Skip to main content
SpringerLink
Log in

Unique clones of the pitch canker fungus, Fusarium circinatum, associated with a new disease outbreak in South Africa

  • Published:
European Journal of Plant Pathology Aims and scope Submit manuscript

Abstract

Pitch canker of pines is caused by the fungus Fusarium circinatum. In South Africa, this pathogen has mostly been a nursery problem. From 2005, however, outbreaks of pitch canker have been reported from established Pinus radiata and P. greggii in the Western and Eastern Cape Provinces. Most recently, pitch canker-like symptoms were observed on 10-year-old P. greggii trees in a plantation in the midlands of the KwaZulu-Natal (KZN) Province. The aim of this study was to: (i) identify the causal agent of the observed symptoms, (ii) determine the genetic diversity, and (iii) the mode of reproduction of this fungal population. Furthermore, the aggressiveness of isolates from these trees was compared with that of isolates obtained previously from P. patula in South Africa. Isolates from the P. greggii trees in KZN were confirmed as F. circinatum based on both morphology and DNA sequence analyses. Microsatellite marker analyses revealed the presence of five genotypes of F. circinatum, not previously reported from other plantations in South Africa, with one of these genotypes being dominant. These genotypes were all pathogenic to P. patula and P. elliottii. No evidence of sexual reproduction was detected in the KZN population of the fungus. This was consistent with the fact that isolates from P. greggii were all of the MAT-2 mating type, in contrast to previously collected isolates from across South Africa that included both mating types. The results suggest that the outbreak of pitch canker on P. greggii in KZN represents a separate introduction of F. circinatum into the region with important implications for managing the disease.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

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

    Article  CAS  Google Scholar 

  • Bartlett, M. S. (1936). The square root transformation in analysis of variance. Supplement to the Journal of the Royal Statistical Society, 3, 68–78.

    Article  Google Scholar 

  • Berbegal, M., Perez-Sierra, A., Armengol, J., & Grunwald, N. J. (2013). Evidence for multiple introductions and clonality in Spanish populations of Fusarium circinatum. Phytopathology, 103, 851–861.

    Article  CAS  PubMed  Google Scholar 

  • Britz, H., Coutinho, T. A., Wingfield, B. D., Marasas, W. F. O., & Wingfield, M. J. (2005). Diversity and differentiation in two populations of Gibberella circinata in South Africa. Plant Pathology, 54, 46–52.

    Article  CAS  Google Scholar 

  • Britz, H., Wingfield, M. J., Coutinho, T. A., Marasas, W. F. O., & Leslie, J. F. (1998). Female fertility and mating type distribution in a South African population of Fusarium subglutinans f. sp. pini. Applied and Environmental Microbiology, 64, 2094.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Burnett, J. H. (2003). Fungal populations and species. Oxford university press on demand. Oxford: United Kingdom.

    Google Scholar 

  • Correll, J. C., Gordon, T. R., & McCain, A. H. (1992). Genetic diversity in California and Florida populations of the pitch canker fungus Fusarium subglutinans f. Sp. pini. Phytopathology, 82, 415–420.

    Article  Google Scholar 

  • Coutinho, T. A., Steenkamp, E. T., Mongwaketsi, K., Wilmot, M., & Wingfield, M. J. (2007). First outbreak of pitch canker in a south African pine plantation. Australasian Plant Pathology, 36, 256–261.

    Article  Google Scholar 

  • DAFF (Department of Agriculture, Forestry and Fisheries), (2009). Report on commercial timber resources and primary roundwood processing in South Africa 2008/9.

  • Edgar, R. C. (2004). MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics, 5, 113.

    Article  PubMed  PubMed Central  Google Scholar 

  • Engelbrecht, C. J., & Engelbrecht, F. A. (2016). Shifts in Köppen-Geiger climate zones over southern Africa in relation to key global temperature goals. Theoretical and Applied Climatology, 123, 247–261.

    Article  Google Scholar 

  • Geiser, D. M., Aoki, T., Bacon, C. W., et al. (2013). One fungus, one name: defining the genus Fusarium in a scientifically robust way that preserves long-standing use. Phytopathology, 103, 400–408.

    Article  PubMed  Google Scholar 

  • Geiser, D. M., Jiménez-Gasco, M., Kang, S., Makalowska, I., Veeraraghavan, N., Ward, T. J., Zhang, N., Kuldau, G. A., & O’Donnell, K. (2004). FUSARIUM-ID: a DNA sequence database for identifying Fusarium. European Journal of Plant Pathology, 110, 473–479.

