Leaf microbiota of strawberries as affected by biological control agents

Phytopathology

Volumn 103, Issue 10, 2013, Pages 1001-1011

  Sylla, Justine ^a,b   Alsanius, Beatrix W ^b   Krüger, Erika ^a   Reineke, Annette ^a   Strohmeier, Stephan ^c   Wohanka, Walter ^a  

^a HOCHSCHULE GEISENHEIM UNIVERSITY   (Germany)

^b SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^c FreshX Consulting and Development   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL CONTROL AGENT; RNA 16S;

BIOLOGICAL CONTROL AGENT; FRAGARIA; GENETICS; MICROBIOLOGY; MICROFLORA; PLANT DISEASE; PLANT LEAF;

BIOLOGICAL CONTROL AGENTS; FRAGARIA; MICROBIOTA; PLANT DISEASES; PLANT LEAVES; RNA, RIBOSOMAL, 16S;

EID: 84885133657     PISSN: 0031949X     EISSN: None     Source Type: Journal    
DOI: 10.1094/PHYTO-01-13-0014-R     Document Type: Article

References (52)

1. Andrews, J. H., and Harris, R. F. 2000. The ecology and biogeography of microorganisms of plant surfaces. Annu. Rev. Phytopathol. 38:145-180.
2. Beattie, G. A., and Lindow, S. E. 1999. Bacterial colonization of leaves: A spectrum of strategies. Phytopathology 89:353-359.
3. Bernard, E., Larkin, R. P., Tavantzis, S., Erich, M. S., Alyokhin, A., Sewell, G., Lannan, A., and Gross, S. D. 2012. Compost, rapeseed rotation, and biocontrol agents significantly impact soil microbial communities in organic and conventional potato production systems. Appl. Soil Ecol. 52:29-41.
4. Bilu, A., Dag, A., Elad, Y., and Shafir, S. 2004. Honey bee dispersal of biocontrol agents: An evaluation of dispensing devices. Biocontrol Sci. Technol. 14:607-617.
5. Brimner, T. A., and Boland, G. J. 2003. A review of the non-target effects of fungi used to biologically control plant diseases. Agric. Ecosyst. Environ. 100:3-16.
6. Buée, M., Reich, M., Murat, C., Morin, E., Nilsson, R. H., Uroz, S., and Martin, F. 2009. 454 Pyrosequencing analyses of forest soils reveal an unexpectedly high fungal diversity. New Phytol. 184:449-456.
7. Cook, J., Bruckart, W. L., Coulson, J. R., Goettel, M. S., Humber, R. A., Lumsden, R. D., Maddox, J. V., McManus, M. L., Moore, L., Meyer, S. F., Quimby, P. C., Stack, J. P., and Vaughn, J. L. 1996. Safety of microorganisms intended for pest and plant disease control: A framework for scientific evaluation. Biol. Control 7:333-351.
8. Delmotte, N., Knief, C., Chaffron, S., Innerebner, G., Roschitzki, B., Schlapbach, R., von Mering, C., and Vorholt J. A. 2009. Community proteogenomics reveals insights into the physiology of phyllosphere bacteria. Proc. Natl. Acad. Sci. USA 106:16428-16433.
9. Droby, S., and Lichter, A. 2004. Post-harvest Botrytis infection: Etiology, development and management. Pages 349-367 in: Botrytis: Biology, Pathology and Control. Y. Elad, B. Williamson, P. Tudzynski, and N. Delen, eds. Springer, The Netherlands.
10. Edel-Hermann, V., Brenot, S., Gautheron, N., Aimé, S., Alabouvette, C., and Steinberg, C. 2009. Ecological fitness of the biocontrol agent Fusarium oxysporum Fo47 in soil and its impact on the soil microbial communities. FEMS Microbiol. Ecol. 68:37-45.
11. Elad, Y. 2000. Biological control of foliar pathogens by means of Trichoderma harzianum and potential modes of action. Crop Prot. 19:709-714.
12. Elad, Y., and Stewart, A.. 2004. Microbial control of Botrytis spp. Pages 223-241 in: Botrytis: Biology, Pathology and Control. Y. Elad, B. Williamson, P. Tudzynski, and N. Delen, eds. Springer, The Netherlands.
13. Finkel, O. M., Burch, A. Y., Lindow, S. E., Post, A. F., and Belkin, S. 2011. Geographical location determines the population structure in phyllosphere microbial communities of a salt-excreting desert tree. Appl. Environ. Microbiol. 77:7647-7655.
14. Freeman, S., Minz, D., Kolesnik, I., Barbul, O., Zveibil, A., Maymon, M., Nitzani, Y., Kirshner, B., Rav-David, D., Bilu, A., Dag, A., Shafir, S., and Elad, Y. 2004. Trichoderma biocontrol of Colletotrichum acutatum and Botrytis cinerea and survival in strawberry. Eur. J. Plant Pathol. 110:361-370.
