research article four new species records of umbelopsis

Hindawi Publishing CorporationJournal of MycologyVolume 2013 Article ID 970216 6 pageshttpdxdoiorg1011552013970216

Research ArticleFour New Species Records of Umbelopsis (Mucoromycotina)from China

Ya-ning Wang12 Xiao-yong Liu1 and Ru-yong Zheng1

1 State Key Laboratory of Mycology Institute of Microbiology Chinese Academy of Sciences Beijing 100101 China2University of Chinese Academy of Sciences Beijing 100049 China

Correspondence should be addressed to Xiao-yong Liu liuxiaoyongimaccn

Received 18 January 2013 Accepted 15 April 2013

Academic Editor MarcoThines

Copyright copy 2013 Ya-ning Wang et al This is an open access article distributed under the Creative Commons Attribution Licensewhich permits unrestricted use distribution and reproduction in any medium provided the original work is properly cited

Four species of Umbelopsis newly found in China that is U angularis U dimorpha U nana and U versiformis are reported inthis paper Descriptions and illustrations are provided for each of them

1 Introduction

The genus Umbelopsis Amos and H L Barnett typifiedby U versiformis Amos and H L Barnett was placed inDeuteromycetes by Amos and Barnett in 1966 [1] VonArx [2] proposed that this genus should be classified inZygomycetes in 1982 Meyer and Gams [3] erected the familyUmbelopsidaceae of Mucorales to accommodate it in 2003This family occupies a basal phylogenetic position within theMucorales [4]Members of this genus grow slowly and form avelvety layer sporangiophores typically arise from vesicles onsubstrates cymosely or umbellately branched sporangia areuni- andor multispored and ochraceous reddish or hyalinecolumellae are usually small or absent sporangiospores arevariously shaped and have the same color as the sporangiachlamydospores if present are often abundant and mostlyintercalary on mycelia [3 5ndash8] So far 15 species have beendescribed in this genus 13 of which are accepted by MeyerandGams [3] andMahoney et al [8]Three species have beenrecorded from China by Chen [9] U isabellina (Oudem)W Gams (as Mortierella isabellina Oudem) U ramanniana(Moller)WGams (asM ramanniana (Moller) Linnem) andU vinacea (Dixon-Stew) Arx (asM vinaceaDixon-Stew) Inthis paper four species newly recorded from soil and plantresidues in China are described and illustrated

2 Materials and Methods

Details of materials studied are presented under the descrip-tion of each taxon Strains found in China were isolatedusing the method of Zheng et al [10] For morphologicalobservations fungi grew at 20∘C or 25∘C for 6ndash10 days undernatural light onmalt extract agar ((MEA) 2malt extract 2glucose 01 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 growthtemperatures were tested twice on PDA For inducing theformation of zygospores 01 lecithinwas added to PDA [10]Capitalized color designations refer to the Color Standardsand Color Nomenclature published by Ridgway [11]

3 Taxonomy

31 Umbelopsis angularis WGams ampM Sugiy in Sugiyamaet alMycoscience 44 221 2003 (Figure 1)

Colonies on MEA after 5 days reaching 42mmdiamat 20∘C 1-2mm high flat etruscan red to prussian red(Ridgway Pl XXVII) velvety zonate on CMA after 5days reaching 35mmdiam at 20∘C low hyaline to slightlyvinaceous sparser than on MEA Sporangiophores oftenarising from swollen stalk on substrate mycelia cymosely

2 Journal of Mycology

50120583m

50120583m

25120583m

10120583m

10120583m

10120583m

(a)

(b)

(c)

(d)

(e)

(f)

