MycoKeys

MycoKeys. (41): 39-50

The first smut fungus, Thecaphoraanthemidis sp. nov. (Glomosporiaceae), described from Anthemis (Asteraceae)

Julia Kruse¹, Volker Kummer², Roger G. Shivas¹, Marco Thines³⁴⁵

1. Centre for Crop Health, Institute for Agriculture and the Environment, University of Southern Queensland, Toowoomba 4350, Queensland, Australia

2. University Potsdam, Institute for Biochemistry and Biology, Maulbeerallee 1, D-14469 Potsdam, Germany

3. Goethe University Frankfurt am Main, Department of Biosciences, Institute of Ecology, Evolution and Diversity, Max-von-Laue-Str. 9, D-60438 Frankfurt am Main, Germany

4. Biodiversity and Climate Research Centre (BiK-F), Senckenberg Gesellschaft für Naturforschung, Senckenberganlage 25, D-60325 Frankfurt am Main, Germany

5. Integrative Fungal Research Cluster (IPF), Georg-Voigt-Str. 14-16, D-60325 Frankfurt am Main, Germany

Corresponding author: Julia Kruse (Julia.Kruse@usq.edu.au)

Academic editor: T. Lumbsch

Julia Kruse, Volker Kummer, Roger G. Shivas, Marco Thines

DOI: 10.3897/mycokeys.41.28454

Published online: 11 October 2018

Abstract

Abstract.

There are 63 known species of Thecaphora (Glomosporiaceae, Ustilaginomycotina), a third of which occur on Asteraceae. These smut fungi produce yellowish-brown to reddish-brown masses of spore balls in specific, mostly regenerative, plant organs. A species of Thecaphora was collected in the flower heads of Anthemischia (Anthemideae, Asteraceae) on Rhodes Island, Greece, in 2015 and 2017, which represents the first smut record of a smut fungus on a host plant species in this tribe. Based on its distinctive morphology, host species and genetic divergence, this species is described as Thecaphoraanthemidissp. nov. Molecular barcodes of the ITS region are provided for this and several other species of Thecaphora. A phylogenetic and morphological comparison to closely related species showed that Th.anthemidis differed from other species of Thecaphora. Thecaphoraanthemidis produced loose spore balls in the flower heads and peduncles of Anthemischia unlike other flower-infecting species.

Introduction

Thecaphora species belong to the Glomosporiaceae (Urocystidales, Ustilaginomycotina). The type species is Th.seminis-convolvuli described from Convolvulusarvensis (Convolvulaceae) collected in France (Desmazièrs 1827). Until now, 63 species of Thecaphora have been recognised (Vánky 2012), infecting host plant species in 16 different eudicot families (Vánky and Lutz 2007, Roets et al. 2008, Vánky et al. 2008, Vánky 2012). Species of Thecaphora produce sori in flowers, fruits, seeds, stems, leaves or roots, often in galls or pustules. The granular to powdery spore balls are yellowish-brown to reddish-brown, but never black. The majority of Thecaphora species produce loose or permanent spore balls without sterile cells. An exception to this is Th.smallanthi, which was reported to have large spore balls with outer spores and an internal layer of hyaline (sterile) cells (Piepenbring 2001). Three species have single spores (not united in spore balls), namely, Th.thlaspeos, Th.oxalidis (Vánky et al. 2008) and Th.capensis (Roets et al. 2008).

The Asteraceae is the largest family of eudicots with an estimated number of 30,000 species (Funk et al. 2009). The Asteraceae is divided into 13 subfamilies, including four (Asteroideae, Cichorioideae, Carduoideae and Mutisioideae) that contain about 99% of all taxa. Anthemis is a large genus in the tribe Anthemideae (subfamily Asteroideae), along with Cota, Gonospermum (including Lugoa), Nananthea, Tanacetum and Tripleurospermum (Bremer and Humphries 1993, Oberprieler et al. 2009, Presti et al. 2010). Species of Anthemis are distributed in western Eurasia, including the Mediterranean region, northern Africa and a small part of eastern Africa (Oberprieler 1998, 2001, Oberprieler et al. 2009, Presti et al. 2010). There are 62 species of Anthemis in Europe. Anthemischia belongs to the section Chiae and is a Mediterranean species common on Rhodes Island, Greece.

