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129
MYCOLOGIA BALCANICA 8: 129–135 (2011)
Tubisorus, a new genus of smut fungi (Ustilaginomycetes) for
Sorosporium pachycarpum
Kálmán Vánky ¹* & Matthias Lutz ²
¹ Herbarium Ustilaginales Vánky (H.U.V.), Gabriel-Biel-Str. 5, D-72076 Tübingen, Germany
² Organismische Botanik, Institut für Evolution und Ökologie, Universität Tübingen, Auf der Morgenstelle 1, D-72076
Tübingen, Germany
Received 22 October 2011 / Accepted 21 November 2011
Abstract. A new genus of smut fungi, Tubisorus, is proposed for Sorosporium pachycarpum on Mnesithea
rottboellioides, Poaceae.
Key words: molecular analysis, new combination, new genus, smut fungi, taxonomy, Tubisorus, T. pachycarpus
*Corresponding author: e-mail: vanky.k@cityinfonetz.de
Introduction
A peculiar smut fungus, Sorosporium pachycarpum was
described by H. Sydow (in Sydow & Petrak 1928) on
Rottboellia ophiuroides (= Mnesithea rottboellioides), from the
Philippines. e sori are very long, tubiform, in the axis of
spikes with aborted spikelets. ey are lled with a black,
granular powdery mass of spore balls. e spore balls are
permanent, composed of globoid, thick-walled, ornamented
spores. e fungus was placed into the genus Tolyposporella
by Ling (1949), and into the genus Endosporisorium by
Vánky (1995); the latter genus turned out to be a synonym of
Macalpinomyces. irumalachar et al. (1967: 395) treated it
also under Tolyposporella. Vánky (1998: 93–95) considered the
genus Sorosporium F. Rudolphi to be a synonym of ecaphora
Fingerh., parasitising only dicotyledonous host plants.
Based on the peculiar sorus, spore ball and spore
morphology, as well as on molecular phylogenetic analyses of
ITS and LSU rDNA sequences, a new genus is proposed for
S. pachycarpum.
Materials and methods
e following specimens were examined for the present work:
Philippines, Luzon, Pampanga Prov., Stotsenberg, XI.1923,
coll. M.S. Clemens 2313 (BPI 180089; syntype); Papua
New Guinea, Morobe, 19.XI.1939, coll. M.S. Clemens
(BPI 71558, H.U.V. 10504 & 16772); PNG, Moresby,
20.III.1998, coll. R.G. Shivas, G.R. Kula, C. & K. Vánky, in
Vánky, Ust. exs. No. 1036 (H.U.V. 18515 & 18606); PNG,
Port Moresby, 21.III.1998, coll. R.G. Shivas, C. & K. Vánky
(H.U.V. 18520); PNG, Finschafen, 31.III.1998, coll. R.G.
Shivas, G.R. Kula, C. & K. Vánky (H.U.V. 18521); Australia,
Queensland, Townsville, James Cooke Univ. Campus, coll.
C. Bretzel, IX.1996 (H.U.V. 18206); Queensland, Cape York
Peninsula, 3 km N of Bamaga, coll. R.G. Shivas, C. & K.
Vánky (H.U.V. 19237); Queensland, 65 km S of Cairns,
Eubenangee Swamp, 17.VIII.2006, coll. R.G. Shivas, C. &
K. Vánky (H.U.V. 21582); Australia, Northern Territory,
between Pine Creek and Adelaide River, 12.4 km o Stuart
Hwy, Dorat Road, coll. M. & R.G. Shivas, Y.C. Tran, T. & K.
Vánky, 23.IV.2011 (H.U.V. 21891).
e nomenclatural novelty was registered in MycoBank
(www.MycoBank.org, Crous et al. 2004).
