Tilletia Tul. & C. Tul., Annls Sci. Nat., Bot., sér. 3 7: 112 (1847)



            Tulasne and Tulasne (1847) named Tilletia (Tilletiaceae, Exobasidiales) after Matthieu du Tillet (1714–1791), who first determined the pathogenicity of T. caries on wheat in France (Vánky and Shivas 2008). Tillet showed that washed seed reduced the spread of smut, although he was unaware the disease was caused by a fungus (Carefoot and Sprott 1967).

Species of Tilletia cause smut in the inflorescences and leaves of grasses (Poaceae). They are either localized in individual ovaries or systemic in the inflorescence. The species of Tilletia on cultivated grasses can cause economic losses and have been intensively studied. For example, several species, including T. caries, replace the grains of wheat with masses of spores that produce trimethylamine, which has an odour of rotten fish. Consequently, ginger-bread was invented as a solution to mask the smell of smutted grain (Carefoot and Sprott 1967). Tilletia indica is a billion-dollar threat to the wheat industries in Australia and the USA (Murray and Brennan 1998; Rossman 2009). The misidentification of T. indica in grain from both of these countries has been discussed (Castlebury and Carris 1999; Pascoe et al. 2005).

Castlebury et al. (2005) determined that the association of spore morphology, germination patterns and relationships with hosts were unclear in some clades of Tilletia. Systemic species of Tilletia germinate to form basidiospores that conjugate while attached to the basidium, and form dikaryotic hyphae that infect host seedlings. Localized species of Tilletia form basidiospores that do not conjugate on germination from the basidium (Castlebury et al. 2005). The systemic species usually have reticulate spores, whereas the localized species have verrucose spores (Castlebury et al. 2005).

ClassificationExobasidiomycetes, Exobasidiomycetidae, Tilletiales, Tilletiaceae

Type speciesTilletia caries (DC.) Tul. & C. Tul., Annls Sci. Nat., Bot., sér. 3 7: 113 (1847)

Distribution – Worldwide

Disease Symptoms – Sori mostly replace ovaries of infected grasses with a mass of powdery black or brown spores. The ovaries are often hypertrophied and the infection can be systemic or localised. Sori are sometimes produced on the leaves and culms of infected plants.


 Morphological based identification and diversity     

            Vánky (2011) listed 178 taxa in his world monograph of smut fungi. Since then only three further species, T. geeringii, T. mactaggartii and T. marjaniae, have been described, all from Australia on species of Eriachne (Li et al. 2014). Castlebury et al. (2005) found that Conidiosporomyces, Ingoldiomyces and Neovossia, collectively represented by only five species, were congeneric with Tilletia. Chandra and Huff (2008) established the monotypic Salmacisia, which was sister to Tilletia. Salmacisia buchloeana grouped with Tilletia, sister to T. dactyloctenii, in the present analysis. Vánky (2011) used host taxonomy as the most important character to identify species of Tilletia. The size and ornamentation of spores is used to further identify species on the same host genera (see http://collections.daff.qld.gov.au/web/key/smutfungi/ Shivas et al. 2014).

Molecular based identification and diversity

Castlebury et al. (2005) used the large subunit (LSU) region of ribosomal DNA (rDNA) to first study species of Tilletia with a molecular approach. Single species descriptions have since been based on the internal transcribed spacer (ITS) and LSU regions (Shivas et al. 2009; McTaggart and Shivas 2009; Li et al. 2014). The present study builds on work by previous authors and provides molecular barcodes for the ITS and LSU regions sequenced from type specimens in the private collection of Kálmán Vánky (Herbarium Ustliaginales Vánky), which is held at the Queensland Plant Pathology Herbarium (BRIP).

There are five publicly available genomes in GenBank for species of Tilletia, all of which are agriculturally important taxa. These are T. controversa, T. caries, T. walkeri (Nguyen et al. unpublished), T. horrida (Wang et al. 2015) and T. indica (Sharma et al. 2016). Their genomes range in size from 20–37 Mb with an average size of ~28 Mb. An 18 Mb genome for Tilletia buchloeana (as Salmacisia buchloeana) was recently released (Huff et al. 2017). An ongoing challenge for genomic studies of Tilletia is that these taxa are difficult to grow in culture, which limits the amount of DNA available for genomic analysis.

 This study reconstructs the phylogeny of Tilletia based on analyses of combined ITS and LSU sequence data. The molecular barcodes of rDNA gene regions provided from type specimens in the present study will aid identification of known taxa. However, for further resolution within Tilletia, additional markers will be required. There was no phylogenetic support for the larger clades in the current analyses.

Recommended genetic marker (genus level) – LSU

Recommended genetic marker (species level) – ITS

Accepted number of species: There are 336 species epithets in Index Fungorum (2018) under this genus, of which 181 are in use.

References: Castlebury et al. 2005, Shivas et al. 2009, 2014, McTaggart and Shivas 2009, Vánky 2011, Li et al. 2014 (morphology and phylogeny); Wang et al. 2015, Sharma et al. 2016, Huff et al. 2017 (genome).

Table Details of the isolates used in the phylogenetic analyses. Ex-type (ex-epitype) strains are in bold and marked with an * and voucher strains are in bold.

