Couch smut, an economically important disease of Cynodon dactylon in Australia

Abstract

Couch smut, caused by Ustilago cynodontis, is an economically important disease of Cynodon dactylon, the most widely planted warm season turfgrass in Australia. The disease is distributed across all states and mainland territories of Australia, and is found worldwide wherever the host plant is present. The most characteristic disease symptoms are expressed at the flowering stage, when the inflorescence is partly or entirely destroyed and covered by a mass of black powdery spores. However, there are also less obvious impacts of the disease on plant growth such as a more erect growth habit, and a reduced rate of stolon extension and root development, leading to lower levels of tolerance of the turf to wear during usage, and greater amounts of wastage during harvest due to the roll breaking at points of infection. Ustilago cynodontis was first described nearly 130 years ago but pathogen biology and disease epidemiology are still poorly understood, hindering development of disease management strategies. We review the current knowledge and understanding of couch smut biology, the history of its occurrence, distribution and impact, and existing disease management practices to identify the gaps in knowledge that require further research.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  1. Aldous DE, Haydu JJ, Moir RN (2009) Benchmarking the Australian sod industry. Int Turfgrass Res J 11:299–311

    Google Scholar 

  2. Aydogdu M, Boyraz N (2011) Effects of nitrogen and organic fertilization on corn smut (Ustilago maydis (DC) Corda.). Afr J Agric Res 6:4539–4553

    Google Scholar 

  3. Bailey R (1979) Possibilities for the control of sugarcane smut (Ustilago scitaminea) with fungicides. S Afr Sug Tech Assoc 53:137–142

    Google Scholar 

  4. Banuett F, Herskowitz I (1989) Different a alleles of Ustilago maydis are necessary for maintenance of filamentous growth but not for meiosis. Proc Natl Acad Sci 86:5878–5882

    CAS  PubMed  Google Scholar 

  5. Banuett F, Herskowitz I (1996) Discrete developmental stages during teliospore formation in the corn smut fungus, Ustilago maydis. Development 122:2965–2976

    CAS  PubMed  Google Scholar 

  6. Barnabas EL (2015) A report of Ustilago cynodontis infecting the Bermuda grass - Cynodon dactylon in Coimbatore, Tamil Nadu. J Sug Res 5:77–80

    Google Scholar 

  7. Batts CCV (1955a) Infection of wheat by loose smut, Ustilago tritici (Pers) Rostr. Nature 175:467–468

    Google Scholar 

  8. Batts CCV (1955b) Observations on the infection of wheat by loose smut (Ustilago tritici (Pres.) Rostr.). Trans Brit Mycol Soc 38:465–475

    Google Scholar 

  9. Batts CCV, Jeater A (1958) The development of loose smut (Ustilago tritici) in susceptible varieties of wheat, and some observations on field infection. Trans Brit Mycol Soc 41:115–125

    Google Scholar 

  10. Begerow D, Beate J, Oberwinkler F (2004) Evolutionary relationships among β-tubulin gene sequences of basidiomycetous fungi. Mycol Res 108:1257–1263

    CAS  PubMed  Google Scholar 

  11. Bhuiyan SA, Croft BJ, James RS, Cox MC (2012) Laboratory and field evaluation of fungicides for the management of sugarcane smut caused by Sporisorium scitamineum in seedcane. Australas Plant Pathol 41:591–599

    CAS  Google Scholar 

  12. Bhuiyan SA, Croft BJ, Tucker GR (2015) New method of controlling sugarcane smut using Flutriafol fungicide. Plant Dis 99:1367–1373

    CAS  PubMed  Google Scholar 

  13. Boulter J, Boland G, Trevors J (2000) Compost: a study of the development process and end-product potential for suppression of turfgrass disease. World J Microbiol Biotechnol 16:115–134

    CAS  Google Scholar 

  14. Boulter JI, Boland GJ, Trevors JT (2002) Evaluation of composts for suppression of dollar spot (Sclerotinia homoeocarpa) of turfgrass. Plant Dis 86:405–410

    PubMed  Google Scholar 

  15. Christians N (2011) Chapter 4: warm-season grassess. In: Fundamentals of Turfgrass Management. John Wiley & Sons Incorporated, Hoboken, pp 59–74

  16. Cohen C (1946) A note on the biology of Ustilago cynodontis (P. Henn) and Ustilago bromivora (Tul). F. De Waldh. S Afr J Sci 42:135–136

    Google Scholar 

  17. Digby S, Wells K (1989) Compatibility and development in Ustilago cynodontis. Mycologia 81:595–607

    Google Scholar 

  18. Dung J, Carris L, Hamm P (2014) First report of Ustilago cynodontis causing smut of Cynodon dactylon in Washington State, United States. Plant Dis 98:280

