Edward B. Radcliffe

Aphid-transmitted potato viruses: The importance of understanding vector biology

This review addresses some of the biological complexities presented by aphid-transmitted viruses of potato,Solanum tuberosum L., and their vectors and discusses the application of this knowledge to the management of potato viruses with particular emphasis on seed potato production.

Insect resistance in potatoes: sources, evolutionary relationships, morphological and chemical defenses, and ecogeographical associations.

SummaryThe past 25 years, 1686 potato accessions, representing 100 species in the genus Solanum L., subgenus Potatoe, section Petota, were evaluated for field resistance to one or more of the following insect pests: green peach aphid, Myzus persicae (Sulzer); potato aphid, Macrosiphum euphorbiae (Thomas); Colorado potato beetle, Leptinotarsa decemlineata (Say); potato flea beetle, Epitrix cucumeris (Harris); and potato leafhopper, Empoasca fabae (Harris). Accessions highly resistant to green peach aphid were identified within 36 species, to potato aphid within 24 species, to Colorado potato beetle within 10 species, to potato flea beetle within 25 species, and to potato leafhopper within 39 species. Resistance levels were characteristic within Solanum species. Insect resistance appears to be a primitive trait in wild potatoes. Susceptibility was most common in the primitive and cultivated Tuberosa. Insect resistance was also characteristic of the most advanced species. The glycoalkaloid tomatine was associated with field resistance to Colorado potato beetle and potato leafhopper. Other glycoalkaloids were not associated with field resistance at the species level. Dense hairs were associated with resistance to green peach aphid, potato flea beetle, and potato leafhopper. Glandular trichomes were associated with field resistance to Colorado potato beetle, potato flea beetle, and potato leafhopper. Significant correlations between insect score and altitude of original collection were observed in six of thirteen species. Species from hot and arid areas were associated with resistance to Colorado potato beetle, potato flea beetle, and potato leafhopper. Species from cool or moist areas tended to be resistant to potato aphid.

Epidemiology and Field Control of PVY and PLRV

Viral diseases of potatoes can cause significant yield and quality losses for the commercial producer but are of particular concern to the seed potato producer. Potato virus Y (PVY) and Potato leafroll virus (PLRV) are the most common of the 28 viral diseases known to infect potato (Salazar, 1996). Current season (primary) infection with PVY causes little yield loss (Hane and Hamm, 1999; Salazar, 1996) especially if initial infection occurs after flowering. Quality loss caused by PVY results from an increase in the number of undersized tubers (Hane and Hamm, 1999). With PLRV, primary infection rarely reduces yield (Beemster and Rozendaal, 1972) but it can affect tuber quality by causing phloem net necrosis. Net necrosis is expressed in tubers as a darkening of the vascular bundle that becomes more pronounced during storage. Net necrosis is particularly severe in the cultivars Russet Burbank, Norgold Russet, and Green Mountain (Douglas and Pavek, 1972), the former being the most widely grown cultivar in the U.S.

Effects of High and Fluctuating Temperatures on Myzus persicae (Hemiptera: Aphididae)

Abstract Development of green peach aphid, Myzus persicae (Sulzer), was modeled under high and fluctuating temperatures to determine what effects an increase in mean summer temperatures of 2.5–3.5°C would have on green peach aphid populations in Minnesota and North Dakota. Green peach aphid developed faster and had greater fecundity under fluctuating conditions. The constant temperature model failed to predict observed development under fluctuating temperatures (R2 = 0.01). Optimal temperature for green peach aphid population growth was 26.7°C. The lower and upper developmental thresholds were 6.5 and 37.3°C, respectively. Under optimal conditions, intrinsic rate of increase was 0.356, and population doubling time was 1.95 d. At optimal fluctuating temperature conditions, one female aphid produced 12.2 progeny each week while under the most favorable constant temperature conditions; each female aphid produced only 5.9 progeny. Green peach aphid was able to survive 1 h each day above its calculated lethal death point of 38.5°C. It seems that, in midwestern North America, green peach aphid would benefit from an increase in mean summer temperature (20°C) of 2.5–3.5°C.

