Fungi associated with disease symptoms on Pinus mugo needles in the Polish Tatra Mountains
More details
Hide details
Department of Forest Ecosystems Protection, University of Agriculture in Kraków, al. 29 Listopada 46, 31-425 Kraków, Poland
Tatra National Park, Kuźnice 1, 34-500 Zakopane, Poland
Online publication date: 2021-07-30
Publication date: 2021-07-30
Plant and Fungal Systematics 2021; 66(1): 53–65
Dwarf mountain pine, Pinus mugo, is an important component of the subalpine and alpine zone in Europe. For several years, in one of the natural areas of the occurrence of this species in the Polish Tatras, an intensified decline of the assimilation apparatus has been observed. The studies conducted in 2016–2020 were aimed at determining the types of disease symptoms occurring on P. mugo needles and at identifying the species composition of fungi within symptomless and diseased needles. We isolated 57 taxa from 6 types of disease symptoms and from needles without disease symptoms, identified on the basis of morphological features and molecular analyses. Absolute parasites were represented by only one species of Coleosporium senecionis, which was identified by the aecium stage. The genus Lophodermium was represented by three species: L. conigenum, L. corconticum and L. pini-mugonis. So far, L. corconticum was known only from the Karkonosze Mountains in Poland, and L. pini-mugonis from the German Alps. In addition, the more frequently isolated species included: Sydowia polyspora, Hendersonia sp., Nemania serpens, Leptomelanconium allescheri, Cladosporium spp., Biscogniauxia nummularia and Alternaria spp. Some taxa were associated with only one type of disease symptom, while some species of fungi were found to be associated with different symptoms. Twelve species of fungi were isolated from living symptomless needles, some of which were subsequently found in association with nectrotic areas on needles, e.g., Lophodermium corconticum, L. conigenum and Leptomelanconium allescheri. L. pinastri has not been found in the present studies. In the discussion, an attempt was made to assess the role of some of the identified species of fungi in causing the disease process of P. mugo needles.
Andjelič, M. 2000. Disease of the mountain pine (Pinus mugo Turra) in the area of ‘Lovcen’ National Park (Montenegro, Yugoslavia). Zastita prirode 52(1): 69−78.
Ballian, D., Ravazzi, C., de Rigo, D. & Caudullo, G. 2016. Pinus mugo in Europe: Distribution, habitat, usage and threats. In: San-Miguel-Ayanz, J., de Rigo, D., Caudullo, G., Houston Durrant T. & Mauri, A. (eds), European Atlas of Forest Tree Species, pp. 124–125. Luxembourg: Publication Office of the European Union.
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. https://doi.org/10.1111/j.1439....
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(1): 30–36. https://doi.org/10.17221/4484-....
Boratyńska, K. 2002. Needle variability of Pinus mugo Turra in the West Tatra Mts. Dendrobiology 48: 3–8.
Boratyńska, K., Marcysiak, K. & Boratyński A. 2005. Pinus mugo (Pinaceae) in the Abruzzi Mountains: high morphological variation in isolated populations. Botanical Journal of the Linnean Society 147: 309–316. https://doi.org/10.1111/j.1095....
Boroń, P., Lenart-Boroń, A. & Mullett, M. 2016. The distribution of Dothistroma septosporum and its mating types in Poland. Forest Pathology 46: 489–496. https://doi.org/10.1111/efp.12....
Butin, H. 1984. Pilzkrankheiten der Schwarzkiefer. Allgemeine Forstzeitschrift 23: 585–587.
Butin, H. 1986. Endophytic fungi in green needles of Norway spruce (Picea abies Karst). Zeitschrift fuer Mykologie 52(2): 335–346.
Bytnerowicz, A., Arbaugh, M., Schilling, S., Fraczek, W. & Alexander, D. 2008. Ozone distribution and phytotoxic potential in mixed conifer forests of the San Bernardino Mountains, southern California. Environ Pollution 155(3): 398–408. https://doi.org/10.1016/j.envp....
Darriba, D., Taboada, G. L., Doallo, R. & Posada, D. 2012. jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9: 772. https://doi.org/10.1038/nmeth.....
Giordano, L. & Gonthier, P. 2011. An outbreak of Cyclaneusma minus needle cast on Swiss mountain pine (Pinus uncinata) in Italy. Journal of Plant Pathology 93: 4 (Supplement), S4.63–S4.89.
Guindon, S., Dufayard, J. F., Lefort, V., Anisimova, M., Hordijk, W. & Gascuel, O. 2010. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59: 307–321. https://doi.org/10.1093/sysbio....
Guindon, S. & Gascuel, O. 2003. A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Systematic Biology 52: 696–704. https://doi.org/10.1080/106351....
Hall, T. A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/ NT. Nucleic Acids Symposium Series 41: 95–98.
Hata, K. & Futai, K. 1995. Endophytic fungi associated with healthy pine needles and needles infested by the pine needle gall midge Thecodiplosis japonensis. Canadian Journal of Botany 73: 384–390. https://doi.org/10.1139/b95-04....
