John Innes Centre Department of Disease and Stress Biology

References and abstracts from the Hogenhout lab


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MPMII Lab
Personnel in Hogenhout lab. 

Publications
of Hogenhout lab. 

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in the Hogenhout lab. 

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Insectary
Visit the JIC Entomology Facility and Insectary website 

Phytoplasmas
What are phytoplasmas? 

Insect pathogens
Phytoplasmas infect insects. 

Plant pathogens
Phytoplasmas infect plants. 

Genomics
The Aster Yellows phytoplasma strain Witches' Broom (AY-WB) whole genome sequence. 



Peer-reviewed publications:

Hogenhout S. A., Van der Hoorn R. A. L., Terauchi R. and Kamoun S. (2009). Emerging concepts in effector biology of plant-associated organisms. Mol. Plant Microbe Interact. In press.

Bai X., Correa V. R., Toruno T. Y., Ammar E-D., Kamoun S. and Hogenhout S. A. (2009). AY-WB phytoplasma secretes a protein that targets plant cell nuclei. Mol. Plant Microbe Interact. 22: 18-30.

Ammar E-D., Tsai C-W., Whitfield A. E., Redinbaugh M. G. and Hogenhout S. A. (2009). Cellular and Molecular Aspects of Rhabdovirus Interactions with Insects and Plant Hosts. Annu. Rev. Entomol. 54: 447-468.

Hogenhout S. A., Ammar E-D., Whitfield, A. E. and Redinbaugh M. G. (2008). Insect Vector Interactions with Persistently Transmitted Viruses. Annu. Rev. Phytopathol. 46: 327-359

Hogenhout S. A. and Loria R. (2008). Virulence mechanisms of Gram-positive plant pathogenic bacteria. Curr. Opin. Plant Biol. 11: 449-456

Hogenhout S. A., Oshima K., Ammar E-D., Kakizawa S., Kingdom H. N. and Namba S. (2008). Phytoplasmas: Bacteria that manipulate plants and insects. Mol. Plant Pathol. 9: 403-423.

Tsai C-W., McGraw E. A., Dietzgen R. G. and Hogenhout S. A. (2008). Drosophila mounts a unique immune response to Sigma rhabdovirus. Appl. Environ. Microbiol. 74: 3251-3256.

Ammar E-D. and Hogenhout S. A. (2008). A neurotropic route for Maize mosaic virus (Rhabdoviridae) in its planthopper vector Peregrinus maidis. Virus Res. 131: 77-85.

Bai X., Grewal P. S., Hogenhout S. A., Adams B. J., Ciche T. A., Gaugler R., and Sternberg P. W. (2007). Comparative analysis of Heterorhabditis bacteriophora expressed sequence tags (ESTs). J. Parasitol. 93: 1343-1349.

Moya-Raygoza G., Hogenhout S. A. and Nault L. R. (2007). Habitat of the Corn Leafhopper (Hemiptera: Cicadellidae) during the Dry (Winter) Season in Mexico. Environ. Entomol. 36: 1066-1072.

Chakrabarty R., Banerjee R., Chung S-M., Farman M., Citovsky V., Hogenhout S. A., Tzfira T. and Goodin M. (2007). PSITE Vectors for Stable Integration of Transient Expression of Autofluorescent Protein Fusions in Plants: Probing Nicotiana benthamiana-Virus Interactions. Mol. Plant Microbe Interact. 20: 740-750.

Jovic J., Cvrkovic T., Mitrovic M, Krnjajic S., Redinbaugh M. G., Pratt R. C., Gingery R. E., Hogenhout S. A., and Tosevski I. (2007). Roles of stolbur phytoplasma and Reptalus panzeri (Cixiinae, Auchenorrhyncha) in the epidemiology of Maize redness in Serbia. Eur. J. Plant Pathol. 118: 85-89.

Kanneganti T., Bai X., Win J., Meulia T., Goodin M., Kamoun S. and Hogenhout S. A. (2007). A functional genetic assay for nuclear trafficking. Plant J. 50: 149-158.

Bai X., Zhang J., Ewing E., Miller S. A., Radek A., Schevchenko D., Tsukerman K., Walunas T., Lapidus A., Campbell, J. W. and Hogenhout S. A. (2006). Living with genome instability: the adaptation of phytoplasmas to diverse environments of their insect and plant hosts. J. Bact. 188: 3682-3696.

Sandhu S. K., Jagdale G. B., Hogenhout S. A. and Grewal P. S. (2006). Comparative Analysis of the Expressed Genome of the Entomopathogenic Nematode, Heterorhabditis bacteriophora. Mol. Biochem. Parasitology. 145: 239-44.

