Abstract
Wood-staining fungi, moulds and decay fungi colonize freshly cut wood. Of these, only ophiostomatoid fungi are considered major agents of sapstain on logs and freshly sawn lumber because they can cause permanent staining and discoloration. Sapstain in pine pallets significantly reduces their market value and use in the food industry. The aim of this study was to identify the sapstaining fungi that colonize Scots pine wood used in pallet production. In addition, we evaluated the growth and stain intensity of six isolates of ophiostomatoid fungi on freshly cut Scots pine billets. Fungi were isolated from samples of Scots pine and identified based on morphology and DNA sequence comparisons for three gene regions (ITS, β-tubulin, TEF-1α). A total of 1259 isolates representing 31 fungal species were obtained from the pine samples in Poland during July and September. The isolates represented different ecological and taxonomical groups and belonged to the categories of staining fungi, decay fungi and surface moulds. The most frequently isolated fungi were ophiostomatoid fungi (14 species including an unknown Leptographium sp. and Ophiostoma sp.) and moulds (mainly Trichoderma and Mucor spp.). Of the ophiostomatoid species, Ophiostoma floccosum, O. piceae, O. piliferum and Endoconidiophora pinicola were the predominant species. The results of pine billet inoculation showed that among the six fungal species tested, E. pinicola exhibited the fastest growth in all three directions on the billets. Ophiostoma minus and O. piliferum displayed moderate growth rates in pine billets, while O. floccosum, O. piceae, and Leptographium lundbergii grew very slowly, especially in the tangential and radial directions. The information provided in this paper will help develop more effective control strategies for sapstain prevention in Scots pine.
Similar content being viewed by others
References
Carbone, I., & Kohn, L. M. (1999). A method for designing primer sets for speciation studies filamentous ascomycetes. Mycologia, 91(3), 553–556.
Central Statistical Office. (2014). Forestry, Warsaw.
De Beer, Z. W., & Wingfield, M. J. (2013). Emerging lineages in the Ophiostomatales. In K. A. Seifert, Z. W., De Beer, & M. J., Wingfield (Eds.), Ophiostomatoid fungi: expanding frontiers (pp. 21–46). CBS biodiversity series 12.
De Beer, Z. W., Wingfield, B. D., & Wingfield, M. J. (2003). The Ophiostoma piceae complex in the southern hemisphere: a phylogenetic study. Mycological Research, 107(4), 469–476.
De Beer, Z. W., Seifert, K. A., & Wingfield, M.J. (2013). A nomenclator for ophiostomatoid genera and species in the Ophiostomatales and Microascales. In K. A. Seifert, Z. W., De Beer, & M. J., Wingfield (Eds.), Ophiostomatoid fungi: expanding frontiers (pp. 261–268). CBS biodiversity series 12.
De Beer, Z. W., Duong, T. A., Barnes, I., Wingfield, B. D., & Wingfield, M. J. (2014). Redefining Ceratocystis and allied genera. Studies of Mycology, 79, 187–219.
De Beer, Z. W., Duong, T. A., & Wingfield, M. J. (2016). The divorce of Sporothrix and Ophiostoma: solution to a problematic relationship. Study in Mycology, 83, 165–191. doi:10.1016/j.simyco.2016.07. 001.
Dowding, P. (1970). Colonization of freshly bared pine sapwood surfaces by staining fungi. Transactions of the British Mycological Society, 55(3), 399–412.
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.
Gibbs, J. N. (1993). The biology of ophiostomatoid fungi causing sapstain in trees and freshly cut logs. In M. J. Wingfield, K. A. Seifert, & J. F. Webber (Eds.), Ceratocystis and Ophiostoma: Taxonomy, ecology, and pathogenicity (pp. 153–160). St. Paul: APS Press.
Gibbs, J. N., & Inman, A. (1991). The pine shoot beetle Tomicus piniperda as a vector of blue-stain fungi to windblown pine. Forestry, 64, 139–249.
