Skip to main content
SpringerLink
Log in

Potential of combined biological control agents to cope with Phytophthora parasitica, a major pathogen of Choisya ternata

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

Abstract

Phytophthora parasitica infection of Choisya ternata can cause important economical loses due to root rot disease. This research focused on testing the potential benefit of chemical treatment (Mefenoxam) and Biological Control Agents (Glomus intraradices, Gliocladium catenulatum, Trichoderma atroviridae and Bacillus amyloliquefaciens) in protecting C. ternata against P. parasitica. BCAs were applied as individual and/or combined treatments. The effect of the treatment was observed by monitoring C. ternata symptoms. A real-time PCR targeting the ypt1 gene was also adapted to evaluate P. parasitica development in the substrate. The use of Mefenoxam provided the higher level of plant protection. However, a significant reduction in plant symptoms and P. parasitica development was also observed with the combined treatment of G. intraradices with G. catenulatum and G. intraradices with T. atroviridae. Another combined treatment with G. catenulatum and B. amyloliquefaciens increased the pathogen density and severity. No individual treatment had a significant effect on the pathogen. Our results highlight the potential of biological control in protecting C. ternata against P. parasitica and the advantage of combined strategies.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Aragaki, M., & Uchida, J. Y. (2001). Morphological distinctions between Phytophthora capsici and P. tropicalis sp. nov. Mycologia, 93(1), 137–145.

    Article  Google Scholar 

  • Attard, A., Evangelisti, E., Kebdani-Minet, N., Panabières, F., Deleury, E., Maggio, C., Ponchet, M., & Gourgues, M. (2014). Transcriptome dynamics of Arabidopsis thaliana root penetration by the oomycete pathogen Phytophthora parasitica. BMC Genomics, 15, 538.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bellemain, E., Carlsen, T., Brochmann, C., Coissac, E., Taberlet, P., & Kauserud, H. a. (2010). ITS as an environmental DNA barcode for fungi: an in silico approach reveals potential PCR biases. BMC Microbiology, 10(1), 189.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Benfradj, N., Metoui, N., & Boughalleb-M’Hamdi, N. (2016). Screening for tolerance of different citrus rootstocks against zoospores of Phytophthora nicotianae in infested soil. Journal of Phytopathology and Pest Management, 3(3), 63–75.

    Google Scholar 

  • Benitez, T., Rincón, A. M., Limón, M. C., & Codón, A. C. (2004). Biocontrol mechanisms of Trichoderma strains. International Microbiology: The Official Journal of the Spanish Society for Microbiology, 7(4), 249–260.

    CAS  Google Scholar 

  • Boava, L. P., Cristofani-Yaly, M., Mafra, V. S., Kubo, K., Kishi, L. T., Takita, M. A., Ribeiro-Alves, M., & Machado, M. A. (2011). Global gene expression of Poncirus trifoliata, Citrus sunki and their hybrids under infection of Phytophthora parasitica. BMC Genomics, 12(1), 39.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bodker, L., Kjøller, R., & Rosendahl, S. (1998). Effect of phosphate and the arbuscular mycorrhizal fungus Glomus intraradices on disease severity of root rot of peas (Pisum sativum) caused by Aphanomyces euteiches. Mycorrhiza, 8(3), 169–174.

    Article  CAS  Google Scholar 

  • Bora, T., Özaktan, H., Göre, E., & Aslan, E. (2004). Biological control of Fusarium oxysporum f. sp. melonis by wettable powder formulations of the two strains of Pseudomonas putida. Journal of Phytopathology, 152(8–9), 471–475.

    Article  Google Scholar 

  • Boyd, D. R., Sharma, N. D., Loke, P. L., Malone, J. F., McRoberts, W. C., & Hamilton, J. T. G. (2007). Synthesis, structure and stereochemistry of quinoline alkaloids from Choisya ternata. Organic & Biomolecular Chemistry, 5, 2983.

    Article  CAS  Google Scholar 

  • Bridge, P., & Spooner, B. (2001). Soil fungi: diversity and detection. Plant and Soil, 232(1–2), 147–154.