Ammar E-D. and Hogenhout S. A. (2005). Immunofluorescence confocal laser scanning microscopy as a reliable method for studying the distribution of mollicutes in vector leafhoppers (Cicadellidae: Hemiptera) and in host plants. Ann. Entomol. Soc. Am. 98: 820-826.

Reed S. E., Tsai C-W., Willie K. J, Redinbaugh M. G., and Hogenhout S. A. (2005). Shotgun sequencing of the negative-sense RNA genome of the rhabdovirus Maize mosaic virus. J. Virol. Methods. 129: 91-96.

Redinbaugh, M. G. and Hogenhout S. A. (2005). Plant rhabdoviruses. In: The world of rhabdoviruses. Current Topics in Microbiology and Immunology. Vol. 292. Z. Fu and H. Koprowski [Eds.]. pp. 143-153.

Tsai C-W., Redinbaugh M. G., Willie K. J, Reed S., Goodin M., and Hogenhout S. A. (2005). Complete Genome Sequence and in planta Subcellular Localization of Maize Fine Streak Virus Proteins. J. Virol. 79: 5304-5314.

Ammar E-D., Gomez-Luengo R. G., Gordon D. T. and Hogenhout S. A. (2005). Characterization of Maize Iranian Mosaic Virus and Comparison with Hawaiian and Other Isolates of Maize Mosaic Virus (Rhabdoviridae) . J. Phytopathology 153:129-136.

Chaouch Hamada, R., Redinbaugh, M. G., Gingery, R. E., Willie, K. and Hogenhout, S. A. (2004). Accumulation of Maize chlorotic dwarf virus proteins in its plant host and leafhopper vector. Virology 325: 379-388.

Bai, X., Fazzolari, T. and Hogenhout, S.A. (2004). Identification and Characterization of Spiroplasma kunkelii traE genes. Gene 336: 81-91.

Bai, X., Zhang, J., Holford, I. R., and Hogenhout, S.A. (2004). Comparative genomics identifies genes shared by distantly related insect-transmitted plant pathogenic mollicutes. FEMS Microbiol. Lett. 235: 249-258.

Zhang, J., Hogenhout, S. A., Nault, L.R., Hoy, C.W. and Miller, S.A. (2004). Molecular and symptom analyses of phytoplasma strains from lettuce reveal a diverse population. Phytopathology 94: 842-849.

Ammar, E-D, Fulton, D., Bai, X., Meulia, T., and Hogenhout, S. A. (2004). An attachment tip and pili-like structures in insect- and plant-pathogenic spiroplasmas of the class Mollicutes. Arch. Microbiol. 181:97-105.

Hogenhout, S. A., Redinbaugh, M. G., and Ammar, E-D. (2003). Plant and animal rhabdovirus host range: a bug's view. TRENDS Microbiol. 11:264-271.

Ozbek, E., Miller, S. A. Miller, Meulia, T. and Hogenhout, S. A. (2003). Infection and replication sites of Spiroplasma kunkelii (Class: Mollicutes) in midgut and Malpighian tubules of the leafhopper Dalbulus maidis. J. Invertebr. Pathol. 82:167-175.

Redinbaugh M. G., Seifers D. L., Abt J. J., Anderson R. J., Styer W. E., Ackerman J., Meulia T., Salomon R., Houghton W., Creamer R., Gordon D. T. and Hogenhout S. A. (2002). Maize Fine Streak Virus, a New Leafhopper-Transmitted Rhabdovirus. Phytopathology. 92: 1167-1174.

Bai X. and Hogenhout S. A. (2002). Genome sequence survey of the mollicute corn stunt spiroplasma, Spiroplasma kunkelii. FEMS Microbiol. Lett. 210: 7-17.

Montano H.G., Davis R.E., Dally E.L., Hogenhout S.A., Pimental J.P. and Brioso P.S. (2001). Candidatus Phytoplasma brasiliense, a new phytoplasma taxon associated with Hibiscus witches broom disease. Int. J. Syst. Evol. Microbiol. 51: 1109-1118.

Hogenhout S.A., Verbeek M., Van der Wilk F., Goldbach R.W. and Van den Heuvel J.F.J.M. (2000). Identifying the determinants in the equatorial domain of Buchnera GroEL implicated in binding Potato leafroll virus. J. Virol. 74: 4541-4548.

Van den Heuvel J.F.J.M., Hogenhout S.A., and Van der Wilk F. (1999). Recognition and receptors in virus transmission by arthropods. Trends Microbiol. 7: 71-76

Van den Heuvel J.F.J.M., Hogenhout S.A., Verbeek M. and Van der Wilk F. (1998). Azadirachta indica metabolites interfere with the host-endosymbiont relationship and inhibit the transmission of potato leafroll virus by Myzus persicae. Entomol. Exp. Appl. 86: 260-263.

