Advertisement

Response of Quercus ilex seedlings to Phytophthora spp. root infection in a soil infestation test

  • Beatriz Mora-SalaEmail author
  • Paloma Abad-Campos
  • Mónica Berbegal
Article
  • 38 Downloads

Abstract

Phytophthora species are the main agents associated with oak (Quercus spp.) decline, together with the changing environmental conditions and the intensive land use. The aim of this study was to evaluate the susceptibility of Quercus ilex to the inoculation with eight Phytophthora species. Seven to eight month old Q. ilex seedlings grown from acorns, obtained from two Spanish origins, were inoculated with P. cinnamomi, P. cryptogea, P. gonapodyides, P. megasperma, P. nicotianae, P. plurivora, P. psychrophila and P. quercina. All Phytophthora inoculated seedlings showed decline and symptoms including small dark necrotic root lesions, root cankers, and loss of fine roots and tap root. The most aggressive species were P. cinnamomi, P. cryptogea, P. gonapodyides, P. plurivora and P. psychrophila followed by P. megasperma., while Phytophthora quercina and P. nicotianae were the less aggressive species. Results obtained confirm that these Phytophthora species could constituted a threat to Q. ilex ecosystems and the implications are further discussed.

Keywords

Quercus spp Pathogenicity Inoculation Holm oak 

Notes

Acknowledgements

The authors are grateful to A. Solla and his team from the Centro Universitario de Plasencia-Universidad de Extremadura (Spain) for helping in the acorns collection and to the CIEF (Centro para la Investigación y Experimentación Forestal, Generalitat Valenciana, Valencia, Spain) for providing the acorns. This research was supported by funding from the project AGL2011-30438-C02-01 (Ministerio de Economía y Competitividad, Spain).

Compliance with ethical standards

Human and Animal Rights

The authors declare that ethical standards have been followed and that no human participants or animals were involved in this research.

