Skip to main content

Advertisement

Online identification guides for Australian smut fungi (Ustilaginomycotina) and rust fungi (Pucciniales)

Article metrics

Abstract

Interactive identification keysforAustralian smutfungi (Ustilaginomycotina and Pucciniomycotina, Microbotryales) and rust fungi (Pucciniomycotina, Pucciniales) are available online at http://collections.daff.qld.gov.au. The keys were built using Lucid software, and facilitate the identification of all known Australian smut fungi (317 species in 37 genera) and 100 rust fungi (from approximately 360 species in 37 genera). The smut and rust keys are illustrated with over 1,600 and 570 images respectively. The keys are designed to assist a wide range of end-users including mycologists, plant health diagnosticians, biosecurity scientists, plant pathologists, and university students. The keys are dynamic and will be regularly updated to include taxonomic changes and incorporate new detections, taxa, distributions and images. Researchers working with Australian smut and rust fungi are encouraged to participate in the on-going development and improvement of these keys.

Introduction

The smut fungi (Ustilaginomycotina and Pucciniomycotina, Microbotryales) and rust fungi (Pucciniomycotina, Pucciniales) in the Basidiomycota, together represent the most economically important and largest group of plant pathogens (Cummins & Hiratsuka 2003, Vánky 2011). A great diversity of smut and rust fungi occur on both agricultural and environmental species. Worldwide, there are about 1650 species of smut fungi (Vánky 2011) and almost 8000 species of rust fungi (Kirk et al. 2008). Economically important smut and rust species in Australia include wheat common bunt (Tilletia caries), sugarcane smut (Sporisorium scitamineum), wheat stem rust (Puccinia graminis), wheat stripe rust (P. striiformis), and barley leaf rust (P. hordei). Puccinia psidii appeared in Australia in 2010, and now threatens many susceptible, native species of Myrtaceae in natural environments (Pegg et al. 2014). Several species of smut and rust fungi that are absent from Australia pose serious biosecurity threats to agriculture if introduced, e.g. karnal bunt of wheat (T. indica), pine-gall rust (Endocronartium harknessii), coffee leaf rust (Hemileia vastatrix) and grapevine leaf rust (Phakopsora euvitis). Several rust fungi have been introduced to Australia as biological control agents of environmental weeds, with some having considerable success, e.g. Puccinia chondrillina on skeleton weed (Cullen et al. 1973), and Maravalia cryptostegiae on rubbervine (Tomley & Evans 2004).

Vanky & Shivas (2008) revised the Australian smut fungi, and a separate interactive Lucid key to 296 species with over 1000 images was developed to accompany the revision (Shivas et al. 2008). Despite the importance of rust fungi in Australia, the most recent monograph is over a century old and considered about 160 species (McAlpine 1906). The number of known smut and rust fungi in Australia has increased since these revisions through discoveries of new taxa, new incursions, and introductions of biological control agents.

The identification of smut and rust fungi has mostly been based on morphology and knowledge of the host species. Morphological identification of smut fungi is reliant on differences between sori and teliospores (McTaggart et al. 2012a, Vánky 2013). Rust fungi have up to five spore stages in their life cycles (Hennen & Hennen 2000, Cummins & Hiratsuka 2003). Morphological characters of the teliospore and urediniospore stages, such as size, apex shape and wall thickness, ornamentation, and germ pore position and number, are useful for species identification. Identification of a rust fungus may be challenging if a life cycle stage is absent on a specimen. Molecular identification based on sequence data from the Large Subunit (LSU) region or Internal Transcribed Spacer (ITS) region of nuclear ribosomal DNA, may identify species or genera of smut and rust fungi in cases where the host is unknown or morphology is inconclusive (Schoch et al. 2012). This approach is limited to fungi that have an available reference sequence on a public, nucleotide database. Approximately 3% of rust fungi (310 LSU sequences and 210 ITS sequences) and 21% ofsmutfungi (346 ITS sequences) had reference sequences on GenBank when accessed on 18 March 2014.

