Worldwide Genetic Structure Elucidates the Eurasian Origin and Invasion Pathways of Dothistroma septosporum, Causal Agent of Dothistroma Needle Blight
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
CZ.02.1.01/0.0/0.0/15_003/0000453
European Regional Development Fund, Project Phytophthora Research Centre Reg. No. CZ.02.1.01/0.0/0.0/15_003/0000453
PSG136
Estonian Research Council grant PSG136
Dothistroma1
Forestry Commission, UK
PubMed
33546260
PubMed Central
PMC7913368
DOI
10.3390/jof7020111
PII: jof7020111
Knihovny.cz E-zdroje
- Klíčová slova
- ABC, DNB, Mycosphaerella pini, biogeography, global spread, introduction pathways, invasive pathogen,
- Publikační typ
- časopisecké články MeSH
Dothistroma septosporum, the primary causal agent of Dothistroma needle blight, is one of the most significant foliar pathogens of pine worldwide. Its wide host and environmental ranges have led to its global success as a pathogen and severe economic damage to pine forests in many regions. This comprehensive global population study elucidated the historical migration pathways of the pathogen to reveal the Eurasian origin of the fungus. When over 3800 isolates were examined, three major population clusters were revealed: North America, Western Europe, and Eastern Europe, with distinct subclusters in the highly diverse Eastern European cluster. Modeling of historical scenarios using approximate Bayesian computation revealed the North American cluster was derived from an ancestral population in Eurasia. The Northeastern European subcluster was shown to be ancestral to all other European clusters and subclusters. The Turkish subcluster diverged first, followed by the Central European subcluster, then the Western European cluster, which has subsequently spread to much of the Southern Hemisphere. All clusters and subclusters contained both mating-types of the fungus, indicating the potential for sexual reproduction, although asexual reproduction remained the primary mode of reproduction. The study strongly suggests the native range of D. septosporum to be in Eastern Europe (i.e., the Baltic and Western Russia) and Western Asia.
Department Forest Ecosystems Protection University of Agriculture in Kraków 31 425 Kraków Poland
Department of Botany and Zoology Faculty of Science Masaryk University 61137 Brno Czech Republic
Department of Forest Protection Slovenian Forestry Institute Večna pot 2 SI 1000 Ljubljana Slovenia
Department of Plant Pathology and Mycology Institute of Forest Ecology SAS 949 01 Nitra Slovakia
Faculty of Forestry Çankırı Karatekin University 18200 Çankırı Turkey
Faculty of Forestry University of Zagreb 10002 Zagreb Croatia
Institute for Sustainable Plant Protection 50019 Sesto Fiorentino Italy
Institute of Forestry and Rural Engineering Estonian University of Life Sciences 51006 Tartu Estonia
Natural Resources Institute FI 77600 Suonenjoki Finland
Natural Resources Institute Finland Bioeconomy and Environment P O Box 2 FI 00791 Helsinki Finland
Nature Research Centre Institute of Botany Žaliųjų Ežerų Str 49 LT 08406 Vilnius Lithuania
Norwegian institute of Bioeconomy P O Box 115 N 1431 Ås Norway
Swiss Federal Research Institute WSL Swiss Forest Protection 8903 Birmensdorf Switzerland
Vokė Branch of Lithuanian Research Centre for Agriculture and Forestry LT 02232 Vilnius Lithuania
Walloon Agricultural Research Centre Department of Life Sciences B 5030 Gembloux Belgium
Zobrazit více v PubMed
Drenkhan R., Tomešová-Haataja V., Fraser S., Bradshaw R.E., Vahalík P., Mullett M.S., Martín-García J., Bulman L.S., Wingfield M.J., Kirisits T., et al. Global Geographic Distribution and Host Range of Dothistroma Species: A Comprehensive Review. For. Pathol. 2016;46:408–442. doi: 10.1111/efp.12290. DOI
Brown A.V., Webber J. Red Band Needle Blight of Conifers in Britain. Forestry Commission; Edinburgh, UK: 2008. p. 8.
Bulman L. Foliar Diseases of Pine—The New Zealand Experience; Proceedings of the 54th Annual Western International Forest Disease Work Conference; Smithers, BC, Canada. 2–6 October 2006; pp. 57–60.
Price C. Appraising the Economic Impact of Tree Diseases in Britain: Several Shots in the Dark, and Possibly Also in the Wrong Ball-Park? Scand. For. Econ. 2010;43:45–61.