Giordano, L., Gonthier, P., Varese, G. C., Miserere, L., & Nicolotti, G. (2009). Mycobiota inhabiting sapwood of healthy and declining scots pine (Pinus sylvestris L.) trees in the alps. Fungal Diversity, 38, 69–83.
Glass, N. L., & Donaldson, G. C. (1995). Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Applied of Environmental Microbiology, 61(4), 1323–1330.
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 Biolology, 59(3), 307–321.
Harrington, T. C., & Wingfield, M. J. (1998). The Ceratocystis species on conifers. Canadian Journal of Botany, 76(8), 1446–1457.
Harrington, T. C., McNew, D., Steimel, J., Hofstra, D., & Farrell, R. (2001). Phylogeny and taxonomy of the Ophiostoma piceae-complex and the Dutch elm disease. Mycological Research, 93(1), 111–136.
Hicks, B. R., Cobb, F. W., & Gersper, P. L. (1980). Isolation of Ceratocystis wageneri from forest soil with a selective medium. Phytopathology, 70, 880–883.
Jacobs, K., Bergdahl, D. R., Wingfield, M. J., Halik, S., Seifert, K. A., Bright, D. E., & Wingfield, B. D. (2004). Leptographium wingfieldii introduced into North America and found associated with exotic Tomicus piniperda and native bark beetles. Mycological Research, 108(4), 411–418.
Jacobs, K., Solheim, H., Wingfield, B. D., & Wingfield, M. J. (2005). Taxonomic re-evaluation of Leptographium lundbergii based on DNA sequence comparisons and morphology. Mycological Research, 109(10), 1149–1161.
Jankowiak, R. (2012). Ophiostomatoid fungi associated with Ips sexdentatus on Pinus sylvestris in Poland. Dendrobiology, 68, 43–54.
Jankowiak, R., & Bilański, P. (2013a). Association of the pine-infesting Pissodes species with ophiostomatoid fungi in Poland. European Journal of Forest Research, 132(3), 523–534.
Jankowiak, R., & Bilański, P. (2013b). Diversity of ophiostomatoid fungi associated with the large pine weevil, Hylobius abietis and infested scots pine seedlings in Poland. Annals of Forest Science, 70(4), 391–402.
Jankowiak, R., & Bilański, P. (2013c). Ophiostomatoid fungi associated with root-feeding bark beetles in Poland. Forest Pathology, 43(5), 422–428.
Jankowiak, R., & Kolaŕík, M. (2010). Diversity and pathogenicity of ophiostomatoid fungi associated with Tetropium species colonizing Picea abies in Poland. Folia Microbiologica, 55(2), 145–154.
Jankowiak, R., Rossa, R., & Miśta, K. (2007). Survey of fungal species vectored by Ips cembrae to European larch trees in Raciborskie forests (Poland). Czech Mycology, 59(2), 227–239.
Käärik, A. (1975). Succession of microorganisms during wood decay. In W. Liese (Ed.), Biological transformation of wood by microorganisms (pp. 39–51). Berlin: Springer Verlag.
Käärik, A. (1980). Fungi causing sap stain in wood. Institutionen för Virkeslära, Sveriges Lantbruksuniversitet, Uppsala, Sweden, Rapport R114:1–112.
Katoh, K., & Toh, H. (2008). Recent developments in the MAFFT multiple sequence alignment program. Briefings in Bioinformatics, 9(4), 286–298.
Kim, J.-J., Kim, S.-H., Lee, S., & Breuil, C. (2003). Distinguishing Ophiostoma ips and Ophiostoma montium, two bark beetle-associated sapstain fungi. FEMS Microbiology Letters, 222(2), 187–192.
Kim, G.-H., Kim, J.-J., Lim, Y. W., & Breuil, C. (2005). Ophiostomatoid fungi isolated from Pinus radiata logs imported from New Zealand to Korea. Canadian Journal of Botany, 83(3), 272–278.
