Clinoconidium onumae (S. Ito) Kakish., Nagao & Denchev, 2017

Kakishima, Makoto, Nagao, Hideyuki, Ji, Jing-Xin, Sun, Yue & Denchev, Cvetomir M., 2017, Clinoconidium onumae comb. nov. (Cryptobasidiaceae), producing galls on shoot buds of Cinnamomum tenuifolium in Japan, Phytotaxa 313 (2), pp. 175-184 : 178-182

Clinoconidium onumae (S. Ito) Kakish., Nagao & Denchev , comb. nov.

MycoBank number: MB821216

Basionym:— Ustilago onumae S. Ito, Transactions of the Sapporo Natural History Society 14: 89, 1935. [ Anthracoidea onumae Shirai , in Shirai & Miyake, A list of Japanease fungi hitherto known, 2 nd edn, Tokyo, p. 45, 1917 (nom. nud.); in Shirai & Hara, A list of Japanease fungi hitherto known, 3 rd edn, Tokyo, p. 20, 1927 (nom. nud.)].

≡ Melanopsichium onumae (S. Ito) Kakish., Memories of Institute of Agriculture and Forestry, University of Tsukuba (Agriculture and Forest Science) 1: 42, 1982.

Type:— JAPAN. Kyushu: Kagoshima Prefecture, Amami Isl., on shoot buds of Cinnamomum tenuifolium (Makino) Sugim. ex H. Hara , 10 March 1997, H. Nojima (TNS-F-54697, neotype, designated here), GenBank nos. AB177594, 178258.

Galls on hypertrophied shoot buds, irregularly malformed, enlarged, firstly covered by a serrated host epidermis that later ruptures revealing an orange to dark brown, powdery spore mass ( Figs 1A, B, C, D ); inner tissues consisting of fungal hyphae and deformed plant cells ( Figs 1D, E , 2A ). Hyphae intercellular, hyaline, compact, septate ( Figs 2A, B ); haustoria irregular in shape, observed in deformed host cells ( Fig. 2B ). Hymenia formed in peripheral lacunae of the galls, pale yellow to whitish, covered by the host epidermis ( Figs 1E, D, F , 2A , 3C ). Basidia clavate, hyaline, depressed, hard to observe, gastroid, ca. 15–30 × 4–6 μm ( Figs 2A, C ). Paraphyses or sterile hyphae present in the basidial layer, hyaline, thin, long ( Fig. 2A ). Basidiospores ellipsoid, 9–18 × 6–11 μm (av. 12.5 × 7.7 μm) (n = 210), aggregated in a brown coloured mass on the surface of the galls ( Figs 1C, F , 2D , 3A, B ), wall pale brown to brown, rugose when mature; producing long branched hyphae with septa when germinated on PDA ( Fig. 2E ).

Additional specimens examined:— JAPAN. On shoot buds of Ci. tenuifolium : Kagoshima Prefecture, Amami Isl. , 15 June 1996, M. Kakishima (TNS-F-54698) ; Oita Prefecture, Bungoono-shi, Ogata-machi, Oishi , 30 June 1997, Y. Doi (TNS-F-54699) ; Chiba Prefecture, Tateyama-shi, Suzaki , June 2000, Y. Ono (TNS-F-54700) ; Chiba Prefecture, Tateyama-shi, Suzaki , 21 May 2001, M. Kakishima (TNS-F-54701) ; Chiba Prefecture, Kamogawa-shi, Mt. Kiyosumi , 14 July 2000, Y. Ono & R. Kitazawa (TNS-F-54702) ; Kanagawa Prefecture, Fujisawa-shi, Kugenuma , 3 June 2002, M. Sawada (TNS-F-54703) ; Kanagawa Prefecture, Hakone-machi, Miyanoshita , 14 June 2006, S. Nakamura (TNS-F-54704) .

Known host and distribution: —On Lauraceae : Cinnamomum tenuifolium , Japan (Okinawa, Kyushu, Honshu) ( Ito 1935, 1936, Zundel 1953, Shimabukuro & Tamori 1961, Kakishima 1982).

Comments: —In the description of Ito (1935), a host plant of this fungus was indicated but a type specimen was not designated. The specimen, used by Ito for its description, was not found in any fungal collection in Japan, including SAPA. Therefore, a neotype is designated for this fungus.