Brown A.V. Dothistroma Needle Blight. Background for Biosecurtiy Workshop 16 February 2011, Forest Research. [(accessed on 28 January 2021)];2011 Available online: http://saveourwoods.co.uk/wp-content/uploads/2011/03/Tree-Health-Threats-PtLM.pdf.
Barnes I., van der Nest A., Mullett M.S., Crous P.W., Drenkhan R., Musolin D.L., Wingfield M.J. Neotypification of Dothistroma septosporum and Epitypification of D. pini, Causal Agents of Dothistroma Needle Blight of Pine. For. Pathol. 2016;46:388–407. doi: 10.1111/efp.12304. DOI
Mullett M.S., Adamson K., Bragança H., Bulgakov T.S., Georgieva M., Henriques J., Jürisoo L., Laas M., Drenkhan R. New Country and Regional Records of the Pine Needle Blight Pathogens Lecanosticta acicola, Dothistroma septosporum and Dothistroma pini. For. Pathol. 2018;48:e12440. doi: 10.1111/efp.12440. DOI
Gibson I.A.S. Dothistroma Blight of Pinus radiata. Annu. Rev. Phytopathol. 1972;10:51–72. doi: 10.1146/annurev.py.10.090172.000411. DOI
Rodas C.A., Wingfield M.J., Granados G.M., Barnes I. Dothistroma Needle Blight: An Emerging Epidemic Caused by Dothistroma septosporum in Colombia. Plant Pathol. 2016;65:53–63. doi: 10.1111/ppa.12389. DOI
Welsh C., Lewis K.J., Woods A.J. Regional Outbreak Dynamics of Dothistroma Needle Blight Linked to Weather Patterns in British Columbia, Canada. Can. J. For. Res. 2014;44:212–219. doi: 10.1139/cjfr-2013-0387. DOI
Woods A., Coates K.D., Hamann A. Is an Unprecedented Dothistroma Needle Blight Epidemic Related to Climate Change? Bioscience. 2005;55:761–769. doi: 10.1641/0006-3568(2005)055[0761:IAUDNB]2.0.CO;2. DOI
Fabre B., Ioos R., Piou D., Marçais B. Is the Emergence of Dothistroma Needle Blight of Pine in France Caused by the Cryptic Species Dothistroma pini? Phytopathology. 2012;102:47–54. doi: 10.1094/PHYTO-02-11-0036. PubMed DOI
Doroguine G. Une Maladie Cryptogamique Du Pin. Bull. Trimest. Société Mycol. Fr. 1911;27:105–106.
Evans H.C. The Genus Mycosphaerella and Its Anamorphs Cercoseptoria, Dothistroma and Lecanosticta on Pines. [(accessed on 15 January 2021)];1984 :102. Available online: https://www.gov.uk/research-for-development-outputs/the-genus-mycosphaerella-and-its-anamorphs-cercoseptoria-dothistroma-and-lecanosticta-on-pines.
Saccardo P.A. Mycetes Boreali-Americani. Nuovo G. Bot. Ital. 1920;27:75–88.
Thyr B.D., Shaw C.G. Identity of the Fungus Causing Red Band Disease on Pines. Mycologia. 1964;56:103–109. doi: 10.1080/00275514.1964.12018087. DOI
Welsh C., Lewis K., Woods A. The Outbreak History of Dothistroma Needle Blight: An Emerging Forest Disease in Northwestern British Columbia, Canada. Can. J. For. Res. 2009;39:2505–2519. doi: 10.1139/X09-159. DOI
Ivory M.H. Records of Foliage Pathogens of Pinus Species in Tropical Countries. Plant Pathol. 1994;43:511–518. doi: 10.1111/j.1365-3059.1994.tb01585.x. DOI
Gibson I.A.S. Impact and Control of Dothistroma Blight of Pines. Eur. J. For. Pathol. 1974;4:89–100. doi: 10.1111/j.1439-0329.1974.tb00423.x. DOI
Adamson K., Mullett M.S., Solheim H., Barnes I., Müller M.M., Hantula J., Vuorinen M., Kačergius A., Markovskaja S., Musolin D.L., et al. Looking for Relationships between the Populations of Dothistroma septosporum in Northern Europe and Asia. Fungal Genet. Biol. 2018;110:15–25. doi: 10.1016/j.fgb.2017.12.001. PubMed DOI
