Diplotheca Starbäck, Botaniska Notiser

Dissanayake, Asha J., Jayawardena, Ruvishika S., Boonmee, Saranyaphat, Thambugala, Kasun M., Tian, Qing, Mapook, Ausana, Senanayake, Indunil C., Yan, Jiye, Li, Yan Mei, Li, Xinghong, Chukeatirote, Ekachai & Hyde, Kevin D., 2014, The status of Myriangiaceae (Dothideomycetes), Phytotaxa 176 (1), pp. 219-237 : 227-234

Diplotheca Starbäck, Botaniska Notiser : 30 (1893)

Parasitic on bark. Sexual state: Ascostromata superficial, scattered, aggregated, carbonaceous, immersed to erumpent, black, globose to sub-globose, multi-loculate, locules generally located at the lower part of the ascostromata, ostiolate, Ostioles minute. Paraphyses absent. Cells of the ascostromata comprising several layers of thick-walled pale brown cells of textura globosa. Asci 8-spored, bitunicate, fissitunicate, globose or ellipsoid,

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minute pedicel, apically rounded with indistinct ocular chamber. Ascospores hyaline or pale gray, fusiform, both ends bluntly tapered, muriform, 3–6-transverse septa, 1–3-longitudinal septa, constricted at septum, smoothwalled, surrounded by a mucilaginous sheath. Asexual state: Unknown.

Notes:— Diplotheca was introduced by Starbäck (1893). Diplotheca tunae was transferred to Myriangium by Petrak (1929), however, due to its parasitic nature, Miller (1940) suggested retainning the genus name Diplotheca . Petrak (1951) compared the size of ascostromata and accepted the separation of D. tunae from Myriangium . Lumbsch & Huhndorf (2007, 2010) placed Diplotheca in the family Myriangiaceae . Diplotheca is parasitic on various plant species in Cactaceae , especially on Epiphyllum phyllanthus an epiphytic plant, forming scab-like symptoms on most stems ( Pereira & Barreto 2006).

Type species:— Diplotheca tunae (Spreng.) Starbäck, Botaniska Notiser : 30 (1893) MycoBank No: 247593 ( Fig. 5 )

Parasitic on bark. Sexual state: Ascostromata 0.2–0.3 × 0.25–0.3 mm (x = 0.25 × 0.3 mm, n = 5), superficial, scattered, aggregated, carbonaceous, immersed to erumpent, black, globose to sub-globose, multi-loculate, locules located at the lower part of the ascostromata, ostiolate. Ostioles minute. Paraphyses absent. Cells of the ascostromata brown to dark brown, comprising several layers of thick-walled textura globosa. Asci 46–52 × 40–46

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µm (x = 48 × 41 µm, n = 20), 8-spored, bitunicate, fissitunicate, globose or slightly ellipsoid, minute pedicel, apically rounded with indistinct ocular chamber. Ascospores 25–30 × 12–14 µm (x = 27 × 12 µm, n = 20), hyaline or pale grey, oblong-oval to elliptical, both ends bluntly tapered, muriform, with 3-transverse septa, 1–3- longitudinal septa, slightly constricted at the septa, smooth-walled, covered with a mucilaginous sheath. Asexual state: Unknown.

Material examined:— PUERTO RICO. Mayaguez, on Opuntia sp. (Cactaceae) , F.L. Stevens 1913 (BPI, 684149!, isotype).

Eurytheca De Seynes , Bulletin de la Société botanique de France 25: 88 (1878)

Saprobic on bark. Sexual state: Ascostromata superficial, scattered, solitary or aggregated, carbonaceous, erumpent through the ruptured epidermis, black, orbicular to irregular, multi-loculate, locules scattered in the outer region of the ascostromata, one ascus in each locule, ostiolate. Ostiole minute. Paraphyses absent. Cells of the ascostromata comprising several layers of thick-walled textura globosa pigmented cells. Asci 8-spored, bitunicate, fissitunicate, globose to saccate, short pedicellate, with indistinct ocular chamber. Ascospores hyaline, fusiform, 3–6-transverse septa, longitudinal septa absent, not constricted at the septa, base or both base and apical end bluntly tapered, smooth-walled, lacking a sheath. Asexual state: Unknown.