Five species of Clinoconidium have been previously reported: Cl. bullatum Syd. on species of Apollonias , Ocotea , and Phoebe from Canary Islands, Costa Rica, and Venezuela; Cl. cinnamomi (Syd.) R. Kirschner on Ci. burmanii from China; Cl. farinosum Pat. ex Sacc. on species of Nectandra and Ocotea from Puerto Rico, Brazil, and Argentina; Cl. sawadae (G. Yamada) R. Kirschner on Ci. camphora L. from Taiwan; and Cl. globosum from Japan ( Patouillard 1898, Saccardo 1902, Maublanc 1914, Sydow 1926, Hendrichs 2003, Jiang & Kirschner 2016, Kakishima et al. 2017).

The morphology of the sorus structures and the gastroid basidia are similar in each of these species although the affected plant organs are different. However, Clinoconidium omumae differs from the known species by having large ellipsoid basidiospores (9–18 × 6–11 μm versus 6–15 × 5–7 μm for Cl. bullatum , 10–13 × 5–7 μm for Cl. cinnamomi , 8–12 × 6–9 μm for Cl. farinosum , 9–12 × 5–7 μm for Cl. sawadae , and 5–10 μm long for Cl. globosum , after Hendrichs 2003, Jiang & Kirschner 2016, Kakishima et al. 2017).

The phylogenetic analysis in this study, using LSU rDNA sequences, suggested a common ancestor for Cl. cinnamomi on Ci. burmannii and Clinoconidium sp. on Ci. tenuifolium . However, the bootstrap value for Neighbor joining and Maximum parsimony did not strongly support this clade using Exobasidum, in the Exobasidiaceae , Exobasidiales as an outgroup. Maier et al. (2006) noted that Clinoconidium was monophyletic with weakly supported bootstrap value regardless of the phylogenetic analyses using Graphiola , in the Graphiolaceae , Exobasidiales as one of monophyletic outgroups. Jiang & Kirschner (2016) also reported that LSU rDNA sequences from a specimen of this species are phylogenetically different from those of the other four species. However, phylogenetic analyses using other genes will be necessary to clarify their phylogenetic relationships and differentiation.

Because this species has been collected mainly in the seashore of the southern Japanese Archipelago facing the Pacific Ocean and also it has been found only on Cinnamomum tenuifolium , it is suggested that Clinoconidium onumae evolved on this host plant, in this area.

Figures

FIGURE 1. Galls of Clinoconidium onumae on the shoot buds of Cinnamomum tenuifolium. A. A gall formed on a shoot bud of the tree. Photograph was taken at Amami Isl., Kagoshima Prefecture, Kyushu, Japan, on 15 June 1997. B. A young gall (YG) formed on a hypertrophied shoot bud, covered by a pale green to pale brown host epidermis. C. A matured gall (MG) formed on a hypertrophied shoot bud. The host epidermis is ruptured and a brown, powdery spore mass (SM) is observed on the surface of the gall. D. Vertical section of a young gall. The deformed host tissue (PT) is covered by a serrate host epidermis (HE). E. Vertical section of a matured gall. A hymenial layer (HL) is formed in peripheral lacunae of enlarged galls with deformed tissues (PT). F. A hymenial layer on the surface of galls consisting of a basidial layer (BL) and basidiospores (B). Scale bars: B = 3 cm, C, D = 2 cm, E = 1 cm, F = 0.2 mm.

FIGURE 2. A. A hymenial layer of a gall formed by Clinoconidium onumae. A hyphal mass (HM) among deformed plant cells (PC), basidial layer (BL), basidiospores (B), and sterile hyphae (SH). B. Haustoria (HA) formed in a host plant cell (PC) surrounded by hyphal mass (HM). C. Basidia (BA) and basidiospores (B) formed in peripheral lacunae. D. Basidiospores. E. Germination of a basidiospore on PDA producing long hyphae with septa. Scale bars:A, B, C, D = 20 μm, E = 15 μm.

FIGURE 3. A, B. Clinoconidium onumae observed by SEM. A. Basidiospores formed in peripheral lacunae of a gall. B. Basidiospores with rugose surface. C. Schematic structure of a hymenial layer of a gall formed by C. onumae. A hyphal mass (HM) among deformed plant cells (PC), haustoria (HA), basidia (BA), basidiospores (B), and sterile hyphae (SH). Scale bars: A= 20 μm, B = 3 μm, C = 20 μm.