References

  1. Álvarez, L. A., Pérez-Sierra, A., Armengol, J., & García-Jiménez, J. (2007). Characterization of Phytophthora nicotianae isolates causing collar and root rot of lavender and rosemary in Spain. Journal of Plant Pathology, 89, 261–264.Google Scholar
  2. Balci, Y., & Halmschlager, E. (2003a). Incidence of Phytophthora species in oak forests in Austria and their possible involvement in oak decline. Forest Pathology, 33, 157–174.CrossRefGoogle Scholar
  3. Balci, Y., & Halmschlager, E. (2003b). Phytophthora species in oak ecosystems in Turkey and their association with declining oak trees. Plant Pathology, 52, 694–702.CrossRefGoogle Scholar
  4. Brasier, C. M. (1992a). Oak tree mortality in Iberia. Nature, 360, 539.CrossRefGoogle Scholar
  5. Brasier, C. M. ((1992b)). Phytophthora cinnamomi as a contributory factor on European oak declines. In N. by Luisi, P. Lerario, & A. B. Vannini (Eds.), Recent Advances in Studies on Oak Decline. Proc. Int. Congress, Brindisi, Italy, September 13-18, 1992 (pp. 49–58). Italy: Università degli Studi.Google Scholar
  6. Brasier, C. M. (1996). Phytophthora cinnamomi and oak decline in southern Europe. Environmental constraints including climate change. Annales des Sciences Forestieres, 53, 347–358.CrossRefGoogle Scholar
  7. Brasier, C. M. (2008). The biosecurity threat to the UK and global environment from international trade in plants. Plant Pathology, 57, 792–808.CrossRefGoogle Scholar
  8. Brasier, C. M., Hamm, P. B., & Hansen, E. M. (1993a). Cultural characters, protein patterns and unusual mating behaviour of P. gonapodyides isolates from Britain and North America. Mycological Research, 97, 1287–1298.CrossRefGoogle Scholar
  9. Brasier, C. M., Robredo, F., & Ferraz, J. F. P. (1993b). Evidence for Phytophthora cinnamomi involvement in Iberian oak decline. Plant Pathology, 42, 140–145.CrossRefGoogle Scholar
  10. Camilo-Alves, C. S. P., Clara, M. I. E., & Ribeiro, N. M. C. A. (2013). Decline of Mediterranean oak trees and its association with Phytophthora cinnamomi: a review. European Journal of Forest Research, 132, 411–432.Google Scholar
  11. Català, S., Berbegal, M., Pérez-Sierra, A., & Abad-Campos, P. (2017). Metabarcoding and development of new real-time specific assays reveal Phytophthora species diversity in holm oak forests in eastern Spain. Plant Pathology, 66, 115–123.CrossRefGoogle Scholar
  12. Collett, D. (2003). Modelling survival data in medical research (2nd ed.). Boca Raton: Chapman & Hall/CRC, 410 pp.Google Scholar
  13. Corcobado, T., Cubera, E., Pérez-Sierra, A., Jung, T., & Solla, A. (2010). First report of Phytophthora gonapodyides involved in the decline of Quercus ilex in xeric conditions in Spain. New Disease Reports, 22, 33.CrossRefGoogle Scholar
  14. Corcobado, T., Cubera, E., Moreno, G., & Solla, A. (2013). Quercus ilex forests are influenced by annual variations in water table, soil water deficit and fine root loss caused by Phytophthora cinnamomi. Agricultural and Forest Meteorology, 169, 92–99.CrossRefGoogle Scholar
  15. Corcobado, T., Vivas, M., Moreno, G., & Solla, A. (2014). Ectomycorrhizal symbiosis in declining and non-declining Quercus ilex trees infected with or free of Phytophthora cinnamomi. Forest Ecology and Management, 324, 72–80.CrossRefGoogle Scholar
  16. Corcobado, T., Miranda-Torres, J. J., Martín-García, J., Jung, T., & Solla, A. (2017). Early survival of Quercus ilex subspecies from different populations after infections and co-infections by multiple Phytophthora species. Plant Pathology, 66, 792–804.CrossRefGoogle Scholar
  17. Erwin, D. C., & Ribeiro, O. K. (1996). Phytophthora diseases worldwide. St. Paul, Minnesota,USA: APS Press, American Phytopathological. Society 562pp.Google Scholar
  18. Gallego, F. J., Perez de Algaba, A., & Fernandez-Escobar, R. (1999). Etiology of oak decline in Spain. European Journal of Forest Pathology, 29, 17–27.CrossRefGoogle Scholar
  19. Hansen, E., & Delatour, C. (1999). Phytophthora species in oak forests of north-east France. Annals of Forest Science, 56, 539–547.CrossRefGoogle Scholar
  20. Hardham, A. R., & Blackman, L. M. (2010). Molecular cytology of Phytophthora plant interactions. Australasian Plant Pathology, 39, 29.CrossRefGoogle Scholar