    Article  CAS  Google Scholar 

  • Brunner, K., Zeilinger, S., Ciliento, R., Woo, S. L., Lorito, M., Kubicek, C. P., & Mach, R. L. (2005). Improvement of the fungal biocontrol agent Trichoderma atroviride to enhance both antagonism and induction of plant systemic disease resistance. Applied and Environmental Microbiology, 71(7), 3959–3965.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cacciola, S. O., Spica, D., Cooke, D. E. L., Raudino, F., & di San Lio, G. M. (2006). Wilt and collapse of Cuphea ignea caused by Phytophthora tropicalis in Italy. Plant Disease, 90(5), 680–680.

    Article  CAS  PubMed  Google Scholar 

  • Cameron, D. D., Neal, A. L., van Wees, S. C. M., & Ton, J. (2013). Mycorrhiza-induced resistance: more than the sum of its parts? Trends in Plant Science, 18(10), 539–545.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chemeltorit, P. P., Mutaqin, K. H., & Widodo, W. (2017). Combining Trichoderma hamatum THSW13 and Pseudomonas aeruginosa BJ10-86: a synergistic chili pepper seed treatment for Phytophthora capsici infested soil. European Journal of Plant Pathology, 147(1), 157–166.

    Article  Google Scholar 

  • Chen, Y., & Roxby, R. (1996). Characterization of a Phytophthora infestans gene involved in vesicle transport. Gene, 181(1–2), 89–94.

    Article  CAS  Google Scholar 

  • Conrath, U., Beckers, G. J. M., Flors, V., García-Agustín, P., Jakab, G., Mauch, F., et al. (2006). Priming: getting ready for battle. Molecular Plant-Microbe Interactions, 19(10), 1062–1071.

    Article  CAS  PubMed  Google Scholar 

  • Cullen, D. W., & Hirsch, P. R. (1998). Simple and rapid method for direct extraction of microbial DNA from soil for PCR. Soil Biology and Biochemistry, 30(8), 983–993.

    Article  CAS  Google Scholar 

  • Davidse, L. C., Looijen, D., Turkensteen, L. J., & Wal, D. v. d. (1981). Occurrence of metalaxyl-resistant strains of Phytophthora infestans in Dutch potato fields. Netherlands Journal of Plant Pathology, 87(2), 65–68.

    Article  Google Scholar 

  • Drenth, A., & Guest, D.I. (2004). Diversity and management of Phytophthora in Southeast Asia. Canberra, Australia: Australian Centre for International Agricultural Research (ACIAR).

  • Drenth, A., Wagels, G., Smith, B., Sendall, B., O’Dwyer, C., Irvine, G., & Irwin, J. A. G. (2006). Development of a DNA-based method for detection and identification of Phytophthora species. Australasian Plant Pathology, 35(2), 147–159.

    Article  CAS  Google Scholar 

  • Farr, D. F., & Rossman, A. Y. (2017). Fungal Databases, U.S. National Fungus Collections, ARS, USDA. https://nt.ars-grin.gov/fungaldatabases/new_allView.cfm?whichone=FungusHost&thisName=Phytophthora%20parasitica&organismtype=Fungus&fromAllCount=yes. Accessed 3 July 2017.

  • Filion, M., St-Arnaud, M., & Fortin, J. A. (1999). Direct interaction between the arbuscular mycorrhizal fungus Glomus intraradices and different rhizosphere microorganisms. New Phytologist, 141(3), 525–533.

    Article  Google Scholar 

  • Filion, M., St-Arnaud, M., & Jabaji-Hare, S. H. (2003). Quantification of Fusarium solani f. sp. phaseoli in mycorrhizal bean plants and surrounding Mycorrhizosphere soil using real-time polymerase chain reaction and direct isolations on selective media. Phytopathology, 93(2), 229–235.

    Article  CAS  PubMed  Google Scholar 

  • Galiana, E., Rivière, M.-P., Pagnotta, S., Baudouin, E., Panabières, F., Gounon, P., & Boudier, L. (2005). Plant-induced cell death in the oomycete pathogen Phytophthora parasitica. Cellular Microbiology, 7(9), 1365–1378.