Hirose, D. & Osono, T. 2006. Development and seasonal variations of Lophodermium populations on Pinus thunbergi needle litter. Mycoscience 47: 242−247. https://doi.org/10.1007/s10267....
Holdenrieder, O. & Sieber, T. N. 1995. First report of Mycosphaerella dearnessii in Switzerland. European Journal of Plant Pathology 25: 293–295. https://doi.org/10.1111/j.1439....
Hou, Ch., Li, L. & Piepenbring, M. 2009. Lophodermium pini-mugonis sp. nov. on needles of Pinus mugo from the Alps based on morphological and molecular data. Mycological Progress 8: 29. https://doi.org/10.1007/s11557....
Katoh, K. & Standley, D. M. 2013. MAFFT multiple sequence alignment software version 7, improvements in performance and usability. Molecular Biology and Evolution 30: 772–780. https://doi.org/10.1093/molbev....
Koukol, O., Pusz, W. & Minter, D. 2015. A new species of Lophodermium on needles of mountain pine (Pinus mugo) from the Giant Mountains in Poland. Mycological Progress 14: 23. https://doi.org/10.1007/s11557....
Kowalski, T. 1982. Fungi infecting Pinus sylvestris needles of various ages. European Journal of Plant Pathology 12(3): 182–190. https://doi.org/10.1111/j.1439....
Kowalski, T. 1988. Zur Pilzflora toter Kiefernnadeln. Zeitschrift für Mykologie 54(2): 159–173.
Kowalski, T. 1993. Fungi in living symptomless needles of Pinus sylvestris with respect to some observed disease processes. Journal of Phytopathology 139: 129–145. https://doi.org/10.1111/j.1439....
Kowalski, T. & Domański, S. 1983. Występowanie i przyczyny odwierzchołkowego zamierania pędów Pinus nigra, P. silvestris i P. strobus w niektórych drzewostanach południowej Polski w latach 1979–1980. Acta Agraria et Silvestria series Silvestris 20: 19–34.
Kowalski, T. & Zych, P. 2002. Fungi isolated from living symptomless shoots of Pinus nigra growing in different site conditions. Österreichische Zeitschrift für Pilzkunde 11: 107–116.
Kowalski, T., Boroń, P., Bartnik, C. & Rossa, R. 2018. Morphological and molecular characterization of Leptomelanconium allescheri associated with necrotic lesions on Pinus mugo needles in the Polish Tatra Mountains. Forest Pathology 48(3): e12420. https://doi.org/10.1111/efp.12....
Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. 2018. MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Molecular Biology and Evolution 35: 1547–1549. https://doi.org/10.1093/molbev....
La Porta, N. & Capretti, P. 2000. Mycosphaerella dearnessii, a Needle-cast Pathogen on Mountain Pine (Pinus mugo) in Italy. Plant Disease 84(8): 922 https://doi.org/10.1094/pdis.2....
Lang, K. J. & Holdenrieder, O. 1985. Nekrotische Flecken an Nadeln von Picea abies-ein Symptom des Fichtensterbens? European Journal of Forest Pathology 15(1): 52−58. https://doi.org/10.1111/j.1439....
Lutyk, P. 1978. Stan zdrowotny sosny kosówki (Pinus mughus Scop.) na terenie Tatrzańskiego Parku Narodowego. Sylwan 122(10): 51−57.
Map of Polish Tatra Mountains: https://mapa.szukacz.pl/mapnik... [Accessed 14 May 2021].
Maschning, E. & Pehl, L. 1994. Bedrohung autochthoner Latschen durch Dothistroma-Nadelbräune. Allgemeine Forstzeitschrift 49: 249–252.
Minter, D. W., Staley, J. M. & Millar, C. S. 1978. Four species of Lophodermium on Pinus sylvestris. Transactions of the British Mycological Society 71: 295–301. https://doi.org/10.1016/s0007-....
Minter, D. W. & Millar, C. S. 1980. Ecology and biology of three Lophodermium species on secondary needles of Pinus sylvestris. European Journal of Plant Pathology 10: 169–181 https://doi.org/10.1111/j.1439....
Minter, D. W. 1981. Lophodermium on pines. Mycological Papers 147: 1–54.
Mróz, W. & Perzanowska, J. 2004. Zarośla kosodrzewiny (Pinetum mugo). In: Herbich, J. (ed.). Poradniki ochrony siedlisk i gatunków Natura 2000 – poradnik metodyczny. Tom 3. Murawy, łąki, ziołorośla, wrzosowiska, zarośla, pp. 54−62. Wyd. Ministerstwo Środowiska, Warszawa.
Ortiz-Garcia, S., Gernandt, D. S., Stone, J. K., Johnston, P. R., Chapela, I. H., Salas-Lizana, R. & Alvarez-Buylla, E. R. 2003. Phylogenetics of Lophodermium from pine. Mycologia 95(5): 846–859. https://doi.org/10.2307/376201....