    Article  CAS  Google Scholar 

  • Gordon, T. R., Storer, A. J., & Okamoto, D. (1996). Population structure of the pitch canker pathogen, Fusarium subglutinans f. Sp. pini, in California. Mycological Research, 100, 850–854.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Iturritxa, E., Genley, R. J., Wright, J., Heppe, E., Steenkamp, E. T., Gordon, T. R., & Wingfield, M. J. (2011). A genetically homogenous population of Fusarium circinatum causes pitch canker of Pinus radiata in the Basque Country, Spain. Fungal Biology, 115, 288–295.

    Article  PubMed  Google Scholar 

  • Leslie, J. F., & Klein, K. K. (1996). Female fertility and mating type effects on effective population size and evolution in filamentous fungi. Genetics, 144, 557–567.

    CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Mitchell, R. G., Wingfied, M. J., Steenkamp, E. T., Roux, J., Verryn, S., & Coutinho, T. A. (2014). Comparison of the tolerance of Pinus patula seedlings and established trees to infection by Fusarium circinatum. Southern Forests, 76, 151–159.

    Article  Google Scholar 

  • Mitchell, R. G., Wingfield, M. J., Hodge, G. R., Steenkamp, E. T., & Coutinho, T. A. (2012). Selection of Pinus spp. in South Africa for tolerance in infection by the pitch canker fungus. New Forests, 43, 473–489.

    Article  Google Scholar 

  • Mitchell, R. G., Steenkamp, E. T., Coutinho, T. A., & Wingfield, M. J. (2011). The pitch canker fungus, Fusarium circinatum: implications for south African forestry. Southern Forests, 73, 1–13.

    Article  Google Scholar 

  • Möller, E. M., Bahnweg, G., Sandermann, H., & Geiger, H. H. (1992). A simple and efficient protocol for isolation of high molecular weight DNA from filamentous fungi, fruit bodies and infested plant tissues. Nucleic Acids Research, 2, 6115–6116.

    Article  Google Scholar 

  • Morariu, V. I., Srinivasan, B. V., Raykar, V. C., Duraiswami, R., & Davis, L. S. (2008). Automatic online tuning for fast Gaussian summation. Advances in Neural Information Processing Systems, 21, 1113–1120.

    Google Scholar 

  • Nei, M. (1973). Analysis of gene diversity in subdivided populations. Proceedings of the National Academy of Science, 70, 3321–3323.

    Article  CAS  Google Scholar 

  • Nelson, P. E., Toussoun, T. A., & Marasas, W. F. O. (1983). Fusarium species: an illustrated manual of identification. University Park, PA: Pennsylvania State University Press.

    Google Scholar 

  • Nirenberg, H. I., & O’Donnell, K. (1998). New Fusarium species and combinations with the Gibberella fujikuroi species complex. Mycologia, 90, 465–493.

    Article  Google Scholar 

  • O’Donnell, K., Cigelnik, E., & Nirenberg, H. I. (1998). Molecular systematics and phylogeography of Gibberella fujikuroi species complex. Mycologia, 90, 465–493.

    Article  Google Scholar 

  • Porter, B., Wingfield, M. J., & Coutinho, T. A. (2009). Susceptibility of south African native conifers to the pitch canker pathogen, Fusarium circinatum. South African Journal of Botany, 75, 380–382.

    Article  Google Scholar 

  • Posada, D. (2008). jModelTest: phylogenetic model averaging. Molecular Biology and Evolution, 25, 1253–1256.

    Article  CAS  PubMed  Google Scholar 

  • Santana, Q. C., Coetzee, M. P. A., Steenkamp, E. T., Mlonyeni, O. X., Hammond, G. N. A., Wingfield, M. J., & Wingfield, B. D. (2009). Microsatellite discovery by deep sequencing of enriched genomic libraries. BioTechniques, 46, 217–223.

    Article  CAS  PubMed  Google Scholar 

  • Santana, Q. C., Coetzee, M. P. A., Wingfield, B. D., Wingfield, M. J., & Steenkamp, E. T. (2016). Nursery linked plantation-outbreaks and evidence for multiple introductions of the pitch canker pathogen Fusarium circinatum into South Africa. Plant Pathology, 65, 357–368.

    Article  Google Scholar 

  • Schulze, R. E., & Maharaj, M. (1997). South African atlas of agrohydrology and-climatology. Pretoria, South Africa: Water Research Commission.

