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Genetic diversity of Dothistroma septosporum in Estonia, Finland and Czech Republic

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Abstract

Dothistroma needle blight is one of the most damaging foliage diseases in pine plantations worldwide. Recently it has become more aggressive in native pine stands in northern America and has been found frequently on Scots pine stands in northern Europe. In Estonia and Finland it was noticed for the first time in 2006 and 2008, respectively and in Central Europe in the late 1990s. We show considerable diversity in allele patterns of several microsatellite loci in populations of these countries which does not support the hypothesis of a recent introduction. We investigated 104 isolates by using eight microsatellite loci. Estonian and Finnish isolates originated from P. sylvestris and those from the Czech Republic from six species of Pinus spp. and Pseudotsuga menziesii. The genetic diversity was considerable in all three populations, and did not differ significantly between populations. The results suggest slight migration from south to north, even if no similar haplotypes were found between any of the populations. Both, the pairwise genetic differentiation and Nei’s genetic distance reflected geographic distances between the populations. Differentiation between the studied populations of D. septosporum was low but statistically significant. Only 6 % of the genetic variation was due to differences between populations. The high haplotypic diversity, low number of identical haplotypes, and low degree of genetic disequilibrium in all investigated populations suggested occurrence of sexual proliferation in this area, although the sexual state of the fungus has not been recorded in Estonia and Finland. The high diversity may suggest a long presence of D. septosporum in northern Europe, or alternatively, its recent introduction as a massive inoculum from an unknown direction.

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References

  • Agapow, P. M., & Burt, A. (2001). Indices of multilocus linkage disequilibrium. Molecular Ecology Notes, 1, 101–102.

    Article  CAS  Google Scholar 

  • Anonymous. (2005). The diagnostic protocol for Mycosphaerella pini. OEPP/EPPO Bulletin, 35, 303–306.

    Article  Google Scholar 

  • Barnes, I., Crous, P. W., Wingfield, B. D., & Wingfield, M. J. (2004). Multigene phylogenies reveal that red band needle blight is caused by two distinct species of Dothistroma, D. septosporum and D. pini. Studies in Mycology, 50, 551–565.

    Google Scholar 

  • Barnes, I., Cortinas, M. N., Wingfield, M. J., & Wingfield, B. D. (2008). Microsatellite markers for the red band needle blight pathogen, Dothistroma septosporum. Molecular Ecology Resources, 8, 1026–1029.

    Article  PubMed  CAS  Google Scholar 

  • Barnes, I., Kirisits, T., Akulov, A., Chhetri, D. B., Wingfield, B. D., Bulgakov, T. S., & Wingfield, M. J. (2008). New host and country records of the Dothistroma needle blight pathogens from Europe and Asia. Forest Pathology, 38, 178–195.

    Article  Google Scholar 

  • Barnes, I., Kirisits, T., Wingfield, M. J., & Wingfield, B. D. (2011). Needle blight of pine caused by two species of Dothistroma in Hungary. Forest Pathology, 41, 361–369.

    Article  Google Scholar 

  • Bassett, C. (1969). Larix decidua a new host for Dothistroma pini. Plant Disease Reporter, 53, 706.

    Google Scholar 

  • Bednářová, M., Palovčíková, D., & Jankovský, L. (2006). The host spectrum of Dothistroma needle blight Mycosphaerella pini E. Rostrup – new hosts of Dothistroma needle blight observed in the Czech Republic. Journal of Forest Science, 52, 30–36.

    Google Scholar 

  • Beerli, P. (2010). Migrate documentation version 3.2 (p. 114). Tallahassee: Department of Scientific Computing, Florida State University.

    Google Scholar 

  • Beerli, P., & Palczewski, M. (2010). Unified framework to evaluate panmixia and migration direction among multiple sampling locations. Genetics, 185, 313–326.

    Article  PubMed  Google Scholar 

  • Bradshaw, R. E. (2004). Dothistroma (red band) needle blight of pines and the dothistromin toxin: review. Forest Pathology, 34, 163–185.

    Article  Google Scholar 

  • Brown, A., & Webber, J. (2008). Red band needle blight of conifers in Britain. Edinburgh: UK Forestry Commission (Information note).

    Google Scholar 

  • Brown, A., Rose, D., & Webber, J. (2003). Red Band Needle Blight of Pine. Edinburgh: UK Forestry Commission (Information note).

    Google Scholar 

  • Buddle, C. M., Beguin, J., Bolduc, E., Mercado, A., Sackett, T. E., Selby, R. D., Varady-Szabo, H., & Zeran, R. M. (2005). The importance and use of taxon sampling curves for comparative biodiversity research with forest arthropod assemblages. The Canadian Entomologist, 137, 120–127.