Soybean Aphid, Aphis glycines Matsumura, a New Vector of Potato Virus Y in Potato

Soybean aphid (Aphis glycines Matsumura), an exotic species first discovered in the North Central region of the United States in 2000, is a competent vector of severalPotyviridae. Soybean aphid has high fecundity and produces alatae (winged morphs) readily, characteristics typical of proficient virus vectors. When soybean aphids were exposed toPotato virus Y (PVY)-infected potato plants and then clip-caged on healthy potato plants in groups of five or as single aphids, PVY transmission ranged from 14% to 75% across all experiments. PVYo, PVYn, and PVPntn strains were transmitted by soybean aphid.ResumenEl áfido de la soya (Aphid glycines Matsumura), especie exótica que fuera descubierta en la región norcentral de los Estados Unidos en el año 2000 es un vector de variosPotyviridae. El áfido de la soya tiene una alta fecundidad y produce rápidamente formas aladas, característica típica de los vectores de virus. Cuando los áfidos de la soya se pusieron en contacto con el virus Y (PVY) en plantas de papa infectadas y luego se insertaron en plantas sanas en grupos de cinco o como áfidos solitarios, la trasmisión de PVY fue de 14% a 75% en todos los experimentos. Las variantes PVYo, PVYn y PVYntn fueron trasmitidas por el áfido de la soya.

Genetic Resistances to Potato Leafroll Virus, Potato Virus Y, and Green Peach Aphid in Progeny ofSolanum etuberosum

Increasing prevalence of potato leafroll virus (PLRV) and potato virus Y (PVY) has been reported in seed and commercial potato production, resulting in the rejection of potatoes for certification and processing. Host plant resistance to PLRV and PVY and their primary vector, green peach aphid,Myzus persicae, could limit the spread of these viruses. Host plant resistance to PLRV, PVY, and green peach aphid has been identified in non-tuber-bearingSolanum etuberosum (PI 245939) and in its backcross 2 (BC2) progeny. Resistance to green peach aphid involved a reduction in fecundity and adult aphid size. In addition, one BC2 individual was identified as possessing a genetic factor that was detrimental to nymph survival. PVY resistance was identified in all five BC2 progenies evaluated in a field screening under intense virus pressure. PLRV resistance was identified in two of the five BC2 progeny. This resistance was stable in field and cage evaluations with large populations of viruliferous aphids. Based on the segregation of virus resistances in the BC2 , PVY and PLRV resistances appear to result from the action of independent genetic mechanisms that reduce the levels of primary and secondary virus infection. Two BC2 individuals, Etb 6-21-3 and Etb 6-21-5 were identified as having multiple resistances to PLRV, PVY, and green peach aphid derived fromS. etuberosum. This germplasm could prove useful to potato breeders in the development of virus-resistant cultivars.ResumenEI incremento en la prevalencia del virus del enrollamiento de la hoja de papa (PLRV) y del virus Y de la papa (PVY) ha sido reportado tanto en las semillas como en la producción comercial de papa, lo que conlleva al rechazo de las mismas durante las fases de certificación y procesamiento. La resistencia de la planta hospedante al PLRV y al PVY y su principal vector, el pulgón verde,Myzus persicae, podría limitar el esparcimiento de esos virus. Se ha identificado resistencia de la planta hospedante al PLRV, al PVY y al pulgón verde enSolanum etuberosum (PI 245939) no tuberizados y en su progenie 2 (BC2) de retrocruzamiento. La resistencia al pulgón verde implicó una reducción en la fecundidad y tamaño del pulgón adulto. Adicionalmente, se identificó un BC2 individual que posee un factor genético perjudicial para la sobrevivencia de las ninfas. La resistencia al PVY se identificó en las cinco progenies BC2 evaluadas en un campo de prueba bajo intensa presión del virus. Se identificó resistencia al PLRV en dos de las cinco progenies BC2. Esta resistencia fue estable en el campo y en evaluaciones en jaula con una alta población de pulgones virulentos. Basados en la segregación de resistencia a virus del BC2, las resistencias al PVY y al PLRV parecen ser resultado de la acción de mecanismos genéticos independientes que reducen los niveles primarios y secundarios de la infección viral. Se identificaron dos BC2 individuales, Etb 6-21-3 y Etb 6-21-5, con resistencia múltiple al PLRV, PVY y pulgón verde derivada deS. etuberosum. Este germoplasma podría ser útil para los mejoradores que desarrollan cultivares resistentes al virus.