Figure 1Umbelopsis 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 notethat the position of the uppermost septa is often quite uniform (d) Sporangiospores (e) Macrochlamydospores (f) Microchlamydospores

branched 174ndash379 (ndash442)120583m long 25ndash52 (ndash69)120583m widenear the base and 20ndash30 120583m near the tip 2ndash5 septate withone near the base and the uppermost one at 18ndash30 120583m be-low the columella Sporangia globose to subglobose (10ndash)12ndash25 (ndash27)120583mdiam reddish or reddish-brown multispor-ed walls deliquescent leaving no or small collars Columel-lae globose or depressed globose 20ndash61120583mdiam Sporan-giospores angular 25ndash50120583mdiam reddish inmassChlamy-dospores abundant containing oil droplets of one or twotypes macrochlamydospores 11ndash26120583mdiam usually inter-calary microchlamydospores 5ndash8120583mdiam often terminalZygospores unknown

Maximum growth temperature (35ndash) 36ndash38∘CDistribution China Germany andThe NetherlandsMaterials examined Um-1 (=CGMCC 36640 ITS rDNA

GenBank KC489475) was isolated from Ligusticum chuanx-iong Shennongjia Hubei August 7 1984 Hua-zhongKong 401 Um-2 (=CGMCC 36639 ITS rDNA GenBankKC815992) and Um-9 (=CGMCC 316326 ITS rDNAGenBank KC815994) were isolated from broad-leaved forestsoil Shennongjia Hubei September 4 1984 Hua-zhongKong 601 Um-80 (=CGMCC 316342 ITS rDNA GenBankKC816010) was isolated from soil Temple of Soulrsquos RetreatHangzhou Zhejiang October 14 2000 Long Wang 9683Um-30 (=CGMCC 316335 ITS rDNA GenBank KC816003)Um-39 (=CGMCC 316336 ITS rDNA GenBank KC816004)Um-41 (=CGMCC 316337 ITS rDNA GenBank KC816005)Um-42 (=CGMCC 316338 ITS rDNA GenBank KC816006)Um-43 (=CGMCC 316339 ITS rDNA GenBank KC816007)

Um-44 (=CGMCC 316340 ITS rDNAGenBank KC816008)Um-50 (=CGMCC 316341 ITS rDNA GenBank KC816009)and Um-83 (=CGMCC 316344 ITS rDNA GenBankKC816012) were isolated from mixed forest soil 42∘10101584054810158401015840ndash44∘02101584027410158401015840N 126∘35101584039910158401015840ndash128∘55101584081510158401015840 E alt 360ndash2654mChangbai Mountain Jilin July 2011 Xiao-yong Liu 12447

Note This species is different from the other Umbelopsis spe-cies in possessing distinct columellae and angular sporan-giospores U ramanniana is morphologically most similarto this species except for the shape of sporangiosporeswhich is subglobose to ellipsoid in U ramanniana [5 12]but angular in U angularis There are two more specieshaving angular sporangiospores U dimorpha Mahoney andW Gams and U vinacea (Dixon-Stew) Arx The former isdifferent from U angularis in possessing two types of eachof the sporangiophores sporangia and sporangiospores asdescribed in Section 32 and the latter in lacking distinctcolumellae [7]

32 Umbelopsis dimorpha Mahoney amp W Gams in Ma-honey et alMycol Res 108 (1) 109 2004 (Figure 2)

Colonies on MEA after 5 days reaching 40mmdiamat 25∘C 1ndash3mm high flat or high in the center and lowat the edge pinkish vinaceous (Ridgway Pl XXVII) oftenwith white sectors velvety on CMA after 5 days reaching25mmdiam at 25∘C low hyaline to white or slightly pinkishsparser than on MEA Sporangiophores having two kindsshort and long short sporangiophores often present on

Journal of Mycology 3

25120583m

25120583m

25120583m

25120583m

10120583m

10120583m

10120583m

(a)

(b)

(c)

(d)(e)

(f)

Figure 2 Umbelopsis dimorpha (a) Sporangiophores with various types of branching (b) Long sporangiophores with columellae (c)Short sporangiophores with different types of branching and one-spored sporangiola (d) Short sporangiophores without columellae (e)Multispored sporangia (f) Sporangiospores note that the smaller angular ones are from multispored sporangia and the larger globose onesare from one-spored sporangiola