We have developed interactive keys as contemporary online resources to aid the identification of Australian smut and rust fungi. The keys are freely available, dynamic, and will be upgraded to accommodate untreated or newly discovered taxa in Australia, as well as changes in taxonomy, host range and distribution.

Methods

Taxon selection

The taxa covered by the keys include all 317 known Australian smut fungi and 100 rust fungi. The initial 100 rust fungi were chosen from species that are agriculturally important, recently introduced, or endemic. All specimens have been lodged in the Plant Pathology Herbarium, Biosecurity Queensland (BRIP) or other herbaria. Specimens were also borrowed from Australian herbaria (DAR, MEL, PERTH and VPRI) for examination. Biological and distribution data for many of these specimens can be accessed at http://collections.daff.qld.gov.au

Morphology and image capture

Spores of smut or rust fungi were removed from host material with a scalpel and mounted in clear lactic acid (100% v/v) on a microscope slide and gently heated to boiling. Slide preparations were examined with a Leica DM 2500 compound microscope using differential interference microscopy and images taken with a Leica DFC550 or DFC500 camera. Measurements of spore dimensions were made from a minimum of 20 spores, with values expressed as ranges and outliers given in parentheses. Composite images were constructed with image stacking software Helicon Focus (Helicon Soft, Kharkov).

Some of the images of spores were captured in two focal planes, one through the equator of the spores, and the other through the upper surface of the spores. A simple JavaScript was employed to allow users to toggle between the two different focal planes when viewing these spore images in the key. Host symptoms were captured in the field using an array of compact digital cameras and digital SLR cameras. In the laboratory, host symptoms were scanned using Epson Perfection V700 flatbed scanners, with a minimum resolution of 300 dpi. Close-up images of sori, especially aecia, uredinia and telia, were captured with a Leica DFC550 camera mounted on a Leica M165C stereo microscope. Images were selected based on quality and diagnostic potential.

Key development

Lucid 3.5.16 (www.lucidcentral.org) software was used to produce two interactive, multi-access keys, one for the Australian smut fungi, and the other for the Australian rust fungi. The key to smut fungi uses 53 readily observable features (characters) and 334 character states that include host, distribution and morphology of the sori and spores. The Lucid guide for the rust fungi uses 92 features and 512 character states that also includes host, distribution and morphological features of all of the spore stages known to occur in Australia.

Lucid software was used to automatically generate natural language descriptions for all taxa included in the key to Australian rust fungi. Scores for the 92 features were used to provide uniform description formats for all species in the key. Fact sheets for each of the smut and rust taxa were authored using Adobe Dreamweaver CS5.5 software.

Results

Both keys have been compiled for use on the internet, and are freely available at the following URLs:

The keys are wrapped in a web page, along with the applet version of the Lucid Player (Fig. 3). To access the keys, users require a web browser and the Java Runtime Environment, which can be downloaded for free from www.java.com. Each taxon has its own web page (Figs 12), which is accompanied by additional resources including host index, glossary, references, and a tutorial on how to use the key.

Fig. 1
figure1

Fact sheet for Anthracocystis heteropogonicola from the Smut Fungi of Australia Lucid key.

Fig. 2
figure2

Fact sheet for Puccinia stylidii from the Rust Fungi of Australia Lucid key.

Fig. 3
figure3

Screenshot of the Lucid matrix key from Smut Fungi of Australia.

Since the revision of Australian smut fungi by Vánky & Shivas (2008), a further 21 species of smut fungi have been described or recorded as new records (Table 1). Since the revision of Australian rust fungi by McAlpine (1906), 35 new species of rust fungi have been described in Australia (Table 2). There are also about 115 new records of rust fungi in Australia (including introduced biological control agents) that are provided in a comprehensive list, with references, on the website. At least another 50 undescribed species are represented in Australian herbaria (unpublished). Our current estimate of the number of Australian rust fungi is approximately 360 species.

