Bull. Natn. Sci. Mus., Tokyo, Ser. B, 26( I), pp. 23- 34, March 23 , 2000

Smut Fungi from Yunnan Province, China, Collected in 1998*
Makoto Kakishimal, Cvetomir M. Denchev 2, Xuan Zhou 3 and Mu Zang3
1

Institute of Agriculture and Forestry, University ofTsukuba ,Tsukuba, fbaraki 305-8572, Japan
2
Institute of Botany, Bulgarian Academy of Sciences,
23 Acad. G. Bonchev Str. , BG-1113 Sofia, Bulgaria
3Kunming Institute of Botany, Academia Sinica,Kunming, Yunnan 650204, China

Abstract Seven species of smut fungi are reported based on the specimens collected during Botanical Expedition to Yunnan, China in 1998. Among these species, Microbo!ly um cordae, M. nepalense, M. polygoni-alati and Sphacelotheca polygonisenticosi were newly recorded from Yunnan Province. New host plants were also reported in Liroa emodensis, Microbotryum cordae and Sphacelotheca polygoni-senti-cosi.
Key words: Liroa , Microbotryum , Sphacelotheca, smut fungi, Ustilaginomycetes,
Ustilago, Yunnan

Previous compilations of published records included about 190 species of smut
fungi belonging to 24 genera from China (Ling, 1953 ; Wang, 1963 ; Tai, 1979; Guo,1992). Among them , only about 30 species have been reported in Yunnan. However,we believe that more smut fungi are distributed in this area and these species parasitize on many host plant species since vegetation of this area is very rich and diverse.
Therefore, more extensive field survey and collections are required for better understanding of the flora of smut fungi .
We report here I species of Ustilago, I species of Liroa, 3 species of Microbotryum and 2 species of Sphacelotheca based on the specimens collected during Botanical Expedition carried out mainly in Zhantong and Nujiang Districts, Yunnan
Province, China in 1998. Among 7 species of smut fungi reported here, Microbotryum cordae, M. nepalense, M. polygoni-alati and Sphacelotheca polygoni-senticosi
were newly recorded from Yunnan Province. New host plants were also reported inLiroa emodensis, Microbotryum corda e and Sphacelotheca polygoni-senticosi.

* Contributi on No. 149, Laboratory of Plant Pathology and Mycology, Institute of Agriculture andForestry, University ofTsukuba.

24M. Kakishima et al.

Materials and Methods
The dry specimens were examined under light (LM) and scanning electron microscopy (SEM). For LM observations, the ustilospores were mounted in lactopheno lsolution on glass slides by gently heating to the boiling point and then cooling. The
measurements of ustilospores were given in the form: min-m ax (mean±standard deviation). In the description , a symbol 'nix=' was used to indicate the total numbersof measured specimens and ustilospores, respectively. For SEM, the ustilospores wereattached to specimen holders by double-sided adhesive tape and coated with platinum-palladium with H itachi E-1 030 Ion Sputter. The surface structure ofustilospores was observed with a Hitachi S-4200 SEM .
All the specimens cited in this paper were deposited in the following herbaria:
the Mycological Herbarium of the Institute of Agriculture and Forestry of Universityof Tsukuba, Japan (TSH) , the Mycological Herbarium , Department of Botany, National Science Museum , Tokyo, Japan (TNS), the Cryptogamic Herbarium , Kunming
Institute of Botany, Kunming, China (HKAS), the Mycological Herbarium , the lnstiture of Microbiology, Academia Sinica, Beijing, China (HMAS).