Barnes I., Wingfield M.J., Carbone I., Kirisits T., Wingfield B. Population Structure and Diversity of an Invasive Pine Needle Pathogen Reflects Anthropogenic Activity. Ecol. Evol. 2014;4:3642–3661. doi: 10.1002/ece3.1200. PubMed DOI PMC
Dale A.L., Lewis K.J., Murray B.W. Sexual Reproduction and Gene Flow in the Pine Pathogen Dothistroma septosporum in British Columbia. Phytopathology. 2011;101:68–76. doi: 10.1094/PHYTO-04-10-0121. PubMed DOI
Mullett M.S., Brown A.V., Fraser S., Baden R., Tubby K.V. Insights into the Pathways of Spread and Potential Origins of Dothistroma septosporum in Britain. Fungal Ecol. 2017;26:85–98. doi: 10.1016/j.funeco.2017.01.002. DOI
Boroń P., Lenart-Boroń A., Mullett M., Kraj W., Grad B., Kowalski T. Temporal Changes in the Population Structure of Dothistroma septosporum at the Site of the First Recorded Outbreak in Poland. Plant Pathol. 2019;68:383–391. doi: 10.1111/ppa.12947. DOI
Capron A., Feau N., Heinzelmann R., Barnes I., Benowicz A., Bradshaw R.E., Dale A., Lewis K.J., Owen T.J., Reich R., et al. Signatures of Post-Glacial Genetic Isolation and Human-Driven Migration in the Dothistroma Needle Blight Pathogen in Western Canada. Phytopathology. 2020 doi: 10.1094/PHYTO-08-20-0350-FI. PubMed DOI
Drenkhan R., Hantula J., Vuorinen M., Jankovský L., Müller M.M. Genetic Diversity of Dothistroma septosporum in Estonia, Finland and Czech Republic. Eur. J. Plant Pathol. 2013;136:71–85. doi: 10.1007/s10658-012-0139-6. DOI
Mullett M.S., Brown A.V., Barnes I. Population Structure and Reproductive Mode of Dothistroma septosporum in the Brittany Peninsula of France. Eur. J. Plant Pathol. 2015;143:261–275. doi: 10.1007/s10658-015-0678-8. DOI
Oskay F., Tunalı Z., Lehtijärvi A.T., Doğmuş-Lehtijärvi H.T., Woodward S., Mullett M. Distribution and Genetic Diversity of Dothistroma septosporum in Pinus Brutia Forests of South-western Turkey. Plant Pathol. 2020;69:1551–1564. doi: 10.1111/ppa.13242. DOI
Tomšovský M., Tomešová V., Palovčíková D., Kostovčík M., Rohrer M., Hanáček P., Jankovský L. The Gene Flow and Mode of Reproduction of Dothistroma septosporum in the Czech Republic. Plant Pathol. 2013;62:59–68. doi: 10.1111/j.1365-3059.2012.02625.x. DOI
Janoušek J., Wingfield M.J., Monsivais J.G.M., Jankovský L., Stauffer C., Konečný A., Barnes I. Genetic Analyses Suggest Separate Introductions of the Pine Pathogen Lecanosticta acicola Into Europe. Phytopathology. 2015;106:1413–1425. doi: 10.1094/PHYTO-10-15-0271-R. PubMed DOI
Taerum S.J., Hoareau T.B., Duong T.A., de Beer Z.W., Jankowiak R., Wingfield M.J. Putative Origins of the Fungus Leptographium procerum. Fungal Biol. 2017;121:82–94. doi: 10.1016/j.funbio.2016.09.007. PubMed DOI
Guillemaud T., Beaumont M.A., Ciosi M., Cornuet J.-M., Estoup A. Inferring Introduction Routes of Invasive Species Using Approximate Bayesian Computation on Microsatellite Data. Heredity. 2010;104:88–99. doi: 10.1038/hdy.2009.92. PubMed DOI
Boroń P., Lenart-Boroń A., Mullett M. The Distribution of Dothistroma septosporum and Its Mating Types in Poland. For. Pathol. 2016;46:489–496. doi: 10.1111/efp.12262. DOI
Mullett M., Barnes I. Dothistroma Isolation and Molecular Identification Methods. [(accessed on 28 January 2021)];2012 Available online: https://www.forestresearch.gov.uk/documents/305/DIAROD_052012_Isolation_and_indentification_97fNCCI.pdf.
