy característico que origina la denominación “papa chocolate” con la que se conoce la sintomatología. La podredumbre del tubérculo -en un comienzo seca- se transforma en húmeda, si se dan las condiciones, por la acción de agentes secundarios, especialmente bacterias, que se encuentran en el suelo.

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Patogénesis

En la mayoría de los oomicetes parásitos de plantas, la infección generalmente comienza cuando las zoosporas móviles se enquistan y germinan en las superficies vegetales. Los esporangios también pueden iniciar infecciones. Los tubos germinativos forman un apresorio seguido de una clavija de penetración que perfora la cutícula. En algunas especies, como P. infestans, la clavija de penetración penetra en las células epidérmicas donde establece una vesícula de infección. Las especies de Phytophthora son patógenos hemibiotróficos, lo que significa que normalmente adoptan un proceso de infección de dos pasos: una fase temprana de infección «biotrófica» seguida de una necrosis extensa del tejido del hospedante asociada con crecimiento adicional y esporulación. Los patógenos de plantas de oomicetes típicamente establecen asociaciones íntimas con su hospedante vegetal. La colonización parasitaria es posible solo si se altera la fisiología del hospedante y se suprime la inmunidad de la planta (van Damme et al., 2011). Las hifas ramificadas, con estructuras similares a dígitos angostos conocidas como haustorios que invaginan las células del hospedante, se expanden desde el sitio de penetración hacia las células vecinas a través del espacio intercelular. Los haustorios se han relacionado con la introducción de proteínas efectoras dentro de las células vegetales y también puede funcionar en la absorción de nutrientes. Posteriormente, el tejido infectado se necrotiza y el micelio desarrolla zoosporangióforos que emergen a través de los estomas de las hojas o de la superficie de la raíz para producir asexualmente zoosporangios y completar el ciclo de vida.

Las proteínas similares al péptido 1 inductoras de necrosis y etileno (NLP = Necrosis and ethylene-inducing peptide 1–like proteins) son citolíticas y causan muerte celular y necrosis tisular al alterar la membrana plasmática de la planta. Las NLP son los únicos efectores de patógenos citolíticos conocidos que pueden permeabilizar las membranas plasmáticas de las plantas eudicotiledóneas. Recientemente, se identificaron los principales constituyentes de las membranas vegetales, las glicosilinositol fosforilceramidas (GIPC), como objetivos de la unión de la NLP a las membranas plasmáticas de las plantas. Las NLPs se secretan en el apoplasto, el espacio intersticial entre las células vegetales, donde la fuerza iónica es generalmente baja y las variaciones en la concentración de sal pueden afectar los procesos moleculares en la membrana plasmática de la planta. La NLP induce la formación de poros transitorios permeables a moléculas pequeñas. Este es el modo de acción molecular del daño de la membrana para un miembro de una gran familia de efectores de virulencia de este patógeno vegetal. El tamaño relativamente pequeño de las rupturas de la membrana indica que la actividad citotóxica de las NLP puede proporcionar a los patógenos iones y nutrientes de pequeño peso molecular derivados de células vegetales dañadas, mejorando así la virulencia de los patógenos necrotróficos. Esta alteración de la membrana es un proceso de varios pasos que incluye el reconocimiento de lípidos específicos de la planta impulsado electrostáticamente, unión superficial a la membrana, agregación de proteínas y formación transitoria de poros. El daño inducido por la NLP no es causado por una reorganización de la membrana ni por defectos a gran escala, sino por pequeñas roturas de la membrana. Este mecanismo distinto de alteración de la membrana lipídica está altamente adaptado para dañar eficazmente las células vegetales (Pirc et al., 2022).

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Ciclo de la enfermedad

En Argentina, P. infestans se perpetúa en los tubérculos infectados que permanecen en el suelo o en el almacenamiento. En países donde existe el ciclo sexual, este estado tiene importancia, pero en las que se producen cigotas por partenogénesis, no la tiene. En Argentina, lo más aceptado actualmente es que el pseudohongo sobrevive: 1) como micelio en tubérculos afectados que han quedado en el suelo; 2) en las pilas de papas desechadas o basurales; y  3) las “papa semilla” infectadas que se emplean en el momento de la plantación.

Hay dos etapas de infección:

a) A partir de las tres fuentes de inóculo anteriormente citadas, el pseudohongo desarrolla en el tejido que brota de las papas y esporula en la parte aérea de la planta. En el tallo invade rápidamente la región cortical causando clorosis y colapso de las células. Luego desarrolla entre las células de la médula del tallo, pero es raro encontrarlo en el sistema vascular. El micelio invade los brotes y acompaña su crecimiento a través del suelo y sobre la superficie del mismo. Al alcanzar la parte aérea de la planta de papa, esporula produciendo zoosporangios que emergen por los estomas de tallos y hojas y son proyectados al aire. Una vez maduro el esporangio se desprende y es llevado por el viento o dispersado por la lluvia. Cuando los zoosporangios se depositan sobre hojas o tallos húmedos germinan y a través de un tubo germinativo de zoosporas producen la reinfección. El tubo germinativo de una zoopora o de un zoosporangio penetra por la cutícula o por estomas y produce micelio, que crece profusamente entre las células y emite haustorios largos, curvados. Las células en las que el micelio se alimenta mueren y cuando comienzan a decaer el micelio se difunde por la periferia en los tejidos nuevos. Poco día después los nuevos zoosporangióforos son difundidos por el viento infectando nuevas plantas. En condiciones favorables, el tiempo desde infección hasta formación de zoosporangios es de 4 días o menos. Se producen un gran número de generaciones asexuales y nuevas infecciones en una estación. Con el avance de la infección las lesiones crecen y aparecen nuevas, lo que determina la muerte del follaje y la reducción proporcional en el rendimiento.