    Article  CAS  PubMed  Google Scholar 

  • Galli, M., Haegi, A., Vitale, S., Belisario, A., & Luongo, L. (2013). First report of Phytophthora tropicalis on Rhododendron in Italy. Plant Disease, 97(10), 1385–1385.

    PubMed  Google Scholar 

  • Gerlach, W. W. P., & Schubert, R. (2001). A new wilt of Cyclamen caused by Phytophthora tropicalis in Germany and the Netherlands. Plant Disease, 85(3), 334–334.

    Article  CAS  PubMed  Google Scholar 

  • Grünwald, N. J., Werres, S., Goss, E. M., Taylor, C. R., & Fieland, V. J. (2012). Phytophthora obscura sp. nov., a new species of the novel Phytophthora subclade 8d. Plant Pathology, 61(3), 610–622.

    Article  CAS  Google Scholar 

  • Guetsky, R., Shtienberg, D., Elad, Y., & Dinoor, A. (2001). Combining biocontrol agents to reduce the variability of biological control. Phytopathology, 91(7), 621–627.

    Article  CAS  PubMed  Google Scholar 

  • Gullino, M. L., & Kuijpers, L. A. M. (1994). Social and political implications of managing plant diseases with restricted fungicides in Europe. Annual Review of Phytopathology, 32(1), 559–581.

    Article  CAS  PubMed  Google Scholar 

  • Haas, B. J., Kamoun, S., Zody, M. C., Jiang, R. H. Y., Handsaker, R. E., Cano, L. M., Grabherr, M., Kodira, C. D., Raffaele, S., Torto-Alalibo, T., Bozkurt, T. O., Ah-Fong, A. M. V., Alvarado, L., Anderson, V. L., Armstrong, M. R., Avrova, A., Baxter, L., Beynon, J., Boevink, P. C., Bollmann, S. R., Bos, J. I. B., Bulone, V., Cai, G., Cakir, C., Carrington, J. C., Chawner, M., Conti, L., Costanzo, S., Ewan, R., Fahlgren, N., Fischbach, M. A., Fugelstad, J., Gilroy, E. M., Gnerre, S., Green, P. J., Grenville-Briggs, L. J., Griffith, J., Grünwald, N. J., Horn, K., Horner, N. R., Hu, C. H., Huitema, E., Jeong, D. H., Jones, A. M. E., Jones, J. D. G., Jones, R. W., Karlsson, E. K., Kunjeti, S. G., Lamour, K., Liu, Z., Ma, L. J., MacLean, D., Chibucos, M. C., McDonald, H., McWalters, J., Meijer, H. J. G., Morgan, W., Morris, P. F., Munro, C. A., O’Neill, K., Ospina-Giraldo, M., Pinzón, A., Pritchard, L., Ramsahoye, B., Ren, Q., Restrepo, S., Roy, S., Sadanandom, A., Savidor, A., Schornack, S., Schwartz, D. C., Schumann, U. D., Schwessinger, B., Seyer, L., Sharpe, T., Silvar, C., Song, J., Studholme, D. J., Sykes, S., Thines, M., van de Vondervoort, P. J. I., Phuntumart, V., Wawra, S., Weide, R., Win, J., Young, C., Zhou, S., Fry, W., Meyers, B. C., van West, P., Ristaino, J., Govers, F., Birch, P. R. J., Whisson, S. C., Judelson, H. S., & Nusbaum, C. (2009). Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature, 461(7262), 393–398.

    Article  CAS  PubMed  Google Scholar 

  • Hansen, E. M. (2008). Alien forest pathogens: Phytophthora species are changing world forests. Boreal Environment Research, 13, 33–41.

    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(2), 274–274.

    Article  CAS  PubMed  Google Scholar 

  • Harman, G. E., Petzoldt, R., Comis, A., & Chen, J. (2004a). Interactions between Trichoderma harzianum strain T22 and maize inbred line Mo17 and effects of these interactions on diseases caused by Pythium ultimum and Colletotrichum graminicola. Phytopathology, 94(2), 147–153.

