Biological Invasions

, Volume 18, Issue 4, pp 1147–1161 | Cite as

Anthropogenic signature in the incidence and distribution of an emerging pathogen of poplars

  • Padmini Herath
  • Stephanie Beauseigle
  • Braham Dhillon
  • Dario I. Ojeda
  • Guillaume Bilodeau
  • Nathalie Isabel
  • Marie-Claude Gros-Louis
  • Harry Kope
  • Stefan Zeglen
  • Richard C. HamelinEmail author
  • Nicolas FeauEmail author
Original Paper


The introduction and establishment of non-native plant pathogens into new areas can result in severe outbreaks. Septoria leaf spot and canker caused by Sphaerulina musiva is one of the most damaging poplar diseases in northeastern and north-central North America. Stem and branch cankers can be devastating on susceptible trees, leading to tree death and reduced biomass in commercial plantations. In the Pacific Northwest region of North America, the first report of the disease was made in 2006 in the Fraser Valley of British Columbia (BC), Canada. To investigate the incidence and distribution of S. musiva from its point of introduction into BC, five plantations of Populus trichocarpa (black cottonwood), 500 P. trichocarpa trees from natural populations, and 23 plantations of hybrid poplars were surveyed by using real-time PCR assays targeting S. musiva and its native sister species, S. populicola. Our survey suggests a strong anthropogenic signature to the emergence of the non-native S. musiva. Detection frequency of S. musiva was high in hybrid poplar plantations (116 trees infected, 54.2 % of the sampled trees), while detection of the native S. populicola was limited to 13.1 % (22 trees infected). By contrast, in natural stands of P. trichocarpa, less than 2 % of the trees were positive for S. musiva (7 trees) while ~75 % were positive for S. populicola (433 trees). All the S. musiva detections in natural stands of the native P. trichocarpa were from trees located in the vicinity (<2.5 km) of hybrid poplar plantations. Identification of the genotypes found in the hybrid poplar plantations revealed that they are in majority F1 progeny from P. trichocarpa × P. deltoides (T × D) (82 %) and P. nigra × P. maximowiczii (N × M) (7.8 %) crosses, which are generally susceptible (intermediate level of susceptibility between the two parental species) to the canker disease. Our results suggest that the emergence of S. musiva in BC is related to the planting of susceptible hybrid poplars. Even if the disease has not yet established itself in natural poplar populations outside of the Fraser Valley, infected plantations could act as a reservoir that could promote its spread into nearby native P. trichocarpa populations.


Tree diseases Detection assay DNA barcoding Real-time PCR Hybrid poplars Mycosphaerella Septoria canker 



We thank Angela L. Dale from Forest Products Innovation for constructive comments on the manuscript. This work was supported by the Genomic Research and Development Initiative of Natural Resources Canada, Genome Canada, and Genome BC Project 2112 and the BC Ministry of Forests, Lands and Natural Resource Operations Land Base Investment fund.

Supplementary material

10530_2015_1051_MOESM1_ESM.pptx (745 kb)
Supplementary material 1 (PPTX 745 kb)
10530_2015_1051_MOESM2_ESM.xlsx (33 kb)
Supplementary material 2 (XLSX 32 kb)