Pehl, L. & Butin, H. 1992. Dothistroma septospora, a new fungus pest on Pinus mugo. Allgemeine Forst Zeitschrift der Wald 47: 758–760.
Pehl, L. 1995. Eine neue Kiefernkrankheit in der Bundesrepublik Deutschland. Nachrichtenblatt des Deutschen Pflanzenschutzdienstes 47: 305–309.
Pusz, W., Kita, W., Kaczmarek, A., Nowosad, K. & Koukol, O. 2013. Choroby igieł kosodrzewiny (Pinus mugo) w piętrze subalpejskim Karkonoszy. Sylwan 157(10): 761−769.
Pusz, W., Zwijacz-Kozica, T. & Kita, W. 2015. The assessment of the health status of the needles of the Mugo Pine (Pinus mugo) in selected locations of the Tatra National Park. Sylwan 159(5): 411−418.
Rambaut, A. & Drummond, A. J. 2007. Tracer v1.4. [Accessed 8 Mar. 2019].
Reignoux, S. N., Green, S. & Ennos, R. A. 2014. Molecular identification and relative abundance of cryptic Lophodermium species in natural populations of Scots pine, Pinus sylvestris L. Fungal Biology 118: 835−845. https://doi.org/10.1016/j.funb....
Ronquist, F. & Huelsenbeck, J. P. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574. https://doi.org/10.1093/bioinf....
Saikkonen, K., Faeth, S. H., Helander, M. & Sullivan, T. J. 1998. Fungal endophytes: A continuum of interactions with host plants. Annual Review of Ecology, Evolution, and Systematics 29: 319–343. https://doi.org/10.1146/annure....
Salas-Lizana, R. & Oono, R. 2018. A comparative analysis of Lophodermium fissuratum, sp. nov., found in haploxylon pine needles in the Pacific Northwest, and other Lophodermium endophytes. Mycologia 110(5): 797–810. https://doi.org/10.1080/002755....
Schnell, G. R. 1987. Investigations of plant diseases in reforestations of the subalpine region in the central Swiss Alps. European Journal of Forest Pathology 17: 19–33. https://doi.org/10.1111/j.1439....
Schütt, P., Koch, W., Blaschke, H., Lang, K. J., Reigber, E., Schuck, H. J. & Summerer, H. 1985. So stirbt der Wald. Schadbilder und Krankheitsverlauf. BLV Verlaggeselschaft, München.
Sieber, T. N., Ryś, J. & Holdenrieder, O. 1999. Mycobiota in symptomless needles of Pinus mugo ssp. uncinata. Mycological Research 103: 306–310. https://doi.org/10.1017/S09537....
Sieber, T. N. 2007. Endophytic fungi in forest trees: are they mutualists? Fungal Biology Reviews 21: 75–89. https://doi.org/10.1016/j.fbr.....
Sutton, B. C. 1980. The coelomycetes. Fungi imperfecti with pycnidia, acervuli and stromata. Kew Surrey, UK: CMI.
Sutton, B. C. & Chao, R. L. C. 1970. Leptomelanconium. Transactions of the British Mycological Society 55(1): 37–44. https://doi.org/10.1016/ S0007-1536(70)80093-6.
Swofford, D. L. 2003. PAUP*. Phylogenetic analysis using parsimony (* and other methods). Version 4. Sinauer Associates, Sunderland.
Tamura K., Nei, M. & Kumar, S. 2004. Prospects for inferring very large phylogenies by using the neighbor-joining method. Proceedings of the National Academy of Sciences (USA) 101: 11030–11035. https://doi.org/10.1073/pnas.0....
Wang, S-J., Lin, Y-R., Hou, C-L., Gao, X-M., Yang, Z-Z. & Liu, F. 2010. A preliminary study on phylogeny of Lophodermium based on rDNA-ITS sequences. Mycosystema 29: 199–205.
White, T. J., Bruns, T., Lee, S. & Taylor, J. W. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis, M. A., Gelfand, D. H., Sninsky, J. J. & White, T. J. (eds), PCR protocols: A guide to methods and applications, pp. 315–322. New York, NY: Academic Press Inc. https://doi.org/10.1016/b978-0....
Wieser, G., Manning, W. J., Tausz, M. & Bytnerowicz, A. 2005. Evidence for potential impacts of ozone on Pinus cembra L. at mountain sites in Europe: an overview. Environ Pollution 139(1): 53–58. https://doi.org/10.1016/j.envp....
Vujanovic, V. & St-Arnaud, M. 2001. Leptomelanconium abietis sp. nov. on needles of Abies balsamea. Mycologia 93(1): 212–215. https://doi.org/10.1080/002755....
Checking the balance between pathogenic and mutualistic pine needle fungi of the genus Lophodermium in forested and urban areas of Slovakia
Emília Ondrušková, Slavomír Adamčík, Marek Kobza, Zuzana Jánošíková, Radovan Ostrovský, Katarína Pastirčáková, Miroslav Caboň, Katarína Adamčíková
Scandinavian Journal of Forest Research