    Article  PubMed  Google Scholar 

  • Harman, G. E., Howell, C. R., Viterbo, A., Chet, I., & Lorito, M. (2004b). Trichoderma species--opportunistic, avirulent plant symbionts. Nature Reviews. Microbiology, 2(1), 43–56.

    Article  CAS  PubMed  Google Scholar 

  • Hayden, K. J., Rizzo, D., Tse, J., & Garbelotto, M. (2004). Detection and quantification of Phytophthora ramorum from California forests using a real-time polymerase chain reaction assay. Phytopathology, 94(10), 1075–1083.

    Article  CAS  PubMed  Google Scholar 

  • Holmes, K. A., & Benson, D. M. (1994). Evaluation of Phytophthora parasitica var. nicotianae for biocontrol of Phytophthora parasitica on Catharanthus roseus. Plant Disease, 78, 193–199.

    Article  Google Scholar 

  • Hong, C. X., Richardson, P. A., Kong, P., Jeffers, S. N., & Oak, S. W. (2006). Phytophthora tropicalis isolated from diseased leaves of Pieris japonica and Rhododendron catawbiense and found in irrigation water and soil in Virginia. Plant Disease, 90(4), 525–525.

    Article  CAS  PubMed  Google Scholar 

  • Ippolito, A., Schena, L., Nigro, F., Ligorio, V. S., & Yaseen, T. (2004). Real-time detection of Phytophthora nicotianae and P. citrophthorain citrus roots and soil. European Journal of Plant Pathology, 110(8), 833–843.

    Article  CAS  Google Scholar 

  • Karagiannidis, N., Bletsos, F., & Stavropoulos, N. (2002). Effect of Verticillium wilt (Verticillium dahliae Kleb.) and mycorrhiza (Glomus mosseae) on root colonization, growth and nutrient uptake in tomato and eggplant seedlings. Scientia Horticulturae, 94(1), 145–156.

    Article  CAS  Google Scholar 

  • Keinath, A. P. (2007). Sensitivity of populations of Phytophthora capsici from South Carolina to Mefenoxam, Dimethomorph, Zoxamide, and Cymoxanil. Plant Disease, 91(6), 743–748.

    Article  CAS  PubMed  Google Scholar 

  • Ko, W. H. (1978). Heterothallic Phytophthora: evidence for hormonal regulation of sexual reproduction. Microbiology, 107(1), 15–18.

    CAS  Google Scholar 

  • Kong, P., Hong, C. x., Tooley, P. w., Ivors, K., Garbelotto, M., & Richardson, P. a. (2004). Rapid identification of Phytophthora ramorum using PCR-SSCP analysis of ribosomal DNA ITS-1. Letters in Applied Microbiology, 38(5), 433–439.

    Article  CAS  PubMed  Google Scholar 

  • Kroon, L. P. N. M., Brouwer, H., de Cock, A. W. A. M., & Govers, F. (2012). The genus Phytophthora anno 2012. Phytopathology, 102(4), 348–364.

    Article  PubMed  Google Scholar 

  • Larousse, M., & Galiana, E. (2017). Microbial partnerships of pathogenic oomycetes. PLoS Pathogens, 13(1), e1006028. https://doi.org/10.1371/journal.ppat.1006028.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Larsen, J., Ravnskov, S., & Jakobsen, I. (2003). Combined effect of an arbuscular mycorrhizal fungus and a biocontrol bacterium against Pythium ultimum in soil. Folia Geobotanica, 38(2), 145–154.

    Article  Google Scholar 

  • Lee, B. D., Dutta, S., Ryu, H., Yoo, S.-J., Suh, D.-S., & Park, K. (2015). Induction of systemic resistance in Panax ginseng against Phytophthora cactorum by native Bacillus amyloliquefaciens HK34. Journal of Ginseng Research, 39(3), 213–220.

    Article  CAS  PubMed  Google Scholar 

  • Li, S.-B., Fang, M., Zhou, R.-C., & Huang, J. (2012). Characterization and evaluation of the endophyte Bacillus B014 as a potential biocontrol agent for the control of Xanthomonas axonopodis pv. dieffenbachiae – Induced blight of Anthurium. Biological Control, 63(1), 9–16.