    Article  Google Scholar 

  • Butin, H. (1985). Teleomorph- und anamorph-Entwicklung von Scirrhia pini Funk & Parker auf Nadeln von Pinus nigra Arnold. [Teleomorph and anamorph development of Scirrhia pini Funk & Parker of needles from Pinus nigra Arnold]. Sydowia, Annales Mycologici Ser. II, 38, 20–27 (in German).

    Google Scholar 

  • Butin, H., & Richter, J. (1993). Dothistroma - Nadelbräune: Eine neue Kiefernkrankheit in der Bundesepublik Deutschland. [Dothistroma needle cast: new disease of Pines in Germany]. Nachrichtenblatt Deutscher Pflanzenschutzdienst (Braunschweig), 35, 129–131. in German.

    Google Scholar 

  • Chen, R. S., & McDonald, B. A. (1996). Sexual reproduction plays a major role in the genetic structure of populations of the fungus Mycosphaerella graminicola. Genetics, 142, 1119–1127.

    PubMed  CAS  Google Scholar 

  • Dale, L. A., Lewis, K. J., & Murray, B. W. (2011). Sexual reproduction and gene flow in the pine pathogen Dothistroma septosporum in British Columbia. Phytopathology, 101, 68–76.

    Article  PubMed  CAS  Google Scholar 

  • Dieringer, D., & Schlötterer, C. (2003). Microsatellite analyser (MSA): a platform independent analysis tool for large microsatellite data sets. Molecular Ecology Notes, 3, 167–169.

    Article  CAS  Google Scholar 

  • Doroguine, M. (1911). Une maladie cryptogamique du Pin. [Cryptogamic diseases of Pines]. Bulletin de la Societe Mycologique de France, 27, 105–106. in French.

    Google Scholar 

  • Drenkhan, R., & Hanso, M. (2009). Recent invasion of foliage fungi of pines (Pinus spp.) to the Northern Baltics. Forestry Studies, 51, 49–64.

    Article  Google Scholar 

  • Dubin, H. J., & Walper, S. (1967). Dothistroma pini on Pseudotsuga menziesii. Plant Disease Reporter, 51, 454.

    Google Scholar 

  • Finnish Meteorological Institute. (2011). Net page: http://ilmatieteenlaitos.fi/havaitut-ilmastonmuutokset-suomessa. (in Finnish)

  • Gadgil, P. D. (2008). Dothistroma needle blight. Forest Pathology in New Zealand, No. 5 (Second ed.). New Zealand Forest Service, Roturua, New Zealand.

  • Gardes, M., & Bruns, T. D. (1993). ITS primers with enhanced specificity for basidiomycetes - application to the identification of mycorrhizae and rusts. Molecular Ecology, 2, 113–118.

    Article  PubMed  CAS  Google Scholar 

  • Gibson, I. A. S. (1972). Dothistroma blight of Pinus radiata. Annual Review of Phytopathology, 10, 51–72.

    Article  Google Scholar 

  • Gibson, I. A. S. (1974). Impact and control of Dothistroma blight of pines. European Journal of Forest Pathology, 4, 89–100.

    Article  Google Scholar 

  • Gibson, I. A. S. (1979). Diseases of forest trees widely planted as exotics in the tropics and southern hemisphere. Part II. The genus Pinus. Oxford and Kew: Commonwealth Forestry Institute and Commonwealth Mycological Institute.

    Google Scholar 

  • Gilmour, J. W. (1967). Host list for Dothistroma pini in New Zealand. New Zealand Forest Research Service Leaflet No. 16.

  • Gotelli, N. J., & Colwell, R. K. (2001). Quantifying biodiversity: Procedures and pitfalls in the measurement and comparison of species richness. Ecology Letters, 4, 379–391.

    Article  Google Scholar 

  • Hanso, M., & Drenkhan, R. (2008). First observations of Mycosphaerella pini in Estonia. Plant Pathology, 57, 1177.

    Article  Google Scholar 

  • Hanso, M., & Drenkhan, R. (2012). Lophodermium needle cast, insect defoliation and growth responses of young Scots pines in Estonia. Forest Pathology, 42, 124–135.

    Article  Google Scholar 

  • Hantula, J., Lilja, A., & Parikka, P. (1997). Genetic variation and host specificity of Phytophthora cactorum isolated in Europe. Mycological Research, 101, 565–572.

    Article  Google Scholar 

  • Helander, M. L. (1995). Responses of pine needle endophytes to air pollution. New Phytologist, 131, 223–229.

    Article  CAS  Google Scholar 

  • Helander, M. L., Sieber, T. N., Petrini, O., & Neuvonen, S. (1994). Endophytic fungi in Scots pine needles: spatial variation and consequences of simulated acid rain. Canadian Journal of Botany, 72, 1108–1113.