Table 1 New records of smut fungi in Australia since 2008.
Table 2 New species of rust fungi described from host plants in Australia since 1906.

Discussion

The Lucid guides to the Australian smut fungi and rust fungi simplify and promote accurate identification of taxa (genera and species), as the identification is made on available characters selected by the user. These characters are morphology, host range and distribution. Confirmation of specimen identity is enhanced by comparison with high quality images of authentic reference specimens taken in the field and in the laboratory.

Since the last revision of smut fungi in Australia (Vánky & Shivas 2008), six new generic names with type species from Australia have been established: Aizoago (Vánky & Shivas 2013), Langdonia (McTaggart et al. 2012b), Shivasia (Lutz et al. 2012), Stollia (McTaggart et al. 2012b), Triodiomyces (McTaggart et al. 2012b), and Tubisorus (Vánky & Lutz 2011). The genus Anthracosystis was resurrected (McTaggart et al. 2012b), and the first representative of Aurantiosporium from Australia was collected (Table 1).

McAlpine (1906) treated ten genera in the Rusts of Australia, and this number has more than tripled since his revision. McAlpine (1906) included several taxa that were later combined into new genera, such as Ceratocoma (Cronartium) jacksoniae (Cummins & Hiratsuka 2003), Endoraecium (Uromyces) digitatum (Scholler & Aime 2006), Hamaspora (Phragmidium) acutissima (as longissima), Tranzschelia (Puccinia) discolor and Skierka (Uromyces) diploglottidis. There are several additional genera that have been reported from Australia: Atelocauda (Walker 2001), Bibulocystis (Walker et al. 2006), Cerotelium (Simmonds 1966), Coleosporium (Anon. 2014), Cystopsora (Sydow 1937b), Dasturella (Johnson 1985), Diabole (Burrows et al. 2012), Goplana (Langdon & Herbert 1944), Kernkampella (Walker et al. 2006), Maravalia (Tomley & Evans 2004), Masseeëlla (Liberato et al. 2014), Miyagia (Cooke & Dube 1989), Nyssopsora (Sydow 1938), Olivea (Daly et al. 2006), Phakopsora (Weinert et al. 2003), Prospodium (Thomas et al. 2006), Pucciniastrum (Shivas 1989), Ravenelia (Walker 1983), Sphaerophragmium (Alcorn & Walker 1996), Thekopsora (McTaggart et al. 2013), and Uredopeltis (Walker & Shivas 2004).

The keys to the smut and rust fungi of Australia are the first online, taxonomically focused diagnostic tools created for the identification of Australian plant pathogenic fungi. A Lucid based identification key for smut fungi of Thailand has been released at the URL collections.daff.qld.gov.au/web/key/thaismutfungi. A similar key for the rust fungi of southeast Asia is under development. We invite ustilaginologists and uredinologists to contribute to the construction of these keys. Protocols for the submission of images, morphological data, and specimens will be developed. In the future a BLAST database, based on vouchered herbarium specimens will be added to all keys to enable accurate molecular identification of taxa.

References

  1. Alcorn JL, Walker J (1996) Sphaerophragmium quadricellulare sp. nov. (Mycota, Uredinales) on Acacia in Australia, with brief notes on some related rust genera. Mycotaxon 58: 325–330.

  2. Anon. (2014) Fangipani rust. http://www.daff.qld.gov.au/plants/lifestyle-horticulture/nursery/frangipani-rust.

  3. Barrett MD, Barrett RL, Shivas RG, McTaggart AR (2009) Tilletia micrairae. Persoonia 22: 170–171.

  4. Berndt R (2010) Uromycladium naracoortensis, a new species of rust fungi (Uredinales) from Australia, with new observations on described Uromycladium species. Polish Botanical Journal 55: 299–308.

  5. Berndt R (2011) Taxonomic revision of Endoraecium digitatum (rust fungi, Uredinales) with description of four new species from Australia and Hawaii. Mycological Progress 10: 497–517.