Hogenhout S.A., van der Wilk F., Verbeek M., Goldbach R.W. and Van den Heuvel J.F.J.M. (1998). Potato leafroll virus binds to the equatorial domain of the aphid endosymbiotic GroEL homolog. J. Virol. 72: 358-365.

Van den Heuvel J.F.J.M., Bruyere A., Hogenhout S.A., Ziegler-Graff V., Brault V., Verbeek M., Van der Wilk F. and Richards K. (1997). The N-terminal region of the Luteovirus readthrough domain determines virus binding to Buchnera GroEL and is essential for virus persistence in the aphid. J. Virol. 71: 7258-7265.

Kamoun S. and Hogenhout S.A. (1997). Results of a five months expedition (1993-94) to study the tiger beetles of Australia (Coleoptera: Cicindelidae). Cicindela 29: 1-18.

Kamoun S. and Hogenhout S.A. (1996). Flightlessness and Rapid Terrestrial Locomotion in Tiger Beetles of the Cicindela L. subgenus Rivacindela van Nidek from Saline Habitats of Australia (Coleoptera: Cicindelidae). Coleopt. Bull. 50: 221-230.

Karrer E.E., Lincoln J.E., Hogenhout S.A., Bennett A.B., Bostock R.M., Martineau B., Lucas W.J., Gilchrist D.G. and Alexander D. (1994). In situ isolation of mRNA from individual plant cells: creation of cell-specific cDNA libraries. Proc. Natl. Acad. Sci. U.S.A. 92: 3814-3818.

Overduin B., Hogenhout S.A., van der Biezen E.A., Haring M.A., Nijkamp H.J.J. and Hille J. (1993). The Asc locus for resistance to Alternaria stem canker in tomato does not encode the enzyme aspartate carbamoyltransferase. Mol. Gen. Genet. 240: 43-48.


Contributed book chapters (reprints available upon request):

Ammar E. D. and Hogenhout S. A. (2006). Mollicutes associated with arthropods and plants. In: Insect Symbiosis Vol. II. B. Kostas and T. Miller [eds.]. In: Insect Symbiosis v2, pp 97-118.

Ammar E. D., Meulia T., Ozbek E. and Hogenhout S. A. (2004). Assembly and accumulation sites of Maize mosaic virus (Rhabdoviridae) in plant host and insect vector using transmission electron and confocal laser scanning microscopy. In: Current Issues on Multidisciplinary Microscopy Research and Education. A. Mendez-Vilas and L. Labajos-Broncano [eds.]. Formatex Microscopy Book Series, no.2, Badajoz, Spain. Pp. 56-64.


Abstracts of other relevant papers:

Zhou, X., Hoy, C. W., Miller, S. A. and Nault, L. R. (2002). Spatially explicit simulation of aster yellows epidemics and control on lettuce. Ecological Modelling 151:293-307.

Abstract: Aster yellows is a sporadic disease of vegetable crops (lettuce, carrot and celery) in the North Central US. The pathogen, a phytoplasma, is transmitted by the aster leafhopper (Macrosteles quadrilineatus Forbes). A simulation model has been developed to study the effects of spatial patterns of fields of host and non-host crops and spatiotemporal pattern of cultural and chemical controls for the disease and insect vector, respectively, on disease epidemics. The model is spatially explicit, simulating leafhopper reproduction, development and movement among individual fields. Simulations demonstrated that both the pattern of long range dispersal and the arrangement of host and nonhost fields can affect aster yellows epidemics and yield loss. If the source of inoculum is within the production area, insecticidal control of vectors in early plantings can protect later plantings, although protection may be more easily achieved by placing later plantings at a suitable distance from earlier plantings. Sensitivity analysis of model parameters also indicates that an increased crop incubation period, the time between infection and symptom expression, could greatly reduce losses from this disease in lettuce.


Beanland, L., Hoy, C. W., Miller, S. A., and Nault, L. R. (2000). Influence of aster yellows phytoplasma on the fitness of aster leafhopper (Homoptera:Cicadellidae). Ann. Entomol. Soc. Am. 93:271-276.