    Article  Google Scholar 

  • Hunter, G. C., van der Merwe, N. A., Burgess, T. I., Carnegie, A. J., Wingfield, B. D., Crous, P. W., & Wingfield, M. J. (2008). Global movement and population biology of Mycosphaerella nubilosa infecting leaves of cold-tolerant Eucalyptus globules and E. nitens. Plant Pathology, 57, 235–242.

    Article  Google Scholar 

  • Ioos, R., Fabre, B., Saurat, C., Fourrier, C., Frey, P., & Marçais, B. (2010). Development, comparison, and validation of real-time and conventional PCR tools for the detection of the fungal pathogens causing brown spot and red band needle blights of pine. Phytopathology, 100, 105–114.

    Article  PubMed  CAS  Google Scholar 

  • Ito, K., Zinno, Y., & Suto, Y. (1975). Dothistroma needle blight of pines in Japan. Bulletin of the Government Forest Experimental Station, Meguro, 273, 123–140.

    Google Scholar 

  • Ivory, M. H. (1968). Reaction of pines in Kenya to attack by Dothistroma pini var. keniensis. East African Agriculture and Forestry Journal, 33, 236–244.

    Google Scholar 

  • Jaagus, J. (2006). Climatic changes in Estonia during the second half of the 20th century in relationship with changes in large-scale atmospheric circulation. Theoretical and Applied Climatology, 83, 77–88.

    Article  Google Scholar 

  • Jacobs, J. (2011). Individual based rarefaction using R-package. Retrieved March 15, 2012, from http://www.jennajacobs.org/R/rarefaction.html#V%29_References

  • Jankovský, L., Bednářová, M., & Palovčíková, D. (2004). Dothistroma needle blight Mycosphaerella pini E. Rostrup, a new quarantine pathogen of pines in the CR. Journal of Forest Science, 50, 319–326.

    Google Scholar 

  • Jankovský, L., Bednářová, M., Dvořák, M., Palovčíková, D., & Tomšovský, M. (2009). Dothistroma and Lecanosticta needle blight in the CR. SDU Faculty of Forestry Journal, Serial: A, Special Issue, 7–14.

  • Jovaišiené, Z., & Pavilionis, R. (2005). Pušinis rutulgrybis (Mycosphaerella pini) – raudunjuostés spyglių degligés sukéléjas Lietuvoje [Mycospaerella pini is causing red band needle blight of pine in Lithuania]. Mūsų girios, 5, 7. in Lithuanian.

    Google Scholar 

  • Kasanen, R., Hantula, J., Ostry, M., Pinon, J., & Kurkela, T. (2004). North American populations of Entoleuca mammata are genetically more variable than populations in Europe. Mycological Research, 108, 766–774.

    Article  PubMed  CAS  Google Scholar 

  • Keevallik, S., Post, P., & Tuulik, J. (1999). European circulation patterns and meteorological situation in Estonia. Theoretical and Applied Climatology, 63, 117–127.

    Article  Google Scholar 

  • Koltay, A. (1997). Új kórokozók megjelenése a hazai feketefenyő állományokban. [New pathogens in Hungarian black pine stands]. Növényvédelem, 33(7), 339–341. in Hungarian.

    Google Scholar 

  • Kowalski, T., & Jankowiak, R. (1998). First record of Dothistroma septospora (Dorog.) Morelet in Poland: a contribution to the symptomology and epidemiology. Phytopatologia Polonica, 16, 16–29.

    Google Scholar 

  • Kunca, A., & Foffova, E. (2000). Ohrozenie porastov borovice čiernej fytokaranténnym patogénom Dothistroma septospora (Dorog.) Morelet [Threat of stands of Austrian Pines by quarantine pathogen Dothistroma septospora (Dorog.) Morelet]. In: Varinsky J. (ed.): Aktuálne problémy v ochrane lesa 2000. Proceeding Zvolen, Slovak National Forest Centrum Zvolen, 136–139. (in Slovak).

  • Landmann, G. (2000). Forest health in France: assessment for 1998 and new facts. Revue Forestiere Francaise, 52, 9–22.

    Article  Google Scholar 

  • Lang, K. J., & Karadžić, D. (1987). Is Dothistroma pini a danger to Pinus sylvestris? Forstwissenschaftliches Centralblatt, 106, 45–50.

    Article  Google Scholar 

  • Linzer, R. E., Otrosina, W. J., Gonthier, P., Bruhn, J., Laflamme, G., Bussières, G., & Garbelotto, M. (2008). Inferences on the phylogeography of the fungal pathogen Heterobasidion annosum, including evidence of interspecific horizontal genetic transfer and of human-mediated, long-range dispersal. Molecular Phylogenetics and Evolution, 46, 844–862.