Taxon Voucher number ITS LSU
Erratomyces patelii HUV 18697 DQ663692 AF009855
Oberwinkleria anulata HUV 16003* DQ875369 NA
Salmacisia buchloëana WSP 71313 EF204936 DQ659922
Tilletia aegopogonis WSP 67743 AY818967 NA
T. anthoxanthi HUV 18739* MH231773 MH231773
T. asperifolia LMC 90 NA AY818968
T. australiensis BRIP 51874 MH231774 MH231774
T. ayresii HUV 19314 / BRIP 49130 AY819017 MH231775
T. barclayana Strain-832 AF310168 NA
T. barclayana S-104 AF399894 NA
T. barclayana WSP 68658 NA AY818970
T. barclayana WSP 68466 NA AY818971
T. bornmuelleri S 054 AF398452 NA
T. boutelouae WSP 68661 NA AY818973
T. brachypodii-mexicani HUV 16007* MH231776 MH231776
T. bromi BRIP 49095 MH231777 MH231777
T. capeyorkensis BRIP 27011 MH231778 MH231778
T. caries LMC 97-136 AF398438 AY819007
T. cerebrina LMC 125 NA AY818994
T. challinoriae BRIP 52502* NR119757 NA
T. chionachnes BRIP 26898* MH231779 MH231779
T. controversa V 764 AF398440 AY818995
T. dactyloctenii HUV 8887* MH231780 MH231780
T. ehrhartae BRIP 28392 MH231781 MH231781
T. elymi S 064 AF398454 NA
T. eragrostiellae HUV 15805* MH231782 NA
T. eremopoae HUV 19420* MH231783 MH231783
T. filisora BRIP 47729 MH231784 MH231784
T. fusca LMC 214 AF398455 AY818996
T. geeringii BRIP 51851* KF055226 NA
T. gigacellularis HUV 20555* MH231785 MH231785
T. goloskokovii LMC 315 NA AY818999
T. holci V 765 AF398459 AY819008
T. horrida NA AF398435 NA
T. horrida LMC 339 NA AY818974
T. horrida LMC 358 NA AY818975
T. horrid T54899 MH231786 NA
T. hyalospora HUV 16038 AF133576 AF399891
T. imbecillus BRIP 7831 MH231787 MH231787
T. indica BPI 863665 AF398434 AY818977
T. iowensis BPI 863664 NA AY818988
T. ischaemi HUV17453* MH231788 MH231788
T. ixophori WSP 71170 NA AY819010
T. kimberleyensis BRIP 51857 MH231789 MH231789
T. lachnagrostidis BRIP 47300 MH231790 NA
T. laevis V 766 AF398444 AY819005
T. lageniformis BRIP 47749* MH231791 MH231791
T. laguri HUV 16352* MH231792 NA
T. lineate BRIP 26844* MH231793 MH231793
T. lolii S 119 AF398460 NA
T. maclaganii Tm001NY09 JF745116 NA
T. mactaggartii BRIP 51853* KF055227 KF055228
T. majuscule BRIP 51841* NA MH231794
T. marjaniae BRIP 49721* KF055224 KF055225
T. menieri WSP 69115 AF398456 AY819002
T. micrairae BRIP 52433* FJ862995 NA
T. moliniae TUB 018922 EU659134 EU661605
T. narayanaraoana BRIP 47957 GQ497894 NA
T. nigrifaciens BRIP 43865 MH231796 MH231796
T. obscura-reticulata WSP 68357 NA AY819011
T. olida BRIP 44536 MH231797 MH231797
T. opaca BRIP 27896 MH231798 MH231798
T. panici-humilis HUV 205832* MH231799 NA
T. polypogonis V 931 NA AY819015
T. pseudochaetochloae BRIP 46730 MH231800 MH231800
T. pseudoraphidis BRIP 51873* MH231801 MH231801
T. pulcherrima WSP 71501 EU915293 NA
T. rostrariae HUV 14898* MH231802 MH231802
T. rugispora HUV 19147 / BRIP 47127 MH231803 AY818983
T. savilei V 859 AF399885 AY819018
T. sehimicola BRIP 51847* MH231804 MH231804
T. setariae V 934 NA AY819014
T. setariae-parvifolia BRIP 47735* MH231805 NA
T. setariae-pumilae HUV 21399* MH231806 NA
T. shivasii BRIP 52525 MH231807 MH231807
T. sporoboli HUV 1880* MH231808 NA
T. sterilis LMC 363 NA AY819003
T. sumatiae HUV 17529 / V933 MH231809 AY818987
T. thailandica BRIP 48134 NA MH231810
T. trabutii BRIP 46328 MH231811 MH231811
T. trachypogonis HUV 19626* MH231812 MH231812
T. triticoides S 102 AF398446 NA
T. verruculosa WSP 70430 NA AY818984
T. viennotii BRIP 47077 MH231813 MH231813
T. vitatta BRIP 54207 MH231814 MH231814
T. walker BPI 746091 AF399887 AY818978
T. whiteochloae BRIP 51838 MH231815 MH231815
T. xerochloae BRIP 54437 MH231816 MH231816

Fig.  Phylogram of 89 species of Tilletia obtained from a maximum likelihood search (command –f a) of concatenated ITS and LSU gene regions in RAxML v. 8.2 (Stamatakis 2014). Bootstrap values (≥70%) from 1000 maximum likelihood replicates above nodes and posterior probability values (≥0.95) summarized from 30,000 converged trees in a Bayesian search below nodes. Taxa sequenced from a type specimen in bold font. The tree was rooted to Erratomyces patellii.

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