Biological Control of Alfalfa Weevil in North America

Alfalfa weevil, Hypera postica (Gyllenhall) (Coleoptera: Curculionidae), is of Eurasian origin. This destructive pest of alfalfa (lucerne) was accidentally established in North America on three separate occasions. These introductions are commonly identified in the literature as biological strains: western alfalfa weevil, Egyptian alfalfa weevil (=Hypera brunneipennis Boheman), and eastern alfalfa weevil. Alfalfa weevil has been the target of classical biological control almost since its discovery in North America more than 90 years ago. These efforts have resulted in establishment of at least nine exotic parasitoids and egg predators: Bathyplectes curculionis (Thomson), B. anurus (Thomson) and B. stenostigma (Thomson) (Hymenoptera: Ichneumonidae); Microctonus aethiopoides Loan and M. colesi Drea (Hymenoptera: Braconidae), the latter of undetermined origin; Oomyzus incertus (Ratzenberg) (Hymenoptera: Eulophidae); Dibrachoides dynastes (Forester) and Peridesmia discus (Walker) (Hymenoptera: Pteromalidae); and Anaphes luna (Girault) (Hymenoptera: Mymaridae). A fungal pathogen, Zoophthora phytonomi Arthur (Phycomycetes: Entomophthoraceae), of undetermined origin, is becoming an increasingly important alfalfa weevil mortality factor. Most major USA alfalfa production areas now benefit from a complex of alfalfa weevil biological control agents. Collectively, these agents have effected substantial reduction in the economic importance of alfalfa weevil across the northern USA However, biological agents provide only partial control of alfalfa weevil, and importance of their contribution differs considerably with production area. Still, the benefits achieved, especially from reduced need for insecticides in alfalfa production, mark this as one of the great success stories of classical biological control in North America.

Fine screeningSolanum (potato) germplasm accessions for resistance to Colorado potato beetle

This study was conducted to investigate the utility of systematic screening at the genotype level withinSolanum accessions highly resistant to the Colorado potato beetle. Evaluations of clonally replicated genotypes showed that most accessions reported to be uniform when screened as populations contained small but significant variation among genotypes for resistance to oviposition, larvae, and defoliation, differences for numbers of larvae being most common. Adult counts and percentage defoliation were not as useful in evaluating among-genotype variability in beetle resistance. Genotypes ofS. pinnatisectum WRF 343 andS. tarijense PI 473227 were the most uniformly and highly resistant to Colorado potato beetle. Genotypes of S.berthaultii PI 473331,S. chacoense PI 473405, andS. tarijense PI 473336 were moderately to highly resistant, and genotypes ofS. bukasovii PI 473494 andS. canasense PI 230511 were uniformly susceptible to Colorado potato beetle. Nonparametric correlation analyses indicated that number of egg masses, small larvae, large larvae, and defoliation scores were positively correlated, negatively correlated, or not correlated, depending on the species. One generation of selection attempting to segregate resistance and susceptibility in nearly uniform and highly resistantS. pinnatisectum WRF 343 resulted in “divergent” populations that could not be distinguished from each other or the base population. Thus, through genotype (“fine”) screening and selection, we showed that some existing populations are virtually pure for extreme resistance. Use of individuals from such families would make screening breeding populations more efficient, and reduce the risk of losing resistance genes that have non-dominant effects. Fine screening, recurrent selection, and maintenance of such elite populations is recommended as an extension of population-based evaluation usually done by genebanks.CompendioEl objetivo de este estudio fue investigar la utilidad de la evaluación sistemática a nivel de genotipo entre accesiones deSolanum con alta resistencia al gorgojo Colorado de la papa. A pesar que muchas de las accesiones analizadas a nivel poblacional habian sido reportadas como uniformes, la evaluación de genotipos reproducidos clonalmente demostró que existe una variación significativa en la resistencia a la postura de huevos, larvas y defoliación, siendo la diferencia en el número de larvas la más común. El conteo de adultos y el porcentaje de defoliación no fue tan útil en la evaluación de variabilidad entre genotipos con resitencia al gorgojo. Los genotipos de S.pinnatisectum WRF 343 yS. tarijense PI 473227 mostraron la mayor uniformidad y resistencia al gorgojo Colorado de la papa. Los genotipos deS. berthaultii PI 473331,S. chacoense PI 473405, yS. tarijense PI 473336 mostraron entre moderada y alta resistencia, y los genotipos deS. bukasovii PI 473494 yS. canasense PI 230511 fueron unformemente susceptibles al gorgojo. El análisis de correlación no paramétrica indicó que el número de masas de huevos, larvas pequeñas, larvas grandes y defoliación tienen una correlación positiva, negativa, o no tienen correlación, dependiendo de las especies. El intento de utilizar una generación de selección divergente para producir segregación de resistencia y susceptibilidad en una accesión de relativa uniformidad y con alta resistencia (S. pinnatisectum WRF 343) no fue exitoso. En consecuencia, este estudio demuestra la existencia de poblaciones esencialmente puras para la resistencia extrema y por ello no necesitan ser previamente mejoradas para ser utilizadas en los programas de mejoramiento de germoplasma. En conclusión, la evaluación de genotipos o evaluación “fina” y selección podrían ser útiles para la identificación o el establecimiento de poblaciones en las cuales la resistencia máxima es verdadera (homozygota). La evaluación fina, selección recurrente, y el mantenimiento de dichas poblaciones sería una útil extensión de las evaluaciones basadas en poblaciones, las cuales son usualmente hechas por los bancos de germoplasma.

