Assessing winter-survival of Pandora neoaphidis in soil with bioassays and molecular approaches

Biological Control

Volumn 54, Issue 2, 2010, Pages 126-134

  Fournier, Anselme ^a   Widmer, Franco ^a   Enkerli, Jürg ^a  

^a AGROSCOPE RECKENHOLZ TÄNIKON RESEARCH STATION ART   (Switzerland)

Author keywords

Aphid; Conservation biological control; Cultivation independent genotyping; Entomopathogenic fungi; Erynia neoaphidis; Real time PCR; Winter survival

Indexed keywords

ACYRTHOSIPHON PISUM; APHIDIDAE; ENTOMOPHTHORALES; FUNGI; PANDORA NEOAPHIDIS; PISUM SATIVUM;

EID: 77955562387     PISSN: 10499644     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biocontrol.2010.04.001     Document Type: Article

References (57)

1. Anderson I.C., Cairney J.W.G. Diversity and ecology of soil fungal communities: increased understanding through the application of molecular techniques. Environmental Microbiology 2004, 6:769-779.
2. Barta M., Cagan L. Entomophthoralean fungi associated with the common nettle aphid (Microlophium carnosum Buckton) and the potential role of nettle patches as reservoirs for the pathogens in landscape. Journal of Pest Science 2003, 76:6-13.
3. Baverstock J., Clark S.J., Pell J.K. Effect of seasonal abiotic conditions and field margin habitat on the activity of Pandora neoaphidis inoculum on soil. Journal of Invertebrate Pathology 2008, 97:282-290.
4. Bell A.S., Blanford S., Jenkins N., Thomas M.B., Read A.F. Real-time quantitative PCR for analysis of candidate fungal biopesticides against malaria: technique validation and first applications. Journal of Invertebrate Pathology 2009, 100:160-168.
5. Beniston M. Entering into the " greenhouse century": recent record temperatures in Switzerland are comparable to the upper temperature quantiles in a greenhouse climate. Geophysical Research Letters 2007, 34:L16710.
6. Bidochka M.J. Monitoring the fate of biocontrol fungi. Fungi as Biocontrol Agents: Progress, Problems and Potential 2001, 193-218. CAB International, Wallingford. T. Butt, C.W. Jackson, N. Magan (Eds.).
7. Brookes A.J. The essence of SNPs. Gene 1999, 234:177-186.
8. Bustin S.A. A-Z of Quantitative PCR 2004, IUL Press, San Diego, CA.
9. Butt T.M., Wang C., Shah F.A., Hall R. Degeneration of entomogenous fungi. An Ecological and Societal Approach to Biological Control 2006, 213-226. Springer, Dordrecht. J. Eilenberg, H. Hokkanen (Eds.).
10. Castrillo L.A., Thomsen L., Juneja P., Hajek A.E. Detection and quantification of Entomophaga maimaiga resting spores in forest soil using real-time PCR. Mycological Research 2007, 111:324-331.
11. Castrillo L.A., Griggs M.H., Vandenberg J.D. Quantitative detection of Beauveria bassiana GHA (Ascomycota: Hypocreales), a potential microbial control agent of the emerald ash borer, by use of real-time PCR. Biological Control 2008, 45:163-169.
12. Eilenberg J., Hajek A., Lomer C. Suggestions for unifying the terminology in biological control. BioControl 2001, 46:387-400.
13. Ekesi S., Shah P.A., Clark S.J., Pell J.K. Conservation biological control with the fungal pathogen Pandora neoaphidis: implications of aphid species, host plant and predator foraging. Agricultural and Forest Entomology 2005, 7:21-30.
14. Enkerli J., Widmer F. Molecular ecology of fungal entomopathogens: molecular genetic tools and their applications in population and fate studies. BioControl 2010, 55:17-37.
15. Enkerli J., Widmer F., Keller S. Long-term field persistence of Beauveria brongniartii strains applied as biocontrol agents against European cockchafer larvae in Switzerland. Biological Control 2004, 29:115-123.
16. Fargues J., Goettel M.S., Smits N., Ouedraogo A., Vidal C., Lacey L.A., Lomer C.J., Rougier M. Variability in susceptibility to simulated sunlight of conidia among isolates of entomopathogenic Hyphomycetes. Mycopathologia 1996, 135:171-181.
17. Feng M.G., Johnson J.B., Halbert S.E. Natural control of cereal aphids (Homoptera, Aphididae) by entomopathogenic fungi (Zygomycetes, Entomophthorales) and parasitoids (Hymenoptera, Braconidae and Encyrtidae) on irrigated spring wheat in southwestern Idaho. Environmental Entomology 1991, 20:1699-1710.