Morphological examination
Sorus structure and spore characteristics were studied using
dried herbarium specimens. For microscopic studies of
the soral, spore ball and spore characters, young sori were
rehydrated in hot water, xed in 2 % glutaraldehyde in 0.1
M Na-cacodylate bu er at pH 7.2 for several days. After six
transfers in 0.1 M Na-cacodylate bu er, the material was
post xed in 1 % osmiumtetroxide in the same bu er for 1 h
130 , . , . — Tubisorus, (Ustilaginomycetes) Sorosporium pachycarpum
in the dark, washed in distilled water, and stained in 1 %
aqueous uranyl acetate for 1 h in the dark. After ve washes in
distilled water, the material was dehydrated in acetone series,
embedded in Spurr’s plastic and sectioned with a diamond
knife. Semi-thin sections were stained with new fuchsin and
crystal violet, mounted in “Entellan” and studied in a light
microscope. For light microscopy (LM) spore balls were
dispersed in a small droplet of lactophenol, covered with a
cover glass, gently heated to boiling point to rehydrate the
spores and expel air bubbles from the preparation, and studied
at 1000× magni cation. For scanning electron microscopy
(SEM), spore balls were placed on double-sided adhesive
tape, mounted on a specimen stub, sputter-coated with gold-
palladium, ca 35 nm, and examined in a SEM at 10 kV.
DNA extraction, PCR, and sequencing
Genomic DNA was isolated directly from the herbarium
specimen (H.U.V. 21891). For methods of isolation and
crushing of fungal material, DNA extraction, ampli cation,
puri cation of PCR products, sequencing, and processing of
the raw data see Lutz et al. (2004). ITS 1 and ITS 2 regions
of the rDNA including the 5.8S rDNA (ITS) were ampli ed
using the primer pair ITS1-F (Gardes & Bruns 1993) and
ITS4 (White et al. 1990). e 5´-end of the nuclear large
subunit ribosomal DNA (LSU) was ampli ed using the
primer pair NL1 and NL4 (O’Donnell 1993). Primers were
used for both PCR and cycle sequencing. For ampli cation
the annealing temperature was adjusted to 48 °C. DNA
sequences determined in this study were deposited in GenBank
(accession numbers: ITS: JN871718/LSU: JN871717).
Phylogenetic analyses
Blast searches (Altschul et al. 1997) for both the ITS and
LSU sequence revealed closest similarity to members of the
Macalpinomyces/Sporisorium/Ustilago-group. To further elu-
cidate the phylogenetic position of Sorosporium pachy carpum,
its ITS and LSU sequence was analysed against the combined
ITS/LSU-dataset of Stoll et al. (2005). For this analysis, the
dataset was reduced to one specimen per species; the ITS and
LSU sequences of Anomalomyces panici (Vánky et al. 2006)
were added. GenBank accession numbers of sequences used
in the molecular analyses are included in Fig. 8.
Sequence alignment was obtained using MAFFT 6.853
(Katoh et al. 2002, 2005; Katoh & Toh 2008) using the
L-INS-i option. As suggested by Giribet & Wheeler (1999)
and Gatesy et al. (1993), respectively, to obtain reproducible
results manipulation of the alignment by hand as well as
manual exclusion of ambiguous sites were avoided. Instead,
highly divergent portions of the alignment were omitted
using GBlocks 0.91b (Castresana 2000) with the following
options: ‘Minimum Number of Sequences for a Conserved
Position’ to 50, ‘Minimum Number of Sequences for a Flank
Fig. 1. Tubisorus pachycarpus on Mnesithea rottboellioides (Pa-
pua New Guinea, H.U.V. 16 772) – young sori in much elon-
gate, tubular axis of the spikes, with aborted spikelets. Hab-
it. Bar = 1 cm
Position’ to 50, ‘Maximum Number of Contiguous Non-
conserved Positions’ to 8, ‘Minimum Length of a Block’ to 5
and ‘Allowed Gap Positions’ to ‘With half’.
e resulting alignment [new number of positions:
1160 (65 % of the original 1779 positions) number of
variable sites: 372] was used for phylogenetic analyses using
a Bayesian Approach (BA) and Maximum Likelihood (ML).