  6. Burrows NJ, Lukitsch BV, Liberato JR (2012) Rediscovery of the rust Diabole cubensis, released as a classical biological control agent against the invasive weed Mimosa pigra in Australia. Australasian Plant Disease Notes 7: 171–175.

  7. Cooke RP, Dubé AJ (1989). Host-Pathogen Index of Plant Diseases in South Australia. Adelaide: South Australian Department of Agriculture.

  8. Cribb JW (1955) Puccinia visci sp. n. on Viscum in Queensland. Papers, University of Queensland Department of Botany 3: 75–76.

  9. Crous PW, Summerell BA, Shivas RG, Burgess TI, Decock CA, et al. (2012) Fungal Planet description sheets: 107–127. Persoonia 28: 138–182.

  10. Cullen JM, Kable PF, Catt M (1973) Epidemic spread of a rust imported for biological control. Nature 244: 462–464.

  11. Cummins GB (1945) Descriptions of tropical rusts-VII. Bulletin of the Torrey Botanical Club 72: 205–222.

  12. Cummins GB, Hiratsuka Y (2003) Illustrated Genera of Rust Fungi. St Paul, MN: American Phytopathological Society Press.

  13. Daly AM, Shivas RG, Pegg GS, Mackie AE (2006) First record of teak leaf rust (Olivea tectonae) in Australia. Australasian Plant Disease Notes 1: 25–26.

  14. Dietel P von (1922) Einige neue oder bemerkenswerte Uredineen. Annales Mycologici 20: 293–295.

  15. Hansford CG (1954) Australian Fungi. II. New records and revisions. Proceedings of the Linnean Society of New South Wales 79: 97–141.

  16. Hennen JF, Hennen MMW (2000) Terminology applied to sori and life cycles of rust fungi (Uredinales) from 1729 to 2000. Biológico, Säo Paulo 62: 113–126.

  17. Johnson GI (1985) Rust (Dasturella divina) of Bambusa spp. In Australia. Australasian Plant Pathology 14: 54–55.

  18. Kirk PM, Cannon PF, Minter DW, Stalpers JA (2008) Ainsworth & Bisby’s Dictionary of the Fungi. 10th edn. Wallingford: CAB International.

  19. Langdon RF, Herbert DA (1944) Records of Queensland fungi IV. Papers, University of Queensland Department of Botany 2: 1–4

  20. Li Y-M, Shivas RG, Cai L (2014) Three new species of Tilletia on Eriachne from north-western Australia. Mycoscience 55: 361–366.

  21. Liberato JR, McTaggart AR, Shivas RG (2014) First report of Masseeëlla capparis in Australia. Australasian Plant Disease Notes: DOI: 10.1007/s13314-013-0121-y

  22. Lutz M, Vánky K, Piatek M (2012) Shivasia gen. nov. for the Australasian smut Ustilago solida that historically shifted through five different genera. IMA Fungus 3: 143–154.

  23. Makinson RO, Butcher R (2014) The type-host species of Puccinia cygnorum re-determined as Kunzea glabrescens (Myrtaceae). Australasian Plant Disease Notes: DOI: 10.1007/s13314-014-0141-2

  24. Massee GE (1910) Fungi exotici, X. Bulletin of Miscellaneous Information, Royal Botanical Gardens, Kew 3: 1–6.

  25. McAlpine D (1906) The Rusts of Australia. Government Printer Melbourne.

  26. McTaggart AR, Geering ADW, Shivas RG (2013) Thekopsora minima causes blueberry rust in south-eastern Queensland and northern New South Wales. Australasian Plant Disease Notes: DOI: 10.1007/s13314-013-0101-2

  27. McTaggart AR, Ono Y, Berndt R, Shivas RG (2008) Maravalia in Australia, including Maravalia limoniformis sp. nov. on Austrosteenisia blackii. Australasian Mycologist 27: 41–44.