Enumeration of Species
Fam. Usti laginaceae
I. Ustilago maydis (DC.) Corda, !cones Fung. , 5: 3, 1842.
(Fig. I)
Sori in various parts of the host (stems, leaves, male and female inflorescences),
evident as small to large (sometimes more than I 0 cm long) , irregular galls, at firstcovered by a thin , si lvery, later brown peridium which ruptures irregularly to expose
the spore mass. Spore mass powdery, dark brown. Ustilospores globose, subgloboseor ovoid, sometimes slightly irregular, 10- 14.5X9-13 (12.0±0.8X 11.2±0.8) pm(n/1 = 100), reddish-brown ; wa ll (without ornaments) 0.5- 0 .7 pm thick, rather densely echinate; the spines 0.6- 1.5 pm high , under SEM interspersed with a few minutewarts.
Specimen examined: on Zea mays L. (cult.) , Yunnan Province, Zhaotong District, near Mugan, Sept. 19, 1998, leg. M. Kakishima, CH-40 (TSH-S 1107, TNS-F107954 , HKAS 34499, HMAS).
Hosts and distribution : Euchlaena spp. and Zea mays L. , worldwide.
Fam. Microbotryaceae
2. Liroa emodensis (Berk.) Cif., Nuovo Giorn. Bot. !tal. , N. S., 40: 264, 1933. (Fig. 2)
Sori in the flowers , irregularly globose, up to 7 mm in diameter, at first coveredby a hard peridium and greenish, later purplish . Spore mass powdery, purple slate,Smu t fungi from Yunnan , Chi na25

Fig. I. Ustilago may dis on Zea mays (TSH-S 11 07). A. Sori in flowers. B. Usti lospores observed
by LM. C. Usti lospores observed by SEM. Bar: A = 20 mm, B= IO,um, C=2,um.

intermixed with poorly ramified, irregular filaments of host tissue ongm.
Ustilospores globose, subglobose or ovoid, 6- 9.5 X 5.5- 9 (7.2±0.6X6.7±0.6) J..lm(n/ 1=5 0), unusually elongate ones up to 11 J..lm in length, light brown; wall reticulate,under SEM finely and densely irregularly reticulate, 12- 16 meshes per spore diameter, under lower magnifications the spore profile appearing as verruculose.
Specimen examined: on Persicaria nepalensis (Meisn.) H. Gross (=Polygonurn nepalense Meisn.) , Yunnan Province, Nujiang District, Pianma, N 25°59'429" E98°39'750", alt. 2335 m, Sept. 29, 1998, leg. M. Kakishima, CH-146 (TSH-S 1115,TNS-F-107955, HKAS 34507, HMAS).
Hosts and distribution : Persicaria spp. , South and Southeast Asia (India ,Nepal, Mainland and Taiwan of China, Sri Lanka, Indonesia, Philippines).
Liroa emodensis has been reported from China only from Yunnan Province on Pchinensis (L.) Nakai (=Polygonum chinense L.) (Wang, 1963 ; Guo, 1988). Persicaria
nepalensis is a new host for this smut fungus. The ustilospore variability of both

26

M. Kaki shima et al.

Fig. 2. Liroa emodensis on Persicaria nepalensis (TSH-S IllS ). A. Sori in flowers. B.
Ustilospores observed by SEM . Bar: A = 10 mm , B = 2.um.

length (CV=8.3%) and width (8.9%) is at a modal level (5 . 1- 10%, Denchev, 1993).
Because Ling ( 1953 : 3 19) showed high variabi lity of the spore size, additional specimens from Taiwan, India and Sri Lanka were investigated. The spores of all investigated specimens are more or less uniform and the variability of the length and width
is at a modal level , excluding the length of the specimen from Sri Lanka with variability evaluated at an increased degree (I 0.1 - 15%). The spore mass colour of all
specimens is purple slate.
Further specimens on P. chinensis examined: Taiwan, Apr. 12, 1924, K.
Sawada (SAPA), stem (obtained spore measurements) and floral infection,
ustilospores 6.5- 8.5 X6- 7.5 (7.2±0.4 X6.7±0.4)pm (n/1 =30), CV=5 .5%, respectively 6.0%; India, Tamil Nadu , Mt. Palni Hills, pr. pag. Kadaikanal , alt. 1200-1600m, Jan. 29, 1980, K. Vanky (Vanky, Ust. 399), floral infection, ustilospores 7- 9X6-8(7.8±0.4X7.3±0.4) pm (n/ 1=30), CV=5.1%, respectively 5.5%; Sri Lanka, Mt. Totapola, pr. oppid. Nuwara Eliya, alt. ea. 1800 m, Mar. 18, 1975, K. Vanky (Vanky,Ust. 181), floral infection, ustilospores 6.5- 9.5 X6- 8 (7.8±0.8 X7.0±0.5)(ni l =30), CV = I 0.3 %, respectively 7.1 % .