CMA arising from distinct vesicles on agar surface or aerialhyphae simple or cymosely branched 8ndash26 120583m long 18ndash22 120583m wide near the base and 12ndash16 120583m near the tip longsporangiophores abundant on MEA arising from indistinctvesicles or widened hyphae variously branched (95ndash) 197ndash537 120583m long 22ndash30 (ndash40) 120583m wide near the base and 16ndash24 (ndash32) 120583m near the tip septate with one septum nearthe base and one or none near the columella Sporangiolaon short sporangiophores globose 5ndash8120583mdiam hyalineone-spored sporangiaon long sporangiophores globose 95ndash174 120583mdiam reddish multispored walls slowly deliques-cent leaving no collar Columellae absent on short spo-rangiophores present on long sporangiophores subgloboseand 25ndash52 times 25ndash61120583m Sporangiospores having two kindsglobose and hyaline in one-spored sporangiola on shortsporangiophores 45ndash75120583mdiam angular in multisporedsporangia on long sporangiophores 22ndash4120583mdiam reddishin mass Chlamydospores scarce globose to subglobose 6ndash9times 4ndash9 120583m often intercalary Zygospores unknown

Maximum growth temperature 39∘CDistribution China and New ZealandMaterials examined Um-3 (=CGMCC 36641 ITS rDNA

GenBank KC489477) without substrate information wasisolated more than 20 years ago under the name Umbelopsisvinacea and renamed as U dimorpha in this study Um-8

(=CGMCC 316325 ITS rDNA GenBank KC815993) wasisolated from broad-leaved forest soil Shennongjia HubeiSeptember 4 1984 Hua-zhongKong 601 Um-20 (=CGMCC316329 ITS rDNA GenBank KC815997) Um-21 (=CGMCC316330 ITS rDNA GenBank KC815998) Um-22 (=CGMCC316331 ITS rDNA GenBank KC815999) Um-23 (=CGMCC316332 ITS rDNA GenBank KC816000) Um-24 (=CGMCC316333 ITS rDNA GenBank KC816001) and Um-25(=CGMCC 316334 ITS rDNA GenBank KC816002) wereisolated from mixed forest soil 42∘10101584054810158401015840ndash44∘02101584027410158401015840N126∘35101584039910158401015840ndash128∘55101584081510158401015840 E alt 360ndash2654m ChangbaiMountain Jilin July 2011 Xiao-yong Liu 12447

Note This species is distinct from the other Umbelopsisspecies by having two kinds of each of the sporangiophoressporangia and sporangiospores It produces mainly multi-spored sporangia onMEA asU vinacea does while on CMAa number of unispored sporangiola similar to those in Uversiformis are abundantly formed [1 3 7] The number ofsporangiospores in sporangia on CMA tends to decrease dueto hypotrophy sometimes containing only three

33 Umbelopsis nana (Linnem) Arx Sydowia 35 20 1982(Figure 3)equiv Mortierella nana Linnem Pflanzenforschung 23 16

1941 (basionym)


25120583m

10120583m

(a)

(b)

(c)10120583m

Figure 3 Umbelopsis nana (a) Sporangiophores with differentbranching types and one-spored sporangiola (b) Sporangiophores(c) Sporangiospores

= M alba Manka amp Gierczak Prace Komisji NaukRolniczych i Komisji Nauk Lesnych 9 17 1961

Colonies on MEA after 5 days reaching 42mmdiamat 25∘C 2-3mm high high in the center and low at theedge white velvety obscurely zonate on CMA after 5 daysreaching 28mmdiam at 25∘C low hyaline sparser thanon MEA Sporangiophores often umbellately branched fromdistinct vesicles on agar surface or simply branched onaerial hyphae (12ndash) 15ndash50 (ndash55) 120583m long 24ndash36 120583m widenear the base and 16ndash22120583m near the tip with one sep-tum near the base Sporangiola globose or subglobose 49ndash79 120583mdiam hyaline one-spored containing oil dropletsCollars absent or small Columellae absent Sporangiosporesglobose 45ndash75120583mdiam hyaline containing oil dropletsChlamydospores scarce to absent 4ndash9 times 6ndash9120583m Zygosporesunknown