  28. McTaggart AR, Shivas RG (2008) The rusts on Proteaceae, including Puccinia grevilleae sp. nov. from northern Australia. Australasian Plant Pathology 37: 344–346.

  29. McTaggart AR, Shivas RG (2009a) Macalpinomyces mackinlayi. Persoonia 23: 186–187.

  30. McTaggart AR, Shivas RG (2009b) Tilletia challinorae. Persoonia 23: 184–185.

  31. 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.

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

  33. Morin L (2012) Entyloma ageratinae. Australasian Plant Pathology Society, Pathogen of the Month — November 2012.http://www.appsnet.org/Publications/potm/pdf/nov12.pdf

  34. Osborn TGB, Samuel G (1922) Some new records of fungi for South Australia, part II, together with a description of a new species of Puccinia. Transactions and Proceedings of the Royal Society of South Australia 46: 166–180.

  35. Pegg GS, Giblin FR, McTaggart AR, Guymer GP, Taylor H, Ireland KB, Shivas RG, Perry S (2014) Puccinia psidii in Queensland, Australia: disease symptoms, distribution and impact. Plant Pathology 63: 1005–1021.

  36. Petrak F (1953) Ein kleiner Beitrag zur Kenntnis der Uredineen Australiens. Sydowia: 7: 1–7.

  37. Piatek M, Shivas RG (2011) Sporisorium warambiense sp. nov., a fourth smut fungus on Xerochloa in Australia. Mycological Progress 10: 57–60.

  38. Samuel G (1924) Some new records of fungi for South Australia part III. Together with a description of two new species of Puccinia. Transactions and Proceedings of the Royal Society of South Australia 48: 149–161.

  39. Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, Levesque CA, Chen W, Consortium FB (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proceedings of the National Academy of Sciences, USA 109: 6241–6246.

  40. Scholler M, Aime MC (2006) On some rust fungi (Uredinales) collected in an Acacia koa-Metrosideros polymorpha woodland, Mauna Loa Road, Big Island, Hawaii. Mycoscience 47: 159–165.

  41. Shivas RG (1989) Fungal and bacterial diseases of plants in Western Australia. Journal of the Royal Society of Western Australia 72: 1–62.

  42. Shivas RG (1991) Puccinia ursiniae sp. nov. on Ursinia anthemoides. Mycological Research 95: 379–381.

  43. Shivas RG, Beasley DR, Vánky K (2008) Smut Fungi of Australia. [Lucid CD-ROM. Melbourne: CSIRO Publishing].

  44. Shivas RG, McTaggart AR (2009) Three new species of Tilletia on native grasses from northern Australia. Australasian Plant Pathology 38: 128–131.

  45. Shivas RG, Barrett MD, Barrett RL, Vánky K (2011) Two new species of Moreaua (Ustilaginomycetes), on Actinoschoenus and Chrysitrix, from Western Australia. Mycologia Balcanica 8: 137–140.

  46. Shivas RG, Lutz M, McTaggart AR, Vánky K (2013) Emended description of Anomalomyces (Ustilaginales), including Anomalomyces yakirrae sp. nov. on Yakirra pauciflora (Poaceae) from Australia. Mycobiota 1: 17–24.

  47. Shivas RG, McTaggart AR, Ryley MJ, Scharaschkin T, Gambley CF (2010) First report of the smut fungus Ustanciosporium appendiculatum in Australia. Australasian Plant Disease Notes 5: 17–18.

  48. Shivas RG, Walker J (1994) Puccinia cygnorum sp. nov. on Kunzea ericifolia in Australia. Mycological Research 98: 22–24.

  49. Simmonds JH (1966) Host Index of Plant Diseases in Queensland. Brisbane: Government Printer.

  50. Sydow H (1937a) Neue oder bemerkenswerte australische Micromyceten — I. Annales Mycologici 35: 22–49.

  51. Sydow H (1937b) Neue oder bemerkenswerte australische Micromyceten — II. Annales Mycologici 35: 350–361.

  52. Sydow H (1938) Neue oder bemerkenswerte Australische Micromyceten — III. Annales Mycologici 36: 295–313.

  53. Teakle DS (1959) Puccinia argophylli sp. n. on Argophyllum nullumense in Queensland. Queensland Journal of Agricultural and Animal Sciences 16: 91–92.