About 20 species of Thecaphora infect host plant species in six tribes of the Asteraceae. Taxa of the tribes Astereae and Heliantheae in the subfamily Asteroideae are often hosts of several Thecaphora species. Some less species-rich tribes, e.g. Coreopsideae, Millerieae, Polymnieae and Cynareae (subfamily Carduoideae) are also hosts of Thecaphora species. The species of Thecaphora on Asteraceae have not been studied by molecular phylogenetic methods, in contrast to species of Thecaphora on Caryophyllaceae (Vánky and Lutz 2007), Polygonaceae (Vasighzadeh et al. 2014) and Oxalidaceae (Roets et al. 2008, 2012).

Plants of Anthemischia with distorted flower heads containing mostly ligulate (ray) florets and swollen peduncles were collected near Tsambika, Rhodes Island, Greece, in 2015 and 2017. The swollen flower heads contained reddish-brown granular to powdery spore ball masses, typical of species of Thecaphora. The aim of this study was to identify the fungus and to determine its taxonomic assignment based on morphological and phylogenetic analyses of the internal transcribed spacer (ITS, barcoding locus) sequence data.

Materials and methods

Specimens

Herbarium specimens (23) of Thecaphora on a range of host plant species from across Europe and North America were examined (Tables 1, 2). The ITS sequences of specimens available on GenBank (19) and published in previous studies (Table 2) were included in the phylogenetic analysis. The nomenclature of the host plant species follows Euro+Med PlantBase (http://www.emplantbase.org/home.html) and the nomenclature of the fungi is according to Vánky (2012).

The morphology of the spore balls and spores of one specimen (GLM-F112531) of Thecaphora on Anthemischia was microscopically examined at 1000× in 80% lactic acid heated to the boiling point on a glass slide. Measurements of 30 spore balls and 100 spores were made with the Zeiss AxioVision software and micrographs were taken with an Olympus FE-120 camera on a Seben SBX-5 compound microscope (Seben GmbH, Berlin). The measurements are reported as maxima and minima in parentheses and the means are placed in italics.

DNA extraction, amplification and sequencing

Genomic DNA was extracted from 23 herbarium specimens of Thecaphora (Table 1) using the methods reported by Kruse et al. (2017). The ITS nrDNA was amplified by PCR as reported in Kruse et al. (2018), using M-ITS1 (Stoll et al. 2003) as forward primer and either smITS-R1 or smITS-R2 (Kruse et al. 2017) as reverse primer. The ITS of host plants was amplified using primer pair ITS1P/ITS4 (Ridgway et al. 2003) with an annealing temperature of 53 °C. The resulting amplicons were sequenced at the Senckenberg Biodiversity and Climate Research Centre (BiK-F, Senckenberg) using the ITS4 primer (White et al. 1990). Sequences were deposited in GenBank (Table 2).

Phylogenetic analysis

In total, 42 ITS sequences from 21 Thecaphora species were used in the phylogenetic analyses. Sequences were aligned with MAFFT v.7 (Katoh and Standley 2013) employing the G-INS-I algorithm and leading and trailing gaps were trimmed. The resulting alignment length was 534 bp. The methods of phylogenetic analysis were according to Kruse et al. (2018) using Minimum Evolution (

ME

), Maximum Likelihood (

ML

) and Bayesian Inference (

BA

). Thecaphoraitalica and allied species were selected as an outgroup, on the basis of the phylogeny presented by Vánky and Lutz (2007). Host plant species determination was verified by comparison with published sequences from Asteraceae deposited in GenBank (https://www.ncbi.nlm.nih.gov/genbank/) using BLASTN (Altschul et al. 1997).

See full tableTable 1. Collection records for specimens of Thecaphora examined in this study.

See full tableTable 2. Specimens and GenBank sequences used for phylogenetic analyses. Sequences generated in this study are shown in bold.

Results

Molecular phylogenetic reconstruction

The

ML

and

BA

trees yielded consistent topologies with the

ME

tree (Fig. 1). The Thecaphora sp. on Anthemischia, together with three Asteracious species (Th.pustulata, Th.hennenea and Th.spilanthis) and Th.solani from Solanumlycopersicum (Solanaceae), formed a sister clade to the species on other host plant families with strong to intermediate bootstrap support (83% in

ME

, 93% in

ML

). The Thecaphora sp. on Anthemischia was sister to the other Asteracious species with low bootstrap support (59% in

ME

, 59% in

ML

), but high Bayesian posterior probability (96%). The Thecaphora species on Fabaceae were polyphyletic, with Th.frezii on Arachishypogaea sister to Th.oxalidis on Oxalisstricta (Oxalidaceae). Thecaphorafrezii was distant to a monophyletic lineage on Oxytropispilosa and Astragalusglycyphyllos, which was sister to Th.seminis-convolvuli, the type of the genus. All specimens of Th.seminis-convolvuli collected on Calystegiasepium and Convolvulusarvensis (Convolvulaceae) had identical ITS sequences, as was the case with Thecaphorathlaspeos on Arabishirsuta and A.ciliata (Brassicaceae). Within the clade of mostly Caryophyllaceae-infecting species, two species of Thecaphora infected other families of the Caryophyllales, namely Th.molluginis on Mollugocerviana (Molluginaceae) and Th.haumanii on Iresinediffusa (Amaranthaceae).

