Parmulariales D.Q. Dai & K.D. Hyde, 2018

Dai, Dong-Qin, Tang, Li-Zhou, Liu, Chao, Wang, Hai-Bo & Hyde, Kevin D., 2018, Studies on Parmulariaceae I. A phylogeny based on available sequence data; introducing Parmulariales ord. nov., and Hemigraphaceae, Melaspileellaceae and Stictographaceae fam. nov., Phytotaxa 369 (2), pp. 63-79 : 73-76

Parmulariales D.Q. Dai & K.D. Hyde , ord. nov.

Index Fungorum number: IF554065; Facesoffungi number: FoF 03913

Epiphytic or parasitic on living leaves of plants and ferns or lichenicolous. Colonies superficial, dark brown to black, rounded to irregular. Hyphae usually spreading out from ascomata border. Sexual morph: Ascostromata solitary, scattered, gregarious, or in groups, superficial to immersed, shield-like, elliptical, dark brown to black, carbonaceous to membranaceous, strongly flattened. Locules immersed in ascostromata or in longitudinal ridges radiating from the centre. Peridium composed of dark to hyaline, thick to thin cells of textura prismatica to textura angularis . Hamathecium of hyaline, septate pseudoparaphyses with brown apices, or pseudoparaphyses lacking. Asci 8-spored, bitunicate, broad cylindrical to subglobose, with an ocular chamber. Ascospores 2-seriate to irregular arranged, hyaline to dark brown, oblong to ellipsoid, 1-septate, smooth- to verrucose-walled. Asexual morph: Undetermined.

Notes:— Parmulariaceae has had a varied history in terms of its higher-level placement ( Inácio & Cannon 2008), with placements in the orders Dothiorales, Microthyriales , Hemisphaeriales, Dothideales and Hysteriales (Müller & von Arx 1962, Ainsworth 1971, Luttrell 1973, von Arx & Müller 1975, Barr 1979, Hawksworth et al. 1983, 1995). The family has also been placed in Dothideomycetes family incertae sedis, as DNA sequence data was not available ( Eriksson 1999, Kirk et al. 2001). Kirk et al. (2008) followed this placement. Inácio & Cannon (2008) reviewed the family with a detailed study, however they did not assign the family Parmtoulariaceae to any order. Lumbsch & Huhndorf (2010) maintained Parmulariaceae in Dothideomycetes family incertae sedis. Hyde et al. (2013) re-examined the types of bitunicate families and placed Parmulariaceae in the order Asterinales based on morphological similarities with Asterinaceae . Guatimosim et al. (2015) sequenced the type species of type genus of Parmulariaceae and placed this family in order Asterinales , as Parmulariaceae was phylogenetically close to several Asterina species. However, Liu et al. (2017) placed above mentioned Asterina taxa in Asterinaceae sensu lato and their lineages are separate from Asterinales sensu stricto. Thus, the ordinal placement of Parmulariaceae is undetermined. The family Parmulariaceae is morphologically and phylogenetically distinct from families of Asterinales and justifies a separate order in Dothideomycetes ( Fig. 1 ). Thus, Parmulariales is recommended here to accommodate a single family Parmulariaceae .

Type family: Parmulariaceae E. Müll. & Arx ex M.E. Barr, Mycologia 71(5): 944 (1979)

Facesoffungi number: FoF 02296

Epiphytic or parasitic on living leaves of plants and ferns or thallus of lichens. Colonies superficial, dark brown to black, rounded to irregular. Hyphae spreading out from ascomata, brown, septate, branching, sinuous, usually lacking appressoria. Sexual morph: Ascostromata solitary, scattered, or gregarious, superficial to immersed, shield-like, elliptical to boat-shaped, dark brown to black, carbonaceous to membranaceous, strongly flattened, or longitudinal slits slightly protuberant. Locules immersed in ascostromata or in longitudinal ridges radiating from the centre. Stromata wall thin to thick, composed of black, large cells of textura prismatica. Wall of locules thin to thick, composed of dark brown to hyaline smaller cells of textura angularis . Hamathecium of dark brown to hyaline, septate, pseudoparaphyses or pseudoparaphyses lacking. Asci 8-spored, bitunicate, long ovate, broad cylindrical, broad-clavate, or obclavate, globose to subglobose, short pedicellate, with a distinct ocular chamber, thick-walled. Ascospores 2–multi-seriate, hyaline to dark brown, oblong to ellipsoid, 1-septate, smooth- to verrucose-walled. Asexual morph: Undetermined.