  21. Hernández-Lambraño, R. E., González-Moreno, P., & Sánchez-Agudo, J. Á. (2018). Environmental factors associated with the spatial distribution of invasive plant pathogens in the Iberian Peninsula: The case of Phytophthora cinnamomi Rands. Forest Ecology and Management, 419, 101–109.CrossRefGoogle Scholar
  22. Jankowiak, R., Stępniewska, H., Bilański, P., & Kolařík, M. (2014). Occurrence of Phytophthora plurivora and other Phytophthora species in oak forests of southern Poland and their association with site conditions and the health status of trees. Folia Microbiologica, 59, 531–542.CrossRefGoogle Scholar
  23. Jeffers, S. N., & Aldwinckle, H. S. (1987). Enhancing detection of Phytophthora cactorum in naturally infested soil. Phytopathology, 77, 1475–1482.CrossRefGoogle Scholar
  24. Jiménez, A. J., Sánchez, E. J., Romero, M. A., Belbahri, L., Trapero, A., Lefort, F., & Sánchez, M. E. (2008). Pathogenicity of Pythium spiculum and P. sterilum on feeder roots of Quercus rotundifolia. Plant Pathology, 57, 369.CrossRefGoogle Scholar
  25. Jönsson, U. (2006). A conceptual model for the development of Phytophthora disease in Quercus robur. New Phytologist, 171, 55–68.CrossRefGoogle Scholar
  26. Jönsson, U., Jung, T., Rosengren, U., Nihlgard, B., & Sonesson, K. (2003). Pathogenicity of Swedish isolates of Phytophthora quercina to Quercus robur in two different soils. New Phytologist, 158, 355–364.CrossRefGoogle Scholar
  27. Jung, T., & Burgess, T. I. (2009). Re-evaluation of Phytophthora citricola isolates from multiple woody hosts in Europe and North America reveals a new species, Phytophthora plurivora sp. nov. Persoonia, 22, 95–110.CrossRefGoogle Scholar
  28. Jung, T., Blaschke, H., & Neumann, P. (1996). Isolation, identification and pathogenicity of Phytophthora species from declining oak stands. European Journal of Forest Pathology, 26, 253–272.CrossRefGoogle Scholar
  29. Jung, T., Cooke, D. E. L., Blaschke, H., Duncan, J. M., & Oßwald, W. (1999). Phytophthora quercina sp. nov., causing root rot of European oaks. Mycological Research, 103, 785–798.CrossRefGoogle Scholar
  30. Jung, T., Blaschke, H., & Oßwald, W. (2000). Involvement of soilborne Phytophthora species in Central European oak decline and the effect of site factors on the disease. Plant Pathology, 49, 706–718.CrossRefGoogle Scholar
  31. Jung, T., Hansen, E. M., Winton, L., Oßwald, W., & Delatour, C. (2002). Three new species of Phytophthora from European oak forests. Mycological Research, 106, 397–411.CrossRefGoogle Scholar
  32. Jung, T., Orlikowski, L., Henricot, B., Abad-Campos, P., Aday, A. G., Aguín Casal, O., Bakonyi, J., Cacciola, S. O., Cech, T., Chavarriaga, D., Corcobado, T., Cravador, A., Decourcelle, T., Denton, G., Diamandis, S., Dogmus-Lehtijärvi, H. T., Franceschini, A., Ginetti, B., Glavendekic, M., Hantula, J., Hartmann, G., Herrero, M., Ivic, D., Horta Jung, M., Lilja, A., Keca, N., Kramarets, V., Lyubenova, A., Machado, H., Magnano di San Lio, G., Mansilla Vázquez, P. J., Marçais, B., Matsiakh, I., Milenkovic, I., Moricca, S., Nagy, Z. Á., Nechwatal, J., Olsson, C., Oszako, T., Pane, A., Paplomatas, E. J., Pintos Varela, C., Prospero, S., Rial Martínez, C., Rigling, D., Robin, C., Rytkönen, A., Sánchez, M. E., Scanu, B., Schlenzig, A., Schumacher, J., Slavov, S., Solla, A., Sousa, E., Stenlid, J., Talgø, V., Tomic, Z., Tsopelas, P., Vannini, A., Vettraino, A. M., Wenneker, M., Woodward, S., & Peréz-Sierra, A. (2016). Widespread Phytophthora infestations in European nurseries put forest, semi-natural and horticultural ecosystems at high risk of Phytophthora diseases. Forest Pathology, 46, 134–163.CrossRefGoogle Scholar
  33. Kroon, L. P., Brouwer, H., de Cock, A. W., & Govers, F. (2012). The genus Phytophthora anno 2012. Phytopathology, 102, 348–364.CrossRefGoogle Scholar
  34. Linaldeddu, B. T., Scanu, B., Maddau, L., & Franceschini, A. (2014). Diplodia corticola and Phytophthora cinnamomi: the main pathogens involved in holm oak decline on Caprera Island (Italy). Forest Pathology, 44, 191–200.CrossRefGoogle Scholar
  35. Luque, J., Parladé, J., & Pera, J. (2000). Pathogenicity of fungi isolated from Quercus suber in Catalonia (NE Spain). Forest Pathology, 30, 247–263.CrossRefGoogle Scholar
  36. Luque, J., Parladé, J., & Pera, J. (2002). Seasonal changes in susceptibility of Quercus suber to Botryosphaeria stevensii and Phytophthora cinnamomi. Plant Pathology, 51, 338–345.CrossRefGoogle Scholar