Figure 1.View larger versionFigure 1. Phylogenetic tree of Thecaphora species based on ME analysis of the ITS locus. Numbers on branches denote support in ME, ML and BA, respectively. Values below 50% are denoted by ‘–‘. The bar indicates the number of substitutions per site. Ex-type sequences are highlighted with an asterisk.

Taxonomy

Taxon classification. FungiUrocystidalesGlomosporiaceae

Thecaphora anthemidis

J. Kruse, V. Kumm. & Thines sp. nov.

827067

Figure 2A–H

Type.

Greece, Rhodes Island, 3.5 km NE Archangelos, Tsambika, on path to monastery, northeast slope, 36°14'03"N, 28°09'19"E, 90 m a.s.l, on Anthemischia, 26 Apr. 2017, V. Kummer. Holotype GLM-F112531, isotype Herbarium V. Kummer P 1971/chia4; ITS sequence GenBank MH399758.

Etymology.

From the host plant genus Anthemis.

Description.

Sori in swollen and distorted flower heads and peduncles; spore ball mass initially white, later reddish-brown, granular to powdery; spore balls subglobose to ellipsoidal, rarely ovoid, mostly regular in shape, (31–) 36–41–47 (–52) × (28–) 31–38–44 (–50) µm, length/width ratio 0.9–1.1–1.2 (n=30), under light microscopy yellowish-brown to pale yellowish-brown, composed of 2–10 (–12) loosely united spores that separate easily; spores ellipsoidal, subglobose, ovoid or cuneiform, (18–) 20–21–23 (–25) × (14–) 17–18–20 (–23) µm, length/width ratio of 1.1–1.2–1.4 (n=100), with flattened contact surfaces and rounded exposed surfaces; wall at contact surface up to 0.5 µm thick, wall at free surface up to 3 µm thick, densely verrucose with warts 0.5–1 µm high, often confluent and sometimes irregular.

Host range.

Anthemischia.

Distribution.

Greece.

Notes.

Thecaphoraanthemidis has sori in the flower heads and the peduncles, which differentiates it from the following species that produce pustules, galls or swellings on the stems of Asteraceae: Th.ambrosiae, Th.denticulata, Th.heliopsidis, Th.hennenea, Th.melampodii, Th.mexicana, Th.neomexicana, Th.piluliformis, Th.polymniae, Th.pulcherrima, Th.pustulata, Th.smallanthi and Th.spilanthis. Four of the seven previously known species of Thecaphora that infect the flower heads of Asteraceae, namely Th.arnicae, Th.burkartii, Th.californica and Th.cuneata have firmly united spores that only separate after considerable pressure, which differentiate them from Th.anthemidis that has loose spore balls. Further, Th.arnicae (spore balls comprised of up to 25 spores), Th.californica (6–20 spores) and Th.solidaginis (8 to 50 or more spores) have larger spore balls with larger numbers of spores than Th.anthemidis. The spores of Th.cuneata are radially arranged within the spore balls and Th.burkartii has spores with an outer wall 5–9 µm thick, which is more than three times thicker than in Th.anthemidis. Thecaphoralagenophorae and Th.trailii are morphologically most similar to Th.anthemidis. Thecaphoralagenophorae is only known to infect Solenogynegunnii (tribe Astereae) in Australia (Vánky 2012). Thecaphoratrailii infects species of Carduus, Cirsium and Saussurea (Asteraceae, tribe Cynareae, Carduoideae) (Vánky 2012) and further differs from Th.anthemidis by having smaller spore balls (12–30 µm) and fewer spores (2–8) per spore ball.

Figure 2.View larger versionFigure 2. Sori, spore balls and spores of Thecaphoraanthemidis on Anthemischia (GLM-F112531) (A–H), A habit B–C swollen flower heads and peduncles D dissected flower head with reddish granular powdery spore ball mass E young spore balls F mature spore balls G–H single spores. Scale bars: 10 µm.

