Skip to main content
Log in

Biological control of Phytophthora blight by Pseudomonas protegens strain 14D5

  • Published:
European Journal of Plant Pathology Aims and scope Submit manuscript

A Correction to this article was published on 13 January 2020

This article has been updated

Abstract

Foliage blight caused by Phytophthora nicotianae and Ph. tropicalis is an important disease of annual vinca (Catharanthus roseus). In this study, 121 strains of Pseudomonas species originally recovered from recycled irrigation water were evaluated in vitro and in planta for their biological control potentials against this disease. We found 12 strains belonging to Ps. granadensis and Ps. protegens that reduced the radial growth of colonies of Ph. nicotianae isolate 3A12 by >91% in 6-well plates. They also reduced the radial growth of 3A12 and Ph. tropicalis isolate 7G9 by at least 82 and 54%, respectively, in 10-cm plates. In planta, Ps. protegens strain 14D5 reduced the infection by isolate 3A12 on four cultivars of annual vinca by 36 to 59%. Disease control efficacy of 14D5 against isolate 7G9 ranged from 23 to 45% depending on the plant cultivar. Secondary metabolites produced by strain 14D5 significantly reduced the radial growth of both Phytophthora isolates 3A12 and 7G9 in liquid media. Treatments containing these metabolites also reduced encystment, germination, and survival rates of zoospores of isolate 3A12, and foliage blight severity on C. roseus ‘Pacifica Punch Xp’ caused by 3A12. Treatments containing live cells and metabolites of 14D5 resulted in higher zoospore mortality and disease reduction than those only containing metabolites. These findings indicated that producing anti-Phytophthora secondary metabolites is likely the major mode of action of stain 14D5, while other mechanisms such as parasitism might be involved in its biological control against Phytophthora foliage blight.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Change history

  • 13 January 2020

    This erratum is published as vendor overlooked several author corrections related with Table 1 & 2 during proofing.

References

  • Ahonsi, M. O., Banko, T. J., & Hong, C. X. (2007). A simple in-vitro ‘wet-plate’ method for mass production of Phytophthora nicotianae zoospores and factors influencing zoospore production. Journal of Microbiological Methods, 70, 557–560.

    Article  CAS  PubMed  Google Scholar 

  • Alvarez-Rodriguez, B., Ortiz-Meza, J. A., Rojo-Baez, I., Marquez-Zequera, I., Garcia-Estrada, R. S., Carrillo-Fasio, J. A., & Allende-Molar, R. (2013). First report of vinca blight caused by Phytophthora nicotianae in northwestern Mexico. Plant Disease, 97, 1257.

    Article  CAS  PubMed  Google Scholar 

  • Andreolli, M., Zapparoli, G., Angelini, E., Lucchetta, G., Lampis, S., & Vallini, G. (2019). Pseudomonas protegens MP12: A plant growth-promoting endophytic bacterium with broad-spectrum antifungal activity against grapevine phytopathogens. Microbiological Research, 219, 123–131.

    Article  PubMed  Google Scholar 

  • Brendel, N., Partida-Martinez, L. P., Scherlach, K., & Hertweck, C. (2007). A cryptic PKS-NRPS gene locus in the plant commensal Pseudomonas fluorescens Pf-5 codes for the biosynthesis of an antimitotic rhizoxin complex. Organic & Biomolecular Chemistry, 5, 2211–2213.

    Article  CAS  Google Scholar 

  • Burns, J. R., & Benson, D. M. (2000). Biocontrol of damping-off of Catharanthus roseus caused by Pythium ultimum with Trichoderma virens and binucleate Rhizoctonia fungi. Plant Disease, 84, 644–648.

    Article  CAS  PubMed  Google Scholar 

  • Caulier, S., Gillis, A., Colau, G., Licciardi, F., Liepin, M., Desoignies, N., Modrie, P., Legreve, A., Mahillon, J., & Bragard, C. (2018). Versatile antagonistic activities of soil-borne Bacillus spp. and Pseudomonas spp. against Phytophthora infestans and other potato pathogens. Frontiers in Microbiology, 9, 143.

