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Apple nursery trees and irrigation water as potential external inoculum sources of apple replant disease in South Africa

  • S. Moein
  • M. Mazzola
  • N. S. Ntushelo
  • A. McLeod
Article
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Abstract

Apple replant disease (ARD) is a biological phenomenon caused by soilborne agents that include selected species of fungi (Rhizoctonia and ‘Cylindrocarpon’-like), oomycetes (Pythium, Phytopythium and Phytophthora) and nematodes (Pratylenchus). Old orchard soils previously planted to apple or related species are a primary inoculum source of ARD pathogens. In the current study, nursery trees and irrigation water were investigated as potential external ARD inoculum sources in South Africa. Investigations conducted at five nurseries over two years revealed that roots of nursery trees were infested by several ARD agents. In the 2013 sampling year, Pythium irregulare and Pythium ultimum were obtained from trees in five and two of the nurseries, respectively, using isolation studies. Based on isolation studies conducted on individual trees in 2013, 47% and 4% of all surveyed trees contained P. irregulare and P. ultimum, respectively. In the 2014 season, real-time quantitative PCR (qPCR) analyses of root tissue from individual trees demonstrated that all of the nurseries and 95% of trees contained P. irregulare, whereas three nurseries and 41% of trees contained P. utlimum. The only other oomycete pathogens that were detected in nursery tree roots were Pythium spp. complex B2A and Pythium sylvaticum and each only occurred in one nursery in one of the sampling years. For all nurseries in both years, trees were consistently infected with ‘Cylindrocarpon’-like spp. Pratylenchus spp., which were only analysed in 2013, was present in all five nurseries and in 29% of the trees. Infestation levels were high, with 22% of trees having Pratylenchus root densities that exceeded 100 per 5 g of roots. Pythium irregulare was the dominant oomycete pathogen detected in irrigation water samples (31% to 76% of the samples) obtained from 13 orchards over two years on a monthly basis. The ARD pathogens P. ultimum, Phytopythium litorale and Pythium spp. complex B2A were rarely identified in irrigation water, along with five other non-pathogenic Pythium and Phytopythium species. The association of ARD causative agents with nursery trees and irrigation water suggests that these could function as potential ARD inoculum sources that might limit post-plant tree growth.

Keywords

Waterborne pathogens Apple replant disease Inoculum source Oomycetes 

Notes

Acknowledgements

We would like to thank the South African Apple and Pear Producer’s Association (SAAPPA), the Technology and Human Resources for Industry Programme (THRIP) for financially supporting the research. We would also like to thank Marieta Van der Rijst (Agricultural Research Council, Biometry Unit, Stellenbosch, South Africa) for statistical analyses of the data, and Tim Daniell (The James Hutton Institute, Dundee, UK) for providing the plasmid containing the mutated E. coli gene for conducting relative pathogen quantifications.

