Advertisement

European Journal of Plant Pathology

, Volume 146, Issue 2, pp 259–279 | Cite as

Phylogeny, morphology and pathogenicity of Botryosphaeriaceae, Diatrypaceae and Gnomoniaceae associated with branch diseases of hazelnut in Sardinia (Italy)

  • B. T. Linaldeddu
  • A. Deidda
  • B. Scanu
  • A. Franceschini
  • A. Alves
  • J. Abdollahzadeh
  • A. J. L. Phillips
Article

Abstract

Severe trunk and branch diseases of hazelnut trees have recently been observed in several groves in Sardinia (Italy). Since there is little information about the aetiology of these diseases and given the high ecological and economic importance of these agro-systems, an in-depth study was carried out. From autumn 2012 to spring 2014, sixty samples of twigs and branches of hazelnut trees showing exudates and different types of canker (sunken with wedge-shaped necrotic sector, open canker and Cytospora canker) were collected in the main hazelnut growing area in the centre of the island. Based on morphology, colony appearance and DNA sequence data, seven species belonging to four genera and three families were isolated and identified. These included Diplodia sapinea, D. seriata, Dothiorella iberica, Do. parva and Do. symphoricarposicola (Botryosphaeriaceae), Gnomoniopsis smithogilvyi (Gnomoniaceae) and Anthostoma decipiens (Diatrypaceae). In addition, two new species namely Diaporthella cryptica sp. nov. and Dothiorella omnivora sp. nov. are described. Pathogenicity trials carried out on wounded hazelnut branches showed that three species, Anthostoma decipiens, Diaporthella cryptica and Diplodia seriata are aggressive pathogens on hazelnut. Results obtained have allowed us to clarify, almost a century after its first description, the aetiology of the disease known as Cytospora canker of hazelnut and to reveal the existence of three evolutionarily distinct lineages for its causal agent A. decipiens. The diversity of fungal pathogens associated with twig and branch cankers of hazelnut is greater than previously recognised and further studies are necessary to determine the exact role played by each species and their possible synergistic interaction.

Keywords

Anthostoma Diaporthella Dothiorella Phylogeny Pathogenicity 

Notes

Acknowledgments

Antonio Deidda and Bruno Scanu gratefully acknowledge Sardinia Regional Government for the financial support of the PhD scholarship and research grant, respectively (P.O.R. Sardegna F.S.E. Operational Programme of the Autonomous Region of Sardinia, European Social Fund 2007–2013 - Axis IV Human Resources, Objective l.3, Line of Activity l.3.1.). Artur Alves acknowledges financing from the Portuguese Foundation for Science and Technology (FCT) to CESAM (UID/AMB/50017/2013) and himself (FCT Investigator Programme – IF/00835/2013). Artur Alves acknowledges support by the Autonomous Region of Sardinia, Visiting Professor Programme at the University of Sassari, Italy.