    Article  CAS  Google Scholar 

  • Lioussanne, L., Jolicoeur, M., & St-Arnaud, M. (2008). Mycorrhizal colonization with Glomus intraradices and development stage of transformed tomato roots significantly modify the chemotactic response of zoospores of the pathogen Phytophthora nicotianae. Soil Biology and Biochemistry, 40(9), 2217–2224.

    Article  CAS  Google Scholar 

  • Liu, Y., Shi, J., Feng, Y., Yang, X., Li, X., & Shen, Q. (2013). Tobacco bacterial wilt can be biologically controlled by the application of antagonistic strains in combination with organic fertilizer. Biology and Fertility of Soils, 49(4), 447–464.

    Article  Google Scholar 

  • Loyd, A. L., Benson, D. M., & Ivors, K. L. (2014). Phytophthora populations in nursery irrigation water in relationship to pathogenicity and infection frequency of Rhododendron and Pieris. Plant Disease, 98(9), 1213–1220.

    Article  CAS  PubMed  Google Scholar 

  • Matheson, C. D., Gurney, C., Esau, N., & Lehto, R. (2010). Assessing PCR inhibition from humic substances. The Open Enzyme Inhibition Journal, 3(1), 38–45.

    Article  CAS  Google Scholar 

  • Matsubara, Y., Tamura, H., & Harada, T. (1995). Growth enhancement and Verticillium wilt control by vesicular-arbuscular mycorrhizal fungus inoculation in eggplant. Journal of the Japanese Society for Horticultural Science, 64(3), 555–561.

    Article  Google Scholar 

  • Mcquilken, M. P., Gemmell, J., & Lahdenperä, M. L. (2001). Gliocladium catenulatum as a potential biological control agent of damping-off in bedding plants. Journal of Phytopathology, 149(3–4), 171–178.

    Article  Google Scholar 

  • Meng, Y., Zhang, Q., Ding, W., & Shan, W. (2014). Phytophthora parasitica: a model oomycete plant pathogen. Mycology, 5(2), 43–51.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Naher, L., Yusuf, U. K., Ismail, A., & Hossain, K. (2014). Trichoderma spp.: a biocontrol agent for sustainable management of plant diseases. Pakistan Journal of Botany, 46(4), 1489–1493.

    Google Scholar 

  • Parra, G., & Ristaino, J. B. (2001). Resistance to mefenoxam and metalaxyl among field isolates of Phytophthora capsici causing Phytophthora blight of bell pepper. Plant Disease, 85(10), 1069–1075.

    Article  CAS  PubMed  Google Scholar 

  • Pozo, M. J., Verhage, A., García-Andrade, J., García, J. M., & Azcón-Aguilar, C. (2009). Priming plant defence against pathogens by arbuscular mycorrhizal Fungi. In C. Azcón-Aguilar, J. M. Barea, S. Gianinazzi, & V. Gianinazzi-Pearson (Eds.), Mycorrhizas - functional processes and ecological impact (pp. 123–135). Berlin Heidelberg: Springer.

    Chapter  Google Scholar 

  • Rasmussen, R. (2001). Quantification on the LightCycler. In S. Meuer, C. Wittwer, & K.-I. Nakagawara (Eds.), Rapid cycle real-time PCR, methods and applications (pp. 21–34). Berlin Heidelberg: Springer.

  • Roberts, D. P., Lohrke, S. M., Meyer, S. L. F., Buyer, J. S., Bowers, J. H., Jacyn Baker, C., Li, W., de Souza, J. T., Lewis, J. A., & Chung, S. (2005). Biocontrol agents applied individually and in combination for suppression of soilborne diseases of cucumber. Crop Protection, 24(2), 141–155.

    Article  Google Scholar 

  • Schena, L., & Cooke, D. E. L. (2006). Assessing the potential of regions of the nuclear and mitochondrial genome to develop a “molecular tool box” for the detection and characterization of Phytophthora species. Journal of Microbiological Methods, 67(1), 70–85.