Discussion

The present study is the first to identify a species of Thecaphora on a host plant species in the tribe Anthemideae (Asteraceae) (see Vánky 2012). Thecaphoraanthemidis was recovered in a monophyletic group of Thecaphora species on Asteraceae, sister to Thecaphorasolani on Solanumlycopersicum (Solanaceae). Our phylogenetic hypothesis, based on the ITS region, was similar to the analyses of the LSU locus of these taxa in Vánky and Lutz (2007) and Roets et al. (2008). In the latter study, Thecaphorapolymniae, which is known only from the type collection on Polymniariparia (Polymnieae, Asteroideae, Asteraceae) from South America (Vánky 2012), clustered within a clade of taxa that infect Fabaceae, Caryophyllaceae and Amaranthaceae (Roets et al. 2008). Thecaphorapolymniae has spores with a reticulate ornamentation and this may be evidence of a host jump from one of these plant families to Asteraceae. Host jumps have been reported before in the Ustilaginomycotina (e.g. Begerow et al. 2002, Piątek et al. 2017) and are thought to be a driver of plant pathogen diversification (Choi and Thines 2015).

Previously, only two ITS sequences of Thecaphora species infecting Asteraceae (Th.spilanthis and Th.hennenea) were available on GenBank, which together with the new sequences reported in this study, represents only 20% of all Thecaphora species known to occur on Asteraceae. In addition to the sequence of Th.anthemidis, we have provided barcode sequences of the ITS region for eight other taxa not previously available on GenBank (Table I). Future studies should address whether species of Thecaphora that infect the flower heads of Asteraceae form a monophyletic group.

Supplementary Material

Open In Web Browser

Acknowledgements

The authors are grateful to Ulrike Damm and Michaela Schwager of the Herbarium Senckenbergianum Görlitz (GLM) for providing us with herbarium numbers for private collections and to the curators Dagmar Triebel of the Herbarium Munich (M), Ulrike Damm of the Herbarium Senckenbergianum Görlitz (GLM) and Scott LaGreca of the Cornell University New York (CUP) for loaning specimens from their keeping. We also thank all private collectors of the specimens investigated in this study for giving material to public herbaria. Furthermore, we want to thank the Ministry for Environment and Energy, Directorate for Forest Management for the collection permission in Rhodes (Greece). Alistair McTaggart is thanked for proofreading the paper and helpful advice.

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Table 1.

Collection records for specimens of Thecaphora examined in this study.

