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European Journal of Plant Pathology

, Volume 153, Issue 4, pp 1203–1220 | Cite as

Impact of fungal diseases on common box (Buxus sempervirens L.) vegetation in Turkey

  • Seçil Akıllı Şimşek
  • Yakup Zekai Katırcıoğlu
  • Deniz Çakar
  • Daniel Rigling
  • Salih MadenEmail author
Article
  • 187 Downloads

Abstract

In recent years, severe dieback of boxwood (Buxus sempervirens) has been observed in the many forests in Turkey. In this study, boxwood diseases were investigated in the forests and nurseries in the Marmara and Black Sea regions of Turkey. Nurseries and boxwood forests in the above-mentioned regions were visited and leaf, branch, and soil samples were collected from symptomatic plants. Eleven fungal genera were isolated from the samples and identified based on morphological characteristics and sequencing of the ITS region and other barcoding loci. The box blight pathogen, Calonectria pseudonaviculata sensu stricto was most frequently isolated from declining boxwood both in the forest and nurseries. When tested on detached box shoots, C. pseudonaviculata was also the most aggressive pathogen on both wounded and intact leaves. Pseudonectria buxi (anamorph Volutella buxi) caused weak symptoms but only on wounded leaves. Pestalotiopsis asiatica and Gnomoniopsis smitovilgyi also caused necrosis on young shoots and yellowing on leaves. Phytophthora nicotianae was detected in one nursery while P. plurivora in two and P. occultans in one locations in the forests in the Black Sea region. The findings show that the boxwood decline in Black Sea region of Turkey is mainly caused by C. pseudonaviculata but other pathogens may also play a role in the decline. Commonly grown boxwood varieties; B. sempervirens ‘Osmanlı’, B. microphylla ‘Variegata’ and B. microphylla ‘Faulkner’ were found susceptible against box blight alone and mixed infections with Volutella blight while B. sempervirens ‘Rotundifolia’ was tolerant. These box varieties showed similar reactions against Phytophthora spp.

Keywords

Boxwood Dieback Calonectria Phytophthora Volutella 

Notes

Acknowledgements

The authors appreciate funding of this study by the Turkish Scientific and Technical Research Association (Project no: 214O059), and support by staff members of the General Directory of Forestry of Turkey and the COST Action FP1401. The help of Ali Uğur Özcan on the design of the map in Fig. 1 is also appreciated. We also thank Esther Jung, Quirin Kupper and Carolina Cornejo for help with sequencing of the isolates.

Compliance with ethical standards

Conflict of interest

The authors confirm that they do not have any actual or potential conflict of interest, the study described is original, has not been published previously, and is not under consideration for publication elsewhere. All authors have reviewed the manuscript and approved the final version of manuscript before submission.