    CAS  PubMed  Google Scholar 

  19. Farr DF, Rossman AY (2019) Fungal Databases, U.S. National Fungus Collections, ARS, USDA. https://nt.ars-grin.gov/fungaldatabases/. Accessed 16 June 2019

  20. Fensham R, Laffineur B (2019) Defining the native and naturalised flora for the Australian continent. Aust J Bot 67:55–69

    Google Scholar 

  21. García-Guzmán G, Burdon JJ (1997) Impact of the flower smut Ustilago cynodontis (Ustilaginaceae) on the performance of the clonal grass Cynodon dactylon (Gramineae). Am J Bot 84:1565–1571

    PubMed  Google Scholar 

  22. Halisky P, Webster R (1963) Heterothallism in Ustilago cynodontis (pass.) Henn. Nature 197:919

    Google Scholar 

  23. Haydu JJ, Aldous DE, Satterthwaite LN (2008) Economic analysis of the Australian turfgrass industry. http://hortbusiness.ifas.ufl.edu/pubs/Aust-turf-grass.pdf.

  24. Horner W, Helbling A, Salvaggio J, Lehrer S (1995) Fungal allergens. Clin Microbiol Rev 8:161–179

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Ingold CT (1984) Further studies on the basidium of Ustilago. Trans Brit Mycol Soc 83:251–256

    Google Scholar 

  26. Jewell M, Frere C, Harris-Shultz K, Anderson W, Godwin I, Lambrides C (2012) Phylogenetic analysis reveals multiple introductions of Cynodon species in Australia. Mol Phylogen Evol 65:390–396

    CAS  Google Scholar 

  27. Jones P (1999) Control of loose smut (Ustilago nuda and U. tritici) infections in barley and wheat by foliar applications of systemic fungicides. Eur J Plant Pathol 105:729–732

    CAS  Google Scholar 

  28. Kellner R, Vollmeister E, Feldbrügge M, Begerow D (2011) Interspecific sex in grass smuts and the genetic diversity of their pheromone-receptor system. PLoS Genet 7:1–17

    Google Scholar 

  29. Kneebone WR (1966) Bermuda grass—worldly, wily, wonderful weed. Econ Bot 20:94–97

    Google Scholar 

  30. Kostandi S, Soliman M (1991) Effect of nitrogen rates at different growth stages on corn yield and common smut disease [Ustilago maydis (DC) Corda]. J Agron Crop Sci 167:53–60

    CAS  Google Scholar 

  31. Kruse J, Choi Y-J, Thines M (2017a) New smut-specific primers for the ITS barcoding of Ustilaginomycotina. Mycol Progr 16:213–221

    Google Scholar 

  32. Kruse J, Mishra B, Choi Y-J, Sharma R, Thines M (2017b) New smut-specific primers for multilocus genotyping and phylogenetics of Ustilaginaceae. Mycol Progr 16:917–925

    Google Scholar 

  33. León-Ramírez CG, Valdés-Santiago L, Campos-Góngora E, Ortiz-Castellanos L, Aréchiga-Carvajal ET, Ruiz-Herrera J (2010) A molecular probe for Basidiomycota: the spermidine synthase-saccharopine dehydrogenase chimeric gene. FEMS Microbiol Lett 312:77–83

    PubMed  Google Scholar 

  34. Levetin E, Horner WE, Scott JA et al (2016) Taxonomy of allergenic fungi. J Allergy Clin Immunol 4:375–385.e1

    Google Scholar 

  35. Maclennan A (2018) Final Report for TU16001: turf industry statistics and research project. Horticulture Innovation Australia, Sydney, 34 pp.

  36. Marchelo-d’Ragga PW, Misaka BC (2015) First report of [Ustilago cynodontis (Henn.) Henn: Ustilaginales] the causal agent of smut of couch grass Cynodon dactylon (L.) Pers. in South Sudan. Inter J Agri Res Rev 3:356–358

    Google Scholar 

  37. Martínez-Espinoza AD, MaD G-P, Gold SE (2002) The Ustilaginales as plant pests and model systems. Fungal Genet Biol 35:1–20

    PubMed  Google Scholar 

  38. McAlpine D (1910) The smuts of Australia. Government Printer, Melbourne

    Google Scholar 

  39. McTaggart AR, Shivas RG, Geering ADW, Callaghan B, Vánky K, Scharaschkin T (2012a) Soral synapomorphies are significant for the systematics of the Ustilago-Sporisorium-Macalpinomyces complex (Ustilaginaceae). Persoonia 29:63–77

    CAS  PubMed  PubMed Central  Google Scholar 

  40. McTaggart AR, Shivas RG, Geering ADW, Vánky K, Scharaschkin T (2012b) A review of the Ustilago-Sporisorium-Macalpinomyces complex. Persoonia 29:55–62