References

  1. Ali-Shtayeh, M. S., MacDonald, J. F., & Kabashima, J. (1991). A method for using commercial ELISA tests to detect zoospores of Phytophthora and Pythium species in irrigation water. Plant Disease, 75, 305–311.CrossRefGoogle Scholar
  2. Benson, D. M., & Jones, R. K. (1980). Etiology of rhododendron dieback caused by four species of Phytophthora. Plant Disease, 64, 687–691.CrossRefGoogle Scholar
  3. Braun, P. G. (1995). Effects of Cylindrocarpon and Pythium species on apple seedlings and potential role in apple replant disease. Canadian Journal of Plant Pathology, 17, 336–341.CrossRefGoogle Scholar
  4. Cabral, A., Rego, C., Nascimento, T., Oliveira, H., Groenewald, J. Z., & Crous, P. W. (2012). Multi-gene analysis and morphology reveal novel Ilyonectria species associated with black foot disease of grapevines. Fungal Biology, 116, 62–80.CrossRefGoogle Scholar
  5. Chaverri, P., Salgado, C., Hirooka, Y., Rossman, A. Y., & Samuels, G. J. (2011). Delimitation of Neonectria and Cylindrocarpon (Nectriaceae, Hypocreales, Ascomycota) and related genera with Cylindrocarpon-like anamorphs. Studies in Mycology, 68, 57–78.CrossRefGoogle Scholar
  6. Cooke, D. E., & Duncan, J. M. (1997). Phylogenetic analysis of Phytophthora species based on ITS1 and ITS2 sequences of the ribosomal RNA gene repeat. Mycological Research, 101, 667–677.CrossRefGoogle Scholar
  7. Daniell, T. J., Davidson, J., Alexander, C. J., Caul, S., & Roberts, D. M. (2012). Improved real-time PCR estimates of gene copy number in soil extracts using an artificial reference. Journal of Microbiological Methods, 91, 38–44.CrossRefGoogle Scholar
  8. Emmett, B., Nelson, E. B., Kessler, A., & Bauerle, T. L. (2014). Fine-root system development and susceptibility to pathogen colonization. Planta, 239, 325–340.CrossRefGoogle Scholar
  9. Granke, L., & Hausbeck, M. (2010). Effects of temperature, concentration, age, and algaecides on Phytophthora capsici zoospore infectivity. Plant Disease, 94, 54–60.CrossRefGoogle Scholar
  10. Greenacre, M. (2007). Correspondence analysis in practice (2nd ed.). London: Chapman & Hall / CRC.CrossRefGoogle Scholar
  11. Hong, C., & Epelman, G. (2001). Effect of pathogen concentration and exposure frequency on Phytophthora blight of annual vinca under drip irrigation systems. Phytopathology, 91, 40–56.Google Scholar
  12. Hong, C., & Moorman, G. (2005). Plant pathogens in irrigation water: Challenges and opportunities. Critical Reviews in Plant Sciences, 24, 189–208.CrossRefGoogle Scholar
  13. Hugo, H. J., & Malan, A. P. (2010). Occurrence and control of plant-parasitic nematodes in irrigation water – A review. South African Journal of Enology and Viticulture, 31, 169–180.Google Scholar
  14. Jeffers, S. N., & Aldwinckle, H. S. (1988). Phytophthora crown rot of apple trees: Sources of Phytophthora cactorum and Phytophthora cambivora as primary inoculum. Phytopathology, 78, 328–335.CrossRefGoogle Scholar
  15. Jeffers, S. N., & Martin, S. B. (1986). Comparison of two media selective for Phytophthora and Pythium species. Plant Disease, 70, 1038–1043.CrossRefGoogle Scholar
  16. Jenkins, W. (1964). A rapid centrifugal-flotation technique for separating nematodes from soil. Plant Disease Report, 73, 288–300.Google Scholar
  17. Jones, L. A., Worobo, R. W., & Smart, C. D. (2014). Plant-pathogenic oomycetes, Escherichia coli strains, and Salmonella spp. frequently found in surface water used for irrigation of fruit and vegetable crops in New York state. Applied and Environmental Microbiology, 80, 4814–4820.CrossRefGoogle Scholar
  18. Levesque, C. A., & De Cock, A. W. (2004). Molecular phylogeny and taxonomy of the genus Pythium. Mycological Research, 108, 1363–1383.CrossRefGoogle Scholar
  19. Lombard, L., Van Der Merwe, N. A., Groenewald, J. Z., & Crous, P. W. (2014). Lineages in Nectriaceae: Re-evaluating the generic status of Ilyonectria and allied genera. Phytopathologia Mediterranea, 53, 515–532.Google Scholar