References

  1. Abdollahzadeh, J., & Zolfaghari, S. (2014). Efficiency of rep-PCR fingerprinting as a useful technique for molecular typing of plant pathogenic fungal species: Botryosphaeriaceae species as a case study. FEMS Microbiology Letters, 361, 144–157.CrossRefPubMedGoogle Scholar
  2. Abdollahzadeh, J., Javadi, A., Zare, R., & Phillips, A. J. L. (2014). A phylogenetic study of Dothiorella and Spencermartinsia species associated with woody plants in Iran, New Zealand, Portugal and Spain. Persoonia, 32, 1–12.CrossRefPubMedPubMedCentralGoogle Scholar
  3. Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology, 215, 403–410.CrossRefPubMedGoogle Scholar
  4. Alves, A., Barradas, C., Phillips, A. J. L., & Correia, A. (2013). Diversity of Botryosphaeriaceae species associated with conifers in Portugal. European Journal of Plant Pathology, 135, 791–804.CrossRefGoogle Scholar
  5. Azouaoui-Idjer, G., Della Rocca, G., Pecchioli, A., Bouznad, Z., & Danti, R. (2012). First report of Botryosphaeria iberica associated with dieback and tree mortality of Monterey cypress (Cupressus macrocarpa) in Algeria. Plant Disease, 96, 1073.CrossRefGoogle Scholar
  6. Boccacci, P., Aramini, M., Valentini, N., Bacchetta, L., Rovira, M., Drogoudi, P., Silva, A. P., Solar, A., Calizzano, F., Erdoğan, V., Cristofori, V., Ciarmiello, L. F., Contessa, C., Ferreira, J. J., Marra, F. P., & Botta, R. (2013). Molecular and morphological diversity of on-farm hazelnut (Corylus avellana L.) landraces from southern Europe and their role in the origin and diffusion of cultivated germplasm. Tree Genetics & Genomes, 9, 1465–1480.CrossRefGoogle Scholar
  7. Chen, H., Mehlenbacher, S. A., & Smith, D. C. (2007). Hazelnut accessions provide new sources of resistance to eastern filbert blight. Hortscience, 42, 466–469.Google Scholar
  8. Crous, P. W., Gams, W., Stalpers, J. A., Robert, V., & Stegehuis, G. (2004). MycoBank: an online initiative to launch mycology into the 21st century. Studies in Mycology, 50, 19–22.Google Scholar
  9. Elena, G., Garcia-Figueres, F., Reigada, S., & Luque, J. (2014). Intraspecific variation in Diplodia seriata isolates occurring on grapevines in Spain. Plant Pathology. doi: 10.1111/ppa.12296.Google Scholar
  10. Gottwald, T. R., & Cameron, H. R. (1979). Morphology and life history of Anisogramma anomala. Mycologia, 71, 1107–1126.CrossRefGoogle Scholar
  11. Gottwald, T. R., & Cameron, H. R. (1980). Disease increase and dynamics of spread of canker caused by Anisogramma anomala in European filbert in the Pacific Northwest. Phytopathology, 70, 1087–1092.CrossRefGoogle Scholar
  12. Granata, G. (1985). Le principali malattie del nocciolo in Italia. Informatore Fitopatologico, 35, 19–24.Google Scholar
  13. Graniti, A. (1957). Risultati di inoculazioni artificiali con ceppi di Cytospora corylicola Sacc., isolati da Noccioli colpiti da Mal dello stacco in Sicilia. L’Italia Forestale e Montana, 12, 93–98.Google Scholar
  14. Guerrero, J. A., & Pérez, S. M. (2013). First report of shoot blight and canker caused by Diplodia coryli in hazelnut trees in Chile. Plant Disease, 97, 144.CrossRefGoogle Scholar
  15. Hillis, D. M., & Bull, J. J. (1993). An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Systematic Biology, 42, 182–192.CrossRefGoogle Scholar
  16. Inderbitzin, P., Bostock, R. M., Trouillas, F. P., & Michailides, T. J. (2010). A six-locus phylogeny reveals high species diversity in Botryosphaeriaceae from California almond. Mycologia, 102, 1350–1368.CrossRefPubMedGoogle Scholar
  17. Jaklitsch, W. M., Fournier, J., Rogers, J. D., & Voglmayr, H. (2014). Phylogenetic and taxonomic revision of Lopadostoma. Persoonia, 32, 52–82.CrossRefPubMedPubMedCentralGoogle Scholar
  18. Johnson, K. B., Pinkerton, J. N., Mehlenbacher, S. A., Stone, J. K., & Pscheidt, J. W. (1996). Eastern filbert blight of European Hazelnut: It's becoming a manageable disease. Plant Disease, 80, 1308–1316.CrossRefGoogle Scholar
  19. Julian, J. W., Seavert, C. F., & Olsen, J. L. (2008). Orchard economics: the costs and returns of establishing and producing hazelnuts in the Willamette Valley. Oregon State University Extension Service Bulletin EM 8748-E.Google Scholar
  20. Lamichhane, J. R., Fabi, A., & Varvaro, L. (2014). Summer heat and low soil organic matter influence severity of hazelnut cytospora canker. Phytopathology, 104, 387–395.CrossRefPubMedGoogle Scholar
