Anthracoidea obtusatae T. Denchev, Denchev, Begerow & Kemler, 2023

Denchev, Teodor T., Denchev, Cvetomir M., Begerow, Dominik & Kemler, Martin, 2023, Anthracoidea obtusatae (Anthracoideaceae, Ustilaginales), a new smut fungus on Carex obtusata (Cyperaceae) from Central Asia, Phytotaxa 595 (2), pp. 139-148 : 142-146

Anthracoidea obtusatae T. Denchev, Denchev, Begerow & Kemler , sp. nov. ( Figs 2–6 ) Index Fungorum number: IF 900382

Type: —On Carex obtusata Lilj. (Cyperaceae) . RUSSIA. Altay Republic: Altay Mts, Kosh-Agachskiy Rayon, 19 km ENE Kosh-Agach , valley of the Kokorya River , 50°05′56″N, 88°53′35″E, elev. 2060 m, 8 August 2008, leg. B. Martins & M. Schnittler 2468, comm. C.M. Denchev & T.T. Denchev (SOMF 30400, holotype).

LSU rDNA GenBank accession no.: —OQ679943.

Diagnosis: — Anthracoidea obtusatae differs from the Anthracoidea species on hosts in the Carex Capitata Clade by having small-sized spores while A. nardinae and A. rupestris possess medium-sized spores.

Etymology: —The epithet is derived from the host plant, Carex obtusata .

Infection local. Sori in some female flowers, around aborted nuts as ovoid or ellipsoidal, hard bodies, 1.3–2.5 mm long, initially covered by a thin, greyish peridium that later flakes away exposing a black spore mass, powdery on the surface. Spores small-sized, flattened, in plane view irregularly rounded, suborbicular, broadly elliptical, elliptical or ovate, in plane view (12.5–)13.5–19(–20) × (10.5–)11.5–15.5(–17) (15.7 ± 1.3 × 13.2 ± 1.0) μm (n = 300), in side view 12–14.5 μm thick, medium to dark reddish brown; wall unevenly thickened, 0.8–2.0(–2.3) μm thick, with 1–3(–4), well visible internal swellings, light refractive areas and protuberances absent; smooth. In SEM, sparsely punctate, ornaments up to 0.1 μm high. Spore germination unknown.

Known host and distribution: —On Cyperaceae : Carex, Capitata Clade of C. subgen. Euthyceras: Carex obtusata , Central Asia ( Kazakhstan, Mongolia, Russia) ( Fig. 7 ).

Literature records (specimens not seen):— On Carex obtusata . MONGOLIA. Uvs Province: Mongolian Altay Range, Turgen-uul , Burgastayn-gol valley , 15 km S of Uureg-nuur Lake, at approximately 49°53′N, 1 August 1964, leg. M. Schmiedeknecht 2239a (as ‘ Cintractia / Anthracoidea caricis ’) ( Schmiedeknecht & Puncag 1966, Braun 1999). — KAZAKHSTAN. Northern Tian Shan Range , Zailiysky Alatau Range , Big Almaty Gorge , 43°03′50.6″N, 76°59′05.1″Е, elev. 2480 m, 3 September 2018, leg. U.K. Jetigenova s.n. (as ‘ Anthracoidea caricis ’) (AA; Sypabekkyzy et al. 2020). — Northern Tian Shan Range , Ketmen Ridge, Komirchi, elev. ca. 2800 m, 6 August 1946, leg. N. Rubtsov & E. Stepanova s.n. (as ‘ Cintractia caricis ’) ( Schwartzman 1960) .

Additional specimens examined: — Anthracoidea caricis-pauciflorae (Lehtola) Kukkonen on Carex pauciflora Lightf. FINLAND. Satakunta, Kankaanpää, Luomajärvi, Vääräneva, 18 August 1935, leg. L.E. Kari, in Fungi Exsicc. Fenn. 220 (K(M), isoparatype). — Anthracoidea caryophylleae Kukkonen on Carex caryophyllea Latourr. BULGARIA. Pernik Province: above Kralev Dol village, 42°33′42.0″N, 23°05′04.4″E, elev. 845 m, 9 May 2014, leg. C.M. Denchev & T.T. Denchev 1414 (SOMF 30399); LSU rDNA accession no. OQ679944. — Anthracoidea externa on Carex filifolia Nutt. U.S.A. Wyoming: Buffalo, August 1808, leg. Williams & Griffiths, in D. Griffiths, West American Fungi 305 (NY, isotype). — Anthracoidea rupestris on Carex rupestris All. GREENLAND. West Greenland: Ilulissat (as ‘Jakobshavn’), 69°13′N, 51°06′W, 19 July 1892, leg. G.H. Sørensen s.n., comm. C.M. Denchev & T.T. Denchev (CGreenland herb., s.n.). — West Greenland: Sisimiut, 31 July 1947, leg. T. Sørensen s.n., comm. C.M. Denchev & T.T. Denchev (C-Greenland herb., s.n.). — Anthracoidea sp. on Carex obtusata . CANADA. Yukon: Mt. Caribou , 5 mi. N of Carcross, 17 August 1949, leg. J.M. Gillett 4550 & D.A. Mitchell, det. D.B.O. Savile (DAOM 28184, as ‘ Cintractia caricis var. intermedia Savile’, Savile 1952: 425; a paratype of Anthracoidea caryophylleae, Kukkonen 1963: 55 ).