    Article  PubMed  CAS  Google Scholar 

  • Markovskaja, S., & Treigiené, A. (2009). New data on invasive pathogenic fungus Dothistroma septosporum in Lithuania. Botanica Lithuanica, 15, 41–45.

    Google Scholar 

  • McDonald, B. A. (1997). The population genetics of fungi: tools and techniques. Phytopathology, 87, 448–453.

    Article  PubMed  CAS  Google Scholar 

  • McDonald, B. A., & Linde, C. (2002). Pathogen population genetics, evolutionary potential, and durable resistance. Annual Review of Phytopathology, 40, 349–379.

    Article  PubMed  CAS  Google Scholar 

  • Müller, M. M., Hantula, J., & Vuorinen, M. (2009). First observations of Mycosphaerella pini on Scots pine in Finland. Plant Disease, 93, 322.

    Article  Google Scholar 

  • Murray, J. S., & Batko, S. (1962). Dothistroma pini Hulbary: A new disease on pine in Britain. Forestry, 3, 57–65.

    Article  Google Scholar 

  • Nei, M. (1972). Genetic distance between populations. American Naturalist, 106, 283–392.

    Article  Google Scholar 

  • Nei, M. (1978). Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics, 89, 583–590.

    PubMed  CAS  Google Scholar 

  • Parker, A. K., & Collis, D. G. (1966). Dothistroma needle blight of pines in British Columbia. The Forestry Chronicle, 42, 160–161.

    Google Scholar 

  • Peakall, R., & Smouse, P. E. (2006). GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes, 6, 288–295.

    Article  Google Scholar 

  • Peterson, G. W. (1967). Dothistroma needle blight of pines in North America. Proceedings of the XIV Congress of the International Union of Forest Research Organisations, 5, 269–278.

    Google Scholar 

  • Petrak, F. (1961). Die Lecanosticta Krankheit der Föhren in Osterreich. [The disease of pine caused by Lecanosticta in Austria]. Sydowia, 15, 252–256. in German.

    Google Scholar 

  • Rytkönen, A., Lilja, A., Drenkhan, R., Gaitnieks, T., & Hantula, J. (2011). First record of Chalara fraxinea in Finland and genetic variation among samples from Åland, mainland Finland, Estonia and Latvia. Forest Pathology, 141, 169–174.

    Article  Google Scholar 

  • Solheim, H., & Vuorinen, M. (2011). First Report of Mycosphaerella pini Causing Red Band Needle Blight on Scots Pine in Norway. Plant Disease, 95, 875.

    Article  Google Scholar 

  • Vainio, E. J., Korhonen, K., & Hantula, J. (1998). Genetic variation in Phlebiopsis gigantea as detected with random amplified microsatellite (RAMS) markers. Mycological Research, 102, 187–192.

    Article  Google Scholar 

  • Watt, S. M., Kriticos, J. D., Alcaraz, S., Brown, V. A., & Leriche, A. (2009). The hosts and potential geographic range of Dothistroma needle blight. Forest Ecology and Management, 257, 1505–1519.

    Article  Google Scholar 

  • Watt, S. M., Palmer, J. D., & Bulman, S. L. (2011). Predicting the severity of Dothistroma on Pinus radiata under current climate in New Zealand. Forest Ecology and Management, 261, 1792–1798.

    Article  Google Scholar 

  • Weir, B. S., & Cockerham, C. C. (1984). Estimating F-statistics for the analysis of population structure. Evolution, 38, 1358–1370.

    Article  Google Scholar 

  • Woods, A. (2011). Is the health of British Columbia’s forests being influenced by climate change? If so, was this predictable? Canadian Journal of Plant Pathology, 33, 117–126.

    Article  Google Scholar 

  • Woods, A., Coates, K. D., & Hamann, A. (2005). Is an unprecedented Dothistroma needle blight epidemic related to climate change? BioScience, 55, 761–769.

    Article  Google Scholar 

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Acknowledgments

The authors thankfully acknowledge Marja-Leena Santanen, for her help in the laboratory, Annukka Korpijaakko and Allar Padari for technical assistance; Katrin Drenkhan, Věra Tomešová and Dagmar Palovčíková for laboratory work; Dr. Pekka Pamilo for advice in interpretation of statistical results; and Mr. Terry Bush from Madison, Wisconsin, USA, for the language revision. The study was supported by the Estonian Environmental Investments Centre and The National Agency for Agriculture Research of the Czech Republic, grant number QH81039.

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Drenkhan, R., Hantula, J., Vuorinen, M. et al. Genetic diversity of Dothistroma septosporum in Estonia, Finland and Czech Republic. Eur J Plant Pathol 136, 71–85 (2013). https://doi.org/10.1007/s10658-012-0139-6

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