  21. Li, W., Liu, J., Bhat, D. J., Camporesi, E., Xu, J., & Hyde, K. D. (2014). Introducing the novel species, Dothiorella symphoricarposicola, from snowberry in Italy. Cryptogamie Mycologie, 35, 257–270.CrossRefGoogle Scholar
  22. Linaldeddu, B. T., Sirca, C., Spano, D., & Franceschini, A. (2011). Variation of endophytic cork oak-associated fungal communities in relation to plant health and water stress. Forest Pathology, 41(3), 193–201.CrossRefGoogle Scholar
  23. Linaldeddu, B. T., Franceschini, A., Alves, A., & Phillips, A. J. L. (2013). Diplodia quercivora sp. nov.: a new species of Diplodia found on declining Quercus canariensis trees in Tunisia. Mycologia, 105, 1266–1274.CrossRefPubMedGoogle Scholar
  24. Luque, J., Garcia-Figueres, F., Legorburu, F. J., Muruamendiaraz, A., Armengol, J., & Trouillas, F. P. (2012). Species of Diatrypaceae associated with grapevine trunk diseases in Eastern Spain. Phytopathologia Mediterranea, 51, 528–540.Google Scholar
  25. Lynch, S. C., Eskalen, A., Zambino, P. J., Mayorquin, J. S., & Wang, D. H. (2013). Identification and pathogenicity of Botryosphaeriaceae species associated with coast live oak (Quercus agrifolia) decline in Southern California. Mycologia, 105, 125–140.CrossRefPubMedGoogle Scholar
  26. Maresi, G., Oliveira Longa, C. M., & Turchetti, T. (2013). Brown rot on nuts of Castanea sativa Mill: an emerging disease and its causal agent. iForest, 6, 294–301.CrossRefGoogle Scholar
  27. McDonald, V., & Eskalen, A. (2011). Botryosphaeriaceae species associated with avocado branch cankers in California. Plant Disease, 95, 1465–1473.CrossRefGoogle Scholar
  28. Me, G., & Valentini, N. (2006). La corilicoltura in Italia e nel mondo. Petria, 16, 7–18.Google Scholar
  29. Mehlenbacher, S. A., Pinkerton, J. N., Johnson, K. B., & Pscheidt, J. W. (1994). Eastern filbert blight in Oregon. Acta Horticulturae, 351, 551–557.CrossRefGoogle Scholar
  30. Page, R. D. (1996). TreeView: an application to display phylogenetic trees on personal computers. Computer Applications in the Biosciences, 12, 357–358.PubMedGoogle Scholar
  31. Petrak, F. (1924). Mycologische Notizen. VII Annales Mycologici, 22, 1–182.Google Scholar
  32. Phillips, A. J. L., Alves, A., Correia, A., & Luque, J. (2005). Two new species of Botryosphaeria with brown, 1-septate ascospores and Dothiorella anamorphs. Mycologia, 97, 513–529.CrossRefPubMedGoogle Scholar
  33. Phillips, A. J. L., Crous, P. W., & Alves, A. (2007). Diplodia seriata, the anamorph of “Botryosphaeriaobtusa. Fungal Diversity, 25, 141–155.Google Scholar
  34. Phillips, A. J. L., Alves, A., Pennycook, S. R., Johnston, P. R., Ramaley, A., Akulov, A., & Crous, P. W. (2008). Resolving the phylogenetic and taxonomic status of dark-spored teleomorph genera in the Botryosphaeriaceae. Persoonia, 21, 29–55.CrossRefPubMedPubMedCentralGoogle Scholar
  35. Phillips, A. J. L., Alves, A., Abdollahzadeh, J., Slippers, B., Wingfield, M. J., Groenewald, J. Z., & Crous, P. W. (2013). The Botryosphaeriaceae: genera and species known from culture. Studies in Mycology, 76, 51–167.CrossRefPubMedPubMedCentralGoogle Scholar
  36. Pinkerton, J. N., Johnson, K. B., Theiling, K. M., & Griesbach, J. A. (1992). Distribution and characterization of the eastern filbert blight epidemic in Western Oregon. Plant Disease, 76, 1179–1182.CrossRefGoogle Scholar
  37. Piskur, B., Pavlic, D., Slippers, B., Ogris, N., Maresi, G., Wingfield, M. J., & Jurc, D. (2011). Diversity and pathogenicity of Botryosphaeriaceae on declining Ostrya carpinifolia in Slovenia and Italy following extreme weather conditions. European Journal of Forest Research, 130, 235–249.CrossRefGoogle Scholar
  38. Pitt, W. M., Úrbez-Torres, J. R., & Trouillas, F. P. (2013). Dothiorella vidmadera, a novel species from grapevines in Australia and notes on Spencermartinsia. Fungal Diversity, 61, 209–219.CrossRefGoogle Scholar
  39. Pitt, W. M., Úrbez-Torres, J. R., & Trouillas, F. P. (2014). Dothiorella and Spencermartinsia, new species and records from grapevines in Australia. Australasian Plant Pathology, 44, 43–56.CrossRefGoogle Scholar
  40. Rannala, B., & Yang, Z. (1996). Probability distribution of molecular evolutionary trees: a new method of phylogenetic inference. Journal of Molecular Evolution, 43, 304–311.CrossRefPubMedGoogle Scholar