For BA a Markov chain Monte Carlo technique was used
as implemented in the computer program MrBayes 3.1.2
(Huelsenbeck & Ronquist 2001; Ronquist & Huelsenbeck
() 131
2003). Four incrementally heated simultaneous Markov
chains were run over 5 000 000 generations using the general
time reversible model of DNA substitution with gamma
distributed substitution rates and estimation of invariant sites,
random starting trees and default starting parameters of the
DNA substitution model as recommended by Huelsenbeck &
Rannala (2004). Trees were sampled every 100th generation,
resulting in an overall sampling of 50 001 trees. From these,
the rst 5 001 trees were discarded (burnin = 5 001). e trees
sampled after the process had reached stationarity (45 000
trees) were used to compute a 75 % majority rule consensus
tree to obtain estimates for the a posteriori probabilities of
groups of species. is Bayesian approach to phylogenetic
analysis was repeated ve times to test the independence of
the results from topological priors (Huelsenbeck et al. 2002).
ML analysis (Felsenstein 1981) was conducted with the
RAxML 7.2.8 software (Stamatakis 2006), using raxmlGUI
(Silvestro & Michalak 2010), invoking the GTRCAT and the
rapid bootstrap option (Stamatakis et al. 2008) with 1000
replicates.
In line with Stoll et al. (2005), trees were rooted with
sequences of Eriomoeszia eriocauli and Moesziomyces bullatus.
Results
Phylogenetic analyses
e di erent runs of BA that were performed and the ML
analyses yielded consistent topologies in respect to well
supported branchings. To illustrate the results, the consensus
tree of one run of the Bayesian phylogenetic analyses is
presented (Fig. 8). Estimates for a posteriori probabilities are
indicated on branches before slashes, numbers on branches
after slashes are ML bootstrap support values.
In all analyses Sorosporium pachycarpum clustered within
the Macalpinomyces/Sporisorium/Ustilago-group as sister taxon
of Ustilago bouriquetii and U. maydis within a group consisting
of Macalpinomyces loudetiae, M. simplex, M. trichopterygis,
M. tristachyae, Sporisorium trachypogonis-plumosi, and U.
vetiveriae.
Taxonomy
Tubisorus Vánky & M. Lutz, gen. nov.
MB 563575
Sori formationes tubulares plantarum nutrientium familiae
Poacearum. Massa atra granuloso-pulverea glomerulorum
sporarum conferti, columella et cellulae steriles nullae. Glomeruli
sporarum e sporis tantum compositi. Sporae pigmentatae
(brunneae, sine violaceo nec rubro tincto). Sporae verae
hyalinae, in matrice carassa, gelatinosa, hyalina immittae, strato
externo tenui, pigmentato, ornamentis velatis.
Typus generis: T. pachycarpus.
Sori tubular on host plants in the Poaceae, lled with dark,
granular powdery mass of spore balls, columella and sterile
cells lacking. Spore balls composed of spores only. Spores
pigmented (brown, without violet or red tint). e proper
spore is hyaline and embedded in a thick, gelatinous, hyaline
substance, coated by a thin, pigmented, ornamented outer
layer of spore wall.
Type of the genus: T. pachycarpus.
Tubisorus pachycarpus (Syd.) Vánky & M. Lutz, comb. nov.
MB 563576
Basionym: Sorosporium pachycarpum Syd., in Sydow &
Petrak, Ann. Mycol. 26: 431, 1928; Tolyposporella pachycarpa
(Syd.) L. Ling, Sydowia 3: 133, 1949; Endosporisorium
pachycarpum (Syd.) Vánky, Mycotaxon 56: 213, 1995. –
Syntype on Rottboellia ophiuroides (= Mnesithea rottboellioides),
Philippines, Luzon, Pampanga Prov., Stotsenberg, XI.1923,
coll. M.S. Clemens 2313 (BPI 180089!) (another syntype is
probably lost).