  37. MAGRAMA. (2014). Diagnóstico del Sector Forestal Español. Análisis y Prospectiva - Serie Agrinfo/Medioambiente n° 8. Ed. Ministerio de Agricultura, Alimentación y Medio Ambiente. In NIPO: 280-14-081-9.Google Scholar
  38. Martín-García, J., Solla, A., Corcobado, T., Siasou, E., & Woodward, S. (2015). Influence of temperature on germination of Quercus ilex in Phytophthora cinnamomi, P. gonapodyides, P. quercina and P. psychrophila infested soils. Forest Pathology, 45, 215–223.CrossRefGoogle Scholar
  39. Maurel, M., Robin, C., Capron, G., & Desprez-Loustau, M. L. (2001). Effects of root damage associated with Phytophthora cinnamomi on water elations, biomass accumulation, mineral nutrition and vulnerability to water deficit of five oak and chestnut species. Forest Pathology, 31, 353–369.CrossRefGoogle Scholar
  40. McKinney, H. H. (1923). Influence of soil temperature and moisture on infection of wheat seedlings by Helminthosporium sativum. Journal of Agricultural Research, 26, 195–217.Google Scholar
  41. Moralejo, E., Pérez-Sierra, A., Álvarez, L. A., Belbahri, L., Lefort, F., & Descals, E. (2009). Multiple alien Phytophthora taxa discovered on diseased ornamental plants in Spain. Plant Pathology, 58, 100–110.CrossRefGoogle Scholar
  42. Mora-Sala, B., Berbegal, M., & Abad-Campos, P. (2018). The use of qPCR reveals a high frequency of Phytophthora quercina in two Spanish holm oak areas. Forests, 9(11):697.  https://doi.org/10.3390/f9110697.
  43. Moreira, A. C., & Martins, J. M. S. (2005). Influence of site factors on the impact of Phytophthora cinnamomi in cork oak stands in Portugal. Forest Pathology, 35, 145–162.CrossRefGoogle Scholar
  44. Mrázková, M., Černý, K., Tomosovsky, M., Strnadová, V., Gregorová, B., Holub, V., Panek, M., Havrdová, L., & Hejná, M. (2013). Occurrence of Phytophthora multivora and Phytophthora plurivora in the Czech Republic. Plant Protection Science, 49, 155–164.CrossRefGoogle Scholar
  45. Navarro, R. M., Gallo, L., Sánchez, M. E., Fernández, P., & Trapero, A. (2004). Efecto de distintas fertilizaciones de fósforo en la resistencia de brinzales de encina y alcornoque a Phytophthora cinnamomi Rands. Investigación Agraria. Sistemas y Recursos Forestales, 13, 550–558.Google Scholar
  46. Panabières, F., Ali, G., Allagui, M., Dalio, R., Gudmestad, N., Kuhn, M., Guha Roy, S., Schena, L., & Zampounis, A. (2016). Phytophthora nicotianae diseases worldwide: new knowledge of a long-recognised pathogen. Phytopathologia Mediterranea, 55, 20–40.Google Scholar
  47. Pérez-Sierra, A., & Jung, T. (2013). Phytophthora in woody ornamental nurseries. In: Phytophthora: A global perspective (pp. 166-177). Ed. by Lamour, K. Wallingford: CABI.Google Scholar
  48. Pérez-Sierra, A., Mora-Sala, B., León, M., García-Jiménez, J., & Abad-Campos, P. (2012). Enfermedades causadas por Phytophthora en viveros de plantas ornamentales. Boletín de Sanidad Vegetal-Plagas, 38, 143–156.Google Scholar
  49. Pérez-Sierra, A., López-García, C., León, M., García-Jiménez, J., Abad-Campos, P., & Jung, T. (2013). Previously unrecorded low-temperature Phytophthora species associated with Quercus decline in a Mediterranean forest in eastern Spain. Forest Pathology, 43, 331–339.CrossRefGoogle Scholar
  50. Redondo, M. A., Pérez-Sierra, A., & Abad-Campos, P. (2015). Histology of Quercus ilex roots during infection by Phytophthora cinnamomi. Trees - Structure and Function, 29, 1943–5197.CrossRefGoogle Scholar
  51. Ríos, P., Obregón, S., de Haro, A., Fernández-Rebollo, P., Serrano, M. S., & Sánchez, M. E. (2016). Effect of Brassica Biofumigant Amendments on Different Stages of the Life Cycle of Phytophthora cinnamomi. Journal of Phytopathology, 164, 582–594.CrossRefGoogle Scholar
  52. Rizzo, D. M., Garbelotto, M., Davidson, J. M., Slaughter, G. W., & Koike, S. T. (2002). Phytophthora ramorum as the cause of extensive mortality of Quercus spp. and Lithocarpus densiflorus in California. Plant Disease, 86, 205–214.CrossRefGoogle Scholar
  53. Robin, C., Desprez-Loustau, M. L., Capron, G., & Delatour, C. (1998). First record of Phytophthora cinnamomi on cork and holm oaks in France and evidence of pathogenicity. Annales Des Sciences Forestieres, 55, 869–883.CrossRefGoogle Scholar
  54. Robin, C., Capron, G., & Desprez-Loustau, M. L. (2001). Root infection by Phytophthora cinnamomi in seedlings of three oak species. Plant Pathology, 50, 708–716.CrossRefGoogle Scholar