Notes:—The family Parmulariaceae was invalidly introduced by Müller & von Arx (1962) to accommodate species with colonies forming on the surface of living plant tissues, mostly leaves, and was later validated by Barr (1979). Parmulariaceae contains a range of ascomata types, asci and ascospores forms ( Inácio & Cannon 2008), as numerous genera were placed in this family. Lumbsch et al. (2007) included 34 genera in Parmulariaceae and Inácio & Cannon (2008) included 35 genera. Kirk et al. (2008) included 34 genera with 24 synonyms as well as 119 species. Inácio et al. (2012) introduced a new genus Antoniomyces Inácio , according to its similarity of morphology with Parmulariaceae . Hyde et al. (2013) accepted 31 genera and excluded four genera viz. Coccodothis Theiss. & Syd. , Dothidasteroma Höhn. , Englerodothis Theiss. & Syd. and Perischizon Syd. & P. Syd. from this family. Guatimosim et al. (2014b) introduced a new genus Rhagadolobiopsis Guatim. & R.W. Barreto based on morphology. Thambugala et al. (2014b) re-examined the herbarium of type species of Placostromella Petr. and assign it in Parmulariaceae .

The family Parmulariaceae can be compared with Asterinaceae , however, it differs in having ascostromata produce multi-locules which forming longitudinal ridges radiating from the centre surrounded by thick wall, and formed a developed base, pseudoparaphyses, ellipsoidal to obclavate asci, and usually lack appressoria ( Inácio & Cannon 2008, Inácio 2012, Hyde et al. 2013). Species of Asterinaceae have superficial hyphae mostly with appressoria, small thyriothecia with a thin upper wall layer and poorly developed base, subglobose asci, lack pseudoparaphyses, ( Pirozynski & Shoemaker 1970, Inácio 2012, Hongsanan et al. 2014). Parmulariaceae can also be compared with Englerulaceae whose species are usually parasitic on living leaves. Englerulaceae however it differs in having small, superficial, globose and deliquescent ascomata on mycelium ( Dai et al. 2014).

Type genus: Parmularia Lév., Annls Sci. Nat., Bot. , sér. 3 5: 286 (1846)

Facesoffungi number: FoF 02297

Epiphytic on upper surface of leaves. Colonies foliicolous, superficial, dark brown to black, circular. Hyphae growing at base of ascomata, brown, septate, branching, sinuous, lacking appressoria. Sexual morph: Ascostromata large, solitary to groups, gregarious, superficial, shield-like, dark brown to black, carbonaceous, flattened, with ridges radiating from the centre to the outer rim; ridges containing elongated locules, which open by a longitudinal slit and containing numerous asci; cells of ascostromata wall thick-walled and elongated and composed of black, amorphous tissues in the stromatic crust. Locules in vertical section subglobose, immersed within ascostroma. Upper wall of ascostromata thick, comprised of several black layers, composed of dark brown cells of textura prismatica. Cells between locules composed of brown to hyaline cells of texture angularis . Hamathecium of hyaline, septate, filamentous pseudoparaphyses, swollen, brown and verrucose at their apices. Asci 8-spored, thick-walled, bitunicate, cylindrical, short-pedicellate, with a distinct ocular chamber. Ascospores 2–3-seriate, hyaline and becoming pale brown when mature, ellipsoidal, 1-septate, with large and round upper cells, with narrow and long lower cells, constricted at the septum, smooth-walled. Asexual morph: Undetermined.