    Article  PubMed  PubMed Central  Google Scholar 

  • Core Team, R. (2015). R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.

    Google Scholar 

  • Dastur, J. F. (1916). Phytophthora on Vinca rosea. Memoirs of the Department of Agriculture in India. Botanical series, 8, 233–242.

    Google Scholar 

  • de Mendiburu, F. (2015). Agricolae: Statistical procedures for agricultural research. In: R package version 1.2-3. http://CRAN.R-project.org/package=agricolae

  • De Vrieze, M., Germanier, F., Vuille, N., & Weisskopf, L. (2018). Combining different potato-associated Pseudomonas strains for improved biocontrol of Phytophthora infestans. Frontiers in Microbiology, 9, 2573.

    Article  PubMed  PubMed Central  Google Scholar 

  • De Vrieze, M., Gloor, R., Codina, J. M., Torriani, S., Gindro, K., L’Haridon, F., Bailly, A., & Weisskopf, L. (2019). Biocontrol activity of three Pseudomonas in a newly assembled collection of Phytophthora infestans isolates. Phytopathology, 109, 1555–1565.

    Article  PubMed  Google Scholar 

  • Erwin, D. C., & Ribeiro, O. K. (1996). Phytophthora diseases worldwide. St. Paul: APS Press.

    Google Scholar 

  • Ferrin, D. M., & Rohde, R. G. (1992a). In vivo expression of resistance to metalaxyl by a nursery isolate of Phytophthora parasitica from Catharanthus roseus. Plant Disease, 76, 82–84.

    Article  CAS  Google Scholar 

  • Ferrin, D. M., & Rohde, R. G. (1992b). Population dynamics of Phytophthora parasitica, the cause of root and crown rot of Catharanthus roseus, in relation to fungicide use. Plant Disease, 76, 60–63.

    Article  CAS  Google Scholar 

  • Firman, I. D. (1975). Phytophthora and Pythium species and the diseases caused by them in the area of the South Pacific Commission. Fiji Agricultural Journal, 37, 1–8.

    Google Scholar 

  • Gallegly, M. E., & Hong, C. (2008). Phytophthora: Identifying species by morphology and DNA fingerprints (1st ed.). St. Paul: American Phytopathological Society.

    Google Scholar 

  • Garibaldi, A., Bertetti, D., & Gullino, M. L. (2006). First report of leaf blight caused by Rhizoctonia solani AG 1B on Madagascar periwinkle (Catharanthus roseus) in Italy. Plant Disease, 90, 1361–1361.

    Article  CAS  PubMed  Google Scholar 

  • Gill, H. S., Ribeiro, O. K., & Zentmyer, G. A. (1977). Phytophthora blight of periwinkles in the Coachella Valley of California. Plant Disease Reporter, 61, 560–561.

  • Gross, H., Stockwell, V. O., Henkels, M. D., Nowak-Thompson, B., Loper, J. E., & Gerwick, W. H. (2007). The genomisotopic approach: A systematic method to isolate products of orphan biosynthetic gene clusters. Chemistry & Biology, 14, 53–63.

    Article  CAS  Google Scholar 

  • Guyer, A., De Vrieze, M., Bonisch, D., Gloor, R., Musa, T., Bodenhausen, N., Bailly, A., & Weisskopf, L. (2015). The anti-Phytophthora effect of selected potato-associated Pseudomonas strains: From the laboratory to the field. Frontiers in Microbiology, 6, 1309.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hao, W., Richardson, P. A., & Hong, C. X. (2010). Foliar blight of annual vinca (Catharanthus roseus) caused by Phytophthora tropicalis in Virginia. Plant Disease, 94, 274.

    Article  CAS  PubMed  Google Scholar 

  • Holcomb, G. E., & Carling, D. E. (2002). First report of web blight caused by Rhizoctonia solani on Catharanthus roseus in Louisiana. Plant Disease, 86, 1272.