Maximum growth temperature 37∘CDistribution Belgium Britain Canada China Denmark

Germany Japan Poland Russia Sweden The NetherlandsUkraine and USA

Material examined Um-82 (=CGMCC 316343ITS rDNA GenBank KC816011) was isolated from soil underherbaceous ferns Nanyigou Milin Tibet August 4 2009Xue-wei Wang 12608

Note This species is distinct from the other Umbelopsisspecies by white colonies and unispored sporangiola It ismorphologically similar to U versiformis and the differencebetween them will be discussed in the following section

34 Umbelopsis versiformis AmosampH L BarnettMycologia58(5) 807 1966 (Figure 4)

= Mortierella roseonana W Gams amp Gleeson in GamsPersoonia 9 112 1976equivU roseonana (W Gams ampGleeson) Arx Sydowia 35 19

1982Colonies on MEA after 5 days reaching 45mmdiam at

25∘C 1-2mm high flat at first white and then pale vinaceous(Ridgway Pl XXVII) velvety obviously zonate on CMAafter 5 days reaching 26mmdiam at 25∘C low hyalinesparser than on MEA Sporangiophores often arising fromdistinct vesicles on agar surface or aerial hyphae simpleto successively umbellately branched (10ndash) 15ndash35 (ndash45) 120583mlong 18ndash30 120583m wide near the base and 16ndash22 120583m near thetip with one septum near the base Sporangiola globose orsubglobose 47ndash79120583mdiam hyaline one-spored contain-ing oil droplets Collars absent or small Columellae absentSporangiospores globose 43ndash75 120583mdiam hyaline contain-ing oil droplets Chlamydospores not abundant subglobose6 120583mdiam Zygospores unknown

Maximum growth temperature 38∘CDistribution Australia China and USAMaterials examined CBS 15081 (ITS rDNA GenBank

KC489496) roots of a red oak tree (Quercus borealisMichx)Pendleton County WV USA Um-11 (=CGMCC 316327ITS rDNA GenBank KC815995) and Um-19 (=CGMCC316328 ITS rDNA GenBank KC815996) were isolated frommixed forest soil 42∘10101584054810158401015840ndash44∘02101584027410158401015840N 126∘35101584039910158401015840ndash128∘55101584081510158401015840 E alt 360ndash2654m Changbai Mountain JilinJuly 2011 Xiao-yong Liu 12447NoteThe color of colonies is white in the original descriptionof Umbelopsis versiformis [1] However the extype strainCBS 15081 is really white at first but then changes to palevinaceous when it is reexamined on MEA medium in thisstudy Meyer and Gams [3] also noticed the pale pinkpigmentation of CBS 15081 The colonial color of the twoChinese isolates of U versiformis Um-11 and Um-19 is alittle lighter than that of CBS 15081 which might reflectthe geographic differences within the circumscription of aspecies A few chlamydospores are found in both the extypestrain CBS 15081 and the two Chinese isolates though theoriginal description did not mention this trait [1]

Umbelopsis versiformis is close to U nana and the mostremarkable shared characteristic is the one-spored sporan-giola Furthermore the colony color of U nana is alwayswhite and similar to that of U versiformis in its protologue[1] Maybe for these reasons they were synonymized by vonArx [2] However the different color of old colonies whitein U nana and vinaceous or pinkish in U versiformis wasdiscovered in this study and also by Meyer and Gams [3]Besides they disclosed that U nana is different from Uversiformis in ITS rDNA sequences and RFLP data Based onall these differences this study agrees with the treatment ofMeyer and Gams [3] to retain them as different species

4 Conclusions

Four species were recorded in the present study raising thenumber of Umbelopsis species in China to seven More than


25120583m10120583m

(a)

(b)(c)

25120583m

25120583m

10120583m

(d)(e)

Figure 4 Umbelopsis versiformis (a) (b) Sporangiophores showing branching types and one-spored sporangiola (c) Sporangiophores (d)Sporangiospores (e) Chlamydospores

half of the total number of Umbelopsis species worldwidecould be proven to exist in China so far