15. Gao, G., Yin, D., Chen, S., Xia, F., Yang, J., Li, Q., and Wang, W. 2012. Effect of biocontrol agent Pseudomonas fluorescens 2P24 on soil fungal community in cucumber rhizosphere using T-RFLP and DGGE. PLoS ONE 7:e31806.
16. Hamp, T. J., Jones, W. J., and Fodor, A. A. 2009. Effects of experimental choices and analysis noise on surveys of the "rare biosphere". Appl. Environ. Microbiol. 75:3263-3270.
17. Helbig, J., and Bochow, H. 2001. Effectiveness of Bacillus subtilis (isolate 25021) in controlling Botrytis cinerea in strawberry. J. Plant Dis. Prot. 108:545-559.
18. Hirsch, J., Strohmeier, S., Pfannkuchen, M., and Reineke, A. 2012. Assessment of bacterial endosymbiont diversity in Otiorhynchus spp. (Coleoptera: Curculionidae) larvae using a multitag 454 pyrosequencing approach. BMC Microbiol. 12 (Suppl. 1):S6.
19. Kadivar, H., and Stapleton, A. E. 2003. Ultraviolet radiation alters maize phyllosphere bacterial diversity. Microb. Ecol. 45:353-361.
20. Kim, Y., Cho, M., Jeong, J., Lee, H., and Kim, S. 2010. Application of terminal restriction fragment length polymorphism (T-RFLP) analysis to monitor effect of biocontrol agents on rhizosphere microbial community of hot pepper (Capsicum annuum L.). J. Microbiol. 48:566-572.
21. Kovach, J., Petzoldt, R., and Harman, G. E. 2000. Use of honey bees and bumble bees to disseminate Trichoderma harzianum 1295-22 to strawberries for Botrytis control. Biol. Control 18:235-242.
22. Krimm, U., Abanda-Nkpwatt, D., Schwab, W., and Schreiber, L. 2005. Epiphytic microorganisms on strawberry plants (Fragaria ananassa cv. Elsanta): Identification of bacterial isolates and analysis of their interaction with leaf surfaces. FEMS Microbiol. Ecol. 53:483-492.
23. Kronstad, J. W. 2000. Infections strategies of Botrytis cinerea and related necrotrophic pathogens Pages 33-64 in: Fungal Pathology. J. W. Kronstad, ed. Kluwer Academic Publishers, Dordrecht, The Netherlands.
24. Lindow, S. E., and Brandl, M. T. 2003. Microbiology of the phyllosphere. Appl. Environ. Microbiol. 69:1875-1883.
25. Lindow, S. E., and Leveau, J. H. J. 2002. Phyllosphere microbiology. Curr. Opin. Biotechnol. 13:238-243.
26. Mäder, R., Liebl, B., and Wilbois, K.-P. 2011. Betriebsmittelliste 2011 für den ökologischen Landbau in Deutschland. Forschungsinstitut für Biologischen Landbau Deutschland e.V., Frankfurt am Main, Germany.
27. Meier, U., Graf, H., Hack, H., Hess, M., Kennel, W., Klose, R., Mappes, D., Seipp, D., Stauss, R., Streif, J., and van den Boom, T. 1994. Phänologische Entwicklungsstadien des Kernobstes (Malus domestica Borkh. und Pyrus communis L.), des Steinobstes (Prunus-Arten), der Johannisbeere (Ribes-Arten) und der Erdbeere (Fragaria × ananassa Duch.). Nachrichtenbl. Dtsch. Pflanzenschutzd. 46:141-153.
28. Meyer, K. M., and Leveau, J. H. J. 2012. Microbiology of the phyllosphere: A playground for testing ecological concepts. Oecologia 168:621-629.
29. Monier, J. M., and Lindow, S. E. 2005. Aggregates of resident bacteria facilitate survival of immigrant bacteria on leaf surfaces. Microbiol. Ecol. 49:343-352.
30. Okon Levy, N., Elad, Y., Katan, J., Baker, S. C., and Faull, J. L. 2006. Trichoderma and soil solarization induced microbial changes on plant surfaces. IOBC/WPRS Bull. 29:21-26.
31. Ottesen, A. R., White, J. R., Skaltsas, D. N., Newell, M. J., and Walsh, C. S. 2009. Impact of organic and conventional management on the phyllosphere microbial ecology of an apple crop. J. Food Prot. 72:2321-2325.
32. Rappe, M. S., and Giovannoni, S. J. 2003. The uncultured microbial majority. Annu. Rev. Microbiol. 57:369-394.
33. Rastogi, G., Sbodio, A., Tech, J. J., Suslow, T. V., Coaker, G. L., and Leveau, J. H. J. 2012. Leaf microbiota in an agroecosystem: Spatiotemporal variation in bacterial community composition on field-grown lettuce. ISME J. 6:1812-1822.