18. Feng M.G., Chen C., Shang S.W., Ying S.H., Shen Z.C., Chen X.X. Aphid dispersal flight disseminates fungal pathogens and parasitoids as natural control agents of aphids. Ecological Entomology 2007, 32:97-104.
19. Fournier A., Enkerli J., Keller S., Widmer F. A PCR-based tool for the cultivation-independent monitoring of Pandora neoaphidis. Journal of Invertebrate Pathology 2008, 99:49-56.
20. Fournier, A., Widmer, F., Enkerli, J., in press. Development of a single nucleotide polymorphism (SNP) assay for genotyping of Pandora neoaphidis. Fungal Biology. doi:10.1016/j.funbio.2010.03.012.
21. Hajek A.E., Humber R.A., Griggs M.H. Decline in virulence of Entomophaga maimaiga (Zygomycetes, Entomophthorales) with repeated in vitro subculture. Journal of Invertebrate Pathology 1990, 56:91-97.
22. Hartmann M., Frey B., Kölliker R., Widmer F. Semi-automated genetic analyses of soil microbial communities: comparison of T-RFLP and RISA based on descriptive and discriminative statistical approaches. Journal of Microbiological Methods 2005, 61:349-360.
23. Heid C.A., Stevens J., Livak K.J., Williams M. Real time quantitative PCR. Genome Research 1996, 6:986-994.
24. Hemmati F., Pell J.K., McCartney H.A., Deadman M.L. Airborne concentrations of conidia of Erynia neoaphidis above cereal fields. Mycological Research 2001, 105:485-489.
25. Katis N.I., Tsitsipis J.A., Stevens M., Powell G. Transmission of plant viruses. Aphids as Crop Pests 2007, 353-390. CAB International, Wallingford. H.F. van Emden, R. Harrington (Eds.).
26. Keller S. Arthropod-pathogenic Entomophthorales of Switzerland. II. Erynia, Eryniopsis, Neozygites, Zoophthora and Tarichium. Sydowia 1991, 43:39-122.
27. Keller S. The role of Entomophthorales in a sustainable agriculture. Insect pathogens and insect parasitic nematodes. IOBC Bulletin 1998, 21:13-16.
28. Keller S., Suter H. Epizootiologische Untersuchungen über das Entomophthora - Auftreten bei feldbaulich wichtigen Blattlausarten. Acta Oecologica/Oecologia Applicata 1980, 1:63-81.
29. Latteur G. The persistence of infectivity of conidia of Entomophthora obscura at different temperatures on the surface of an unsterilized soil. Acta Oecologica - Oecologia Applicata 1980, 1:29-34.
30. Lievens B., Grauwet T.J.M.A., Cammue B.P.A., Thomma B.P.H.J. Recent developments in diagnostics of plant pathogens: a review. Recent Research Developments in Microbiology 2005, 9:57-79.
31. Luterbacher J., Liniger M.A., Menzel A., Estrella N., Della-Marta P.M., Pfister C., Rutishauser T., Xoplaki E. Exceptional European warmth of autumn 2006 and winter 2007: historical context, the underlying dynamics, and its phenological impacts. Geophysical Research Letters 2007, 34:L12704.
32. Nielsen C., Sommer C., Eilenberg J., Hansen K.S., Humber R.A. Characterization of aphid pathogenic species in the genus Pandora by PCR techniques and digital image analysis. Mycologia 2001, 93:864-874.
33. Nielsen C., Hajek A.E., Humber R.A., Bresciani J., Eilenberg J. Soil as an environment for winter survival of aphid-pathogenic Entomophthorales. Biological Control 2003, 28:92-100.
34. Nielsen C., Jensen A.B., Eilenberg J. Survival of entomophthoralean fungi infecting aphids and higher flies during unfavorable conditions and implications for conservation biological control. Use of Entomopathogenic Fungi in Biological Pest Management 2008, 13-38. Research SignPost, Kerala, India. S. Ekesi, N.K. Maniania (Eds.).
35. Papierok B., Hajek A.E. Fungi: Entomophthorales. Manual of Techniques in Insect Pathology 1997, 187-212. Academic Press, San Diego. L. Lacey (Ed.).
36. Pell J.K., Eilenberg J., Hajek A.E., Steinkraus D.C. Biology, ecology, and pest management potential of Entomophthorales. Fungal Biological Control Agents: Progress, Problems and Potential 2001, 71-153. CAB International, Wallingford. T.M. Butt, C. Jackson, N. Magan (Eds.).