  1. Altschul SF, Gish W, Miller W et al (1990) Basic local alignment search tool. J Mol Biol 215:403–410CrossRefPubMedGoogle Scholar
  2. Amarasekare P (2003) Competitive coexistence in spatially structured environments: a synthesis. Ecol Lett 6:1109–1122CrossRefGoogle Scholar
  3. Bier J (1939) Septoria canker of introduced and native hybrid poplars. Can J Res 17:195–204CrossRefGoogle Scholar
  4. Bilodeau GJ, Lévesque CA, de Cock AWAM et al (2007) Molecular detection of Phytophthora ramorum by real-time PCR using TaqMan, SYBR®Green and molecular beacons. Phytopathology 97:632–642CrossRefPubMedGoogle Scholar
  5. Boutigny A-L, Guinet C, Vialle A et al (2013) Optimization of a real-time PCR assay for the detection of the quarantine pathogen Melampsora medusae f. sp. deltoidae. Fungal Biol 117:389–398CrossRefPubMedGoogle Scholar
  6. Braatne JH, Rood SB, Heilman PE (1996) Life history, ecology, and conservation of riparian cottonwoods in North America. In: Stettler RF, Bradshaw HD Jr, Heilman PE, Hinckley TM (eds) Biology of Populus and its implications for management and conservation. NRC Research Press, Ottawa, pp 57–85Google Scholar
  7. Brasier CM, Buck KW (2001) Rapid evolutionary changes in a globally invading fungal pathogen (Dutch elm disease). Biol Invasions 3:223–233CrossRefGoogle Scholar
  8. Busby PE, Aime MC, Newcombe G (2012) Foliar pathogens of Populus angustifolia are consistent with a hypothesis of Beringian migration into North America. Fungal Biol 116:792–801. doi: 10.1016/j.funbio.2012.04.012 CrossRefPubMedGoogle Scholar
  9. Callan BE, Leal I, Foord B et al (2007) Septoria musiva isolated from cankered stems in hybrid poplar stool beds, Fraser Valley, British Columbia. North Am Fungi 2:1–9CrossRefGoogle Scholar
  10. Daehler CC (2001) Darwin’s naturalization hypothesis revisited. Am Nat 158:324–330CrossRefPubMedGoogle Scholar
  11. Dhillon B, Feau N, Aerts AL et al (2015) Horizontal gene transfer and gene dosage drives adaptation to wood colonization in a tree pathogen. Proc Natl Acad Sci USA 112:3451–3456CrossRefPubMedPubMedCentralGoogle Scholar
  12. Feau N, Bernier L (2004) First report of shining willow as a host plant for Septoria musiva. Plant Dis 88:770CrossRefGoogle Scholar
  13. Feau N, Hamelin RC, Vandecasteele C et al (2005a) Genetic structure of Mycosphaerella populorum (anamorph Septoria musiva) populations in north-central and northeastern North America. Phytopathology 95:608–616CrossRefPubMedGoogle Scholar
  14. Feau N, Weiland JE, Stanosz GR, Bernier L (2005b) Specific and sensitive PCR-based detection of Septoria musiva, S. populicola and S. populi, the causes of leaf spot and stem canker on poplars. Mycol Res 109:1015–1028CrossRefPubMedGoogle Scholar
  15. Feau N, Hamelin RC, Bernier L (2006) Attributes and congruence of three molecular data sets: inferring phylogenies among Septoria-related species from woody perennial plants. Mol Phylogenet Evol 40:808–829CrossRefPubMedGoogle Scholar
  16. Feau N, Mottet M-J, Périnet P et al (2010) Recent advances related to poplar leaf spot and canker caused by Septoria musiva. Can J Plant Pathol 32:122–134CrossRefGoogle Scholar
  17. Feau N, Lauron-Moreau A, Piou D et al (2012) Niche partitioning of the genetic lineages of the oak powdery mildew complex. Fungal Ecol 5:154–162CrossRefGoogle Scholar
  18. Fitt BDL, Huang Y, van den Bosch F, West JS (2006) Coexistence of related pathogen species on arable crops in space and time. Annu Rev Phytopathol 44:163–182CrossRefPubMedGoogle Scholar
  19. Garbelotto M, Pautasso M (2012) Impacts of exotic forest pathogens on Mediterranean ecosystems: four case studies. Eur J Plant Pathol 133:101–116CrossRefGoogle Scholar
  20. Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrihiza and rusts. Mol Ecol 2:113–118CrossRefPubMedGoogle Scholar
  21. Geraldes A, Farzaneh N, Grassa CJ et al (2014) Landscape genomics of Populus trichocarpa: the role of hybridization, limited gene flow, and natural selection in shaping patterns of population structure. Evolution (NY) 68:3260–3280CrossRefGoogle Scholar