References

  1. Aday Kaya, A.G. (2014). Türkiye’nin Batısında Yer Alan Orman Fidanlıklarında Geniş Ve İğne Yapraklı Fidan Türlerinde Kök Çürüklüğüne Neden Olan Ökaryot Patojenlerin Belirlenmesi [Determination of Root Rot Causing Eukaryote Pathogens on Deciduous and Coniferous Seedlings in Forest Tree Nurseries in Western Turkey]. Ph.D Thesis, Süleyman Demirel University, Isparta, Turkey, 126 pp. (in Turkish with English abstract).Google Scholar
  2. Akıllı, S., Katircioglu, Y. Z., Zor, K., & Maden, S. (2012a). First report of box blight caused by Cylindrocladium pseudonaviculatum in the Eastern Black Sea region of Turkey. New Disease Reports, 25, 23.CrossRefGoogle Scholar
  3. Akıllı, S., Ulubaş-Serçe, Ç., Katırcıoğlu, Y. Z., & Maden, S. (2012b). Involvement of Phytophthora spp. in chestnut decline in the Black Sea region of Turkey. Forest Pathology, 42(5), 377–386.CrossRefGoogle Scholar
  4. Avcıoğlu, B., Şenel İ. & Demirtaş A. (2013). Bir Kırsal Çevre Öyküsü, Şimşirlerin Başına gelenler. Kırsal Çevre ve Ormancılık Sorunları Araştırma Derneği Yayını, Yayın No. 16. Ankara.Google Scholar
  5. Balci, Y., & Halmschlager, E. (2003). Phytophthora species in oak ecosystems in Turkey and their association with declining oak trees. Plant Pathology, 52, 694–700.CrossRefGoogle Scholar
  6. Barnett, H. L. & Hunter, B. B. (1998). Illustrated genera of imperfect fungi. Fourth edition. APS press, 217 p.Google Scholar
  7. Blake, J. H. & Williamson, M. (2015). Index of plant diseases in South Carolina, third edition. Clemson University extension. 187 p.Google Scholar
  8. Carbone, I., & Kohn, L. M. (1999). A method for designing primer sets for speciation studies in filamentous ascomycetes. Mycologia, 91, 553–556.CrossRefGoogle Scholar
  9. Cech, T., Diminic, D., & Heungens, K. (2010). Cylindrocladium buxicola causes common box blight in Croatia. Plant Pathology, 59, 1169.  https://doi.org/10.1111/j.1365-3059.2010.02361.x.CrossRefGoogle Scholar
  10. Crepel, C., & Inghelbrecht, S. (2003). First report of blight on Buxus spp. caused by Cylindrocladium buxicola in Belgium. Plant Disease, 87, 1539.  https://doi.org/10.1094/PDIS.2003.87.12.1539A.CrossRefGoogle Scholar
  11. Crous, P. W., Groenewald, J. Z., & Hill, C. F. (2002). Cylindrocladium pseudonaviculatum sp. nov. from New Zealand, and new Cylindrocladium records from Vietnam. Sydowia, 54, 23–33.Google Scholar
  12. Domsch, K. H., Gams, W. & Anderson, T. H. (1980). Compendium of soil fungi. Vol 1. Academic Press. 859 p.Google Scholar
  13. Ellis, M. B. (1971). Dematioceaus Hyphomycetes. Commonwealth Mycological Institute. 608 p.Google Scholar
  14. Ellis, M. B. (1976). More Dematioceaus Hyphomycetes. Commonwealth Mycological Institute. 507 p.Google Scholar
  15. Erwin, D. C. & Ribeiro, O. K. (2005). Phytophthora diseases worldwide. The American Phytopathological Society: St. Paul. 562 p.Google Scholar
  16. European and Mediterranean Plant Protection Organization (2009). “EPPO Reporting Service“, NO. 8. Ascession date: 15.07.2014.Google Scholar
  17. Gallegly, M. E., & Hong C. (2008). Phytophthora: Identifying Species by Morphology and DNA Fingerprints. St. Paul, MN: The American Phytopathological Society Aps.158 p.Google Scholar
  18. Garibaldi, A., Bertetti, D., Ortu, G., & Gullino, M. L. (2016). First report of Volutella blight caused by Pseudonectria buxi on Japanese boxwood (Buxus microphylla) in Italy. Plant Disease, 100(7), 1499.CrossRefGoogle Scholar
  19. Gehesquiere, B., Crouch, J. A., Marra, R. E., Van Poucke, K., Rys, F., Maes, M., Gobin, B., Höfte, M., & Heungens, K. (2016). Characterization and taxonomic reassessment of the box blight pathogen Calonectria pseudonaviculata, introducing Calonectria henricotiae sp. nov. Plant Pathology, 65, 37–52.  https://doi.org/10.1111/ppa.12401.CrossRefGoogle Scholar
