Four New Species Records of Umbelopsis ( Mucoromycotina ) from China

The genus Umbelopsis Amos and H. L. Barnett, typified by U. versiformis Amos and H. L. Barnett, was placed in Deuteromycetes by Amos and Barnett in 1966 [1]. Von Arx [2] proposed that this genus should be classified in Zygomycetes in 1982. Meyer and Gams [3] erected the family Umbelopsidaceae of Mucorales to accommodate it in 2003. This family occupies a basal phylogenetic position within the Mucorales [4].Members of this genus grow slowly and form a velvety layer; sporangiophores typically arise from vesicles on substrates, cymosely or umbellately branched; sporangia are uniand/or multispored and ochraceous, reddish, or hyaline; columellae are usually small or absent; sporangiospores are variously shaped and have the same color as the sporangia; chlamydospores, if present, are often abundant and mostly intercalary on mycelia [3, 5–8]. So far, 15 species have been described in this genus, 13 of which are accepted by Meyer andGams [3] andMahoney et al. [8].Three species have been recorded from China by Chen [9]: U. isabellina (Oudem.) W. Gams (as Mortierella isabellina Oudem.), U. ramanniana (Möller)W.Gams (asM. ramanniana (Möller) Linnem.), and U. vinacea (Dixon-Stew.) Arx (asM. vinaceaDixon-Stew.). In this paper, four species newly recorded from soil and plant residues in China are described and illustrated. 2. Materials and Methods


Introduction
The genus Umbelopsis Amos and H. L. Barnett, typified by U. versiformis Amos and H. L. Barnett, was placed in Deuteromycetes by Amos and Barnett in 1966 [1].Von Arx [2] proposed that this genus should be classified in Zygomycetes in 1982.Meyer and Gams [3] erected the family Umbelopsidaceae of Mucorales to accommodate it in 2003.This family occupies a basal phylogenetic position within the Mucorales [4].Members of this genus grow slowly and form a velvety layer; sporangiophores typically arise from vesicles on substrates, cymosely or umbellately branched; sporangia are uni-and/or multispored and ochraceous, reddish, or hyaline; columellae are usually small or absent; sporangiospores are variously shaped and have the same color as the sporangia; chlamydospores, if present, are often abundant and mostly intercalary on mycelia [3,[5][6][7][8].So far, 15 species have been described in this genus, 13 of which are accepted by Meyer and Gams [3] and Mahoney et al. [8].Three species have been recorded from China by Chen [9]: U. isabellina (Oudem.)W. Gams (as Mortierella isabellina Oudem.),U. ramanniana (Möller) W. Gams (as M. ramanniana (Möller) Linnem.), and U. vinacea (Dixon-Stew.)Arx (as M. vinacea Dixon-Stew.).In this paper, four species newly recorded from soil and plant residues in China are described and illustrated.