Comments: — Carex obtusata is distributed in North, Central, and East Europe, the Caucasus, Siberia, Russian Far East, Central Asia to NE China, Alaska, Canada, and the Rocky Mts ( Egorova 1999, Murray 2002, Koopman 2022). It is an Eurasiatic–amphi-Beringian–North American (western) species ( Egorova 1999, Elven et al. 2018).

Only two smut fungi are known to infect C. obtusata : Anthracoidea / Cintractia caricis ( Savile 1952, Fischer 1953, Zundel 1953, Schwartzman 1960, Jørstad 1962, Sypabekkyzy et al. 2020) and Anthracoidea caryophylleae ( Kukkonen 1963, Nannfeldt 1979, Vánky 2011a). In the past, Anthracoidea / Cintractia caricis was considered in a very broad sense (e.g. Fischer 1953, Zundel 1953, Schwartzman 1960). Vánky (2011a: 26–27) listed many carices that were cited in the literature or preserved in herbaria as hosts of Anthracoidea caricis . Currently, the hosts of A. caricis are reduced to members of Carex sect. Acrocystis ( Vánky 2011a, Denchev et al. 2021a). Similarly, the hosts of A. caryophylleae are reduced to carices in C. sect. Mitratae, in its traditional circumscription ( Denchev et al. 2013). To test the hypothesis that Carex obtusata is not a host of A. caryophylleae , we carried out a molecular study of a specimen of A. caryophylleae on Carex caryophyllea Latourr. (a type host of this smut fungus) from Bulgaria. The data obtained confirmed that Anthracoidea obtusatae is a distinct species from A. caryophylleae ( Fig. 1 , Table 1 ).

From Europe, Anthracoidea on Carex obtusata had been reported only once ( Zundel 1953: 23, as ‘ Cintractia caricis ’), based on the following specimen: Germany, Berlin, Pichelswerder , 30 May 1869, leg. Vatke s.n. (HBC, as ‘ Ustilago urceolorum (DC.) Tul. & C. Tul. ’, q.e. Anthracoidea caricis (Pers.) Bref. ). Scholz & Scholz (1988: 45), however, noted that both the fungus and the host plant of this specimen were misidentified, instead of A. caryophylleae on Carex supina Wahlenb .

From North America, Anthracoidea on Carex obtusata is known from Alaska ( Jørstad 1962), Canada — Yukon ( Savile 1952, as ‘ Cintractia caricis var. intermedia ’; Nannfeldt 1979, as ‘ Anthracoidea caryophylleae ’) and Saskatchewan ( Fischer 1953, as ‘ Ci. caricis ’), and U.S.A.—Montana, Galcier National Park (DAOM, as ‘ Anthracoidea caryophylleae ’). We examined a specimen of Anthracoidea on Carex obtusata from Yukon (DAOM 28184) and found that its spore morphology does not agree with that of Anthracoidea obtusatae . The Canadian specimen differs by having (i) larger spores, (15.5–)16.5–21(–22.5) × (13.5–)14.5–18(–19) (19.0 ± 1.4 × 16.2 ± 1.1) μm (n = 100), (ii) higher warts, up to 0.35 μm high, and (iii) fewer and less conspicuous internal swellings ( Figs. 8–11 ). Additional collections and molecular study are required to further clarify the taxonomic position of the North American Anthracoidea species on Carex obtusata .