b) Infección de los tubérculos: ocurre en el campo cuando con tiempo húmedo los zoosporangios son llevados de las hojas hacia abajo, llegan al suelo llevados por las gotas de lluvia y se infiltran hasta alcanzar la superficie del tubérculo de papa. Los tubérculos cercanos a la superficie del suelo son atacados por las zoosporas que germinan y penetran por lenticelas o heridas. En el tubérculo el micelio crece principalmente entre las células y produce largos haustorios con forma de hoz que penetran las células. Estos órganos subterráneos rara vez son infectados por el micelio que crece en el tallo de una planta madre enferma. Sin embargo, en la cosecha los tubérculos se contaminan con los zoosporangios viables presentes en el suelo o en follaje enfermo aun verde ó, si los tubérculos están expuestos mientras el pseudohongo está esporulando, esta infección se desarrollará durante el almacenaje.

Los zoosporangios de este patógeno son diseminados por el viento y dan lugar a zoosporas móviles que, si hay disponibilidad de agua líquida en la superficie del tejido, penetran a través de los estomas. A temperaturas más elevadas los zoosporangios pueden germinar con un tubo germinativo, sin la intervención de zoosporas. En condiciones favorables, a los pocos días de incubación se forman las lesiones típicas con abundante esporulación. En condiciones controladas de laboratorio se estimó un período de incubación de 2 días y pico (menor a 3 días), por lo que se puede considerar una enfermedad aguda (Lebecka y Sobkowiak, 2013). De esta manera, la epidemia avanza muy rápidamente. Para que esto ocurra debe haber períodos prolongados de alta humedad y temperaturas frescas. Temperaturas mayores de los 30°C interrumpen el avance de la epidemia.
El pseudohongo «inverna» en forma de micelio, en tubérculos de plantas voluntarias, en tubérculos desechados que se apilan o en los tubérculos infectados que se almacenan. Luego de la emergencia de las plantas, el pseudohongo invade brotes en desarrollo y esporula si las condiciones de humedad son favorables. Una vez producida la infección primaria, la diseminación de la enfermedad (infecciones secundarias) se realiza por medio de los zoosporangios transportados por el agua o el viento.

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Condiciones predisponentes

Se manifiesta con tiempo lluvioso, alta humedad y bajas temperaturas. En la Argentina se ha observado que las epidemias de tizón tardío se producen en años de lluvias abundantes. Cuando se registran mañanas frescas (13ºC a 18ºC) sucesivas, acompañadas de abundante rocío y neblinas, seguidas de calor húmedo, las probabilidades de infección son muy altas.

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Medidas de manejo Integrado

* Variedades resistentes: si bien los grupos de investigadores de nuestro país están trabajando en la obtención de variedades resistentes, éstas todavía no están disponibles. Existen variedades tolerantes como Innovator (variedad de papa para industria).

* Eliminación de fuentes de inóculo primario (pilas de descarte, papa guacha). Para evitar la proliferación de la enfermedad en la etapa de poscosecha no deberán almacenarse papas que provengan de cultivos con ataques severos.

* Aplicación de oomyceticidas cuando las condiciones ambientales lo indiquen: al ser una enfermedad estrechamente ligada a los altos niveles de humedad relativa y a las precipitaciones acumuladas, los sistemas de alarma son efectivos cuando están ajustados. Si no se contara con este tipo de herramienta, las aplicaciones se harán según calendario debiendo efectuarse frecuentemente y a períodos cortos. Actualmente se dispone en Argentina de la posibilidad de poder contratar el servicio pago de Phytoalert®– Convenio entre INTA, Universidad de Wageningen (Holanda) y McCain Argentina; el cual es un Sistema de Apoyo para la Toma de Decisiones o DSS (siglas del inglés: Decision Support System) juega un papel fundamental en el uso racional de fungicidas. En otros países se han desarrollado otros modelos de predicción de riesgo de tizón para guiar las aplicaciones de fitosanitarios (Cucak et al. 2019, 2020; Hansen et al., 2017; Dowley et al., 2004).

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Videos

WPC Webinar #17 – Phytophthora Infestans: Late Blight

Zoospore Infection – Phytophthora nicotianae

Zoosporas y Zoosporangios

Identificando y Explorando para el Tizón Tardío en su Campo (español)

Tizón Tardio. INIA

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Bibliografía

Tizón Latino. Red latinoamericana de cooperación para el estudio del tizón tardío de las solanáceas.

Federación Nacional de Productores de Papa

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