  22. Gould S, Vrba ES (1982) Exaptation-A missing term in the science of form. Paleobiology 8:4–15CrossRefGoogle Scholar
  23. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  24. Hansen EA, Ostry ME, Johnson WD, et al (1994) Field performance of Populus in short-rotation intensive culture plantations in the north-central U.S. USDA For Ser Res pap NC-320Google Scholar
  25. Herath P, Hoover GA, Angelini E, Moorman GW (2010) Detection of elm yellows phytoplasma in elms and insects using real-time PCR. Plant Dis 94:1355–1360CrossRefGoogle Scholar
  26. Ioos R, Kowalski T, Claude H, Holdenrieder O (2009) Rapid in planta detection of Chalara fraxinea by a real-time PCR assay using a dual-labelled probe. Eur J Plant Pathol 123:329–335CrossRefGoogle Scholar
  27. Isabel N, Lamothe M, Thompson SL (2013) A second-generation diagnostic single nucleotide polymorphism (SNP)-based assay, optimized to distinguish among eight poplar (Populus L.) species and their early hybrids. Tree Genet Genomes 9:621–626CrossRefGoogle Scholar
  28. Kennedy TA, Naeem S, Howe KM et al (2002) Biodiversity as a barrier to ecological invasion. Nature 417:636–638CrossRefPubMedGoogle Scholar
  29. LeBoldus JM, Isabel N, Floate KD et al (2013) Testing the “hybrid susceptibility” and “phenological sink” hypotheses using the P. balsamiferaP. deltoides hybrid zone and Septoria leaf spot [Septoria musiva]. PLoS ONE 8:e84437CrossRefPubMedPubMedCentralGoogle Scholar
  30. Luchi N, Capretti P, Pinzani P et al (2005) Real-time PCR detection of Biscogniauxia mediterranea in symptomless oak tissue. Lett Appl Microbiol 41:61–68CrossRefPubMedGoogle Scholar
  31. Luley JC, McNabb HSJ (1989) Ascospore production, release, germination, and infection of Populus by Myscosphaerella populorum. Phytopathology 79:1013–1018CrossRefGoogle Scholar
  32. Newcombe G (1996) The specificity of fungal pathogens of Populus. In: Stettler RF, Bradshaw HD Jr, Heilman PE, Hinckley TM (eds) Biology of Populus and its implications for management and conservation. NRC Research Press Canada, Ottawa, pp 223–246Google Scholar
  33. Newcombe G (1998) A review of exapted resistance to diseases of Populus. Eur J For Pathol 28:209–216CrossRefGoogle Scholar
  34. Newcombe G, Bradshaw HDJ (1996) Quantative trait loci conferring resistance in hybrid poplar to Septoria populicola, the cause of leaf spot. Can J For Res 26:1943–1950CrossRefGoogle Scholar
  35. Newcombe G, Ostry ME (2001) Recessive resistance to Septoria stem canker of hybrid poplar. Phytopathology 91:1081–1084CrossRefPubMedGoogle Scholar
  36. Newcombe G, Chastagner GA, Callan B, Ostry ME (1995) An epidemic of Septoria leaf spot on Populus trichocarpa in the Pacific Northwest in 1993. Plant Dis 79:212CrossRefGoogle Scholar
  37. Newcombe G, Ostry ME, Hubbes M et al (2001) Poplar diseases. In: Dickmann DI, Isebrands JG, Eckenwalder JE, Richardson J (eds) Poplar culture in North America. National Research Council of Canada, Ottawa, pp 249–276Google Scholar
  38. Ostry ME (1987) Biology of Septoria musiva and Marssonina brunnea in hybrid Populus plantations and control of Septoria canker in nurseries. For Pathol 17:158–165Google Scholar
  39. Ostry ME, McNabb HS (1983) Diseases of intensively cultured hybrid poplars: a summary of recent research in the north central region. In: Hansen EA (ed) Intensive plantation culture: 12 years research. USDA For Serv Gen Tech Rep NC-91, pp 102–109Google Scholar
  40. Ostry ME, McNabb HS (1985) Susceptibility of Populus species and hybrids to disease in the North Central United States. Plant Dis 69:755–757CrossRefGoogle Scholar
  41. Ostry ME, McNabb HS (1990) Minimizing disease injury to hybrid poplars. J Environ Hort 8:96–98Google Scholar
  42. Ostry ME, Wilson LF, McNabb HSJ (1989) Impact and control of Septoria musiva on hybrid poplars. USDA Forest Service Research paper. USDA For Serv Gen Tech Rep NC-133Google Scholar