Species | Host | Country | Location | Date | Collector | Herbarium accession no.*
Thecaphora affinis | Astragalus glycyphyllos | Slovenia | Lower Styria, region Savinjska, N of Ljubno ob Savinjii, trail to Mt. Greben Smrekovec-Komen from Primož pri Ljubnem, wayside, 46°24'21"N, 14°49'54"E, 1150 m asl | 14 July 2015 | J. Kruse | GLM F112522
A. glycyphyllos | Germany | Saxony-Anhalt, SW of Zschornewitz, forestry trail nearby SW-shore of „Gürke“ (Zschornewitzer Lake) | 26 June 2007 | H. Jage | GLM F094059
Th. anthemidis | Anthemis chia | Greece | Island Rhodes, 3.5 km NE Archangelos, Tsambika, way up to monastery, northeastslope, 36°14'03"N, 28°09'19"E, 90 m asl | 26 April 2017 | V. Kummer | GLM F112531
Th. haumanii | Iresine diffusa | Costa Rica | Prov. Guanacaste, 6 km NW de la barrada de la Laguna de Arenal | 1 April 1992 | R. Berndt, M. Piepenbring | M 0236177
Th. leptideum | Chenopodium album | France | Lotharingia, Forbach, Kreuzberg Mt. | Aug.-Oct. 1912/1913 | A. Ludwig | M 0230099
Th. molluginis | Mollugo cerviana | Romania | Bratovesti, Oltenia | 15 July 1963 | K. Lug. Eliart | M 0236178
M. cerviana | Romania | Oltenia, Timburesti | 19 Sept. 1958 | L. Pop | M 0236180
Th. oxalidis | Oxalis stricta | Austria | Upper Austria, Braunau at Inn, Hagenau Inncounty, Hagenauer Street, wayside, 48°16'24"N, 13°06'03"E, 340 m asl | 18 Aug. 2014 | J. Kruse | GLM F112523
O. stricta | Germany | Bavaria, Upper Franconia, Fichtelmountains, Fichtelberg, Sandgrubenway, cemetery, 605 m asl | 17 Sept. 2012 | J. Kruse | GLM F112524
O. stricta | Germany | Saxony-Anhalt, county Anhalt-Bitterfeld, Bitterfeld-Wolfen, Mühlstreet, allotment garden area „Kühler Grund“, 51°37'23"N, 12°20'08"E | 13 July 2014 | J. Kruse & H. Jage | GLM F112525
Th. pustulata | Bidens pilosa | Puerto Rico, USA | Mayagüez | 13 Mar. 1920 | H. H. Whetzel, E. W. Olive | CUP PR000458
Th. seminis-convolvuli | Convolvulus arvensis | Germany | Saxony, Middlesaxony, Freiberg, Halsbrücker Street, roadside, 50°55'31"N, 13°20'56"E, 400 m asl | 11 Aug. 2017 | J. Kruse | GLM F112527
C. arvensis | Germany | Hesse, c. 8.5 km SE Eschwege, Weißenborn, Sandhöfe, path, 51°07'35"N, 10°07'25"E, 250 m asl | 22 July 2017 | J. Kruse | GLM F112528
C. arvensis | Germany | Saxony-Anhalt, SSE Seeben, at Franzosenstein, wayside | 26 Aug. 2002 | H. Jage | GLM F065278
Calystegia sepium | Germany | Mecklenburg-Western Pomerania, county Vorpommern-Rügen, 1,5 km NE of Barth, Glöwitz, rest area, 54°22'15"N, 12°45'38"E, 0 m asl | 24 Aug. 2014 | J. Kruse | GLM F112526
C. sepium | Germany | North Rhine-Westphalia, county Steinfurt, Rheine, castle grounds Bentlage, between parking area and Gradierwerk, 52°17'49"N, 07°25'11"E, 35 m asl | 14 July 2017 | J. Kruse | GLM F112529
Th. seminis-convolvuli | C. sepium | Germany | Schleswig-Holstein, county Schleswig-Flensburg, Schaalby, W of Winningmay, parking area at „Reesholm“, wayside, 54°31'44"N, 09°37'53"E, 2 m asl | 30 Aug. 2014 | J. Kruse | GLM F112530
Th. thlaspeos | Arabis ciliata | Austria | Tyrol, district Kufstein, county Walchsee, Kaiserwinkel, track from hickinghut towards Niederkaseralm, over Hintere Abendpoit, eastslope Mt. Hochköpfl, 47°41'25"N, 12°19'37"E, 1300 m asl | 21 July 2014 | J. Kruse | GLM F112533
A. ciliata | Germany | Bavaria, Chiemgauer Alps, county Rosenheim, Priener Hut, track 8,20, way up towards Kampenwand, alpine meadow, 47°42'29"N, 12°19'27"E, 1570 m asl | 18 July 2014 | J. Kruse | GLM F112536
A. ciliata | Germany | Bavaria, Chiemgauer Alps, county Traunstein, Priener Hut, track 8,20 towards Priener Hut, alpine meadow, 47°42'07"N, 12°20'36"E, 1310 m asl | 19 July 2014 | J. Kruse | GLM F112537
A. hirsuta | Germany | Hesse, Meißnerfoothills, Werra-Meißner-county, Großalmerode, S of Weißenbach, “Bühlchen”, calcareous grassland, 51°14'55"N, 09°51'08"E, 500 m asl | 13 June 2015 | J. Kruse | GLM F112532
A. hirsuta | Germany | Bavaria, county Donau-Ries, Harburg, N of Ronheim, dry grassland, 435 m asl | 20 June 2013 | J. Kruse | GLM F112534
A. hirsuta | Germany | Bavaria, Upper Bavaria, county Weilheim, N of Pähl, E at Hartschimmelhof, N „Goaslweide“, wayside, 720 m asl | 20 July 2013 | J. Kruse | GLM F112535

* Acronyms: GLM = Herbarium Senckenbergianum, Görlitz, Germany; CUP = Plant Pathology Herbarium, Cornell University, New York, USA; M = Botanische Staatssammlung, Munich, Germany.

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Table 2.

Specimens and GenBank sequences used for phylogenetic analyses. Sequences generated in this study are shown in bold.