Notes:— The genus Eurytheca was erected by De Seynes (1878), and placed under family Saccardiaceae by Höhnel (1917). Wolf & Wolf (1947) remarked that this genus belongs to “Myriangiaceen”. Lumbsch & Huhndorf (2007) placed this genus under family Myriangeaceae . In the original description of the type species E. trinitensis ( Sydow & Sydow 1914) , the ascospores are described as 10–14-septate while Theissen & Sydow (1917) describe them as 4–5-septate. Lumbsch & Huhndorf (2007, 2010) placed Eurytheca in family Myriangiaceae . The spores examined in the current study showed only 3–6-transverse septa. There are only three species epithets for this genus (Index Fungorum 2013). Fresh collections and phylogenetic analysis are needed to confirm the familial placement of this genus in Myriangiaceae .

Type species:— Eurytheca trinitensis Sydow & P. Sydow, Annales Mycologici 13(1): 40 (1915) MycoBank No: 221235 ( Fig. 6 )

Saprobic on bark. Sexual state: Ascostromata 1–2 × 0.6–1 mm (x = 1.5 × 0.9 mm, n = 5), superficial, scattered, solitary or aggregated, carbonaceous, erumpent through the ruptured epidermis, black, orbicular to irregular, multiloculate, locules scattered in the outer region of the ascostromata, one ascus in each locule, ostiolate. Ostioles minute. Paraphyses absent. Cells of the ascostromata comprising several layers of thick-walled textura globosa pigmented cells. Asci 10–16 × 8–15 µm (x = 13 × 11 µm, n = 10), 8-spored, bitunicate, fissitunicate, globose to

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saccate, short pedicellate, with indistinct ocular chamber. Ascospores 8–23 × 2–7 µm (x = 14 × 5 µm, n = 10), hyaline, fusiform, 3–6-transverse septa, longitudinal septa absent, not constricted at the septa, base or both base and apical end bluntly tapered, smooth-walled, lacking a sheath. Asexual state: Unknown.

Material examined:— TRINIDAD. Tobago, Balanchisseuse, on Truncum arboris viventis ( Bromeliaceae ), W.E. Broadway, 15 May 1908 (S, F11411!, holotype) .

Hemimyriangium Reid & Pirozynski, Canadian Journal of Botany 44: 650 (1966)

Saprobic on twigs forming spots. Sexual state: Ascostromata superficial, scattered, solitary or gregarious, carbonaceous, semi-immersed to erumpent, black, globose to oval, multi-loculate, locules arrange in two layers in the outer layer of the ascostromata, one ascus in each locule, ostiolate. Ostioles minute. Paraphyses absent. Cells of the ascostromata comprised thick-walled textura angularis. Asci 8-spored, bitunicate, fissitunicate, globose, apedicellate, apically rounded with indistinct ocular chamber. Ascospores hyaline, oblong to oval, 1–4- transverse

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septa, longitudinal septa absent, constricted at the septa, smooth-walled, lacking a sheath. Asexual State: Unknown.

Notes:— The hemispherical shape of the ascostromata of Hemimyriangium has been assumed due to the sporogenous layer, which has formed a hemispherical resin droplet. As the resin diffuses the ascostromata seems flat in shape.

This genus was placed in the family Myriangiaceae by Reid & Pirozynski (1966). Though Lumbsch & Huhndorf (2007) placed Hemimyriangium in the family Elsinoaceae it shows similarity to type genus Myriangium having one ascus in each locule and the arrangement of locules in the outer layer of the ascostromata. Hemimyriangium also bears some superficial resemblance to ascostromata of genus Anhellia ( Reid & Pirozynski 1966) . Piley & Larsen (1968) also were able to show that Hemimyriangium has a close phylogenetic relationship with Myriangium and Diplotheca . This taxon does not appear to be a candidate for Elsinoaceae as it has a single ascus in locules scattered throughout the outer layer of ascostromata. We suggest Hemimyriangium is better referred to the family Myriangiaceae than in Elsinoaceae . Fresh collections and molecular analyses are needed to clarify the familial position of this genus.

Type species:— Hemimyriangium betulae Reid & Pirozynski, Canadian Journal of Botany 44: 651 (1966) MycoBank No: 331874 ( Fig. 7 )

Saprobic on twigs forming black superficial spots on drops of transparent, yellowish resinous secretions produced by peltate glandular hairs of the host. Sexual state: Ascostromata 2–4 × 3–4 mm (x = 3.2 × 3.6 mm, n = 12), superficial, scattered, solitary or gregarious, carbonaceous, semi-immersed to erumpent, black, hemispherical or globose to oval, multi-loculate, locules arrange in two layers in the outer layer of the ascostromata, one ascus in each locule, ostiolate. Ostioles minute. Paraphyses absent. Cells of the ascostromata comprising thick-walled textura angularis. Asci 17–47 × 15–3 µm (x = 33.0 × 24 µm, n = 12), 8-spored, bitunicate, fissitunicate, subglobose to globose, apedicellate, apically rounded with indistinct ocular chamber. Ascospores 15–29 × 4–8 µm (x = 19 × 7 µm, n = 34), hyaline, oblong to oval, 1–3-transverse septa, longitudinal septa absent, constricted at the septa, smooth-walled, lacking a sheath. Asexual state: Unknown.