Carex obtusata has been traditionally included in a monotypic section, C. sect. Obtusatae (Tuck.) Mack. ( Egorova 1999, Murray 2002) of Carex subgen. Psyllophora (Degl.) Peterm. A recently proposed classification of Carex places this sedge within the Capitata Clade of Carex subgen. Euthyceras Peterm. ( Roalson et al. 2021). The Capitata Clade is an informal group of species that includes 11 carices with a single, terminal androgynous spike: C. arctogena Harry Sm. , C. argunensis Turcz. ex Trevir. , C. capitata Sol. , C. microglochin Wahlenb. , C. monostachya A. Rich. , C. motuoensis Y.C. Yang , C. nardina (Hornem.) Fr. , C. obtusata , C. oreophila C.A. Mey. , C. runssoroensis K. Schum. , and C. rupestris ( Roalson et al. 2021) . Two Anthracoidea species have been previously reported on carices in the Capitata Clade: A. nardinae (Kukkonen) Nannf. on Carex nardina , and A. rupestris Kukkonen on Carex rupestris ( Vánky 2011a, Denchev et al. 2020). Anthracoidea obtusatae differs from A. nardinae by having small-sized spores versus medium-sized spores, (16–)17–22(–23) (19.2 ± 0.9) μm long, for A. nardinae (after Denchev et al. 2020). Anthracoidea obtusatae can be distinguished from A. rupestris by having (i) small-sized spores versus medium-sized spores, (16–)17–23(–26) (20.3 ± 1.5) μm long, for A. rupestris , (ii) thinner spore wall, 0.8–2.0(–2.3) μm thick versus 1–3(–3.8) μm thick for A. rupestris , and (iii) sparsely punctate wall ornamentation, with ornaments up to 0.1 μm high, versus densely spaced, minutely verruculose ornamentation for A. rupestris (data for A. rupestris based on our study of Greenlandic specimens in C-Greenland herb.).

In the most recent infrageneric classification of Carex, Roalson et al. (2021) applied combinations of informally named clades that have the potential to be described as formal sections, but that are not currently recognized as such, and formally named sections to reflect the current state of knowledge of Carex phylogeny. The Capitata–Schiedeanae Clade comprises species mainly with unbranched terminal spikes (excl. C. sect. Schiedeanae), and it is divided into five named clades/sections (Roalson et al. op.cit.). In these phylogenetic clades, there are additional carices with known Anthracoidea species on them: A. breweri Salo & Vánky on Carex breweri Boott and C. subnigricans Stacey , A. caricis-pauciflorae (Lehtola) Kukkonen on Carex pauciflora Lightf. , A. externa (Griffiths) Kukkonen on Carex filifolia Nutt. , and A. kenaica (Savile) Piątek on Carex micropoda C.A. Mey. ( Kukkonen 1963, Nannfeldt 1979, Vánky 2011a, b, Denchev et al. 2020, Denchev & Denchev 2022).

Anthracoidea obtusatae can easily be differentiated from these species by spore size and other features. Anthracoidea breweri (after Vánky 2011b) has medium-sized to large-sized spores, 20–27 μm long; evenly thickened spore wall, ca. 1.5 μm thick, without internal swellings; and presence of distinctly and densely minutely verruculose ornamentation. Anthracoidea caricis-pauciflorae (our study of Fungi Exsicc. Fenn. 220, K(M), isoparatype) has large-sized spores, (18.5–)19.5–28(–30.5) (23.3 ± 2.1) μm long; spore wall without internal swellings; light refractive areas common (often with more than one); and minutely to moderately verruculose ornamentation, warts 0.2–0.4 μm high. Anthracoidea externa (our study of D. Griffiths, West American Fungi 305, NY, isotype) has medium-sized spores, (16–)17–21.5(–23) (18.8 ± 1.5) μm long, with more regular shape (in plane view orbicular or broadly elliptical); absence of internal swellings; presence of a well developed hyaline sheath. Anthracoidea kenaica (after Denchev & Denchev 2022) has medium-sized spores, (16–)17–21(–23) (19.3 ± 1.1) μm long; evenly or almost evenly thickened spore wall, 0.8–1.2(–1.5) μm thick, presence of a thin hyaline sheath around some spores.

Five other species in the Capitata–Schiedeanae Clade, C. capillacea Boott , C. capitata L., C. leptalea Wahlenb. , C. microglochin Wahlenb. , and C. rara Boott , are recorded as hosts of Anthracoidea caricis (see Vánky 2011a: 26), but as was stated above, currently, the host range of A. caricis includes only sedges in Carex sect. Acrocystis , and the phylogenetic placement of the Anthracoidea species on these carices remains unresolved.