Thecaphora species | Host | Herbarium accession no. ¹ | ITS GenBank accession no. | Reference
Th. affinis | Astragalus glycyphyllos | GLM F112522 | MH399748 | this paper
GLM F094059 | MH399749 | this paper
Th. alsinearum | Stellaria holostea | HUV 10535 | EF200032 | Vánky and Lutz 2007
Th. amaranthi | Amaranthus hybridus | HUV 20727 | EF200013 | Vánky and Lutz 2007
Th. anthemidis | Anthemis chia | GLM F112531 | MH399758 | this paper
Th. frezii | Arachis hypogaea | Sa-EM1* | KP994420 | Cazón et al. 2016
Cba-GD2* | KP994419 | Cazón et al. 2016
Th. haumanii | Iresine diffusa | M 0236177 | MH399764 | this paper
Th. hennenea | Melampodium divaricatum | HUV 14434 | EF200014 | Vánky and Lutz 2007
Th. italica | Silene italica | HUV 20345 | EF200026 | Vánky and Lutz 2007
HUV 20344 | EF200025 | Vánky and Lutz 2007
Th. leptideum | Chenopodium album | M 0230099 | MH399756 | this paper
Th. melandrii | Silene alba | HUV 12677 | EF200024 | Vánky and Lutz 2007
Th. molluginis | Mollugo cerviana | M 0236178 | MH399762 | this paper
M 0236180 | MH399763 | this paper
Th. oxalidis | Oxalis stricta | GLM F112524 | MH399759 | this paper
GLM F112523 | MH399760 | this paper
GLM F112525 | MH399761 | this paper
Th. oxytropis | Oxytropis pilosa | Kummer P 1146/3* | KF640685 | Kummer et al. 2014
Kummer P 1146/2* | KF640684 | Kummer et al. 2014
Th. pustulata | Bidens pilosa | CUP PR000458 | MH399757 | this paper
Th. saponariae | Saponaria officinalis | TUB 012796 | EF200022 | Vánky and Lutz 2007
Th. schwarzmaniana | Rheum ribes | BASU 4242 | JX006079 | Vasighzadeh et al. 2014
KRAM F-49788 | KF297811 | Vasighzadeh et al. 2014
Th. seminis-convolvuli | Calystegia sepium | GLM F112529 | MH399742 | this paper
GLM F112526 | MH399743 | this paper
GLM F112530 | MH399744 | this paper
Convolvulus arvensis | GLM F112527 | MH399745 | this paper
GLM F112528 | MH399746 | this paper
GLM F065278 | MH399747 | this paper
Th. solani | Solanum lycopersicum | HUV 11180 | EF200037 | Vánky and Lutz 2007
Th. sp. | Rheum palmatum | S. Wang 1991* | KJ579177 | Piątek et al. unpublished
Y. Wang 2013* | KJ579176 | Piątek et al. unpublished
HUV 21117 | KF297812 | Vasighzadeh et al. 2014
Th. spilanthis | Acmella sp. | AFTOL 1913 | DQ832243 | Matheny et al. 2006
Th. thlaspeos | Arabis hirsuta | GLM F112532 | MH399752 | this paper
TUB 015857 | KJ579178 | Vasighzadeh et al. 2014
GLM F112534 | MH399750 | this paper
GLM F112535 | MH399751 | this paper
Arabis ciliata | GLM F112537 | MH399753 | this paper
GLM F112533 | MH399754 | this paper
GLM F112536 | MH399755 | this paper

¹ Acronyms: AFTOL = Assembling the Fungal Tree Of Life, http://aftol.org; BASU: Herbarium of Bu-Ali Sina University, Iran; CUP = Plant Pathology Herbarium, Cornell University, New York, USA; GLM = Herbarium Senckenbergianum, Görlitz, Germany; HUV = Herbarium Ustilaginales Vánky, deposited in BRIP = Queensland Plant Pathology Herbarium, Brisbane, Australia; KRAM F = Mycological Collection of the W. Szafer Institute of Botany, Polish Academy of Sciences, Kraków, Poland; M = Botanische Staatssammlung, Munich, Germany; TUB = Herbarium Tubingense, Eberhard-Karls-Universität Tübingen, Germany; * not deposited in any public herbaria.

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Figure 1.

Phylogenetic tree of Thecaphora species based on ME analysis of the ITS locus. Numbers on branches denote support in ME, ML and BA, respectively. Values below 50% are denoted by ‘–‘. The bar indicates the number of substitutions per site. Ex-type sequences are highlighted with an asterisk.

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Figure 2.

Sori, spore balls and spores of Thecaphoraanthemidis on Anthemischia (GLM-F112531) (A–H), A habit B–C swollen flower heads and peduncles D dissected flower head with reddish granular powdery spore ball mass E young spore balls F mature spore balls G–H single spores. Scale bars: 10 µm.

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