Material examined:— SWEDEN. Österlövsta parish, Skyttskär, on the resinous warts of young Betula pendula (= B. verrucosa , Betulaceae ), K. & L. Holm, 1981 (S, F30030!, isotype).

Micularia Boedijn, Persoonia 2(1): 67 (1961)

Parasitic on the upper surface of leaves forming darkened areas. Sexual state: Ascostromata superficial, scattered, solitary or gregarious, coriaceous, semi-immersed, dark brown to black, globose to sub-globose, multi-loculate, locules scattered throughout the ascostromata, containing a single ascus in each locule, ostiolate. Ostioles minute, with dark brown hairs around apex. Paraphyses absent. Cells of ascostromata comprising dark brown cells of textura angularis. Asci 8-spored, bitunicate, fissitunicate, sub-globose to pyriform, short pedicellate, apically rounded with small ocular chamber. Ascospores hyaline, oblong to ellipsoid, 1-transverse septum, longitudinal septa absent, constricted at the septum, smooth-walled to verruculose, lacking a sheath. Asexual state: Unknown.

Notes:— Micularia was introduced by Boedijn (1961) and remained monotypic until Peres & Bezerra (1981) added Micularia tabebuiae to the genus. Micularia is characterized by having bundles of small spreading hairs at the apex ( Boedijn 1961). Boedijn (1961) placed this genus in the family Saccardiaceae , while Lumbsch & Huhndorf (2007, 2010) placed Micularia in the family Elsinoaceae . This placement was followed by Hyde et al. (2013). Even though it is a parasite on leaves, the inclusion of this genus in Elsinoaceae causes confusion, and as it has only one ascus in each locule we suggest to place it in Myriangiaceae .

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Type species:— Micularia merremiae Boedijn, Persoonia 2(1): 67 (1961) MycoBank: 334354 ( Fig. 8 )

Parasitic on the upper surface of leaves forming black spots. Sexual state: Ascostromata 0.5–0.65 × 0.63–0. x 75 mm (= 0.6 × 0.7 mm, n = 5), superficial, scattered, solitary or gregarious, coriaceous, immersed, dark brown to black, globose to sub-globose, multi-loculate, locules generally scattered throughout the ascostromata, comprising a single ascus in each locule, ostiolate. Ostioles minute; dark brown hairs frequently set around the blunt or acute apex of the ascostromata, 20–40 × 3–6 µm (x = 28 × 4 µm, n = 10). Paraphyses absent. Cells of ascostromata comprising dark brown cells of textura angularis. Asci 20–30 × 19–23 µm (x = 26 × 21 µm, n = 10), 8-spored, bitunicate, fissitunicate, sub-globose to pyriform, short pedicellate, apically rounded with small ocular chamber. Ascospores

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11–15 × 5–7 µm (x = 13 × 6 µm, n = 20), hyaline, oblong to ellipsoid, 1-transverse septum, longitudinal septa absent, constricted at the septum, smooth-walled or verruculose, lacking a sheath. Asexual state: Unknown.

Material examined:— INDONESIA. Java, Hortus Bogor, on leaves of Merremia sp. (Convolvulaceae) , K.B. Boedijn, 17 May 1954, (L, 0793023!, holotype).

Zukaliopsis Hennings, Hedwigia 43: 367 (1904)

Parasitic on leaves. Sexual state: Ascostromata superficial, scattered, solitary, coriaceous to sub-carbonaceous, semi-immersed to erumpent, black to brown, sub-globose, multi-loculate, locules arranged in the outer margin of the ascostromata, one ascus in each locule, ostiolate. Ostioles minute. Paraphyses absent. Cells of the ascostromata comprising dark brown pseudoparenchymatous textura angularis. Asci 8-spored, bitunicate, fissitunicate, ovoid, short pedicellate, narrowly pointed at the base, rounded at the apex with indistinct ocular chamber. Ascospores hyaline, oblong to cylindro-clavate, muriform, with 4–6-transverse septa, 0–1-longitudinal septum, slightly constricted at the septa, smooth-walled to veruculose, lacking a sheath. Asexual state: Unknown.