  55. Rodríguez-Molina, M. C., Torres-Vila, L. M., Blanco-Santos, A., Núñez, E. J. P., & Torres-Álvarez, E. (2002). Viability of holm and cork oak seedlings from acorns sown in soils naturally infected with Phytophthora cinnamomi. Forest Pathology, 32, 365–372.CrossRefGoogle Scholar
  56. Romero, M. A., Sánchez, J. E., Jiménez, J. J., Belbahri, L., Trapero, A., Lefort, F., & Sánchez, M. E. (2007). New Pythium taxa causing root rot in Mediterranean Quercus species in southwest Spain and Portugal. Journal of Phytopathology, 115, 289–295.CrossRefGoogle Scholar
  57. Sánchez de Lorenzo-Cáceres J. M. (2001). Guía de las plantas ornamentales. S.A. Mundi-Prensa Libros. ISBN 9788471149374. 688 pp.Google Scholar
  58. Sánchez, M. E., Caetano, P., Ferraz, J., & Trapero, A. (2002). Phytophtora disease of Quercus ilex in south-western Spain. Forest Pathology, 32, 5–18.CrossRefGoogle Scholar
  59. Sánchez, M. E., Sánchez, J. E., Navarro, R. M., Fernández, P., & Trapero, A. (2003). Incidencia de la podredumbre radical causada por Phytophthora cinnamomi en masas de Quercus en Andalucía. Boletín de Sanidad Vegetal-Plagas, 29, 87–108.Google Scholar
  60. Sánchez, M. E., Andicoberry, S., & Trapero, A. (2005). Pathogenicity of three Phytophthora spp. causing late seedling rot of Quercus ilex ssp. ballota. Forest Pathology, 35, 115–125.CrossRefGoogle Scholar
  61. Sánchez, M. E., Caetano, P., Romero, M. A., Navarro, R. M., & Trapero, A. (2006). Phytophthora root rot as the main factor of oak decline in southern Spain. In: Progress in Research on Phytophthora Diseases of Forest Trees. Proceedings of the Third International IUFRO Working Party S07.02.09. Meeting at Freising. Germany 11-18 September 2004. Brasier C. M., Jung T., Oßwald W. (Eds). Forest Research. Farnham, UK. pp. 149-154.Google Scholar
  62. Scanu, B., Linaldeddu, B. T., Deidda, A., & Jung, T. (2015). Diversity of Phytophthora species from declining Mediterranean maquis vegetation, including two new species, Phytophthora crassamura and P. ornamentata sp. nov. PLoS ONE, 10.  https://doi.org/10.1371/journal.pone.0143234.
  63. Schmitthenner, A. F., & Canaday, C. H. (1983). Role of chemical factors in the development of Phytophthora diseases. In: Phytophthora. Its biology, taxonomy, ecology, and pathology (pp.189-196). Ed. by Erwin D. C., Bartnicki-Garcia S., Tsao P. H. St. Paul, : The American Phytopathological Society.Google Scholar
  64. Scibetta, S., Schena, L., Chimento, A., Cacciola, S. A., & Cooke, D. E. L. (2012). A molecular method to assess Phytophthora diversity in environmental samples. Journal of Microbiological Methods, 88, 356–368.CrossRefGoogle Scholar
  65. Sena, K., Crocker, E., Vincelli, P., & Barton, C. (2018). Phytophthora cinnamomi as a driver of forest change: Implications for conservation and management. Forest Ecology and Management, 409, 799–807.CrossRefGoogle Scholar
  66. Thines, M. (2013). Taxonomy and phylogeny of Phytophthora and related oomycetes In: Phytophthora: A global perspective (pp. 11-18). Ed. by Lamour, K. Wallingford: CABI.Google Scholar
  67. Tsao, P. H. (1990). Why many Phytophthora root rots and crown rots of tree and horticultural crops remain undetected. EPPO Bulletin, 20, 11–17.CrossRefGoogle Scholar
  68. Tuset, J. J., Hinarejos, C., Mira, J. L., & Cobos, M. (1996). Implicación de Phytophthora cinnamomi Rands en la enfermedad de la seca de encinas y alcornoques. Boletín de Sanidad Vegetal-Plagas, 22, 491–499.Google Scholar
  69. Vettraino, A. M., Barzanti, G. P., Bianco, M. C., Ragazzi, A., Capretti, P., Paoletti, E., & Vannini, A. (2002). Occurrence of Phytophthora species in oak stands in Italy and their association with declining oak trees. Forest Pathology, 32, 19–28.CrossRefGoogle Scholar
  70. Xia, K., Hill, L. M., Li, D. Z., & Walters, C. (2014). Factors affecting stress tolerance in recalcitrant embryonic axes from seeds of four Quercus (Fagaceae) species native to the USA or China. Annals of Botany, 114, 1747–1759.CrossRefGoogle Scholar

Copyright information

© Koninklijke Nederlandse Planteziektenkundige Vereniging 2018

Authors and Affiliations

  • Beatriz Mora-Sala
    • 1
    Email author
  • Paloma Abad-Campos
    • 1
  • Mónica Berbegal
    • 1
  1. 1.Instituto Agroforestal MediterráneoUniversitat Politècnica de ValènciaValenciaSpain

Personalised recommendations