    Article  CAS  PubMed  Google Scholar 

  • Howell, C. R., & Stipanovic, R. D. (1979). Control of Rhizoctonia solani in cotton seedlings with Pseudomonas fluorescens and with an antibiotic produced by the bacterium. Phytopathology, 69, 480–482.

    Article  CAS  Google Scholar 

  • Howell, C. R., & Stipanovic, R. D. (1980). Suppression of Pythium ultimum induced damping-off of cotton seedlings by Pseudomonas fluorescens and its antibiotic, pyoluteorin. Phytopathology, 70, 712–715.

    Article  CAS  Google Scholar 

  • Hu, J. H., Hong, C. X., Stromberg, E. L., & Moorman, G. W. (2008). Mefenoxam sensitivity and fitness analysis of Phytophthora nicotianae isolates from nurseries in Virginia, USA. Plant Pathology, 57, 728–736.

    Article  CAS  Google Scholar 

  • Huang, Y., Ma, L., Fang, D. H., Xi, J. Q., Zhu, M. L., Mo, M. H., Zhang, K. Q., & Ji, Y. P. (2015). Isolation and characterisation of rhizosphere bacteria active against Meloidogyne incognita, Phytophthora nicotianae and the root knot-black shank complex in tobacco. Pest Management Science, 71, 415–422.

    Article  CAS  PubMed  Google Scholar 

  • Hwang, J., & Benson, D. M. (2005). Identification, mefenoxam sensitivity, and compatibility type of Phytophthora spp. attacking floriculture crops in North Carolina. Plant Disease, 89, 185–190.

    Article  CAS  PubMed  Google Scholar 

  • Keim, R. (1977). Foliage blight of periwinkle in southern California. Plant Disease Reporter, 61, 182–184.

    Google Scholar 

  • Khatun, A., Farhana, T., Sabir, A. A., Islam, S. M. N., West, H. M., Rahman, M., & Islam, T. (2018). Pseudomonas and Burkholderia inhibit growth and asexual development of Phytophthora capsici. Zeitschrift Fur Naturforschung Section C- Journal of Biosciences, 73, 123–135.

    Article  CAS  Google Scholar 

  • Kidarsa, T. A., Goebel, N. C., Zabriskie, T. M., & Loper, J. E. (2011). Phloroglucinol mediates crosstalk between the pyoluteorin and 2,4-diacetylphloroglucinol biosynthetic pathways in Pseudomonas fluorescens Pf-5. Molecular Microbiology, 81, 395–414.

    Article  CAS  PubMed  Google Scholar 

  • Kong, P., Hong, C. X., Richardson, P. A., & Gallegly, M. E. (2003). Single-strand-conformation polymorphism of ribosomal DNA for rapid species differentiation in genus Phytophthora. Fungal Genetics and Biology, 39, 238–249.

    Article  CAS  PubMed  Google Scholar 

  • Kraus, J., & Loper, J. E. (1992). Lack of evidence for a role of antifungal metabolite production by Pseudomonas fluorescens Pf-5 in biological control of Pythium damping-off of cucumber. Phytopathology, 82, 264–271.

    Article  Google Scholar 

  • Lim, Y.-S., Choi, C.-D., & Kim, B.-S. (2004). Foliage blight of vinca (Catharanthus roseus) by Phytophthora nicotianae. Research in Plant Disease, 10, 17–20.

    Article  Google Scholar 

  • Lin, S., Martin, D. E., Taylor, N. J., Gabriel, C. K., Ganeshan, V. D., & Hand, F. P. (2018). First report of Phytophthora aerial blight caused by Phytophthora nicotianae on vinca, lobelia, and calibrachoa in Ohio. Plant Disease, 102, 456–456.

    Article  Google Scholar 

  • Luongo, L., Vitale, S., Galli, M., Haegi, A., Wagner, S., Werres, S., & Belisario, A. (2016). Morphological and molecular identification of Phytophthora tropicalis as causal agent of crown and root rot on Albizia julibrissin. Journal of Phytopathology, 164, 959–966.