  20. Loyd, A., Benson, D., & Ivors, K. (2014). Phytophthora populations in nursery irrigation water in relationship to pathogenicity and infection frequency of Rhododendron and Pieris. Plant Disease, 98, 1213–1220.CrossRefGoogle Scholar
  21. Manici, L. M., Ciavatta, C., Kelderer, M., & Erschbaumer, G. (2003). Replant problems in South Tyrol: Role of fungal pathogens and microbial population in conventional and organic apple orchards. Plant and Soil, 256, 315–324.CrossRefGoogle Scholar
  22. Manici, L. M., Kelderer, M., Franke-Whittle, I. H., Ruhmer, T., Baab, G., Nicoletti, F., Caputo, F., Topp, A., Insam, H., & Naef, A. (2013). Relationship between root-endophytic microbial communities and replant disease in specialized apple growing areas in Europe. Applied Soil Ecology, 72, 207–214.CrossRefGoogle Scholar
  23. Manici, L. M., Kelderer, M., Caputo, F., Sacca, M. L., Nicoletti, F., Topp, A. R., & Mazzola, M. (2018). Involvement of Dactylonectria and Ilyonectria spp. in tree decline affecting multi-generation apple orchards. Plant and Soil, 425, 217–230.CrossRefGoogle Scholar
  24. Mazzola, M. (1998). Elucidation of the microbial complex having a causal role in the development of apple replant disease in Washington. Phytopathology, 88, 930–938.CrossRefGoogle Scholar
  25. Mazzola, M., & Manici, L. M. (2012). Apple replant disease: Role of microbial ecology in cause and control. Annual Review of Phytopathology, 50, 45–65.CrossRefGoogle Scholar
  26. Mazzola, M., Andrews, P. K., Reganold, J. P., & Levesque, C. A. (2002). Frequency, virulence, and metalaxyl sensitivity of Pythium spp. isolated from apple roots under conventional and organic production systems. Plant Disease, 86, 669–675.CrossRefGoogle Scholar
  27. Mazzola, M., Brown, J., Zhao, X., Izzo, A. D., & Fazio, G. (2009). Interaction of Brassicaceous seed meal and apple rootstock on recovery of Pythium spp. and Pratylenchus penetrans from roots grown in replant soils. Plant Disease, 93, 51–57.CrossRefGoogle Scholar
  28. McLeod, A., Botha, W. J., Meitz, J. C., Spies, C. F., Tewoldemedhin, Y. T., & Mostert, L. (2009). Morphological and phylogenetic analyses of Pythium species in South Africa. Mycological Research, 113, 933–951.CrossRefGoogle Scholar
  29. Moein, S., Mazzola, M., Spies, C.F.J. and McLeod. (2018) Evaluating different approaches for the quantification of oomycete apple replant pathogens, and their relationship with seedling growth reductions. European Journal of Plant Pathology, In pressGoogle Scholar
  30. Nagel, J. H., Gryzenhout, M., Slippers, B., Wingfield, M. J., Hardy, G. E., Stukely, M. J. C., & Burgress, T. I. (2013). Characterization of Phytophthora hybrids from ITS clade 6 associated with riparian ecosystems in South Africa and Australia. Fungal Biology, 117, 329–347.CrossRefGoogle Scholar
  31. Parkunan, V., & Ji, P. (2013). Isolation of Pythium litorale from irrigation ponds used for vegetable production and its pathogenicity on squash. Canadian Journal of Plant Pathology, 35, 415–423.CrossRefGoogle Scholar
  32. Rankovic, B. (2005). Five Serbian reservoirs contain different fungal propagules. Mycologia, 97, 50–56.CrossRefGoogle Scholar
  33. Raudales, R. E., Fisher, P. R., & Hall, C. R. (2017). The cost of irrigation sources and water treatment in greenhouse production. Irrigation Science, 35, 43–54.CrossRefGoogle Scholar
  34. Robideau, G. P., De, C. O. C. K., arthur, W., Coffey, M. D., Voglmayr, H., Brouwer, H., Bala, K., Chitty, D. W., Désaulniers, N., Eggertson, Q. A., & Gachon, C. M. (2011). DNA barcoding of oomycetes with cytochrome c oxidase subunit I and internal transcribed spacer. Molecular Ecology Resources, 11, 1002–1011.CrossRefGoogle Scholar
  35. Sánchez, J., & Gallego, E. (2001). Pythium spp. present in irrigation water in the Poniente region of Almeria (South-Eastern Spain). Mycopathologia, 150, 29–38.CrossRefGoogle Scholar