  54. Thomas SE, Ellison CA, Tomley AJ (2006) Studies on the rust Prospodium tuberculatum, a new classical biological control agent released against the invasive alien weed Lantana camara in Australia. 2. Host range. Australasian Plant Pathology 35: 321–328.

  55. Tomley AJ, Evans HC (2004) Establishment of, and preliminary impact studies on, the rust, Maravalia cryptostegiae, of the invasive alien weed, Cryptostegia grandiflora in Queensland, Australia. Plant Pathology 53: 475–484.

  56. Vánky K (2009) Taxonomic studies on Ustilaginomycetes — 29. Mycotaxon 110: 289–324.

  57. Vénky K (2011) [“2012”] Smut Fungi of the World. St Paul, MN: American Phytopathological Society Press.

  58. Vánky K (2013) Illustrated Genera of Smut Fungi. St Paul, MN: American Phytopathological Society Press.

  59. Vánky K, Lutz M (2011) Tubisorus, a new genus of smut fungi (Ustilaginomycetes) for Sporisorium pachycarpum. Mycologica Balcanica 8: 129–135.

  60. Vánky K, Shivas RG (2008) Fungi of Australia. The Smut Fungi. Melbourne: CSIRO Publishing.

  61. Vánky K, Shivas RG (2013) Aizoago, a new genus, and two new species of smut fungi (Ustilaginales) on Tetragonia (Aizoaceae) in Australia. Mycobiota 1: 1–7.

  62. Vánky K, Shivas RG, Barrett MD, Lutz M (2013) Eriocortex eriocauli, gen. et sp. nov. (Ustilaginomycetes) from Australia. Mycobiota 1: 9–16.

  63. Walker J (1983) Pacific mycogeography: deficiencies and irregularities in the distribution of plant parasitic fungi. Australian Journal of Botany Supplementary series 13: 89–136.

  64. Walker J (2001) A revision of the genus Atelocauda (Uredinales) and description of Racospermyces gen. nov. for some rusts of Acacia. Australasian Mycologist 20: 3–28.

  65. Walker J, Beilharz V, Pascoe IG, Priest MJ (2006) Bibulocystis gen. nov. (Uredinales) on Daviesia (Fabaceae) and Albizia (Mimosaceae) in Australasia, with comments on the genera Cystomyces and Dicheirinia and rust genera with teliospore cysts. Australasian Plant Pathology 35: 1–22.

  66. Walker J, Shivas RG (2004) Uredopeltis chevalieri sp. nov., the rust of Grewia (Tiliaceae) formerly known as Phakopsora (or Dasturella) grewiae, its first record in Australia and a summary of the known rusts of Grewia. Australasian Plant Pathology 33: 41–47.

  67. Walker J, Shivas RG (2009) Bibulocystis gloriosa sp. nov. (Pucciniales) on Caesalpinia scortechinii in Queensland, with comments on Spumula caesalpiniae. Australasian Plant Pathology 38: 29–35.

  68. Walker J, van der Merwe M (2009) Two previously undescribed rusts of Acanthocarpus and Lomandra (Lomandraceae) in Australia. Australasian Plant Pathology 38: 525–532.

  69. Weinert MP, Shivas RG, Pitkethley RN, Daly AM (2003) First record of grapevine leaf rust in the Northern Territory, Australia. Australasian Plant Pathology 32: 117–118.

Download references

Acknowledgements

This work was partly funded by the Australian Biological Resources Study, grant number RFL212-33.

Author information

Correspondence to Roger G. Shivas.

Rights and permissions

This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Key words

  • Australia
  • Key
  • Lucid
  • Morphology
  • Uredinales
  • Taxonomy
  • Ustilaginales