Bradshaw R.E., Ganley R.J., Jones W.T., Dyer P.S. High Levels of Dothistromin Toxin Produced by the Forest Pathogen Dothistroma pini. Mycol. Res. 2000;104:325–332. doi: 10.1017/S0953756299001367. DOI
Groenewald M., Barnes I., Bradshaw R.E., Brown A.V., Dale A., Groenewald J.Z., Lewis K.J., Wingfield B.D., Wingfield M.J., Crous P.W. Characterization and Distribution of Mating Type Genes in the Dothistroma Needle Blight Pathogens. Phytopathology. 2007;97:825–834. doi: 10.1094/PHYTO-97-7-0825. PubMed DOI
Barnes I., Cortinas M.N., Wingfield M.J., Wingfield B.D. Microsatellite Markers for the Red Band Needle Blight Pathogen, Dothistroma septosporum. Mol. Ecol. Resour. 2008;8:1026–1029. doi: 10.1111/j.1755-0998.2008.02142.x. PubMed DOI
Kamvar Z.N., Tabima J.F., Grünwald N.J. Poppr: An R Package for Genetic Analysis of Populations with Clonal, Partially Clonal, and/or Sexual Reproduction. PeerJ. 2014;2:e281. doi: 10.7717/peerj.281. PubMed DOI PMC
Oksanen J., Blanchet F.G., Friendly M., Kindt R., Legendre P., McGlinn D., Minchin P.R., O’Hara R.B., Simpson G.L., Solymos P., et al. Vegan: Community Ecology Package. [(accessed on 28 January 2021)];2013 Available online: https://cran.r-project.org/web/packages/vegan/index.html.
Shannon C.E., Weaver W. The Mathematical Theory of Communication. University of Illinois Press; Urbana, IL, USA: 1949.
Grünwald N.J., Goodwin S.B., Milgroom M.G., Fry W.E. Analysis of Genotypic Diversity Data for Populations of Microorganisms. Phytopathology. 2003;93:738–746. doi: 10.1094/PHYTO.2003.93.6.738. PubMed DOI
Stoddart J.A., Taylor J.F. Genotypic Diversity: Estimation and Prediction in Samples. Genetics. 1988;118:705–711. doi: 10.1093/genetics/118.4.705. PubMed DOI PMC
Simpson E.H. Measurement of Diversity. Nature. 1949;163:688. doi: 10.1038/163688a0. DOI
Zhan J., Pettway R.E., McDonald B.A. The Global Genetic Structure of the Wheat Pathogen Mycosphaerella graminicola Is Characterized by High Nuclear Diversity, Low Mitochondrial Diversity, Regular Recombination, and Gene Flow. Fungal Genet. Biol. 2003;38:286–297. doi: 10.1016/S1087-1845(02)00538-8. PubMed DOI
Nei M. Estimation of Average Heterozygosity and Genetic Distance from a Small Number of Individuals. Genetics. 1978;89:583–590. PubMed PMC
Peakall R., Smouse P.E. GenAlEx 6.5: Genetic Analysis in Excel. Population Genetic Software for Teaching and Research—An Update. Bioinformatics. 2012;28:2537–2539. doi: 10.1093/bioinformatics/bts460. PubMed DOI PMC
Szpiech Z.A., Jakobsson M., Rosenberg N.A. ADZE: A Rarefaction Approach for Counting Alleles Private to Combinations of Populations. Bioinformatics. 2008;24:2498–2504. doi: 10.1093/bioinformatics/btn478. PubMed DOI PMC
Excoffier L., Lischer H.E.L. ARLEQUIN Suite Ver 3.5: A New Series of Programs to Perform Population Genetics Analyses under Linux and Windows. Mol. Ecol. Resour. 2010;10:564–567. doi: 10.1111/j.1755-0998.2010.02847.x. PubMed DOI
McDonald J.H. Handbook of Biological Statistics. 3rd ed. Sparky House Publishing; Baltimore, MD, USA: 2014. [(accessed on 28 January 2021)]. Available online: http://www.biostathandbook.com/exactgof.html.