Figures

FIGURE 1. RAxML phylogeny of species in the genus Anthracoidea based on a MAFFT alignment of partial rDNA LSU sequences. Bootstrap values ≥ 50 are shown above branches.The phylogenetic tree was rooted with Moreaua bulbostylidis and M.kochiana (according to Denchev et al. 2021b).

FIGURES 2–7. Anthracoidea obtusatae sp. nov. on Carex obtusata. 2. Habit (from holotype). 3–4. Spores in LM (from holotype). 5–6. Spores in SEM (from holotype). 7. Geographic distribution of A. obtusatae (generated with Simple-Mappr, Shorthouse 2010): type locality indicated by a red circle, literature records – by blue circles. Scale bars: 2 = 1 mm, 3–4 = 10 µm, 5–6 = 5 µm.

FIGURES 8–11. Anthracoidea sp. on Carex obtusata from Canada (DAOM 28184). 8–9. Spores in LM. 10–11. Spores in SEM. Scale bars: 8–9 = 10 µm, 10–11 = 5 µm.

Tables

TABLE 1. Specimens and NCBI nucleotide database accession numbers used for phylogenetic analysis (newly generated sequences indicated in boldface).

Species	Host	LSU rDNA accession no.	Reference
A. arenaria	Carex arenaria	AY563606	Hendrichs et al. 2005
A. aspera	C. chordorrhiza	AY563607	Hendrichs et al. 2005
A. baldensis	C. baldensis	AY563599	Hendrichs et al. 2005
A. bigelowii	C. bigelowii	AY563566	Hendrichs et al. 2005
A. bigelowii	C. bigelowii	AY563567	Hendrichs et al. 2005
A. buxbaumii	C. buxbaumii	AY563582	Hendrichs et al. 2005
A. capillaris	C. capillaris	AY563596	Hendrichs et al. 2005
A. caricis	C. pilulifera	AY563589	Hendrichs et al. 2005
A. caricis-albae	C. alba	AY563594	Hendrichs et al. 2005
A. caricis-meadii	C. meadii	JN863083	Savchenko et al. 2013
A. carphae	Carpha alpina	AY563614	Hendrichs et al. 2005
A. caryophylleae	Carex caryophyllea	OQ679944	this study
A. curvulae	C. curvula	AY563611	Hendrichs et al. 2005
A. elynae	C. myosuroides	AY563609	Hendrichs et al. 2005
A. globularis	C. globularis	AY563593	Hendrichs et al. 2005
A. hallerianae	C. halleriana	MT628661	Denchev et al. 2021a
A. heterospora	C. elata	AY563601	Hendrichs et al. 2005
A. hostianae	C. hostiana	AY563581	Hendrichs et al. 2005
A. inclusa	C. rostrata	AY563605	Hendrichs et al. 2005
A. irregularis	C. ornithopoda	AY563590	Hendrichs et al. 2005
A. irregularis	C. digitata	AY563592	Hendrichs et al. 2005
A. karii	C. paniculata	AY563574	Hendrichs et al. 2005
A. karii	C. brunnescens	AY563575	Hendrichs et al. 2005
A. karii	C. echinata	AY563576	Hendrichs et al. 2005
A. karii	C. lachenalii	AY563579	Hendrichs et al. 2005
A. cf. karii	C. davalliana	AY563608	Hendrichs et al. 2005
A. lasiocarpae	C. lasiocarpa	AY563583	Hendrichs et al. 2005
A. limosa	C. limosa	AY563572	Hendrichs et al. 2005
A. misandrae	C. atrofusca	AY563584	Hendrichs et al. 2005
A. obtusatae	C. obtusata	OQ679943	this study
A. pamiroalaica	C. koshewnikowii	KT006854	Piątek et al. 2015
A. paniceae	C. panicea	AY563580	Hendrichs et al. 2005
A. pratensis	C. flacca	AY563564	Hendrichs et al. 2005
A. rupestris	C. rupestris	AY563598	Hendrichs et al. 2005
A. cf. rupestris	C. glacialis	AY563588	Hendrichs et al. 2005
A. sclerotiformis	C. punicea	AY563613	Hendrichs et al. 2005
A. sempervirentis	C. sempervirens	AY563586	Hendrichs et al. 2005
A. sempervirentis	C. firma	AY563585	Hendrichs et al. 2005
A. sempervirentis	C. ferruginea	AY563587	Hendrichs et al. 2005
A. subinclusa	C. riparia	AY563603	Hendrichs et al. 2005
A. subinclusa	C. vesicaria	AY563602	Hendrichs et al. 2005

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