37. Powell W., Pell J.K. Biological control. Aphids as Crop Pests 2007, 469-513. CAB International, Wallingford. H.F. van Emden, R. Harrington (Eds.).
38. Quisenberry S.S., Ni X. Feeding injury. Aphids as Crop Pests 2007, 331-352. CAB International, Wallingford. H.F. van Emden, R. Harrington (Eds.).
39. Rohel E., Couteaudier Y., Papierok B., Cavelier N., Dedryver C.A. Ribosomal internal transcribed spacer size variation correlated with RAPD-PCR pattern polymorphisms in the entomopathogenic fungus Erynia neoaphidis and some closely related species. Mycological Research 1997, 101:573-579.
40. Roy H.E., Pell J.K., Alderson P.G. Targeted dispersal of the aphid pathogenic fungus Erynia neoaphidis by the aphid predator Coccinella septempunctata. Biocontrol Science and Technology 2001, 11:99-110.
41. Rutishauser T., Luterbacher J., Defila C., Frank D., Wanner H. Swiss spring plant phenology 2007: extremes, a multi-century perspective, and changes in temperature sensitivity. Geophysical Research Letters 2008, 35:L05703.
42. Schwarzenbach K., Widmer F., Enkerli J. Cultivation-independent analysis of fungal genotypes in soil by using simple sequence repeat markers. Applied and Environmental Microbiology 2007, 73:6519-6525.
43. Schwarzenbach K., Enkerli J., Widmer F. Effects of biological and chemical insect control agents on fungal community structures in soil microcosms. Applied Soil Ecology 2009, 42:54-62.
44. Shah P.A., Pell J.K. Entomopathogenic fungi as biological control agents. Applied Microbiology and Biotechnology 2003, 61:413-423.
45. Shah P.A., Clark S.J., Pell J. Assessment of aphid host range and isolate variability in Pandora neoaphidis (Zygomycetes: Entomophthorales). Biological Control 2004, 29:90-99.
46. Shah F.A., Allen N., Wright C.J., Butt T.M. Repeated in vitro subculturing alters spore surface properties and virulence of Metarhizium anisopliae. FEMS Microbiology Letters 2007, 276:60-66.
47. Steenberg T., Eilenberg J. Natural occurrence of entomopathogenic fungi on an agricultural field site. Czech Mycology 1995, 48:89-96.
48. Steinkraus D.C. Factors affecting transmission of fungal pathogens of aphids. Journal of Invertebrate Pathology 2006, 92:125-131.
49. Steinkraus D.C., Boys G.O., Slaymaker P.H. Culture, storage, and incubation period of Neozygites fresenii (Entomophthorales, Neozygitaceae) a pathogen of the cotton aphid. Southwestern Entomologist 1993, 18:197-202.
50. Steinkraus D.C., Hollingsworth R.G., Boys G.O. Aerial spores of Neozygites fresenii (Entomophthorales: Neozygitaceae): density, periodicity, and potential role in cotton aphid (Homoptera: Aphididae) epizootics. Environmental Entomology 1996, 25:48-57.
51. Tymon A.M., Pell J.K. ISSR, ERIC and RAPD techniques to detect genetic diversity in the aphid pathogen Pandora neoaphidis. Mycological Research 2005, 109:285-293.
52. Tymon A.M., Shah P.A., Pell J.K. PCR-based molecular discrimination of Pandora neoaphidis isolates from related entomopathogenic fungi and development of species-specific diagnostic primers. Mycological Research 2004, 108:419-433.
53. Versalovic J., Koeuth T., Lupski J.R. Distribution of repetitive DNA sequences in Eubacteria and application to fingerprinting of bacterial genomes. Nucleic Acids Research 1991, 19:6823-6831.
54. Wilding N. The effect of introducing aphid pathogenic Entomophthoraceae into field populations of Aphis fabae. Annals of Applied Biology 1981, 99:11-23.
55. Wilding N., Mardell S.K., Brobyn P.J. Introducing Erynia neoaphidis into a field population of Aphis fabae: form of the inoculum and effect of irrigation. Annals of Applied Biology 1986, 108:373-385.
56. Williams J.G.K., Kubelik A.R., Livak K.J., Rafalski J.A., Tingey S.V. DNA polymorphisms amplified by arbitrary primers are useful as genetic markers. Nucleic Acids Research 1990, 18:6531-6535.
57. Zietkiewicz E., Rafalski A., Labuda D. Genome fingerprinting by simple sequence repeat (SSR)-anchored polymerase chain reaction amplification. Genomics 1994, 20:176-183.