  36. Sewell, G. W. F. (1981). Effects of Pythium species on the growth of apple and their possible causal role in apple replant disease. Annals of Applied Biology, 97, 31–42.CrossRefGoogle Scholar
  37. Shokes, F., & McCarter, S. (1979). Occurrence, dissemination, and survival of plant pathogens in surface irrigation ponds in southern Georgia. Phytopathology, 69, 510–516.CrossRefGoogle Scholar
  38. Shrestha, S. K., Zhou, Y., & Lamour, K. (2013). Oomycetes baited from streams in Tennessee 2010-2012. Mycologia, 105, 1516–1523.CrossRefGoogle Scholar
  39. Tambong, J. T., De Cock, A. W. A. M., Tinker, N. A., & Lévesque, C. A. (2006). Oligonucleotide array for identification and detection of Pythium species. Applied and Environmental Microbiology, 72, 2691–2706.CrossRefGoogle Scholar
  40. Tewoldemedhin, Y. T., Mazzola, M., Labuschagne, I., & McLeod, A. (2011a). A multi-phasic approach reveals that apple replant disease is caused by multiple biological agents, with some agents acting synergistically. Soil Biology and Biochemistry, 43, 1917–1927.CrossRefGoogle Scholar
  41. Tewoldemedhin, Y. T., Mazzola, M., Botha, W. J., Spies, C. F., & McLeod, A. (2011b). Characterization of fungi (Fusarium and Rhizoctonia) and oomycetes (Phytophthora and Pythium) associated with apple orchards in South Africa. European Journal of Plant Pathology, 130, 215–229.CrossRefGoogle Scholar
  42. Tewoldemedhin, Y. T., Mazzola, M., Mostert, L., & McLeod, A. (2011c). Cylindrocarpon species associated with apple tree roots in South Africa and their quantification using real-time PCR. European Journal of Plant Pathology, 129, 637–651.CrossRefGoogle Scholar
  43. Tjosvold, S. A., Chambers, D. L., Koike, S. T., & Mori, S. R. (2008). Disease on nursery stock as affected by environmental factors and seasonal inoculum levels of Phytophthora ramorum in stream water used for irrigation. Plant Disease, 92, 1566–1573.CrossRefGoogle Scholar
  44. Vallance, J., Le Floch, G., Deniel, F., Barbier, G., Levesque, C. A., & Rey, P. (2009). Influence of Pythium oligandrum biocontrol on fungal and oomycete population dynamics in the rhizosphere. Applied and Environmental Microbiology, 75, 4790–4800.CrossRefGoogle Scholar
  45. Van Schoor, L., Denman, S., & Cook, N. (2009). Characterisation of apple replant disease under South African conditions and potential biological management strategies. Scientia Horticulturae, 119, 153–162.CrossRefGoogle Scholar
  46. Werres, S., Wagner, S., Brand, T., Kaminski, K., & Seipp, D. (2007). Survival of Phytophthora ramorum in recirculating irrigation water and subsequent infection of Rhododendron and Viburnum. Plant Disease, 91, 1034–1044.CrossRefGoogle Scholar
  47. White, T. J., Bruns, T., Lee, S. J. W. T., & Taylor, J. W. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In M. A. Innis, D. H. Gelfand, J. J. Sninsky, & T. J. White (Eds.), PCR protocols, a guide to methods and applications (pp. 315–322). Academic Press: San DiegoGoogle Scholar
  48. Yamak, F., Peever, T., Grove, G., & Boal, R. (2002). Occurrence and identification of Phytophthora Spp. pathogenic to pear fruit in irrigation water in the Wenatchee river valley of Washington State. Phytopathology, 92, 1210–1217.CrossRefGoogle Scholar
  49. Zappia, R., Hüberli, D., Hardy, G. S. J., & Bayliss, K. (2014). Fungi and oomycetes in open irrigation systems: Knowledge gaps and biosecurity implications. Plant Pathology, 63, 961–972.CrossRefGoogle Scholar

Copyright information

© Koninklijke Nederlandse Planteziektenkundige Vereniging 2018

Authors and Affiliations

  • S. Moein
    • 1
  • M. Mazzola
    • 1
    • 2
  • N. S. Ntushelo
    • 3
  • A. McLeod
    • 1
  1. 1.Department of Plant PathologyUniversity of StellenboschStellenboschSouth Africa
  2. 2.United States Department of Agriculture, Agricultural Research ServiceWenatcheeUSA
  3. 3.Agricultural Research Council (Biometry)StellenboschSouth Africa

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