    Article  CAS  PubMed  Google Scholar 

  • Schena, L., Hughes, K. J. D., & Cooke, D. E. L. (2006). Detection and quantification of Phytophthora ramorum, P. kernoviae, P. citricola and P. quercina in symptomatic leaves by multiplex real-time PCR. Molecular Plant Pathology, 7(5), 365–379.

    Article  CAS  PubMed  Google Scholar 

  • Schisler, D. A., Slininger, P. J., & Bothast, R. J. (1997). Effects of antagonist cell concentration and two-strain mixtures on biological control of fusarium dry rot of potatoes. Phytopathology, 87(2), 177–183.

    Article  CAS  PubMed  Google Scholar 

  • Shen, S.-S., Piao, F.-Z., Lee, B. W., & Park, C. S. (2007). Characterization of antibiotic substance produced by Serratia plymuthica A21-4 and the biological control activity against pepper Phytophthora blight. The Plant Pathology Journal, 23, 180–186.

    Article  CAS  Google Scholar 

  • Smith, V. L., Wilcox, W. F., & Harman, G. E. (1990). Potential for biological control of Phytophthora root and crown rots of apple by Trichoderma and Gliocladium spp. Phytopathology, 80, 880–885.

    Article  Google Scholar 

  • Souto, G. i., Correa, O. s., Montecchia, M. s., Kerber, N. l., Pucheu, N. l., Bachur, M., & García, A. f. (2004). Genetic and functional characterization of a Bacillus sp. strain excreting surfactin and antifungal metabolites partially identified as iturin-like compounds. Journal of Applied Microbiology, 97(6), 1247–1256.

    Article  CAS  PubMed  Google Scholar 

  • Spadaro, D., & Gullino, M. L. (2005). Improving the efficacy of biocontrol agents against soilborne pathogens. Crop Protection, 24(7), 601–613.

    Article  Google Scholar 

  • Steyaert, J. M., Ridgway, H. J., Elad, Y., & Stewart, A. (2003). Genetic basis of mycoparasitism: A mechanism of biological control by species of Trichoderma. New Zealand Journal of Crop and Horticultural Science, 31(4), 281–291.

    Article  Google Scholar 

  • Talbot, D., & Wedgwood, E. (2009). Choisya: surveys of the occurrence of root rotting and potential causes. Horticultural Development Company Project HNS 196. Horticultural Development Company.

  • Thilagavathi, R., Saravanakumar, D., Ragupathi, N., & Samiyappan, R. (2007). A combination of biocontrol agents improves the management of dry root rot (Macrophomina phaseolina) in greengram. Phytopathologia Mediterranea, 46(2), 157–167.

    CAS  Google Scholar 

  • Vernière, C., Cohen, S., Raffanel, B., Dubois, A., Venard, P., & Panabières, F. (2004). Variability in pathogenicity among Phytophthora spp. isolated from Citrus in Corsica. Journal of Phytopathology, 152(8–9), 476–483.

    Article  Google Scholar 

  • Vigo, C., Norman, J. R., & Hooker, J. E. (2000). Biocontrol of the pathogen Phytophthora parasitica by arbuscular mycorrhizal fungi is a consequence of effects on infection loci. Plant Pathology, 49(4), 509–514.

    Article  Google Scholar 

  • Vinale, F., Sivasithamparam, K., Ghisalberti, E. L., Marra, R., Woo, S. L., & Lorito, M. (2008). Trichoderma–plant–pathogen interactions. Soil Biology and Biochemistry, 40(1), 1–10.

    Article  CAS  Google Scholar 

  • Wehner, J., Antunes, P. M., Powell, J. R., Mazukatow, J., & Rillig, M. C. (2010). Plant pathogen protection by arbuscular mycorrhizas: A role for fungal diversity? Pedobiologia, 53(3), 197–201.

    Article  Google Scholar 

  • White, T. J., Bruns, T., Lee, S., & Taylor, J. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for Phylogenetics. In M. A. Innis, D. H. Gelfand, J. J. Sninski, & T. J. White (Eds.), PCR protocols: A guide to methods and applications (pp. 315–322). San Diego: Academic Press.

    Google Scholar 

  • Xu, J. (2016). Fungal DNA barcoding. Genome, 59(11), 913–932.