Brown A.H.D., Feldman M.W., Nevo E. Multilocus Structure of Natural Populations of Hordeum spontaneum. Genetics. 1980;96:523–536. PubMed PMC
Agapow P.-M., Burt A. Indices of Multilocus Linkage Disequilibrium. Mol. Ecol. Notes. 2001;1:101–102. doi: 10.1046/j.1471-8278.2000.00014.x. DOI
Milgroom M.G. Recombination and the Multilocus Structure of Fungal Populations. Annu. Rev. Phytopathol. 1996;34:457–477. doi: 10.1146/annurev.phyto.34.1.457. PubMed DOI
Falush D., Stephens M., Pritchard J.K. Inference of Population Structure Using Multilocus Genotype Data: Linked Loci and Correlated Allele Frequencies. Genetics. 2003;164:1567–1587. PubMed PMC
Pritchard J.K., Stephens M., Donnelly P. Inference of Population Structure Using Multilocus Genotype Data. Genetics. 2000;155:945–959. PubMed PMC
Kopelman N.M., Mayzel J., Jakobsson M., Rosenberg N.A., Mayrose I. Clumpak: A Program for Identifying Clustering Modes and Packaging Population Structure Inferences across K. Mol. Ecol. Resour. 2015;15:1179–1191. doi: 10.1111/1755-0998.12387. PubMed DOI PMC
Evanno G., Regnaut S., Goudet J. Detecting the Number of Clusters of Individuals Using the Software Structure: A Simulation Study. Mol. Ecol. 2005;14:2611–2620. doi: 10.1111/j.1365-294X.2005.02553.x. PubMed DOI
Rosenberg N.A. Distruct: A Program for the Graphical Display of Population Structure. Mol. Ecol. Notes. 2004;4:137–138. doi: 10.1046/j.1471-8286.2003.00566.x. DOI
Jombart T., Devillard S., Balloux F. Discriminant Analysis of Principal Components: A New Method for the Analysis of Genetically Structured Populations. BMC Genet. 2010;11:94. doi: 10.1186/1471-2156-11-94. PubMed DOI PMC
Jombart T. Adegenet: A R Package for the Multivariate Analysis of Genetic Markers. Bioinformatics. 2008;24:1403–1405. doi: 10.1093/bioinformatics/btn129. PubMed DOI
Jombart T., Collins C. A Tutorial for Discriminant Analysis of Principal Components (DAPC) Using Adegenet 2.0.0. [(accessed on 28 January 2021)];2015 Available online: https://adegenet.r-forge.r-project.org/files/tutorial-dapc.pdf.
Cornuet J.-M., Pudlo P., Veyssier J., Dehne-Garcia A., Gautier M., Leblois R., Marin J.-M., Estoup A. DIYABC v2.0: A Software to Make Approximate Bayesian Computation Inferences about Population History Using Single Nucleotide Polymorphism, DNA Sequence and Microsatellite Data. Bioinformatics. 2014;30:1187–1189. doi: 10.1093/bioinformatics/btt763. PubMed DOI
Konečný A., Estoup A., Duplantier J.-M., Bryja J., Bâ K., Galan M., Tatard C., Cosson J.-F. Invasion Genetics of the Introduced Black Rat (Rattus Rattus) in Senegal, West Africa. Mol. Ecol. 2013;22:286–300. doi: 10.1111/mec.12112. PubMed DOI
Cornuet J.-M., Ravigné V., Estoup A. Inference on Population History and Model Checking Using DNA Sequence and Microsatellite Data with the Software DIYABC (v1.0) BMC Bioinform. 2010;11:401. doi: 10.1186/1471-2105-11-401. PubMed DOI PMC
Cornuet J.-M., Santos F., Beaumont M.A., Robert C.P., Marin J.-M., Balding D.J., Guillemaud T., Estoup A. Inferring Population History with DIY ABC: A User-Friendly Approach to Approximate Bayesian Computation. Bioinformatics. 2008;24:2713–2719. doi: 10.1093/bioinformatics/btn514. PubMed DOI PMC
Price R.A., Liston A., Strauss S.H. Phylogeny and systematics of Pinus. In: Richardson D.M., editor. Ecology and Biogeography of Pinus. Cambridge University Press; Cambridge, UK: 2000. pp. 49–68.
Richardson D.M., Rundel P.W. Ecology and bio- geography of Pinus: An introduction. In: Richardson D.M., editor. Ecology and Biogeography of Pinus. Cambridge University Press; Cambridge, UK: 2000. pp. 3–46.
Fielding J.M. The Introduction of Monterey Pine into Australia. Aust. For. 1957;21:15–16. doi: 10.1080/00049158.1957.10675333. DOI
Le Maitre D.C. Pines in cultivation: A global view. In: Richardson D.M., editor. Ecology and Biogeography of Pinus. Cambridge University Press; Cambridge, UK: 2000. pp. 407–431.