Acknowledgments

The project was supported by the National Natural ScienceFoundation of China (nos 31070016 and 31070019) CBS isgratefully acknowledged for supplying cultures used in thisstudy The authors thank Ms Hong-mei Liu of this researchgroup for her assistance with mating experiments They alsothank Ms Xing-xian Wang for her help in improving theline drawings Special thanks are due to authorsrsquo colleagueProfessor Yi-jian Yao for acting as a presubmission reviewer

References

[1] R E Amos and H L Barnett ldquoUmbelopsis versiformis a newgenus and species of the imperfectsrdquoMycologia vol 58 pp 805ndash808 1966

[2] J A von Arx ldquoOn Mucoraceae s str and other families of theMucoralesrdquo Sydowia vol 35 pp 10ndash26 1982

[3] W Meyer and W Gams ldquoDelimitation of Umbelopsis (Muco-rales Umbelopsidaceae fam nov) based on ITS sequence andRFLP datardquo Mycological Research vol 107 no 3 pp 339ndash3502003

[4] M M White T Y James K OrsquoDonnell M J Cafaro YTanabe and J Sugiyama ldquoPhylogeny of the Zygomycota basedon nuclear ribosomal sequence datardquo Mycologia vol 98 no 6pp 872ndash884 2006

[5] G Linnemann ldquoMortierella Coemans 1863rdquo in Mucorales HZycha and R Siepmann Eds pp 155ndash241 J Cramer LehreGermany 1969

[6] M Turner ldquoStudies in the genusMortierella IMortierella isabel-lina and related speciesrdquo Tansactions of the British MycologicalSociety vol 46 pp 262ndash272 1963

[7] M Sugiyama S Tokumasu and W Gams ldquoUmbelopsis gib-berispora sp nov from Japanese leaf litter and a clarification ofMicromucor ramannianus var angulisporusrdquo Mycoscience vol44 no 3 pp 217ndash226 2003

[8] D Mahoney W Gams W Meyer and M Starink-WillemseldquoUmbelopsis dimorpha sp nov a link between U vinacea andU versiformisrdquoMycological Research vol 108 no 1 pp 107ndash1112004


[9] F J Chen ldquoMortierella species in Chinardquo Mycosystema vol 5pp 23ndash64 1992

[10] R Y Zheng G Q Chen H Huang and X Y Liu ldquoA mono-graph of Rhizopusrdquo Sydowia vol 59 no 2 pp 273ndash372 2007

[11] R Ridgway Color Standards and Color Nomenclature RobertRidgway Washington DC USA 1912

[12] Y Ogawa M Sugiyama D Hirose K Kusama-Eguchi andS Tokumasu ldquoPolyphyly of intraspecific groups of Umbelopsisramanniana and their genetic and morphological variationrdquoMycoscience vol 52 no 2 pp 91ndash98 2011

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50120583m

50120583m

25120583m

10120583m

10120583m

10120583m

(a)

(b)

(c)

(d)

(e)

(f)

Figure 1Umbelopsis 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 notethat the position of the uppermost septa is often quite uniform (d) Sporangiospores (e) Macrochlamydospores (f) Microchlamydospores

branched 174ndash379 (ndash442)120583m long 25ndash52 (ndash69)120583m widenear the base and 20ndash30 120583m near the tip 2ndash5 septate withone near the base and the uppermost one at 18ndash30 120583m be-low the columella Sporangia globose to subglobose (10ndash)12ndash25 (ndash27)120583mdiam reddish or reddish-brown multispor-ed walls deliquescent leaving no or small collars Columel-lae globose or depressed globose 20ndash61120583mdiam Sporan-giospores angular 25ndash50120583mdiam reddish inmassChlamy-dospores abundant containing oil droplets of one or twotypes macrochlamydospores 11ndash26120583mdiam usually inter-calary microchlamydospores 5ndash8120583mdiam often terminalZygospores unknown