    CAS  PubMed  PubMed Central  Google Scholar 

  41. McTaggart AR, Shivas RG, Geering ADW, Vánky K, Scharaschkin T (2012c) Taxonomic revision of Ustilago, Sporisorium and Macalpinomyces. Persoonia 29:116–132

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Read JJ, Pratt RG (2012) Potassium influences forage Bermudagrass yield and fungal leaf disease severity in Mississippi. Forag Grazinglands 10:1–11

    Google Scholar 

  43. Reasor EH, Brosnan JT, Trigiano RN, Elsner JE, Henry GM, Schwartz B (2016) The genetic and phenotypic variability of interspecific hybrid bermudagrasses (Cynodon dactylon (L.) Pers.× C. transvaalensis Burtt-Davy) used on golf course putting greens. Planta 244:761–773

    CAS  PubMed  PubMed Central  Google Scholar 

  44. Shivas RG, Vánky K (2001) The smut fungi on Cynodon, including Sporisorium normanensis sp. nov. from Australia. Fungal Divers 8:149–154

    Google Scholar 

  45. Shivas RG, Vánky K (2007) Four new species of smut fungi (Ustilaginomycetes) from Australia. Mycologia Balc 4:5–10

    Google Scholar 

  46. Singh G, Khare K (1980) Teliospore germination and culture of Ustilago cynodontis. Indi Phytophathol 33:315–317

    Google Scholar 

  47. Smiley RW, Dernoeden PH, Clarke BB (1992) Compendium of turfgrass diseases. The American Phytopathological Society, St. Paul

    Google Scholar 

  48. Stoll M, Piepenbring M, Begerow D, Oberwinkler F (2003) Molecular phylogeny of Ustilago and Sporisorium species (Basidiomycota, Ustilaginales) based on internal transcribed spacer (ITS) sequences. Can J Bot 81:976–984

    CAS  Google Scholar 

  49. Stoll M, Begerow D, Oberwinkler F (2005) Molecular phylogeny of Ustilago, Sporisorium, and related taxa based on combined analyses of rDNA sequences. Mycol Res 109:342–356

    CAS  PubMed  Google Scholar 

  50. Taliaferro CM, Martin DL, Anderson J, Anderson MP (2006) Patriot turf bermudagrass. US Plant Patent and Trademark Office, p 14

  51. Tapke VF (1931) Influence of humidity on floral infection of wheat and barley by loose smut. J Agri Res 43:503–516

    Google Scholar 

  52. Tomaso-Peterson M, Hunter Perry D (2007) The role of biofungicides and organic fertilizer in the management of dollar spot in bermudagrass. Applied Turfgrass Sci 4:1–9

    Google Scholar 

  53. Vánky K (2005) The smut fungi of Ethiopia and Eritrea. Lidia 6:93–120

    Google Scholar 

  54. Vánky K (2012) Smut fungi of the world. American Phytopathological Society, St. Paul

    Google Scholar 

  55. Vialle A, Feau N, Allaire Met al. (2009) Evaluation of mitochondrial genes as DNA barcode for Basidiomycota. Mol Ecol Resour 9:99–113

    CAS  PubMed  Google Scholar 

  56. Walsh NG, Entwisle TJ (1994) Flora of Victoria, vol 2: Ferns and allied plants, conifers and monocotyledons. Inkata, Melbourne

    Google Scholar 

  57. Wennström A (1993) Systemic fungal diseases in natural plant populations. Umeå Universitet, Sweden, Doctoral Thesis, p 29

    Google Scholar 

  58. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis M, Gelfand D, Sninsky J, White T (eds) PCR protocols: a guide to methods and applications. Academic Press, San Diego, pp 315–322

    Google Scholar 

  59. Wu Y (2011) Cynodon. In: Kobe C ed Wild crop relatives: genomic and breeding resources, Millets and Grasses. Springer-Verlag, Berlin, pp 53–71

    Google Scholar 

Download references

Acknowledgements

This literature review has been funded by Hort Innovation (project code TU17002), using the turf industry research and development levy and contributions from the Australian Government. Hort Innovation is the grower-owned, not-for-profit research and development corporation for Australian horticulture. This research was also jointly supported by the Queensland Department of Agriculture and Fisheries and The University of Queensland. We are thankful to Dr. Dean Beasley for extracting records of Ustilago cynodontis from the Australian Plant Disease Database and for also assisting with generating the distribution map; the turf farm managers and growers who kindly shared their knowledge and experience on smut disease of turfgrass during our field surveys.

Author information

Affiliations

Authors

Corresponding author

Correspondence to N. T. Tran.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Tran, N.T., McTaggart, A.R., Drenth, A. et al. Couch smut, an economically important disease of Cynodon dactylon in Australia. Australasian Plant Pathol. 49, 87–94 (2020). https://doi.org/10.1007/s13313-020-00680-1

Download citation

Keywords

  • Green couch grass
  • Bermudagrass
  • Turf diseases
  • Fungicides