Skip to main content
Log in

Three genetic groups of the Eucalyptus stem canker pathogen Teratosphaeria zuluensis introduced into Africa from an unknown source

  • Original Paper
  • Published:
Antonie van Leeuwenhoek Aims and scope Submit manuscript

Abstract

The Eucalyptus stem canker pathogen Teratosphaeria zuluensis was discovered in South Africa in 1988 and it has subsequently been found in several other African countries as well as globally. In this study, the population structure, genetic diversity and evolutionary history of T. z uluensis were analysed using microsatellite markers to gain an enhanced understanding of its movement in Africa. Isolates were collected from several sites in Malawi, Mozambique, Uganda and Zambia. Data obtained were compared with those previously published for a South African population. The data obtained from 334 isolates, amplified across eight microsatellite loci, were used for assignment, differentiation and genetic diversity tests. STRUCTURE analyses, θ st and genetic distances revealed the existence of two clusters, one dominated by isolates from South Africa and the other by isolates from the Zambezi basin including Malawi, Mozambique and Zambia. High levels of admixture were found within and among populations, dominated by the Mulanje population in Malawi. Moderate to low genetic diversity of the populations supports the previously held view that the pathogen was introduced into Africa. The clonal nature of the Ugandan population suggests a very recent introduction, most likely from southern Africa.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Agapow PM, Burt A (2001) Indices of multilocus linkage disequilibrium. Mol Ecol Notes 1:101–102

    Article  CAS  Google Scholar 

  • Chamshama SAO, Nwonwu FOC (2004) Forest plantations in sub-saharan Africa. A report prepared for the project: lessons learnt on sustainable forest management in Africa. Report, KSLA, AFORNET, FAO

  • Chen SF, Barnes I, Chungu D, Roux J, Wingfield MJ, Xie YJ, Zhou XD (2011) High population diversity and increasing importance of the Eucalyptus stem canker pathogen, Teratosphaeria zuluensis, in South China. Australas Plant Pathol 40:407–415

    Article  Google Scholar 

  • Chungu D, Muimba-Kankolongo A, Wingfield MJ, Roux J (2010) Identification of fungal pathogens occurring in eucalypt and pine plantations in Zambia by comparing DNA sequences. Forestry 83:507–515

    Article  Google Scholar 

  • Cortinas MN, Barnes I, Wingfield BD, Wingfield MJ (2006a) Polymorphic microsatellite markers for the Eucalyptus fungal pathogen Colletogloeopsis zuluensis. Mol Ecol Notes 6:780–783

    Article  CAS  Google Scholar 

  • Cortinas MN, Burgess T, Dell B, Xu D, Crous PW, Wingfield BD, Wingfield MJ (2006b) First record of Colletogloeopsis zuluense comb.nov., causing a stem canker of Eucalyptus in China. Mycol Res 110:229–236

    Article  PubMed  Google Scholar 

  • Cortinas MN, Barnes I, Wingfield MJ, Wingfield BD (2010) Genetic diversity in the Eucalyptus stem pathogen Teratosphaeria zuluensis. Australas Plant Pathol 39:383–393

    Article  Google Scholar 

  • Cortinas MN, Crous PW, Wingfield BD, Wingfield MJ (2006b) Multigene phylogenies and phenotypic characters distinguish two species within the Colletogloeopsis zuluensis complex associated with Eucalyptus stem cankers. Stud Mycol 55:133–146

    Article  PubMed  PubMed Central  Google Scholar 

  • Cortinas MN, Koch N, Thain J, Wingfield BD, Wingfield MJ (2004) First record of the Eucalyptus stem canker pathogen, Coniothyrium zuluense from Hawaii. Australas Plant Pathol 33:309–312

    Article  Google Scholar 

  • Crous PW, Groenewald JZ, Summerel BA, Wingfield BD, Wingfield MJ (2009a) Co-occurring species of Teratosphaeria on Eucalyptus. Persoonia 22:38–48

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Crous PW, Summerell BA, Carnegie AJ, Wingfield MJ, Groenewald JZ (2009b) Novel species of Mycosphaerellaceae and Teratosphaeriaceae. Persoonia 23:119–146

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Earl D, vonHoldt B (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361

    Article  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    Article  CAS  PubMed  Google Scholar 

  • Ewens WJ (1972) The sampling theory of selectively neutral alleles. Theor Popul Biol 3:87–112

    Article  CAS  PubMed  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinf Online 1:47–50

    CAS  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587

    CAS  PubMed  PubMed Central  Google Scholar 

  • FAO (2011) Eucalyptus in East Africa: Socio-economic and environmental issues. Working Paper FP46/EFAO, Rome

  • Ficetola GF, Bonin A, Miaud C (2008) Population genetics reveals origin and number of founders in a biological invasion. Mol Ecol 17:773–782