Abstract: This study revealed that feral aster leafhoppers, Macrosteles quadrilineatus Forbes, exposed to aster yellows phytoplasma live longer and may lay more eggs than nonexposed leafhoppers. Aster leafhoppers were reared on asters infected with either of 2 strains of aster yellows phytoplasma or uninfected asters. After eclosion, adults were placed on uninfected healthy lettuce or oat plants and transferred periodically. The life span of test leafhoppers and the number of offspring they produced were compared. Females reared on noninfected aster plants lived for an average of 19 d, those reared on ësevereí and ëboltí strain aster yellows phytoplasma-infected plants lived 26 and 28 d, respectively. The mean number of offspring produced by females reared on the bolt strain of aster yellows phytoplasma-infected asters was almost twice the number produced by nonexposed leafhoppers. The life span of feral leafhoppers or the number of eggs laid did not differ for leafhoppers maintained on either oats or lettuce after exposure to aster yellows phytoplasma-infected asters. Female leafhoppers lived twice as long as males. Our results suggest that the aster leafhopper may have had a long association with aster yellows phytoplasma. The longer life and higher fecundity of phytoplasma-infected leafhoppers may influence disease dynamics of aster yellows in lettuce.


Hoy, C. W., Zhou, X. L., Nault, L. R., Miller, S. A. and Styer, J. (1999). Host plant, phytoplasma, and reproductive status effects on flight behavior of aster leafhopper (Homoptera: Cicadellidae). Annals Entomol. Soc. Am. 92:523-528.

Abstract: Factors that affect aster leafhopper flight were examined in laboratory and field experiments. In both the laboratory and the field, differences between males and females in flight between plants within or just above the canopy were documented. Host plant and phytoplasma infection had no effect on the within-canopy flight behaviors, which were consistent with reproductive biology for the Cicadellidae. Plant species and size did affect the number of vertical flights out of the canopy. Male aster leafhoppers infected with the phytoplasma moved more frequently than uninfected males between plants, although plant residence times for uninfected and infected males were similar.


Murral, D. J., Nault, L. R., Hoy, C. W., Madden, L. V. and Miller, S. A. (1996). Effects of temperature and vector age on transmission of two Ohio strains of aster yellows phytoplasma by the aster leafhopper (Homoptera: Cicadellidae). J. Economic Entomology 89:1223-1232.

Abstract: Mean latent period and transmission rate of 2 strains (bolt and severe) of aster yellows phytoplasma in nymph and adult aster leafhoppers, Macrosteles quadrilineatus Forbes, were studied under controlled conditions at 15, 20, 25, and 30 degree C. There was a nonlinear relationship between mean latent period and temperature with shorter mean latent periods at higher temperatures ( apprxeq 20-25 d) than at lower temperatures ( apprxeq 40-80 d) for both aster yellows phytoplasma strains and both ages of leafhoppers. The proportion of leafhoppers that became vectors was significantly higher for bolt strain when leafhoppers acquired aster yellows phytoplasma as nymphs than as adults. However, there was no difference in the proportion that became vectors of the severe strain by the 2 age groups. Once leafhoppers became inoculative, the rate of transmission remained constant over their life spans when monitored by serial transfers at 48-h intervals. Increases in temperature and access time of leafhoppers increased the proportion of leafhoppers that became vectors after feeding on bolt strain-infected plants. Also, the effect of aster yellows phytoplasma exposure on life spans of leafhoppers was studied at 4 temperatures. At 25 and 30 degree C, leafhoppers exposed to both aster yellows phytoplasma strains lived longer than those leafhoppers not exposed. Data can be used in an aster yellows epidemiological model to evaluate strategies for aster yellows management.


Hoy, C. W., Heady, S. E., and Koch, T. A. 1992. Species composition, phenology, and possible origins of leafhoppers (Cicadellidae) in Ohio vegetable crops. J. Econ. Entomol. 85:2336-2343.

Abstract: Leafhopper populations were sampled with sweep nets in grain cover and vegetable crops during 1988 and 1989. Populations in vegetable crops consisted primarily of aster leafhopper, Macrosteles quadrilineatus Forbes, except for potato crops in which Empoasca spp. were ocmmon. Adult aster leafhoppers were caught several weeks before nymphs in each year. Peak catches of aster leafhopper adults and nymphs occurred in both June and July. Data were consistent with the hypothesis that aster leafhoppers migrate to Ohio vegetable-growing areas in late May and June. Air trajectory analysis indicated three possible source areas of M. quadrilineatus migrating into Ohio vegetable-production areas: Arkansas, Louisiana, Texas, and Oklahoma; western Ohio, Indiana, and Illinois; and a corridor extending from Ohio to the Dakotas. Bioassays for aster yellows during 1989 and 1990 indicated that the leafhopper populations present during those years contained very few inoculative individuals. Growers should base treatment decisions on monitoring for inoculative aster leafhoppers.