  20. Gorgiladze, L., Meparishvili, G., Sikharulidze, Z., Natsarishvili, K., & Davitadze, R. (2011). First report of box blight caused by Cylindrocladium buxicola in Georgia. New Disease Reports, 23, 24.  https://doi.org/10.5197/j.2044-0588.2011.023.024.CrossRefGoogle Scholar
  21. Grünwald, N. J., Martin, F. N., Larsen, M. M., Sullivan, C. M., Press, C. M., Coffey, M. D., Hansen, E. M., & Parke, J. L. (2011). Phytophthora-ID.org: A sequence-based Phytophthora identification tool. Plant Disease, 95, 337–342.CrossRefGoogle Scholar
  22. Henricot, B., Pérez Sierra, A., & Prior, C. (2000). A new blight disease on Buxus in the UK caused by the fungus Cylindrocladium. Plant Pathology, 49, 805.CrossRefGoogle Scholar
  23. Henricot, B., Gorton, C., Denton, G., & Denton, J. (2008). Studies on the control of Cylindrocladium buxicola using fungicides and host resistance. Plant Disease, 92, 1273–1279.CrossRefGoogle Scholar
  24. Ivors, K. & LeBude, A. (2011). A new pest to the U.S. Ornamental Industry: The “box blight” pathogen Cylindrocladium pseudonaviculatum = Cylindrocladium buxicola. North Carolina State University Extension, Accessed October 21, 2011.Google Scholar
  25. Ivors, K. L., Lacey, L. W., Milks, D. C., Douglas, S. M., Inman, M. K., Marra, R. E., & LaMondia, J. A. (2012). First report of boxwood blight caused by Cylindrocladium pseudonaviculatum in the United States. Plant Disease, 96(7), 1070.CrossRefGoogle Scholar
  26. Jeffers, S. N., & Aldwinckle, H. S. (1987). Enhancing detection of Phytophthora cactorum in naturally infested soil. Phytopathology, 77, 1475–1482.CrossRefGoogle Scholar
  27. Jung, T., Blaschke, H., & Neumann, P. (1996). Isolation, identification, and pathogenicity of Phytophthora species from declining oak stands. European Journal Forest Pathology, 26, 253–272.CrossRefGoogle Scholar
  28. Konukoğlu, F. & Maden, M. (2007). Biberlerde Kök Boğazı yanıklığı (Phytophthora capsici Leon.)' nın primer inokulum kaynakları ve savaş yöntemleri üzerinde araştırmalar. Ankara Üniversitesi Fen Bilimleri Enstitüsü Bitki Koruma Anabilim Dalı. Doktora tezi, Sayfa 94.Google Scholar
  29. Leach, C. M. (1962). Sporulation of diverse species of fungi under near-ultraviolet radiation. Canadian Journal of Botany, 40(1), 151–161.  https://doi.org/10.1139/b62-016.CrossRefGoogle Scholar
  30. Lehtijärvi, A., Doğmuş-Lehtijärvi, H. T., & Oskay, F. (2014). Cylindrocladium buxicola is threatening the native Buxus sempervirens populations in Turkey. Plant Protection Science, 50(4), 227–229.CrossRefGoogle Scholar
  31. Lehtijärvi, A., Doğmuş-Lehtijärvi, H. T., & Oskay, F. (2017). Boxwood blight in Turkey: Impact on natural boxwood populations and management challenges. Baltic Forestry, 23(1), 274–278.Google Scholar
  32. Lombard, L., Crous, P. W., Wingfield, B. D., & Wingfield, M. J. (2010). Phylogeny and systematics of the genus Calonectria. Studies in Mycology, 66, 31–69.  https://doi.org/10.3114/sim.2010.66.03. CrossRefGoogle Scholar
  33. Luongo, L., Galli, M., Haegi, A., Proietti, P., & Belisario, A. (2013). First report of Phytophthora nicotianae causing wilting and desiccation on Buxus sempervirens in Italy. New Disease Reports, 28, 5.CrossRefGoogle Scholar
  34. Maharachchikumbura, S. S. N., Hyde, K. D., Groenewald, J. Z., Xu, J., & Crous, P. W. (2014). Pestalotiopsis revisited. Studies in Mycology, 79, 121–186.CrossRefGoogle Scholar
  35. Man in’tVeld, W. A., Rosendahl, K. C. H. M., van Rijswick, P. C. J., Meffert, J. P., Westenberg, M., & van de Vossenberg, B. T. L. H. (2015). Phytophthora terminalis sp. nov. and Phytophthora occultans sp. nov., two invasive pathogens of ornamental plants in Europe. Mycologia, 107(1), 54–65.  https://doi.org/10.3852/12-371.CrossRefGoogle Scholar