    Article  CAS  PubMed  Google Scholar 

  • Fukunaga K, Hill J, Vigouroux Y, Matsuoka Y, Sánchez GJ, Liu K, Buckler ES, Doebley J (2005) Genetic diversity and population structure of teosinte. Genetics 169:2241–2254

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gezahgne A, Cortinas MN, Wingfield MJ, Roux J (2005) Characterisation of the Coniothyrium stem canker pathogen on Eucalyptus camaldulensis in Ethiopia. Australas Plant Pathol 34:85–90

    Article  Google Scholar 

  • Gezahgne A, Roux J, Wingfield MJ (2003) Diseases of exotic Eucalyptus and Pinus species in Ethiopian plantations. S Afr J Sci 99:29–33

    Google Scholar 

  • Graça RN, Ross-Davis AL, Klopfenstein N, Kim M-S, Peever TL, Cannon PG, Aun CP, Mizubuti ESG, Alfenas AC (2013) Rust disease of eucalypts, caused by Puccinia psidii, did not originate via host jump from guava in Brazil. Mol Ecol 22:6033–6047

    Article  PubMed  Google Scholar 

  • Isenegger DA, Macleod WJ, Ford R, Taylor PWJ (2008) Genotypic diversity and migration of clonal lineages of Botrytis cinerea from chickpea fields of Bangladesh inferred by microsatellite markers. Plant Pathol 57:967–973

    Article  Google Scholar 

  • Jimu L, Kemler M, Wingfield MJ, Mwenje E, Roux J (2015b) The Eucalyptus stem canker pathogen Teratosphaeria zuluensis detected in seed samples. Forestry. doi:10.1093/forestry/cpv037

  • Jimu L, Wingfield MJ, Mwenje E, Roux J (2014) First report of Teratosphaeria zuluensis causing stem canker of Eucalyptus grandis in Uganda. For Pathol 44:242–245

    Article  Google Scholar 

  • Jimu L, Wingfield MJ, Mwenje E, Roux J (2015) Diseases of Eucalyptus species in Zimbabwean plantations and woodlots. South For. doi:10.2989/20702620.2014.1001682

    Google Scholar 

  • Kopelman NM, Mayzel J, Jakobsson M, Rosenberg NA, Mayrose I (2015) CLUMPAK: a program for identifying clustering modes and packaging population structure inferences across K. Mol Ecol Resour. doi:10.1111/1755-0998.12387

    PubMed  Google Scholar 

  • Liu J, Goodman M, Muse S, Smith JS, Buckler E, Doebley J (2003) Genetic structure and diversity among maize inbred lines as inferred from DNA microsatellites. Genetics 165:2117–2128

    CAS  PubMed  PubMed Central  Google Scholar 

  • McDonald BA (1997) The population genetics of fungi: tools and techniques. Phytopathology 87:448–453

    Article  CAS  PubMed  Google Scholar 

  • Milgroom MG (1996) Recombination and the multilocus structure of fungal populations. Annu Rev Phytopathol 34:457–477

    Article  CAS  PubMed  Google Scholar 

  • Möller EM, Bahnweg G, Sandermann H, Geiger HH (1992) A simple and efficient protocol for isolation of high molecular weight DNA from filamentous fungi, fruit bodies, and infected plant tissues. Nucleic Acids Res 20:6115–6116

    Article  PubMed  PubMed Central  Google Scholar 

  • Nei M (1973) Analysis of gene diversity in subdivided populations. Proc Natl Acad Sci USA 70:3321–3323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Old KM, Wingfield MJ, Yuan ZQ (2003) A manual of diseases of eucalypts in South-East Asia. CIFOR, Jakarta

    Google Scholar 

  • Pérez G, Slippers B, Wingfield BD, Hunter GC, Wingfield MJ (2010) Micro- and macro spatial scale analyses illustrates mixed mating strategies and extensive gene flow in populations of an invasive haploid pathogen. Mol Ecol 19:1801–1813

    Article  PubMed  Google Scholar 

  • Pérez G, Slippers B, Wingfield MJ, Wingfield BD, Carnegie AJ, Burgess TI (2012) Cryptic species, native populations and biological invasions by a eucalypt forest pathogen. Mol Ecol 21:4452–4471

    Article  PubMed  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rejmánek M, Richardson DM (2011) Eucalypts. In: Simberloff Daniel, Rejmánek Marcel (eds) Encyclopedia of biological invasions. University of California Press, Berkeley

    Google Scholar 

  • Roux J, Meke G, Kanyi B, Mwangi L, Mbaga A, Hunter GC, Nakabonge G, Heath RN, Wingfield MJ (2005) Diseases of plantation forestry tree species in eastern and southern Africa. S Afr J Sci 101:409–413

    Google Scholar 

  • Roux J, Wingfield MJ, Cibrian D (2002) First report of Coniothyrium canker of Eucalyptus in Mexico. Plant Pathol 51:382