Kirisits, T. (2004). Fungal associates of European bark beetles with special emphasis on the ophiostomatoid fungi. In F. Lieutier, K. R. Day, A. Battisti, J. C. Grégoire, & H. F. Evans (Eds.), Bark and wood boring insects in living trees in Europe, a synthesis (pp. 185–223). Dordrecht: Kluwer.
Lagerberg, T., Lundberg, G., & Melin, E. (1927). Biological and practical researches into blueing in pine and spruce. Svenska Skogsvårdsföreningens Tidskrift, 2, 145–272.
Linnakoski, R., de Beer, Z. W., Ahtiainen, J., Sidorov, E., Niemelä, P., Pappinen, A., & Wingfield, M. J. (2010). Ophiostoma spp. associated with pine- and spruce-infesting bark beetles in Finland and Russia. Persoonia, 25, 72–93.
Linnakoski, R., de Beer, Z. W., Niemelä, P., & Wingfield, M. J. (2012a). Associations of conifer-infesting bark beetles and fungi in Fennoscandia. Insects, 3(1), 200–227.
Linnakoski, R., de Beer, Z. W., Duong, T. A., Niemelä, P., Pappinen, A., & Wingfield, M. J. (2012b). Grosmannia and Leptographium spp. associated with conifer-infesting bark beetles in Finland and Russia, including Leptographium taigense sp. nov. Antonie Van Leeuwenhoek, 102(2), 375–399.
Loo, J. A. (2009). Ecological impacts of non-indiegenous invasive fungi as forest pathogens. Biological Invasions, 11(1), 81–96.
Marin, M., Preisig, O., Wingfield, B. D., Kirisits, T., Yamaoka, Y., & Wingfield, M. J. (2005). Phenotypic and DNA sequence data comparisons reveal three discrete species in the Ceratocystis polonica species complex. Mycological Research, 109(10), 1137–1148.
Münch, E. (1907). Die Blaufäule des Nadelholzes. I-II. Naturwissenschaftliche Zeitschrift für Land- und Forstwirtschaft, 5, 531–573.
O'Donnell, K., Kistler, H. C., Cigelnik, E., & Ploetz, R. C. (1998). Multiple evolutionary origins of the fungus causing Panama disease of banana: Concordant evidence from nuclear and mitochondrial gene genealogies. Proceedings of the National Academy of Sciences of the United of States of America, 95(5), 2044–2049.
Posada, D. (2008). jModelTest: Phylogenetic Model Averaging. Molecular Biology and Evolution, 25(7), 1253–1256.
Rambaut, A., & Drummond, A. J. (2007). Tracer v1.4, Available from http://beast.bio.ed.ac.uk/Tracer).
Reay, S. D., Thwaites, J. M., & Farrell, R. L. (2005). A survey of Ophiostoma species vectored by Hylastes ater to pine seedlings in New Zealand. Forest Pathology, 35(2), 105–113.
Reid, J., Iranpour, M., Rudski, S. M., Loewen, P. C., & Hausner, G. (2010). A new conifer-inhabiting species of Ceratocystis from Norway. Canadian Journal of Botany, 88(11), 971–983.
Ronquist, F., & Huelsenbeck, J. P. (2003). MrBayes 3: bayesian phylogenetic inference under mixed models. Bioinformatics, 19(12), 1572–1574.
Rykowski, K. (1974). Występowanie sinizny w miejscu w miejscach zawieszania zbiorników żywiczarskich. Prace Instytutu Badawczego Leśnictwa, 458, 14–40 (in Polish with English summary).
Savonmäki, S., Salonen, A., & Ruokola, A.-L. (1992). Microfungi isolated from wood of scots pine in Finland. Karstenia, 32(2), 65–70.
Seifert, K. A. (1993). Sapstain of commercial lumber by species of Ophiostoma and Ceratocystis. In M. J. Wingfield, K. A. Seifert, & J. F. Webber (Eds.), Ceratocystis and Ophiostoma: Taxonomy, ecology, and pathogenicity (pp. 141–151). St. Paul: APS Press.
Siemaszko, W. (1939). Zespoły grzybów towarzyszących kornikom polskim. Planta Polonica, 7, 1–54 (in Polish with English summary).