    Article  CAS  Google Scholar 

  • McGovern, R. J., McSorley, R., & Urs, R. R. (2000). Reduction of Phytophthora blight of Madagascar periwinkle in Florida by soil solarization in autumn. Plant Disease, 84, 185–191.

    Article  CAS  PubMed  Google Scholar 

  • Michavila, G., Adler, C., De Gregorio, P. R., Lami, M. J., Caram Di Santo, M. C., Zenoff, A. M., de Cristobal, R. E., & Vincent, P. A. (2017). Pseudomonas protegens CS1 from the lemon phyllosphere as a candidate for citrus canker biocontrol agent. Plant Biology, 19, 608–617.

    Article  CAS  PubMed  Google Scholar 

  • Miguelez-Sierra, Y., Acebo-Guerrero, Y., El Jaziri, M., Bertin, P., & Hernández-Rodríguez, A. (2019). Pseudomonas chlororaphis CP07 strain reduces disease severity caused by Phytophthora palmivora in genotypes of Theobroma cacao. European Journal of Plant Pathology, In Press, https://doi.org/10.1007/s10658-10019-01842-10658.

  • Moruzzi, S., Firrao, G., Polano, C., Borselli, S., Loschi, A., Ermacora, P., Loi, N., & Martini, M. (2017). Genomic-assisted characterisation of Pseudomonas sp strain Pf4, a potential biocontrol agent in hydroponics. Biocontrol Science and Technology, 27, 969–991.

    Article  Google Scholar 

  • Nowakthompson, B., Gould, S. J., Kraus, J., & Loper, J. E. (1994). Production of 2,4-diacetylphloroglucinol by the biocontrol agent Pseudomonas fluorescens Pf-5. Canadian Journal of Microbiology, 40, 1064–1066.

    Article  CAS  Google Scholar 

  • Olson, H. A., Jeffers, S. N., Ivors, K. L., Steddom, K. C., Williams-Woodward, J. L., Mmbaga, M. T., Benson, D. M., & Hong, C. X. (2013). Diversity and mefenoxam sensitivity of Phytophthora spp. associated with the ornamental horticulture industry in the southeastern United States. Plant Disease, 97, 86–92.

    Article  CAS  PubMed  Google Scholar 

  • Ortega-Acosta, S. A., Hernandez-Morales, J., Ochoa-Martinez, D. L., & Ayala-Escobar, V. (2017). First report of Phytophthora tropicalis causing stem and root rot on sesame (Sesamum indicum) in Mexico. Plant Disease, 101, 258.

    Article  Google Scholar 

  • Pane, A., Cacciola, S. O., Scibetta, S., Bentivenga, G., & Lio, G. M. D. (2009). Four Phytophthora species causing foot and root rot of apricot in Italy. Plant Disease, 93, 844–845.

    Article  CAS  PubMed  Google Scholar 

  • Pasquier, E., & Kavallaris, M. (2008). Microtubules: A dynamic target in cancer therapy. IUBMB Life, 60, 165–170.

    Article  CAS  PubMed  Google Scholar 

  • Philmus, B., Shaffer, B. T., Kidarsa, T. A., Yan, Q., Raaijmakers, J. M., Begley, T. P., & Loper, J. E. (2015). Investigations into the biosynthesis, regulation, and self-resistance of toxoflavin in Pseudomonas protegens Pf-5. Chembiochem, 16, 1782–1790.

    Article  CAS  PubMed  Google Scholar 

  • Polano, C., Martini, M., Savian, F., Moruzzi, S., Ermacora, P., & Firrao, G. (2019). Genome sequence and antifungal activity of two niche-sharing Pseudomonas protegens related strains isolated from hydroponics. Microbial Ecology, 77, 1025–1035.

    Article  PubMed  Google Scholar 

  • Quecine, M. C., Kidarsa, T. A., Goebel, N. C., Shaffer, B. T., Henkels, M. D., Zabriskie, T. M., & Loper, J. E. (2016). An interspecies signaling system mediated by fusaric acid has parallel effects on antifungal metabolite production by Pseudomonas protegens strain Pf-5 and antibiosis of Fusarium spp. Applied and Environmental Microbiology, 82, 1372–1382.