Maximum growth temperature (35ndash) 36ndash38∘CDistribution China Germany andThe NetherlandsMaterials examined Um-1 (=CGMCC 36640 ITS rDNA

GenBank KC489475) was isolated from Ligusticum chuanx-iong Shennongjia Hubei August 7 1984 Hua-zhongKong 401 Um-2 (=CGMCC 36639 ITS rDNA GenBankKC815992) and Um-9 (=CGMCC 316326 ITS rDNAGenBank KC815994) were isolated from broad-leaved forestsoil Shennongjia Hubei September 4 1984 Hua-zhongKong 601 Um-80 (=CGMCC 316342 ITS rDNA GenBankKC816010) was isolated from soil Temple of Soulrsquos RetreatHangzhou Zhejiang October 14 2000 Long Wang 9683Um-30 (=CGMCC 316335 ITS rDNA GenBank KC816003)Um-39 (=CGMCC 316336 ITS rDNA GenBank KC816004)Um-41 (=CGMCC 316337 ITS rDNA GenBank KC816005)Um-42 (=CGMCC 316338 ITS rDNA GenBank KC816006)Um-43 (=CGMCC 316339 ITS rDNA GenBank KC816007)

Um-44 (=CGMCC 316340 ITS rDNAGenBank KC816008)Um-50 (=CGMCC 316341 ITS rDNA GenBank KC816009)and Um-83 (=CGMCC 316344 ITS rDNA GenBankKC816012) were isolated from mixed forest soil 42∘10101584054810158401015840ndash44∘02101584027410158401015840N 126∘35101584039910158401015840ndash128∘55101584081510158401015840 E alt 360ndash2654mChangbai Mountain Jilin July 2011 Xiao-yong Liu 12447

Note This species is different from the other Umbelopsis spe-cies in possessing distinct columellae and angular sporan-giospores U ramanniana is morphologically most similarto this species except for the shape of sporangiosporeswhich is subglobose to ellipsoid in U ramanniana [5 12]but angular in U angularis There are two more specieshaving angular sporangiospores U dimorpha Mahoney andW Gams and U vinacea (Dixon-Stew) Arx The former isdifferent from U angularis in possessing two types of eachof the sporangiophores sporangia and sporangiospores asdescribed in Section 32 and the latter in lacking distinctcolumellae [7]

32 Umbelopsis dimorpha Mahoney amp W Gams in Ma-honey et alMycol Res 108 (1) 109 2004 (Figure 2)

Colonies on MEA after 5 days reaching 40mmdiamat 25∘C 1ndash3mm high flat or high in the center and lowat the edge pinkish vinaceous (Ridgway Pl XXVII) oftenwith white sectors velvety on CMA after 5 days reaching25mmdiam at 25∘C low hyaline to white or slightly pinkishsparser than on MEA Sporangiophores having two kindsshort and long short sporangiophores often present on


25120583m

25120583m

25120583m

25120583m

10120583m

10120583m

10120583m

(a)

(b)

(c)

(d)(e)

(f)








1941 (basionym)


25120583m

10120583m

(a)

(b)

(c)10120583m















4 Conclusions



25120583m10120583m

(a)

(b)(c)

25120583m

25120583m

10120583m

(d)(e)



Acknowledgments


References





















Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology


25120583m

25120583m

25120583m

25120583m

10120583m

10120583m

10120583m

(a)

(b)

(c)

(d)(e)

(f)








1941 (basionym)


25120583m

10120583m

(a)

(b)

(c)10120583m















4 Conclusions



25120583m10120583m

(a)

(b)(c)

25120583m

25120583m

10120583m

(d)(e)



Acknowledgments


References





















Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology


25120583m

10120583m

(a)

(b)

(c)10120583m















4 Conclusions



25120583m10120583m

(a)

(b)(c)

25120583m

25120583m

10120583m

(d)(e)



Acknowledgments


References





















Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology


25120583m10120583m

(a)

(b)(c)

25120583m

25120583m

10120583m

(d)(e)



Acknowledgments


References





















Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology













Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology

research article four new species records of umbelopsis

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