Sori (Figs 1, 7) in much elongated axis of the spikes with
aborted spikelets, tubular, 0.5–1.5 mm wide, up to 20–25
cm long, yellowish to greyish brown, at maturity rupture
longitudinally, on several places between the veins, exposing
the black, granular-powdery mass of spore balls. Spore balls
(Figs 2–5) globoid, long ellipsoidal to irregular, composed of
5–50 or more spores, apparently loose but rather permanently
connected, 25–50 (–65) × 45–100 (–150) µm, dark olivaceous
brown. Spores (Figs 3–5) subglobose, ovoid or irregular with
one or several attened contact sides, 12–20 × 16–24 µm,
olivaceous brown; wall 3-layered (Figs 3, 5): outer layer 1.5–
2 µm thick, pigmented, densely provided with irregular,
prismatic warts, c. 1 µm high on the free surface, smaller and
ner on the contact sides; middle layer hyaline, gelatinous,
homogenous, 2.5–7 µm thick; inner layer 0.5–1.5 µm thick,
smooth, surrounding the nely granular, hyaline proper
spores which in squashed spores are eliberated (Fig. 6). ese
are subglobose, broadly ellipsoidal, ovoid, subpolyhedrally
irregular or elongated, (7–) 8–10.5 × 9–14.5 µm; wall 0.5–
1 µm thick, composed of a very thin inner layer and and a
hyaline sheath, smooth. Spore germination unknown.
On Poaceae: Mnesithea rottboellioides (R. Br.) de Koning &
Sosef (Coelorachis rottboellioides (R. Br.) A. Camus; Manisuris
rottboellioides (R. Br.) Kuntze; Rottboellia ophiuroides Benth.).
Geographic distribution: Australia, Papua New Guinea,
Philippines (comp. Sydow & Petrak 1928: 431; Shivas et al.
2001: 335; Vánky & Shivas 2008: 105).
Discussion
H. Sydow (in Sydow & Petrak 1928: 431) described
Sorosporium pachycarpum to be in the leaves of the host plant.
Ling (1949: 133) also considered that the sori are in the leaves,
which was the reason that he transferred the fungus into the
genus Tolyposporella. Zundel (1953: 68) described the sori on
the abaxial side of the leaves, and treated the fungus under
132 , . , . — Tubisorus, (Ustilaginomycetes) Sorosporium pachycarpum
Figs 2–4. Tubisorus pachycarpus on Mnesithea rottboellioides (Papua New Guinea, H.U.V. 16772). 2. Semi-thin, stained, transversal
section of a part of a sorus with sectioned spore balls. Bar = 25 µm. 3–4. Spores balls and spores in LM and in SEM. Bars = 10 µm
the genus Sorosporium. Despite the fact that irumalachar
et al. (1967: 395) wrote that “Many Sorosporium species are
foliicolous . . . . ” and that “ e smut was correctly placed
in the genus Sorosporium by Sydow”, they treated it as
Tolyposporella pachycarpa (Syd.) Ling. Vánky & Shivas (2008:
166) wrote that the sori of Tolyposporella pachycarpa are “in
the axis of aborted in orescence”, which is inaccurate. e
exact place of the sori is rst described by Vánky (2012: 995).
e type of the genus Tolyposporella G.F. Atk. is T.
chrysopogonuis G.F. Atkinson (1897) on Sorghastrum nutans
(L.) Nash, USA. Its sori form linear, more or less con uent,
initially subepidermal, later bursting striae on the inner
surface of leaf sheaths. e spore balls are composed of rmly
agglutinated, smooth spores with unevenly thickened wall. It is
quite di erent from the smut on Mnesithea. Tolyposporella is a
genus of ve species, four on Poaceae, and one on Eriocaulaceae,
which probably does not belong to this genus (comp. Vánky
2012). All Tolyposporella species have spores with smooth,
unevenly thick, multilamellar wall and sori on the surface
of the leaves or leaf sheaths. In contrast, the spore wall of
Tubisporus pachycarpus is ornamented and three-layered (for
description see above). Similar spore wall structure, in which
() 133
Figs 5–6. Tubisorus pachycarpus on Mnesithea rottboellioides (Pa-
pua New Guinea, H.U.V. 16772). 5. Sectioned and stained
spore balls and spores showing the thin, pigmented, ornament-
ed outer spore wall, the thick, homogenous mass in which the
thin-walled proper spores with granular content are embed-
ded. Bar = 10 µm. 6. Ruptured outer, pigmented spore walls
permitting the thin-walled, hyaline proper spores to emerge.