Wu H.X., Eldridge K.G., Matheson A.C., Powell M.B., McRae T.A., Butcher T.B., Johnson I.G. Achievements in Forest Tree Improvement in Australia and New Zealand 8. Successful Introduction and Breeding of Radiata Pine in Australia. Aust. For. 2007;70:215–225. doi: 10.1080/00049158.2007.10675023. DOI
de Villebonne D., Maugard F. Rapid Development of Dothistroma Needle Blight (Scirrhia pini) on Corsican Pine (Pinus nigra subsp. laricio) in France. Sante For. Annu. Rep. 1998;1:30–32.
Case T.J., Taper M.L. Interspecific Competition, Environmental Gradients, Gene Flow, and the Coevolution of Species’ Borders. Am. Nat. 2000;155:583–605. doi: 10.1086/303351. PubMed DOI
Hallatschek O., Hersen P., Ramanathan S., Nelson D.R. Genetic Drift at Expanding Frontiers Promotes Gene Segregation. Proc. Natl. Acad. Sci. USA. 2007;104:19926–19930. doi: 10.1073/pnas.0710150104. PubMed DOI PMC
Sexton J.P., McIntyre P.J., Angert A.L., Rice K.J. Evolution and Ecology of Species Range Limits. Annu. Rev. Ecol. Evol. Syst. 2009;40:415–436. doi: 10.1146/annurev.ecolsys.110308.120317. DOI
Rubal M., Veiga P., Maldonado C., Torres C., Moreira J. Population Attributes and Traits of Siphonaria pectinata (Mollusca: Siphonariidae) in Range-Edge and Non Range-Edge Populations at Its Eastern Atlantic Northern Distribution Boundary. J. Exp. Mar. Biol. Ecol. 2015;471:41–47. doi: 10.1016/j.jembe.2015.05.015. DOI
Hargreaves A.L., Eckert C.G. Local Adaptation Primes Cold-Edge Populations for Range Expansion but Not Warming-Induced Range Shifts. Ecol. Lett. 2019;22:78–88. doi: 10.1111/ele.13169. PubMed DOI
Hereford J. A Quantitative Survey of Local Adaptation and Fitness Trade-Offs. Am. Nat. 2009;173:579–588. doi: 10.1086/597611. PubMed DOI
Wallen R.M., Perlin M.H. An Overview of the Function and Maintenance of Sexual Reproduction in Dikaryotic Fungi. Front. Microbiol. 2018;9:503. doi: 10.3389/fmicb.2018.00503. PubMed DOI PMC
Hurst L.D., Peck J.R. Recent Advances in Understanding of the Evolution and Maintenance of Sex. Trends Ecol. Evol. 1996;11:46–52. doi: 10.1016/0169-5347(96)81041-X. PubMed DOI
Taylor J., Jacobson D., Fisher M. The Evolution of Asexual Fungi: Reproduction, Speciation and Classification. Annu. Rev. Phytopathol. 1999;37:197–246. doi: 10.1146/annurev.phyto.37.1.197. PubMed DOI
Ennos R.A., Sjökvist E.I., Piotrowska M.J., Riddell C., Hoebe P.N. Using Genome Resequencing to Investigate Racial Structure, Genetic Diversity, Sexual Reproduction and Hybridisation in the Pine Pathogen Dothistroma septosporum. Fungal Ecol. 2020;45:100921. doi: 10.1016/j.funeco.2020.100921. DOI
Piotrowska M.J., Riddell C., Hoebe P.N., Ennos R.A. Planting Exotic Relatives Has Increased the Threat Posed by Dothistroma septosporum to the Caledonian Pine Populations of Scotland. Evol. Appl. 2018;11:350–363. doi: 10.1111/eva.12562. PubMed DOI PMC
Markovskaja S., Raitelaitytė K., Kačergius A., Kolmakov P., Vasilevich V. Occurrence of Dothistroma Needle Blight in Lithuania and Belarus: The Risk Posed to Native Scots Pine Forests. For. Pathol. 2020:e12626. doi: 10.1111/efp.12626. DOI
Ennos R.A. The Introduction of Lodgepole Pine as a Major Forest Crop in Sweden: Implications for Host–Pathogen Evolution. For. Ecol. Manag. 2001;141:85–96. doi: 10.1016/S0378-1127(00)00491-6. DOI
Harrington T.C., Wingfield M.J. Ecology and Biogeography of Pinus. Cambridge University Press; Cambridge, UK: 1998. Diseases and the ecology of indigenous and exotic pines; pp. 381–401.