.urn

3. Microbotryum cordae (Liro) G. Deml & Prillinger in Prillinger et al. , Bot. Acta,
104: I 0, 1991 (sensu fat ., incl. Ustilago bungeana W. Y. Yen) .
(Fig. 3)
Sori in the swollen and deformed flowers , protected by the perianths, filled by apowdery, dark reddish-brown spore mass. Infection systemic. Ustilospores globose,subglobose, ovoid or broadly ellipsoidal, 9.5- 13 X8.5- 12.5 (11.3±0.7 X 10.5±0.7)

Smut fungi from Yunnan , C hina27Fig. 3. Microbot1y um cordae on Persicaria y okusaiana (TSH-S ll 09). A. Sori in flowers. B.
Ustilospores observed by LM . C. Ustilospores observed by SEM. Bar: A = 5 mm , B = l 0 ,urn,
C= 2,um.

J..Lm (n/1 =50), light yellowish-brown; wall reticulate; 4- 6 meshes per spore diameter,
muri 0.9-1.2 J..Lm high, under SEM the interspace of the meshes with a coarsely verrucose tuberculum.
Specimen examined: on Persicaria y okusaiana (Makino) Nakai ( =Polygonum
caespitosum Blume), Yunnan Province, Zhaotong District, Yiliang, Xiaocaoba, N
27°47'391" E 104° 14'437", alt. 1760m, Sept. 17, 1998, leg. M. Kakishima, CH-18/2(TSH-S1109, TNS-F-107956, HMAS).
Hosts and distribution : Persicaria spp., worldwide.
This species is a new one for the Yunnan Province. Persicaria y okusaiana is a
new host for this smut fungus.

28

M. Kaki shima e/ al.

Fig. 4. Microbolry um nepalense on Persicaria nepalensis (TSH-S 1113). A. Sari in stems. B, C.
Usti lospores observed by SEM. Bar: A = I 0 mm , B = I J.im , C =3 J.lm.