Materials and Methods
Details of materials studied are presented under the description of each taxon.Strains found in China were isolated using the method of Zheng et al. [10].For morphological observations, fungi grew at 20 ∘ C or 25 ∘ C for 6-10 days under natural light on malt extract agar ((MEA) 2% malt extract, 2% glucose, 0.1% peptone, and 2% agar), cornmeal agar ((CMA) 2% cornmeal and 2% agar), and potato dextrose agar ((PDA) 20% potato, 2% glucose, and 2% agar).Maximum growth temperatures were tested twice on PDA.For inducing the formation of zygospores, 0.1% lecithin was added to PDA [10].Capitalized color designations refer to the Color Standards and Color Nomenclature published by Ridgway [11].Colonies on MEA after 5 days reaching 42 mm diam.at 20 ∘ C, 1-2 mm high, flat, etruscan red to prussian red (Ridgway, Pl.XXVII), velvety, zonate; on CMA after 5 days reaching 35 mm diam.at 20 ∘ C, low, hyaline to slightly vinaceous, sparser than on MEA.Sporangiophores often arising from swollen stalk on substrate mycelia, cymosely branched, 174-379 (-442) m long, 2.5-5.2(-6.9) m wide near the base, and 2.0-3.0 m near the tip, 2-5 septate, with one near the base and the uppermost one at 18-30 m below the columella.Sporangia globose to subglobose, (10-) 12-25 (-27) m diam., reddish or reddish-brown, multispored; walls deliquescent, leaving no or small collars.Columellae globose or depressed globose, 2.0-6.1 m diam.Sporangiospores angular, 2.5-5.0 m diam., reddish in mass.Chlamydospores abundant, containing oil droplets, of one or two types: macrochlamydospores 11-26 m diam., usually intercalary; microchlamydospores 5-8 m diam., often terminal.Note.This species is different from the other Umbelopsis species in possessing distinct columellae and angular sporangiospores.U. ramanniana is morphologically most similar to this species, except for the shape of sporangiospores which is subglobose to ellipsoid in U. ramanniana [5,12] but angular in U. angularis.There are two more species having angular sporangiospores, U. dimorpha Mahoney and W. Gams and U. vinacea (Dixon-Stew.)Arx.The former is different from U. angularis in possessing two types of each of the sporangiophores, sporangia, and sporangiospores as described in Section 3.2 and the latter in lacking distinct columellae [7].Colonies on MEA after 5 days reaching 40 mm diam.at 25 ∘ C, 1-3 mm high, flat or high in the center and low at the edge, pinkish vinaceous (Ridgway, Pl.XXVII), often with white sectors, velvety; on CMA after 5 days reaching 25 mm diam.at 25 ∘ C, low, hyaline to white or slightly pinkish, sparser than on MEA.Sporangiophores having two kinds, short and long: short sporangiophores often present on Note.This species is distinct from the other Umbelopsis species by having two kinds of each of the sporangiophores, sporangia and sporangiospores.It produces mainly multispored sporangia on MEA as U. vinacea does, while on CMA a number of unispored sporangiola similar to those in U. versiformis are abundantly formed [1,3,7].The number of sporangiospores in sporangia on CMA tends to decrease due to hypotrophy, sometimes containing only three.Colonies on MEA after 5 days reaching 42 mm diam.at 25 ∘ C, 2-3 mm high, high in the center and low at the edge, white, velvety, obscurely zonate; on CMA after 5 days reaching 28 mm diam.at 25 ∘ C, low, hyaline, sparser than on MEA.Sporangiophores often umbellately branched from distinct vesicles on agar surface or simply branched on aerial hyphae, (12-) 15-50 (-55) m long, 2.4-3.6 m wide near the base, and 1.6-2.2m near the tip, with one septum near the base.Sporangiola globose or subglobose, 4.9-7.9m diam., hyaline, one-spored, containing oil droplets.Collars absent or small.Columellae absent.Sporangiospores globose, 4.5-7.5 m diam., hyaline, containing oil droplets.Chlamydospores scarce to absent, 4-9 × 6-9 m.Zygospores unknown.
Note.This species is distinct from the other Umbelopsis species by white colonies and unispored sporangiola.It is morphologically similar to U. versiformis, and the difference between them will be discussed in the following section.Note.The color of colonies is white in the original description of Umbelopsis versiformis [1].However, the extype strain CBS 150.81 is really white at first but then changes to pale vinaceous when it is reexamined on MEA medium in this study.Meyer and Gams [3] also noticed the pale pink pigmentation of CBS 150.81.The colonial color of the two Chinese isolates of U. versiformis, Um-11 and Um-19, is a little lighter than that of CBS 150.81, which might reflect the geographic differences within the circumscription of a species.A few chlamydospores are found in both the extype strain CBS 150.81 and the two Chinese isolates, though the original description did not mention this trait [1].
Umbelopsis versiformis is close to U. nana, and the most remarkable shared characteristic is the one-spored sporangiola.Furthermore, the colony color of U. nana is always white and similar to that of U. versiformis in its protologue [1].Maybe for these reasons, they were synonymized by von Arx [2].However, the different color of old colonies, white in U. nana and vinaceous or pinkish in U. versiformis, was discovered in this study and also by Meyer and Gams [3].Besides, they disclosed that U. nana is different from U. versiformis in ITS rDNA sequences and RFLP data.Based on all these differences, this study agrees with the treatment of Meyer and Gams [3] to retain them as different species.

Conclusions
Four species were recorded in the present study, raising the number of Umbelopsis species in China to seven.More than half of the total number of Umbelopsis species worldwide could be proven to exist in China so far.

Figure 1 :
Figure 1: Umbelopsis angularis.(a) Sporangiophores with various types of branching.(b) Branching pattern of lower parts of sporangiophores.(c) Sporangiophores with different sizes and shapes of columellae at their tips after the sporangia have been dissolved or detached; also note that the position of the uppermost septa is often quite uniform.(d) Sporangiospores.(e) Macrochlamydospores. (f) Microchlamydospores.