  36. Mathews, P. G. (2005). Design of experiments with MINITAB. American Society for Quality, quality press, Milwaukee. ISBN 0–87389–637-8.Google Scholar
  37. Mirabolfathy, M., Ahangaran, Y., Lombard, L., & Crous, P. W. (2013). Leaf blight of Buxus sempervirens in northern forests of Iran caused by Calonectria pseudonaviculata. Plant Disease, 97(8), 1121.CrossRefGoogle Scholar
  38. Norm, D. N., Hansen, M. A. & Bush, E. (2011). Boxwood blight: A new disease of boxwoods recently found in the South eastern U. S. Virginia Cooperative Extension On-line http://www.ppws.vt.edu/~clinic/alerts/11-04-11_boxwo od_blight_alert.pdf. Accessed 7 Nov, 2016.
  39. Oskay, F., Doğmuş–Lehtijärvi, H.T. & Lehtijärvi, A. (2015). Impact of boxwood blight pathogens; Cylindrocladium buxicola and Pseudonectria buxi on Buxus balearica and Buxus sempervirens. IUFRO 2015 WP 7.02.02 Foliage, Shoot and Stems Diseases of Forest Trees& WP 7.03.04 Diseases and Insects in Forest Nurseries, Uppsala, Sweden, 7–12 June 2015: 48.Google Scholar
  40. Reeser, P. W., Sutton, W., Hansen, E. M., Goheen, E. M., Fieland, V. J., & Grunwald, N. J. (2015). First report of phytophthora occultans causing root and collar rot on ceanothus, boxwood, rhododendron, and other hosts in horticultural nurseries in Oregon, USA. Plant Disease, 99(9), 1282.CrossRefGoogle Scholar
  41. Sajeewa, S. N. Maharachchikumbura, ., Guo, Liang-Dong, Cai, L., Chukeatirote, E., Wu W. P., Sun X., Crous, P.W., Bhat, D.J., Eric H,. McKenzie, C., Bahkali, A.H. & Hyde, K.D. (2012). A multi-locus backbone tree for Pestalotiopsis, with a polyphasic characterization of 14 new species. Fungal Diversity, 56, 95–129.  https://doi.org/10.1007/s13225-012-0198-1. CrossRefGoogle Scholar
  42. Shi, F., & Hsiang, T. (2014a). First report of Pseudonectria buxi causing Volutella blight on boxwood (Buxus sp.) in Beijing, China. Plant Disease, 98(9), 1282.CrossRefGoogle Scholar
  43. Shi, F., & Hsiang, T. (2014b). Pseudonectria buxi causing leaf and stem blight on Buxus in Canada. European Journal of Plant Pathology, 138(4), 763–773.CrossRefGoogle Scholar
  44. Shishkoff, N., Daughtrey, M., Aker, S., & Olsen, R. T. (2015). Evaluating boxwood susceptibility to Calonectria pseudonaviculata using cuttings from the National Boxwood Collection. Plant Health Progress, 16(1), 11–15.  https://doi.org/10.1094/PHP-RS-14-0033.CrossRefGoogle Scholar
  45. Stamps, D. J., Waterhouse, G. M., Newhook, F. J., & Hall, G. S. (1990). Revised tabular key to the species of Phytophthora. Mycology Paper, 162, 28p.Google Scholar
  46. Sutton, B. C. (1980). The Coelomycetes. Commonwealth Mycological Institute. 696 p.Google Scholar
  47. 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(2), 411–419.Google Scholar
  48. 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. Sninsky, & T. J. White (Eds.), PCR protocols: A guide to methods and applications (pp. 315–322). San Diego: Academic Press.Google Scholar
  49. Wilcox, J. S., & Ellis, M. A. (1989). Phytophthora root and crown rots of peach trees in eastern great lakes region. Plant Disease, 73, 794–798.CrossRefGoogle Scholar

Copyright information

© Koninklijke Nederlandse Planteziektenkundige Vereniging 2018

Authors and Affiliations

  • Seçil Akıllı Şimşek
    • 1
  • Yakup Zekai Katırcıoğlu
    • 2
  • Deniz Çakar
    • 3
  • Daniel Rigling
    • 4
  • Salih Maden
    • 2
    Email author
  1. 1.Science Faculty, Biology DepartmentÇankırı Karatekin UniversityÇankırıTurkey
  2. 2.Agricultural Faculty, Plant Protection DepartmentAnkara UniversityAnkaraTurkey
  3. 3.Forestry Research Institute of Western Black Sea RegionBoluTurkey
  4. 4.Swiss Federal Research Institute WSLBirmensdorfSwitzerland

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