    Article  CAS  PubMed  Google Scholar 

  • Xu, X.-M., Jeffries, P., Pautasso, M., & Jeger, M. J. (2011). A numerical study of combined use of two biocontrol agents with different biocontrol mechanisms in controlling foliar pathogens. Phytopathology, 101(9), 1032–1044.

    Article  PubMed  Google Scholar 

  • Zhang, Z. G., Zhang, J. Y., Zheng, X. B., Yang, Y. W., & Ko, W. H. (2004). Molecular distinctions between Phytophthora capsici and Ph. tropicalis based on ITS sequences of ribosomal DNA. Journal of Phytopathology, 152(6), 358–364.

    Article  CAS  Google Scholar 

  • Zhang, M., Li, J., Shen, A., Tan, S., Yan, Z., Yu, Y., Xue, Z., Tan, T., & Zeng, L. (2016). Isolation and identification of Bacillus amyloliquefaciens IBFCBF-1 with potential for biological control of Phytophthora blight and growth promotion of pepper. Journal of Phytopathology, 164(11–12), 1012–1021.

    Article  CAS  Google Scholar 

  • Zheng, H., Cui, C., Zhang, Y., Wang, D., Jing, Y., & Kim, K. Y. (2005). Active changes of lignification-related enzymes in pepper response to Glomus intraradices and/or Phytophthora capsici. Journal of Zhejiang University SCIENCE, 6B(8), 778–786.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank SFR Normandie Végétal, Astredhor Seine Manche and their experimental station at Saint Germain En Laye for the technical monitoring, Agnès Attard from Institut Sophia Agrobiotech for providing the P. parasitica INRA-310 strain, the region of Normandy for the doctoral grant and all the people who actively contributed to this work.

Author information

Authors and Affiliations

  1. AGHYLE Unit, UniLaSalle, 3 Rue du Tronquet, 76130, Mont Saint Aignan, France

    Youssef Manasfi, Wassila Riah, Mélanie Bressan, Karine Laval & Isabelle Trinsoutrot-Gattin

  2. Laboratoire de Glycobiologie et Matrice Extracellulaire Végétale, EA4358, SFR FED 4277 “Normandie Végétal”, Université de Rouen Normandie, 76821, Mont-Saint-Aignan cedex, France

    Youssef Manasfi, Azeddine Driouich & Maïté Vicré

  3. ASTREDHOR Seine-Manche, 32 rue Alfred Kastler, 76130, Mont Saint Aignan, France

    Marc-Antoine Cannesan

Authors
  1. Youssef Manasfi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marc-Antoine Cannesan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wassila Riah
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mélanie Bressan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Karine Laval
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Azeddine Driouich
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Maïté Vicré
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Isabelle Trinsoutrot-Gattin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Isabelle Trinsoutrot-Gattin.

Ethics declarations

Authors declare that:

• This manuscript has not been submitted to more than one journal for simultaneous consideration.

• This manuscript has not been published previously (partly or in full).

• This paper relate a single study and has not been split up into several parts.

• No data, including images, have been fabricated or manipulated to support our conclusions.

• No data or text by others are presented as if they were the author’s own.

• Consent to submit has been received explicitly from all co-authors, as well as from the responsible authorities - tacitly or explicitly - at the institute/organization where the work has been carried out, before the work is submitted.

• Authors whose names appear on the submission have contributed sufficiently to the scientific work and therefore share collective responsibility and accountability for the results.

• Authors group, corresponding author, and order of authors have been validate by both authors and responsible authorities before submission of this manuscript.

• Upon request, we are prepared to send relevant documentation or data in order to verify the validity of the results.

Electronic supplementary material

ESM 1

(DOCX 13 kb)

ESM 2

(DOCX 22 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Manasfi, Y., Cannesan, MA., Riah, W. et al. Potential of combined biological control agents to cope with Phytophthora parasitica, a major pathogen of Choisya ternata. Eur J Plant Pathol 152, 1011–1025 (2018). https://doi.org/10.1007/s10658-018-1495-7

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-018-1495-7

Keywords

Search

Navigation