Solheim, H. (1992a). The early stages of fungal invasion in Norway spruce infested by the bark beetle Ips typographus. Canadian Journal of Botany, 70(1), 1–5.
Solheim, H. (1992b). Fungal succession in sapwood of Norway spruce infested by bark beetle Ips typographus. European Journal of Forest Pathology, 22(3), 136–148.
Taerum, S. J., Duong, T. A., de Beer, Z. W., Gillette, N., Sun, J.-H., et al. (2013). Large shift in symbiont assemblage in the invasive red turpentine beetle. PLoS ONE, 8. doi:10.1371/journal.pone.0078126.
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.
Tarociński, E., & Stolarski, P. (1972). Wpływ okresów pozyskania i składowania sosnowego drewna tartacznego na stopień rozwoju i skład zespołów grzybów wywołujących siniznę. Zeszyty Naukowe SGGW, 18, 160–173 (in Polish with English summary).
Tarociński, E., & Zieliński, M. (1978). Wpływ czynników ekologicznych na występowanie grzybów sinizny drewna sosnowego. Zeszyty Problemowe Postępów Nauk Rolniczych, 209, 72–79 (in Polish with English summary).
Thwaites, J. M., Farrell, R. L., Duncan, S. M., Reay, S. D., Blanchette, R. A., Hadar, E., Hadar, Y., Harrington, T. C., & Mc New, D. (2005). Survey of potential sapstain fungi on Pinus radiata in New Zealand. New Zealand Journal of Botany, 43(3), 653–663.
Uzunović, A., & Webber, J. F. (1998). Comparison of bluestain fungi grown in vitro and in freshly cut pine billets. European Journal of Forest Pathology, 28(5), 323–334.
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.
Wingfield, M. J., & Gibbs, J. N. (1991). Leptographium and Graphium species associated with pine-infesting bark beetles in England. Mycological Research, 95(11), 1257–1260.
Wingfield, M. J., Brockerhoff, E. G., Wingfield, B. D. & Slippers, B. (2015). Planted forest health: The need for a global strategy. Science, 349(6250), 832–836.
Yang, D.-Q. (2001). Staining ability of various sapstaining fungi on jack pine short log sections. Forest Products Journal, 51(2), 1–4.
Yang, D.-Q. (2004). Isolation of staining fungi from jack pine trees. Forest Products Journal, 54(12), 245–249.
Zhou, X. D., de Beer, Z. W., & Wingfield, M. J. (2006). DNA sequence comparisons of Ophiostoma spp., including Ophiostoma aurorae sp. nov., associated with pine bark beetles in South Africa. Studies in Mycology, 55, 269–277.
Zipfel, R. D., de Beer, Z. W., Jacobs, K., Wingfield, B. D., & Wingfield, M. J. (2006). Multi-gene phylogenies define Ceratocystiopsis and Grosmannia distinct from Ophiostoma. Studies in Mycology, 55, 75–97.
Acknowledgements
Funding was provided by a bilateral agreement between the University of Agriculture in Krakow and Innovation Support Centre sp. z o. o. (Andrychów, Poland). The study was also supported financially by the Ministry of Science and Higher Education of the Republic of Poland. I thank Prof. Wilhelm de Beer from the University of Pretoria for reviewing the manuscript draft and helpful comments.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Funding
This study was funded by a bilateral agreement between the University of Agriculture in Krakow and Innovation Support Centre sp. z o. o. (Andrychów, Poland), and by the Ministry of Science and Higher Education of the Republic of Poland.
Conflict of interest
The authors declare that have no conflict of interest.
Electronic supplementary material
ESM 1
(DOCX 119 kb)
Rights and permissions
About this article
Cite this article
Jankowiak, R., Bilański, P., Chyrzyński, Ł. et al. Identification of sapstain fungi from Scots pine pallets and assessment of their staining ability. Eur J Plant Pathol 150, 307–322 (2018). https://doi.org/10.1007/s10658-017-1279-5
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10658-017-1279-5