Potato fungicides interfere with entomopathogenic fungi impacting population dynamics of green peach aphid

Fungicides applied to potato can enhance green peach aphid,Myzus persicae (Sulzer), outbreaks by interference with entomopathogenic fungi. (Order Entomophthorales). Late season aphid numbers were highest in potatoes sprayed with metalaxyl + mancozeb, captafol, or mancozeb, and lowest in potatoes sprayed with benomyl, triphenyltin hydroxide, chlorothalonil, or copper hydroxide. In field-collected aphids,Pandora (= Ernyia) neoaphidis (Remaudière et Hennebert) andEntomophthora planchoniana Cornu (F. Entomophthtoraceae) were the predominant cause of mycoses, 66.7% and 22.3%, respectively.Conidiobolus obscurus (Hall and Dunn) Remaudièe and Keller (F. Ancylistaceae) accounted for 8.5% of mycoses. In the laboratory, fungicides were shown to have direct effects on these entomopathogens. Metalaxyl + mancozeb, mancozeb and captafol were strongly inhibitory of germination of conidia, copper hydroxide was intermediate, and chlorothalonil had little effect. Triphenyltin hydroxide, benomyl, metalaxyl + mancozeb, and mancozeb were strongly inhibitory of growth of mycelia, copper hydroxide was intermediate, and chlorothalonil and copper hydroxide had least effect. Benomyl was highly toxic to green peach aphid, copper hydroxide and chlorothalonil intermediate, and captafol, mancozeb, and metalaxyl + mancozeb least toxic. Possible interference of potato fungicides with aphid pathogens is now an important consideration because of the intensity of spraying required to protect the crop from infection by metalaxyl-resistant strains of the late blight pathogen,Phytophthora infestans (Mont.) de Bary. Minnesota potato growers reported high green peach pressure in both 1995 and 1996, years of intensive fungicide spraying. Concomitantly, there was a marked increased in the incidence of PLRV in seed lots entered for winter testing.ResumenFungicidas aplicados a la papa pueden reforzar brotes del áfido verde del melocotonero,Myzus persicae (Sulzer), por interferencia con los hongos entomopatogénicos (Orden Entomophthorales). El número de áfidos en la estación tardía fue superior en papas rociadas con captafol, mancozeb o metalaxyl, y menor en papas rociadas con benomyl, hidróxido de trifeniltin, clorotalonilo o hidróxido de cobre. En áfidos recolectados en el campo,Pandora (=Ernyia)neoaphidis (Remaudière et Hennebert) yEntomophthora planchoniana Cornu (F. Entomophthtoraceae) fueron la causa principal de la micosis en un 66.7% y 22.3%, respectivamente.Conidiobolus obscurus (Hall y Dunn) Remaudière y Keller (F. Ancylistaceae) fue responsable de un 8.5% de la micosis. En el laboratorio, los fungicidas mostraron tener efectos directes sobre estos entomopatogenós. Metalaxyl, mancozeb y captafol fueron potentes inhibidores de la germinación de los conidios, el hidróxido de cobre fue intermedio y el clorotalonilo tuvo poco efecto. El hidróxido de trifeniltin, benomyl, metalaxyl y mancozeb fueron potentes inhibidores del crecimiento de los micelios, el hidróxido de cobre fue intermedio y el hidróxido de cobre y el clorotalonilo tuvieron poco efecto. El Benomyl fue altamente tóxico al áfido verde del melocotonero, el hidróxido de cobre y clorotalonil fueron intermedios y captafol, mancozeb y metalaxyl fueron los menos tóxicos. Actualmente una consideración importante es la posible interferencia de los fungicidas de papa con patógenos de áfidos debido a la intensidad de la aspersión requerida para proteger a los cultivos de la infección causada por variantes resistentes del patógeno del tizón tardío,Phytophthora infestans (Mont.) de Bary al metalaxyl. Los agricultores de papa de Minnesota reportaron una gran presión del áfido verde del melocotonero dorante 1995 y 1996, años en que hubo intensas aspersiones de fangicidas. También hubo un claro incremento de la incidencia de PLRV en lotes de semilla que ingresaron para pruebas de invierno.