    Google Scholar 

  • Schweigkofler, W., O’Donnell, K., & Garbelotto, M. (2004). Detection and quantification of airborne conidia of Fusarium circinatum, the causal agent of pine pitch canker, from two California sites by using a real-time PCR approach combined with a simple spore trapping method. Applied and Environmental Microbiology, 70, 3512–3520.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Steenkamp, E. T., Makhari, O. M., Coutihno, T. A., Wingfield, B. D., & Wingfield, M. J. (2014). Evidence for a new introduction of the pitch canker fungus Fusarium circinatum in South Africa. Plant Pathology, 63, 530–538.

    Article  Google Scholar 

  • Steenkamp, E. T., Wingfield, B. D., Coutinho, T. A., Zeller, K. A., Wingfield, M. J., Marasas, W. F. O., & Leslie, J. F. (2000). PCR-based identification of MAT-1 and MAT-2 in the Gibberella fujikuroi species complex. Applied and Environmental Microbiology, 66, 4378–4382.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stoddart, J. A., & Taylor, J. F. (1988). Genotype diversity: estimation and prediction in samples. Genetics, 118, 705–711.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Swett, C. L., Porter, B., Fourie, G., Steenkamp, E. T., Gordon, T. R., & Wingfield, M. J. (2014). Association of the pitch canker fungus Fusarium circinatum with grass hosts in commercial pine production areas of South Africa. Southern Forests, 76, 161–166.

    Article  Google Scholar 

  • Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., & Kumar, S. (2011). MEGA 5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance and maximum parsimony methods. Molecular Biology and Evolution, 28, 2731–2739.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Viljoen, A., Wingfield, M. J., & Marasas, W. F. O. (1994). First report of Fusarium subglutinans f.Sp. pini on pine seedlings in South Africa. Plant Disease, 78, 309–312.

    Article  Google Scholar 

  • Viljoen, A., Wingfield, M. J., Gordon, T. R., & Marasas, W. F. O. (1997). Genotypic diversity of a south African population of the pitch canker fungus Fusarium subglutinans f. Sp. pini. Plant Pathology, 46, 590–593.

    Article  Google Scholar 

  • Wikler, K. R., & Gordon, T. R. (2000). An assessment of genetic relationships among populations of Fusarium circinatum in different parts of the world. Canadian Journal of Botany, 78, 709–717.

    Article  Google Scholar 

  • Wingfield, M. J., Hammerbacher, R. J., Ganley, R. J., Gordon, T. R., Wingfield, B. D., & Coutinho, T. A. (2008). Pitch canker caused by Fusarium circinatum-a growing threat to pine plantations and forests worldwide. Australasian Plant Pathology, 37, 319–334.

    Article  Google Scholar 

  • Wright, S. (1931). Evolution in Mendelian populations. Genetics, 16, 97–159.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yeh F.C., Yang, R. C., & Boyle, T. (1999). POPEGENE version 1.31 Microsoft windows based freeware for population genetic analysis. Alberta. [https://www.ualberta.ca/~fyeh/popgene.pdf]. Accessed 22 October 2015.

Download references

Acknowledgments

We are grateful to members of the Tree Protection Cooperative Programme (TPCP) and Department of Science and Technology (DST)/National Research Foundation (NRF) and the Centre of Excellence in Tree Health Biotechnology (CTHB) of South Africa, for providing funding and support for this study. The assistance of foresters in the identification of the site and assistance with sampling in Demagtenberg, KwaZulu-Natal Province is appreciated.

Author information

Authors and Affiliations

  1. Department of Plant and Soil Sciences, Forestry and Agricultural Biotechnology Institute (FABI), Faculty of Natural and Agricultural Sciences, Private Bag X20, University of Pretoria, Pretoria, 0028, South Africa

    Felix F. Fru, Michael J. Wingfield & Jolanda Roux

  2. Department of Microbiology, Forestry and Agricultural Biotechnology Institute (FABI), Faculty of Natural and Agricultural Sciences, Private Bag X20, University of Pretoria, Pretoria, 0028, South Africa

    Emma T. Steenkamp

  3. Department of Genetics, Forestry and Agricultural Biotechnology Institute (FABI), Faculty of Natural and Agricultural Sciences, Private Bag X20, University of Pretoria, Pretoria, 0028, South Africa

    Quentin C. Santana

Authors
  1. Felix F. Fru
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Emma T. Steenkamp
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Michael J. Wingfield
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Quentin C. Santana
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jolanda Roux
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jolanda Roux.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fru, F.F., Steenkamp, E.T., Wingfield, M.J. et al. Unique clones of the pitch canker fungus, Fusarium circinatum, associated with a new disease outbreak in South Africa. Eur J Plant Pathol 148, 97–107 (2017). https://doi.org/10.1007/s10658-016-1073-9

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-016-1073-9

Keywords

Search

Navigation