Smut fungi from Yunn an, China

294. Microbotryum nepalense (Liro) Vanky, Mycotaxon, 67:47 , 1998.
(Fig. 4)
Sori as spindle-shaped, 0.8- 2 cm long swellings in the stems, situated closely
below the intact inflorescence. Spore mass powdery, dark reddish-brown ; numerous
fibrous fascicles of host tissue origin through the spore mass present. Ustilospores
subglobose, globose or ovoid, rarely broadly ellipsoidal , 10.5- 13.5 X 10- 12( 12.0±0.6 X 11.0±0.5) J..Lm (n/ 1=50); wall very finely and densely reticulate, sometimes incompletely reticulate; I 0- 15 meshes per spore diameter, muri low (0.3- 0.6J..Lm), under SEM the interspace of the meshes verruculose, under lower magnifications the spore profile is finely serrulate.
Specimen examined: on Persicaria nepalensis (Meisn.) H. Gross (=Polygonurn nepalense Meisn.), Yunnan Province, Nujiang District, Pianma, N 25°59'429" E
98°39'750", alt. 2335 m, Sept. 29, 1998, leg. M. Kakishima, CH-14511 (TSH-S 1113 ,TNS-F-107957 , HKAS 34505 , HMAS).
Host and distribution: Persicaria nepalensis (Meisn.) H. Gross, Asia (China,Nepal , Pakistan, India, Tadzhikistan, Japan , Far East of Russia).
This species is a new one for the Yunnan Province.
5. Microbotryum polygoni-alati (Thirum. & Pavgi emend. L. Guo) Vanky, Mycotaxon, 67: 49, 1998.
(Fig. 5)Sori in the flowers as globoid or reniform swellings, a few mm up to I cm long,at first covered by a greenish, later to rosy vinaceous membrane which ruptures irregularly to expose the spore mass. Spore mass powdery, dark purple. Ustilospores subglobose, broadly ellipsoidal or globose, 9.5- 13 X9.5- 12 (11.5 ± 0.6 X 10.9±0.6) J..Lm(n/1 = 50), light reddish-brown; wall ea. I J..Lm thick, reticulate, sometimes incompletely reticulate, under SEM with tubercles on the muri ; interspace of the meshes tuberculate and foveolate (0- 3, sometimes up to 5 cavities per interspace).
Specimen examined: on Persicaria nepalensis (Meisn .) H. Gross (=Polygonurn nepalense Meisn.), Yunnan Province, Nujiang District, Pianma, N 25°59 '429" E
98°39 ' 750", alt. 2335 m, Sept. 29, 1998, leg. M. Kakishima, CH-145/2 (TSH-S 1114,TNS-F-107958, HKAS 34506, HMAS).
Host and distribution: Persicaria nepalensis (Meisn.) H. Gross, China, India.
This species has been previously recorded from China only once (Sichuan: Guo ,1993). The present record is a new one for the Yunnan Province.
6. Sphacelotheca hydropiperis (Schumach.) De Bary, Vergl. Morphol. Bioi. Pilze,Mycetozoen & Bact. , p. 187, 1884.
(Figs. 6 and 7)
Sori in the swollen ovaries, forming oblong or ovate bodies, 2.5-4 mm in length,
at first covered by a greyish-brown peridium; with a central columella. Spore masspowdery, dark purplish-brown or purple slate; sterile cells usually present amongst
the ustilospores being derived from the peridium or columella. Infection systemic.
Sterile cells of the peridium and columella variable in shape and size, globose, sub-30M. Kaki shima et al.

Fig. 5. Microbot1ywn polygoni-alati on Persicaria nepalensis (TSH-Slll4). A. Sori in flowers.
B, C. Ustilospores observed by SEM. Bar: A = IOmm, B = l,Um , C=S.um.

Smut fun gi from Yunnan , C hin a31Fi g. 6. Sphacelotheca hydropiperis on Persicaria aff. praetermissa (TSH-S Ill 0). A. Sori infl owers. B. Ustilospores observed by SEM. Bar: A= I 0 mm , B = 2 pm.

globose, broadly ellipsoidal, or slightly irregular, 7- 13 .5 X5.5-11.5 J..lm, smaller thanor equal to the size of the ustilospores, hyaline. Ustilospores more or less flattened, inplane view subcircular, broadly elliptical, ovate or slightly irregular, 9- 16.5 X 8-14.5( 11.8::1::: I. OX I 0.5 ::1:::0.9) J..lm (n/3 =!50); middle reddish-brown; wall verruculose,
often some warts connecting (2 or 3 warts per group). Young spores near the base of
the sorus in chains, separated by small disjunctors. Mature spores single; the disjunctors remaining as small , hyaline, oppositely situated appendages.
Specimens examined: on Persicaria aff. praetermissa Hook. f. , Yunnan
Province, Zhaotong District, Mugan , Sanchanco, N 28° 12 '6 10" E 103°56'686", alt.
1695- 1720 m, Sept. 20, 1998, leg. M. Kakishima, CH-41 (TSH-S Ill 0, TNS-F107959, HKAS 34502, HMAS); on P hy dropiper (L.) Spach (=Polygonum hy dropiper L.), Yunnan Province, Nujiang District, Pianma, N 26°00'561" E
98°37'524' , alt. 1987m, Sept. 28, 1998, leg. M. Kakishima, CH-97 (TSH-Slll2,TNS-F-107960, HKAS 34504, HMAS); Yunnan Province, Zhaotong District,Mugan , Sanchanco, N 28° 13'778" E 103°56'710", alt. 1700- 1885m, Sept. 21, 1998,
leg. M. Kakishima, CH-65 (TSH-Sllll , TNS-F-107961 , HMAS).
Hosts and distribution: Persicaria spp. and Polygonum spp. , worldwide.
7. Sphacelotheca polygoni-senticosi (Henn.) Miyabe & Takah. ex S. Ito, Tran s.
Sapporo Nat. Hist. Soc., 14: 90, 1935.
(Fig. 8)