  43. Riemenschneider DE, Stanton BJ, Vallée G, Périnet P (2001) Poplar breeding strategies. In: Dickmann DI, Isebrands JG, Eckenwalder JE, Richardson J (eds) Poplar culture in North America. National Research Council of Canada, Ottawa, pp 43–76Google Scholar
  44. Roe AD, MacQuarrie CJK, Gros-Louis M-C et al (2014) Fitness dynamics within a poplar hybrid zone: I. Prezygotic and postzygotic barriers impacting a native poplar hybrid stand. Ecol Evol 4:1629–1647CrossRefPubMedPubMedCentralGoogle Scholar
  45. Sakalidis ML, Feau N, Dhillon B, Hamelin R (2014) Genetic patterns reveal introduction pathways of the invasive poplar pathogen Mycosphaerella populorum. Can J Plant Pathol 36:136Google Scholar
  46. Schaad NW, Frederick RD (2002) Real-time PCR and its application for rapid plant disease diagnostics. Can J Plant Pathol 24:250–258CrossRefGoogle Scholar
  47. Sinclair WA, Lyon HH, Johnson WT (1987) Diseases of trees and shrubs. Cornell University Press, IthacaGoogle Scholar
  48. Spielman LJ, Hubbes M, Lin D (1986) Septoria musiva on hybrid poplar in southern Ontario. Plant Dis 70:968–971CrossRefGoogle Scholar
  49. Strobl S, Fraser K (1989) Incidence of Septoria canker of hybrid poplars in eastern Ontario. Can Plant Dis Surv 69:109–112Google Scholar
  50. Talbot P, Schroeder WR, Bousquet J, Isabel N (2012) When exotic poplars and native Populus balsamifera L. meet on the Canadian Prairies: spontaneous hybridization and establishment of interspecific hybrids. For Ecol Manage 285:142–152CrossRefGoogle Scholar
  51. Thomas KD, Comeau PG, Brown KR (2000) The silviculture of hybrid poplar plantations. BC Ministry of forests Ext Note No. 47Google Scholar
  52. Thompson JD, Gibson TJ, Plewniak F et al (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882CrossRefPubMedPubMedCentralGoogle Scholar
  53. Thompson SL, Lamothe M, Meirmans PG et al (2010) Repeated unidirectional introgression towards Populus balsamifera in contact zones of exotic and native poplars. Mol Ecol 19:132–145CrossRefPubMedGoogle Scholar
  54. Waterman AM, Aldrich KF (1952) Surface sterilization of poplar cuttings. Plant Dis Rep 36:203–207Google Scholar
  55. Waterman AM, Aldrich KF (1954) Additional information on the surface sterilization of poplar cuttings. Plant Dis Report 38:96–100Google Scholar
  56. Wingfield MJ, Slippers B, Roux J, Wingfield BD (2001) Worldwide movement of exotic forest fungi, especially in the tropics and the Southern Hemisphere. Bioscience 51:134–140CrossRefGoogle Scholar
  57. Zalasky H (1978) Stem and leaf spot infections caused by Septoria musiva and Septoria populicola on poplar seedlings. Phytoprotection 59:43–50Google Scholar
  58. Zeglen S, Kope HH, Beauseigle S, Hamelin RC (2011) Preliminary distribution surveys for Septoria musiva on poplar in the upper Fraser Valley. Can Plant Dis Surv 91:155–156Google Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Padmini Herath
    • 1
  • Stephanie Beauseigle
    • 1
  • Braham Dhillon
    • 1
  • Dario I. Ojeda
    • 1
  • Guillaume Bilodeau
    • 2
  • Nathalie Isabel
    • 3
  • Marie-Claude Gros-Louis
    • 3
  • Harry Kope
    • 4
  • Stefan Zeglen
    • 5
  • Richard C. Hamelin
    • 1
    • 6
    Email author
  • Nicolas Feau
    • 1
    Email author
  1. 1.Department of Forest and Conservation Sciences, British ColumbiaThe University of British ColumbiaVancouverCanada
  2. 2.Canadian Food Inspection AgencyOttawaCanada
  3. 3.Laurentian Forestry Centre, Canadian Forest ServiceNatural Resources CanadaQuebecCanada
  4. 4.British Columbia Ministry of Forests, Lands and Natural Resource OperationsVictoriaCanada
  5. 5.British Columbia Ministry of Forests, Lands and Natural Resource OperationsNanaimoCanada
  6. 6.Institut de Biologie Intégrative et des Systèmes (IBIS)Université Laval/Pavillon Charles-Eugène MarchandQuebecCanada

Personalised recommendations