  41. Rocchi, F., Quaroni, S., Sardi, P., & Saracchi, M. (2010). Studies on Anthostoma decipiens involved in Carpinus betulus decline. Journal of Plant Pathology, 92, 637–644.Google Scholar
  42. Rodriguez, F., Oliver, J. F., Marin, A., & Medina, J. R. (1990). The general stochastic model of nucleotide substitutions. Journal of Theoretical Biology, 142, 485–501.CrossRefPubMedGoogle Scholar
  43. Ronquist, F. R., & Huelsenbeck, J. P. (2003). MrBayes3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574.CrossRefPubMedGoogle Scholar
  44. Salerno, M. (1961). Cytospora corylicola Sacc. e patogenesi del «Mal dello stacco» del nocciolo (Corylus avellana L.) in Sicilia. Rivista Di Patologia Vegetale, 1, 38–64.Google Scholar
  45. Saracchi, M., Rocchi, F., & Quaroni, S. (2008). Further studies on the etiological agents of Carpinus betulus decline. Journal of Plant Pathology, 90, S2–453.Google Scholar
  46. Scortichini, M., & Di Prospero, P. (2002). Alterazioni del legno del nocciolo nel Viterbese. L’Informatore Agrario LVIII, 38, 65–67.Google Scholar
  47. Servazzi, O. (1950). Brevi notizie sulla «Moria» o «Seccume» del Nocciolo gentile delle Langhe. Nuovo Giornale Botanico Italiano, 57, 679–682.Google Scholar
  48. Shivas, R. G., Tree, D. J., Tan, Y. P., & Ballard, E. L. (2009). Dothiorella thripsita sp. nov. Persoonia, 22, 168–169.Google Scholar
  49. Shuttleworth, L. A., Liew, E. C. Y., & Guest, D. I. (2012). Gnomoniopsis smithogilvyi sp. nov. Persoonia, 28, 142–143.Google Scholar
  50. Swofford, D. L. (2003). PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4.0. Sunderland: Sinauer Associates.Google Scholar
  51. Tamura, K., Stecher, G., Peterson, D., Filipski, A., & Kumar, S. (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 30, 2725–2729.CrossRefPubMedPubMedCentralGoogle Scholar
  52. Tavella, L., & Giannetti, G. (2006). Le principali avversità del nocciolo in Piemonte. Petria, 16, 45–48.Google Scholar
  53. Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F., & Higgins, D. G. (1997). The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research, 25, 4876–4882.CrossRefPubMedPubMedCentralGoogle Scholar
  54. Trotter, A. (1933). Contributi alla patologia del Nocciolo. I - Il seccume dei fusti da Cytospora. Ricerche, osservazioni e divulgazione fitopatologica per la Campania e il Mezzogiorno, 2, 17–27.Google Scholar
  55. Úrbez-Torres, J. R., Gubler, W. D., & Luque, J. (2007). First report of Botryosphaeria iberica and B. viticola associated with grapevine decline in California. Plant Disease, 91, 772.CrossRefGoogle Scholar
  56. Vasilyeva, L. N., Rossman, A. Y., & Farr, D. F. (2007). New species of the Diaporthales from eastern Asia and eastern North America. Mycologia, 99, 916–923.CrossRefPubMedGoogle Scholar
  57. Visentin, I., Gentile, S., Valentino, D., Gonthier, P., Tamietti, G., & Cardinale, F. (2012). Gnomoniopsis castanea sp. nov. (Gnomoniaceae, Diaporthales) as the causal agent of nut rot in sweet chestnut. Journal of Plant Pathology, 94, 411–419.Google Scholar
  58. Walker, D. M., Castlebury, L. A., Rossman, A. Y., Sogonov, M. V., & White, J. F. (2010). Systematics of genus Gnomoniopsis (Gnomoniaceae, Diaporthales) based on a three gene phylogeny, host associations and morphology. Mycologia, 102, 1479–1496.CrossRefPubMedGoogle Scholar
  59. White, T. J., Bruns, T., Lee, S., & Taylor, J. (1990). Amplified and direct sequencing of fungal ribosomal RNA genes for phylogenies. 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). San Diego: Academic.Google Scholar

Copyright information

© Koninklijke Nederlandse Planteziektenkundige Vereniging 2016

Authors and Affiliations

  • B. T. Linaldeddu
    • 1
  • A. Deidda
    • 1
  • B. Scanu
    • 1
  • A. Franceschini
    • 1
  • A. Alves
    • 2
  • J. Abdollahzadeh
    • 3
  • A. J. L. Phillips
    • 4
  1. 1.Dipartimento di Agraria, Sezione di Patologia vegetale ed EntomologiaUniversità degli Studi di SassariSassariItaly
  2. 2.Departamento de Biologia, CESAMUniversidade de AveiroAveiroPortugal
  3. 3.Department of Plant Protection, Faculty of AgricultureUniversity of KurdistanSanandajIran
  4. 4.Biosystems and Integrative Sciences Institute (BioISI), Faculty of ScienceUniversity of LisbonLisbonPortugal

Personalised recommendations