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M. Kaki shima et al.

Sphacelotheca hydropiperis on Persicaria hydropiper (TSH-S Ill I). A. Sori in flowers . B,
C. Ustilopsores observed by SEM. Bar: A= I 0 mm , B = I ,Lilll, C=5,um.

Fig. 7.

Smut fungi from Yunnan , C hina

33Fig. 8. Sphacelotheca polygoni-senticosi on Persicaria y ukusaiana (TSH-S 11 08). A. Sari inflowers. B. Usti lospores observed by SEM. Bar: A = I 0 mm, B = 2 ,urn.

Sori in the swollen ovaries, forming oblong or ovate bodies, 2- 3.5 mm in length,with a central, unbranched columella, at first covered by a greyish-brown peridium.
Spore mass powdery, dark reddish-brown; sterile cells usually present amongst theustilospores. Sterile cells globose, subglobose, broadly ellipsoidal, ellipsoidal orslightly irregular, 5- 19.5 X4.5- 14 ,um, hyaline. Ustilospores more or less flattened, inplane view subcircular, broadly elliptical , ovate or slightly irregular, 9- 14 X8. 5- 12.5
(11.6± 1.1 X I 0.3 ±0.9) ,um (nil =50); middle reddish-brown; wall verruculose withwarts often arranged in rows, incompletely reticulate or incompletely cerebriform.
Young spores in chains, separated by small disjunctors . Mature spores single; the disjunctors remaining as small , hyaline , oppositely situated appendages.
Specimen examined: on Persicaria y okusaiana (Makino) Nakai ( = Polygonum
caespitosum Blume), Yunnan Province, Zhaotong District, Yiliang, Xiaocaoba, N
27°47 '39 1" E 104° 14 ' 437", alt. 1760m, Sept. 17, 1998, leg. M. Kakishima, CH-18/1(TSH-S\108 , TNS-F-107962 , HKAS 34500, HMAS) .
Hosts and distribution: Persicaria spp. and Polygonum spp., China, Japan.
Sphacelotheca polygoni-senticosi has been reported from China on Persicaria
longiseta (De Bruyn) Kitag. ( =Polygonum longisetum De Bruyn) and Polygonum posumbu Hamilt. (Guo, 1992). This record is a new one for the Yunnan Province. Persicaria yokusaiana is a new host for this smut fungus.

34

M. Kakishima et al.

Acknowledgements
This study was partly supported by Grants-in-Aid for International Scientific
Research Program No. I 0041186 of Ministry of Education, Science, Sports, and Culture, Japan. We thank Dr. H. Koyama, the Principal Researcher of the Program, Director of Department of Botany, National Science Museum, Tokyo, Japan and Dr. Y.
Doi , Department of Botany, National Science Museum, Tokyo, Japan, for providing
us with an opportunity to participate in this program and to study plant parasiticfungi. We also thank Dr. Y. Kadota, Department of Botany, National Science Museum, Tokyo, Japan for identification of host plants.

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