    Article  Google Scholar 

  • Silva MRC, Diogo E, Bragança H, Machado H, Phillips AJL (2014) Teratosphaeria gauchensis associated with trunk, stem and foliar lesions of Eucalyptus globulus in Portugal. For Pathol. doi:10.1111/efp.12160

    Google Scholar 

  • Slippers B, Stenlid J, Wingfield MJ (2005) Emerging pathogens: fungal host jumps following anthropogenic introduction. Trends Ecol Evol 20:420–421

    Article  PubMed  Google Scholar 

  • Stukenbrock EH, Banke S, Javan-Nikkhah M, McDonald BA (2007) Origin and domestication of the fungal wheat pathogen Mycosphaerella graminicola via sympatric speciation. Mol Biol Evol 24:398–411

    Article  CAS  PubMed  Google Scholar 

  • Stukenbrock EH, McDonald BA (2008) The origins of plant pathogens in agro-ecosystems. Annu Rev Phytopathol 46:75–100

    Article  CAS  PubMed  Google Scholar 

  • Taylor JW, Jacobson DJ, Fisher MC (1999) The evolution of asexual fungi: reproduction, speciation and classification. Annu Rev Phytopathol 37:197–246

    Article  CAS  PubMed  Google Scholar 

  • van der Merwe NA, Steenkamp ET, Rodas C, Wingfield BD, Wingfield MJ (2013) Host switching between native and non-native trees in a population of the canker pathogen Chrysoporthe cubensis from Colombia. Plant Pathol 62:642–648

    Article  Google Scholar 

  • van Zyl LM, Couthinho TA, Wingfield MJ, Pongpanich K, Wingfield BD (2002) Morphological and molecular relatedness of geographically diverse isolates of Coniothyrium zuluense from South Africa and Thailand. Mycol Res 106:51–59

    Article  Google Scholar 

  • Vigouroux Y, Glaubitz JC, Matsuoka Y, Goodman MM, Sánchez GJ, Doebley J (2008) Population structure and genetic diversity of new world maize races assessed by DNA microsatellites. Am J Bot 95:1240–1253

    Article  PubMed  Google Scholar 

  • Watterson GA (1978) The homozygosity test of neutrality. Genetics 88:405–417

    CAS  PubMed  PubMed Central  Google Scholar 

  • Weir BS (1996) Genetic data analysis II. Sinauer Associates, Sunderland

    Google Scholar 

  • White TJ, Bruns T, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylognetics. In: Innis MA, Gelfand DH, Sninsky JJ, White JW (eds) A guide to molecular methods and applications. Academic Press, New York, pp 315–322

    Google Scholar 

  • Wingfield MJ, Crous PW, Coutinho TA (1997) A serious canker disease of Eucalyptus in South Africa caused by a new species of Coniothyrium. Mycopathologia 136:139–145

    Article  Google Scholar 

  • Wingfield MJ, Slippers B, Hurley BP, Coutinho TA, Wingfield BD, Roux J (2008) Eucalypt pests and diseases: growing threats to plantation productivity. South For 70:139–144

    Google Scholar 

  • Wingfield MJ, Brockerhoff EG, Wingfield BD, Slippers B (2015) Planted forest health: the need for a global strategy. Science 349:832–836

    Article  CAS  PubMed  Google Scholar 

  • Yeh FC, Yang RC, Boyle T (1999) POPGENE. Version 1.31. Microsoft Windows based freeware for population genetic analysis. University of Alberta: Alberta

Download references

Acknowledgments

This work is based on research supported by the National Research Foundation of South Africa (Grant specific unique reference number (UID83924). The grant holders acknowledge that opinions, findings and conclusions or recommendations expressed in any publication generated by the NRF supported research are that of the authors and that the NRF accepts no liability what so ever in this regard. We thank the members of the Tree Protection Co-operative Program (TPCP), the THRIP initiative of the Department of Trade and Industry and the DST/NRF Centre of Excellence in Tree Health Biotechnology (CTHB) of the Forestry and Agricultural Biotechnology Institute (FABI), University of Pretoria, South Africa for financial support. We further thank forestry companies and private farmers in Malawi, Mozambique and Uganda for permission to collect samples in their plantations; the Forestry Research Institute of Malawi (FRIM) and the Sawlog Production Grant Scheme (SPGS) of Uganda for assisting with sample collection.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Luke Jimu.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jimu, L., Chen, S., Wingfield, M.J. et al. Three genetic groups of the Eucalyptus stem canker pathogen Teratosphaeria zuluensis introduced into Africa from an unknown source. Antonie van Leeuwenhoek 109, 21–33 (2016). https://doi.org/10.1007/s10482-015-0606-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10482-015-0606-0

Keywords

Navigation