34. Rice, W. R. 1989. Analyzing tables of statistical tests. Evolution 43:223-225.
35. Russell, D., Chard, J., and McKinlay, R. 1999. Effect of Bacillus thuringiensis and a pyrethroid insecticide on the leaf microflora of Brassica oleracea. Lett. Appl. Microbiol. 28:359-362.
36. Savazzini, F., Longa, C. M. O., and Pertot, I. 2009. Impact of the biocontrol agent Trichoderma atroviride SC1 on soil microbial communities of a vineyard in northern Italy. Soil Biol. Biochem. 41:1457-1465.
37. Scherwinski, K., Grosch, R., and Berg, G. 2008. Effect of bacterial antagonists on lettuce: Active biocontrol of Rhizoctonia solani and negligible, short-term effects on nontarget microorganisms. FEMS Microbiol. Ecol. 64:106-116.
38. Scherwinski, K., Wolf, A., and Berg, G. 2007. Assessing the risk of biological control agents on the indigenous microbial communities: Serratia plymuthica HRO-C48 and Streptomyces sp. HRO-71 as model bacteria. BioControl 52:87-112.
39. Schmid, F., Moser, G., Müller, H., and Berg, G. 2011. Functional and structural microbial diversity in organic and conventional viticulture: Organic farming benefits natural biocontrol agents. Appl. Environ. Microbiol. 77:2188-2191.
40. Shafir, S., Dag, A., Bilu, A., Abu-Toamy, M., and Elad, Y. 2006. Honey bee dispersal of the biocontrol agent Trichoderma harzianum T39: Effectiveness in suppressing Botrytis cinerea on strawberry under field conditions. Eur. J. Plant Pathol. 116:119-128.
41. Shtienberg, D. 2004. Rational management of Botrytis-incited diseases: Integration of control measures and use of warning systems. Pages 335-347 in: Botrytis: Biology, Pathology and Control. Y. Elad, B. Williamson, P. Tudzynski, and N. Delen, eds. Springer, The Netherlands.
42. Suda, W., Nagasaki, A., and Shishido, M. 2009. Powdery mildewinfection changes bacterial community composition in the phyllosphere. Microbes Environ. 24:217-223.
43. Tefera, T., and Vidal, S. 2009. Effect of inoculation method and plant growth medium on endophytic colonization of sorghum by the entomopathogenic fungus Beauveria bassiana. BioControl 54:663-669.
44. Timms-Wilson, T. M., Kilshaw, K., and Bailey, M. J. 2004. Risk assessment for engineered bacteria used in biocontrol of fungal disease in agricultural crops. Plant Soil 266:57-67.
45. Vega, F. E., Posada, F., Aime, M. C., Pava-Ripoll, M., Infante, F., and Rehner, S. A. 2008. Entomopathogenic fungal endophytes. Biol. Control 46:72-82.
46. Walter, M., Frampton, C. M., Boyd-Wilson, K. S. H., Harris-Virgin, P., and Waipara, N. W. 2007. Agrichemical impact on growth and survival of non-target apple phyllosphere microorganisms. Can. J. Microbiol. 53:45-55.
47. Weber, R. W. S. 2011. Resistance of Botrytis cinerea to multiple fungicides in northern German small-fruit production. Plant Dis. 95:1263-1269.
48. Whipps, J. M., Hand, P., Pink, D., and Bending, G. D. 2008. Phyllosphere microbiology with special reference to diversity and plant genotype. J. Appl. Microbiol. 105:1744-1755.
49. Yang, C. H., Crowley, D. E., Borneman, J., and Keen, N. T. 2001. Microbial phyllosphere populations are more complex than previously realized. Proc. Natl. Acad. Sci. USA 98:3889-3894.
50. Zhang, B., Bai, Z., Hoefel, D., Tang, L., Wang, X., Li, B., Li, Z., and Zhuang, G. 2009. The impacts of cypermethrin pesticide application on the non-target microbial community of the pepper plant phyllosphere. Sci. Total Environ. 407:1915-1922.
51. Zhang, B., Bai, Z., Hoefel, D., Tang, L., Yang, Z., Zhuang, G., Yang, J., and Zhang, H. 2008. Assessing the impact of the biological control agent Bacillus thuringiensis on the indigenous microbial community within the pepper plant phyllosphere. FEMS Microbiol. Lett. 284:102-108.
52. Zhang, B., Zhang, H., Jin, B., Tang, L., Yang, J., Li, B., Zhuang, G., and Bai, Z. 2008. Effect of cypermethrin insecticide on the microbial community in cucumber phyllosphere. J. Environ. Sci. 20:1356-1362.