Resistance to green peach aphid,Myzus persicae (Sulzer), and potato aphid,Macrosiphum euphorbiae (Thomas), in potato cultivars

Previous research suggests that extant potato cultivars offer little promise as sources of useful aphid resistance. However, few prior studies have critically measured the effects of host cultivar on aphid age-dependent life table statistics or related these measures to field performance. Therefore, a comprehensive field and greenhouse study was undertaken to assess 49 commercial potato cultivars, primarily of North American origin, for resistance to green peach aphid,Myzus persicae (Sulzer), and potato aphid,Macrosiphum euphorbiae (Thomas). Cultivars were found to show considerable differences in resistances to each aphid species, but these resistances were not significantly correlated (R2=0.032). In greenhouse life table studies, the intrinsic rate of increase (rm) of green peach aphid was lowest (0.167) on cv Russet Norkotah and highest (0.350) on cv Red La Soda. Potato aphidrm was lowest (0.122) on cv Aracy and highest (0.229) on cv Irish Cobbler. Among cultivars, year of release, maturity class and yield potential did not significantly influence number of progeny per female per day for either green peach aphid or potato aphid (P=0.987 and 0.954, respectively). In field trials (2004 and 2005), yield potential was significantly correlated with green peach aphid counts, (P=0.006 and <0.0001, respectively). Aphid/predator population models using aK value of 15.2 predicted that following colonization green peach aphid populations would remain stable for 20 days on Russet Norkotah (resistant), whereas on Red La Soda (susceptible) populations would reach over 54,000. With non-persistent foliar insecticides as the only control, population models indicated that three applications would be necessary to maintain green peach aphid below the Minnesota recommended action threshold on Red La Soda for 21 days, while just one application would be needed for green peach aphid on Russet Norkotah. In combination with biological control or insecticide use, this resistance could provide substantial control while reducing the reliance on pesticides.ResumenInvestigaciones previas sugieren que los cultivares existentes ofrecen muy pocas posibilidades como fuente útil de resistencia a los áfidos. Sin embargo, pocos estudios previos han medido crítica y estadísticamente los efectos del cultivar hospedante sobre la edad del áfido o han relacionado estas medidas con el comportamiento en el campo. Por consiguiente, se realizaron estudios detallados de invernadero y campo para probar 49 cultivares de papa, principalmente de origen norteamericano para resistencia al áfido verde del melocotón,Myzus persicae (Sulzer) y al áfido de la papaMacrosiphum euphorbiae (Thomas). Los cultivares mostraron considerables diferencias en resistencia a cada especie de áfido, pero estas resistencias no estuvieron significativamente correlacionadas (R2= 0.032). En estudios de invernadero sobre edad, la tasa intrínseca de incremento (rm) del áfido verde fue más baja (0.167) en el cv Russet Norkotah y más alta (0.350) en el cv Red La Soda. Larm del áfido de la papa fue más baja (0.122) en el cv Aracy y más alta (0.229) en el cv Irish Cobbler. Entre cultivares, el año de liberación, la clase de madurez y el potencial de rendimiento no influenciaron significativamente el número de progenie por hembra por día, tanto para el áfido verde como para el áfido de la papa (P=0.987 y 0.954, respectivamente). En pruebas de campo (2004 y 2005), el potencial de rendimiento fue significativamente correlacionado con el número de áfidos (P=0.006 y <0.0001, respectivamente). Los modelos de población áfido/predator utilizando un valorK de 15.2 predijeron que la siguiente colonizatión de la población del áfido verde quedaría estable por 20 días en Russet Norkotah (resistente), mientras que en Red La Soda (susceptible), las poblaciones serían más de 54,000. Con insecticidas foliares no persistentes como sólo método de control, los modelos de población indicaron que serían necesarias tres aplicaciones para mantener el áfido verde por debajo del umbral de actión recomendado en Minnesota para 21 días sobre Red La Soda, mientras que una sola aplicación sería necesaria para el áfido verde sobre Russet Norkotah. En combinatión con control biológico o uso de insecticida, esta resistencia podría proporcionar control substancial reduciendo la dependencia sobre pesticidas.