Notes: — Parmularia is typified by P. styracis Lév. , introduced by Léveillé (1846). Parmularia is similar to Mintera in having elongate locules radiating from a central point. However, Mintera has mycelium with appressoria, and each black ascostroma with a single locule which aggregate into star-shaped structures. In Parmularia , a single ascostroma contains many locules. Parmularia comprises numerous species with 53 names in Index Fungorum (2018) and Kirk et al. (2008) estimated there are 30 species. However, Inácio & Cannon (2008) compared only six Parmularia species, all from Brazil and only one species from New Zealand. Parmularia is characterized by large, black, shield-like, flattened ascostromata with ridges radiating from the centre to the outer rim, and the ridges comprising elongated, radiating locules, filamentous pseudoparaphyses with brown and verrucose apices and ellipsoid, 1-septate ascospores ( Inácio & Cannon 2008, Hyde et al. 2013).

Type species: Parmularia styracis Lév., Annls Sci. Nat., Bot. , sér. 3 5: 286 (1846). Figure 5

Facesoffungi number: FoF 02298

Epiphytic on upper surface of leaves. Colonies foliicolous, superficial, dark brown to black, round. Hyphae growing out from ascomata, brown, septate, branching, sinuous, lacking appressoria. Sexual morph: Ascostromata 1– 3 mm diam., solitary to gregarious, or in groups, superficial, shield-like, dark brown to black, carbonaceous, flattened, with ridges radiating from the centre to outer rim; ridges containing elongated locules, which open by a longitudinal slit and contain numerous asci, cells of ascostromata thick-walled and elongate and composed of black, amorphous tissues in the stromatic crust. Locules in vertical section: 150–250 μm diam., 80–120 μm high, subglobose, immersed in ascostromata. Upper wall of ascostromata 20–40 μm thick, comprising several black layers, composed of dark brown cells of textura prismatica. Cells between locules composed of brown to hyaline cells of texture angularis . Hamathecium of hyaline, septate, filamentous pseudoparaphyses, 50–80 × 2–3.5 μm, swollen, brown and verrucose at their apices. Asci 45–70 × 12–16 μm (= 58.2 × 13.9 μm, n = 20), 8-spored, thick-walled, bitunicate, broadly cylindrical, short-pedicellate, with a distinct ocular chamber. Ascospores 13.5–16.5 × 4–6 μm (= 15.6 × 5.1 μm, n = 20), 2–3-seriate, hyaline becoming pale brown when mature, ellipsoidal, 1-septate, with larger and rounder upper cells, with narrow and longer lower cells, constricted at the septum, smooth-walled. Asexual morph: Undetermined.

Material examined:— BRAZIL, Brasilia, São Paolo, near Urbem Faxina, on leaves of Styracis sp., August 1901, v. Wettstein & Schiffner (S F21306).

Notes: — Parmularia styracis described from leaves of Styrax L., collected in Brazil ( Léveillé 1846). Guatimosim et al. (2015) recollected and epitypified this species and provided a phylogenetic analysis based on LSU sequence data. Inácio & Cannon (2008) recorded the ascostromata of P. styracis as 0.3–1.6 mm in diam.; however, Guatimosim et al. (2015) indicated the epitype having 1–3 mm diam. ascostromata. We also found the ascostromata to be 1–3 mm diam. on the material we examined. The holotype of this species was collected in Brazil on the leaves of Styracis sp. and was deposited in PC ( Index Herbariorum 2018), however, a later specimen collected from same country on same host was examined in this study.

Figures

FIGURE 1. Maximum likelihood phylogenetic tree generated by RAxML (GTR+G model) based on analysis of combined LSU and SSU sequence data. ML values (>50 %) resulting from 1000 bootstrap replicates and Bayesian posterior probabilities greater than 0.80 are given at the nodes. The strain numbers are noted after the species names. The tree is rooted to Dendrographa decolorans (DUKE 0047570).

FIGURE 5. Parmularia styracis (S F21306).A. Herbarium material. B.Appearance of ascostromata on upper of leaf surface.c, e, f. Black shield-like ascostroma. d. Dark brown ascostroma wall. G. Sections of ascostroma showing multi-locules. H. Wall cells of ascostroma. i, j. Asci with ascospores. K. Pseudoparaphyses with brown swollen apices. l–n. Immature hyaline ascospores. Scale bars: b =10 mm, c =1 mm, d = 5 μm, e, f = 500 μm, g=100 μm, h = 50 μm, i–k = 10 μm, l–n = 10 μm.