Notes:— Zukaliopsis was introduced by Hennings (1904) with Z. amazonica as type species and placed in the family Perisporiaceae . Höhnel (1909) proposed that Zukaliopsis is morphologically related to Molleriella . von Arx

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(1963) synonymized Zukaliopsis with Molleriella and suggested that this genus resembles a transition to Saccardinula Speg. (1885) more than Molleriella . Sydow & Theissen (1917) placed this genus into the family Myriangiaceae providing a detailed description. We observed that Zukaliopsis has one ascus in each locule and, therefore, suggest placing it in the family Myriangiaceae . New collections and molecular analysis are needed to clarify the familial position of this genus.

Type species:— Zukaliopsis amazonica Hennings, Hedwigia 43(6): 367 (1904) MycoBank No: 213216 ( Fig. 9 )

Parasitic on leaves of Sapindaceae . Sexual state: Ascostromata 0.3–0.4 × 2–3 mm (x = 0.38 × 2.3 mm, n = 10), superficial, scattered, solitary or aggregated, coriaceous to sub-carbonaceous, semi-immersed to erumpent, black to brownish grey, ovoid to sub-globose, multi-loculate, numerous locules distributed throughout the upper part of the ascostromata, one ascus in each locule, ostiolate. Ostioles minute. Paraphyses not observed. Cells of the ascostromata comprising dark brown pseudoparenchymatous textura angularis. Asci 7–8 × 6–7 µm (x = 7.5 × 7 µm, n = 20), 8-spored, bitunicate, fissitunicate, ovoid to clavate, short pedicellate, narrowly pointed at the base, apically rounded with indistinct ocular chamber. Ascospores 5–6 × 1–2 µm (x = 6 × 2 µm, n = 40), hyaline, oblong to cylindro-clavate, muriform, with 4–6-transverse septa, 0–1-longitudinal septum, slightly constricted at the septa, smooth-walled to verruculose, lacking a sheath. Asexual state: Unknown.

Material examined:— PERU. Iquitos, Rio Amazon, on Paullinia sp. (Sapindaceae) , 1902, (S, F5604!, isotype).

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Figures

FIGURE 5. Diplotheca tunae (isotype). a. Herbarium material. b. Ascostromata occurring on substrate. c. Partial section through ascostroma. d. Peridium wall. e–f. Asci. g. Ascospores. Note colour change in 3% KOH, becoming pinkish or purple in c, f and g. Scale bars: b = 500 µm, c = 100 µm, d–g = 20 µm.

FIGURE 6. Eurytheca trinitensis (holotype). a. Herbarium material. b. Ascostromata on host substrate. c. Section of ascostroma. d–e. Asci arrangement within hamathecium. f. Immature ascus. g–h. Mature asci with short pedicel bearing eight irregularly arranged ascospores. i–k. Smooth-walled, hyaline ascospores. l. Ascospore stained with cotton blue. Scale bars: c–f = 100 mm, g–l = 10 mm.

FIGURE 7. Hemimyriangium betulae (isotype). a. Herbarium material. b–c. Ascostromata on host substrate. d. Cross section of ascostroma. e–f. Peridium of locules. g. Immature and mature asci stained with cotton blue. h. Immature ascus. i. Immature ascus stained with cotton blue. j–k. Mature asci. l–n. Mature asci stained with cotton blue. o–p. Smooth to verrculose walled ascospores. q–s. Ascospore stained with cotton blue. Scale bars: b = 2 mm, c = 200 µm, d = 400 µm, e = 100 µm, f–g = 40 µm, h–s = 10 µm.

FIGURE 8. Micularia merremiae (holotype). a. Herbarium specimen. b–d. Superficial ascostromata on substrate. e. Section through ascostroma. f. Dark brown hairs around apex of ascostroma. g. Cells of ascostroma. h–j. Immature and mature asci. k. Mature ascus stained with cotton blue. l–p. Ascospores. Scale bars: b, c = 1 mm, d = 50 µm, e–f = 10 µm, g = 5 µm, h–p = 10 µm.

FIGURE 9. Zukaliopsis amazonica (isotype). a–b. Herbarium specimen. c–d. Ascostromata on natural substrate. e–f. Cross section of ascostromata. g. Ascus in water. h–k. Asci in cotton blue. l–n. Ascospores in water. o. Ascospore in cotton blue. p. Ascospores in Melzer’s. Scale bars: c = 1 mm, d = 200 µm, e–f = 50 µm, g–p = 10 µm.