Bar = 10 µm
the proper spore is embedded in a gelatinous layer and coated
by a thin, pigmented outer layer occurs in the smut fungi only
in the genus Kuntzeomyces Henn. ex Sacc., with two closely
related species in the spikelets of Rhynchospora (Cyperaceae;
comp. Piepenbring 2001). In them, however, the spores are
smooth and single. ese characters of the spores, in addition
to the soral characters, exclude Tubisorus pachycarpus from
Tolyposporella. Tubisorus neither belongs to the genus Spori-
sorium Ehrenb. ex Link, nor to Macalpinomyces Langdon &
Full., in which sterile cells, or groups of sterile cells, and in the
sori often also columella/ae are present (comp. Vánky 2002).
Piepenbring et al. (1998: 210, Fig. 28) reported presence
of germ pores in the spores of “Sorosporium” pachycarpum,
which could not be con rmed.
Molecular phylogenetic analyses based on BA and
ML analyses of ITS + LSU rDNA sequence data suggest a
Fig. 7. Mature sori of Tubisorus pachycarpus on Mnesithea rot-
tboellioides (Photo: Christine Vánky)
common ancestor of Tubisorus pachycarpus and the Ustilago
maydis/U. bouriquetii clade. U. maydis (DC.) Corda produces
galls on the stems, leaves or in orescence of Zea (including
Euchlaena) species (subtribe Tripsacinae, tribe Andropogoneae,
subfam. Panicoideae), lled with single spores. U. bouriquetii
Maubl. & Roger produces considerably hypertrophied
laments of Stenotaphrum species (subtribe Setariinae, tribe
Paniceae, subfam. Panicoideae), lled by single spores.
Mnesithea Kunth belongs to the subtribe Rottboelliinae
of the tribe Andropogoneae, subfam. Panicoideae (Clayton
& Renvoize 1986: 368). ree other known smut fungi on
members of this genus are: Sporisorium operculatum Vánky
& R.G. Shivas (2001: 154; Australia), S. perforatum Vánky
(2004: 104; India), and S. mnesitheae (Mishra) Vánky (2004:
107; India). None of these, including Ustilago maydis and U.
bouriquetii is similar to Tubisorus pachycarpus.
134 , . , . — Tubisorus, (Ustilaginomycetes) Sorosporium pachycarpum
Fig. 8. Bayesian inference of
phylogenetic position of So-
rosporium pachycarpum: Markov
chain Monte Carlo analysis of an
alignment of concatenated ITS
+ LSU base sequences using the
GTR+I+G model of DNA sub-
stitution with gamma distribut-
ed substitution rates and estima-
tion of invariant sites, random
starting trees and default start-
ing parameters of the DNA sub-
stitution model. A 75 % major-
ity-rule consensus tree is shown
computed from 45 000 trees that
were sampled after the process
had reached stationarity. e to-
pology was rooted with sequenc-
es of Eriomoeszia eriocauli and
Moesziomyces bullatus. Numbers
on branches before slashes are
estimates for a posteriori prob-
abilities, numbers on branches
after slashes are ML bootstrap
support values. Branch lengths
were averaged over the sampled
trees. ey are scaled in terms
of expected numbers of nucle-
otide substitutions per site. Spo.
= Sporisorium, Ust. = Ustilago
() 135
Acknowledgements. We are grateful to Dr. Sándor Tóth (St. István University,
Gödöllő, Hungary) for preparing the Latin diagnosis, to Dr. Eric H.C.
McKenzie (Landcare Research, Auckland, New Zealand) and Dr. Michael Weiß
(University of Tübingen, Germany) for checking the manuscript , or part of it,
and for useful suggestions. We thank Dr. Michael Weiß, Dr. Sigisfredo Garnica
and Dr. Robert Bauer (University of Tübingen) for providing the molecular lab.
e technical assistance of Mrs. Christine Vánky with the illustrations (H.U.V.,
Tübingen, Germany), Mrs. Magda Eha-Wagner with preparation of semi-thin
sections, and Mrs. Monika Meinert (both from University of Tübingen) with
preparation of the SEM pictures of the spores, is gratefully acknowledged.
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