    Article  CAS  PubMed Central  Google Scholar 

  • Ramette, A., Frapolli, M., Fischer-Le Saux, M., Gruffaz, C., Meyer, J.-M., Defago, G., Sutra, L., & Moenne-Loccoz, Y. (2011). Pseudomonas protegens sp. nov., widespread plant-protecting bacteria producing the biocontrol compounds 2,4-diacetylphloroglucinol and pyoluteorin. Systematic and Applied Microbiology, 34, 180–188.

    Article  CAS  PubMed  Google Scholar 

  • Schubert, T. S., & Leahy, R. M. (1989). Phytophthora blight of the Catharanthus roseus. Florida Department of Agriculture & Consumer Services. Plant Pathology Circular, 321, 174–175.

  • Shi, J. Y., Liu, A. Y., Li, X. P., & Chen, W. X. (2013). Control of Phytophthora nicotianae disease, induction of defense responses and genes expression of papaya fruits treated with Pseudomonas putida MGP1. Journal of the Science of Food and Agriculture, 93, 568–574.

    Article  CAS  PubMed  Google Scholar 

  • Smits, T. H. M., Rezzonico, F., Frasson, D., Vesga, P., Vacheron, J., Blom, J., Pothier, J. F., Keel, C., Maurhofer, M., & Sievers, M. (2019). Updated genome sequence and annotation for the full genome of Pseudomonas protegens CHA0. Microbiology Resource Announcements, 8, e01002–e01019.

    Article  PubMed  PubMed Central  Google Scholar 

  • Sowanpreecha, R., & Rerngsamran, P. (2018). Biocontrol of orchid-pathogenic mold, Phytophthora palmivora, by antifungal proteins from Pseudomonas aeruginosa RS1. Mycobiology, 46, 129–137.

    Article  PubMed  PubMed Central  Google Scholar 

  • Stearn, W. (1975). A synopsis of the genus Catharanthus (Apocynaceae). In W. Taylor & N. Fransworth (Eds.), Catharanthus alkaloids (pp. 9–44). New York: Marcel Dekker.

    Google Scholar 

  • Takeuchi, K., Noda, N., & Someya, N. (2014). Complete genome sequence of the biocontrol strain Pseudomonas protegens Cab57 discovered in Japan reveals strain-specific diversity of this species. PLoS One, 9, e93683.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wagner, A., Norris, S., Chatterjee, P., Morris, P. F., & Wildschutte, H. (2018). Aquatic pseudomonads inhibit oomycete plant pathogens of Glycine max. Frontiers in Microbiology, 9, 1007.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang, S., & Buk, J. (2013). First detection and molecular identification of Phytophthora parasitica from annual vinca in Nevada. Phytopathology, 103, 155–156.

    Article  Google Scholar 

  • Yang, X., & Hong, C. X. (2018). Biological control of boxwood blight by Pseudomonas protegens recovered from recycling irrigation systems. Biological Control, 124, 68–73.

    Article  Google Scholar 

  • Ziegler, J., & Facchini, P. J. (2008). Alkaloid biosynthesis: Metabolism and trafficking. Annual Review of Plant Biology, 59, 735–769.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors wish to thank Dr. Giovanni Cafà for isolating bacterial strains and Mrs. Patricia Richardson for her assistance in identifying bacterial strains and Phytophthora isolates used in this study.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Xiao Yang.

Ethics declarations

This paper reports original research by the authors which has not been published elsewhere nor submitted for publication elsewhere.

Conflict of interest

The authors declare that they have no conflict of interest.

Human and animal rights

This article does not contain any studies with human or animal subjects performed by any of the authors.

Electronic Supplementary Material

ESM 1

(XLSX 18 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yang, X., Hong, C. Biological control of Phytophthora blight by Pseudomonas protegens strain 14D5. Eur J Plant Pathol 156, 591–601 (2020). https://doi.org/10.1007/s10658-019-01909-6

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-019-01909-6

Keywords

Navigation