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Pyriculariopsis calatheae sp. nov., a novel anamorphic hyphomycete from the

Atlantic forest of Brazil causing leaf spots on Calathea longifolia

Article  in  Mycological Progress · August 2011

DOI: 10.1007/s11557-010-0704-3

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Mycol Progress (2011) 10:315–321
DOI 10.1007/s11557-010-0704-3
ORIGINAL ARTICLE
Pyriculariopsis calatheae sp. nov., a novel anamorphic
hyphomycete from the Atlantic forest of Brazil causing leaf
spots on Calathea longifolia
Dartanhã J. Soares & Fabiano B. Rocha &
Lidiane L. Duarte & Robert W. Barreto
Received: 14 June 2010 / Revised: 3 August 2010 / Accepted: 24 August 2010 / Published online: 14 September 2010
# German Mycological Society and Springer 2010
Abstract The new species Pyriculariopsis calatheae is
described causing leaf spots on Calathea longifolia
(Marantaceae). It represents an addition to the mycobiota
of the tropical seasonal semi-deciduous montane forest, a
component of the Brazilian Atlantic forest and a highly
threatened ecosystem.
Keywords Anamorphic fungi . Dematiaceous
hyphomycetes . Marantaceae . Mycodiversity
Introduction
In December 2003, during a 4-day fungal survey in a
stretch of tropical seasonal semi-deciduous montane forest,
a component of the Brazilian Atlantic forest and a highly
threatened ecosystem (see Soares and Barreto 2005, for
more details) in the municipality of Viçosa (state of Minas
Gerais) Brazil, leaves of Calathea longifolia (Schauer)
Klotzsch ex Körn (Marantaceae) showing large necrotic
spots were collected (Fig. 1).
Taxonomical novelty: Pyriculariopsis calatheae D.J. Soares, F.B.
Rocha & R.W. Barreto
D. J. Soares : F. B. Rocha : L. L. Duarte : R. W. Barreto (*)
Departamento de Fitopatologia, Universidade Federal de Viçosa,
Viçosa, Minas Gerais 36570-00, Brazil
e-mail: rbarreto@ufv.br
D. J. Soares
e-mail: dartjs@yahoo.com.br
Present Address:
D. J. Soares
Embrapa Algodão,
Rua Oswaldo Cruz 1143,
Centenário, Campina Grande/PB, Brazil 58428-095
The Marantaceae (prayer-plant family), has a pantropical
distribution, but is absent from Australia (Heywood et al.
2007), it occurs mainly in the Americas, where more than 30
genera and 350 species occur (Souza and Lorenzi 2008). In
Brazil, there are 12 native genera and about 150 native
species on record. The largest group of species belongs to
the genus Calathea. Sometimes, plants in this genus become
the main component of the forest understory, especially in
wet areas, as in some valleys of the Atlantic rainforest.
Species in the genus Calathea are widely used as ornamental
and this is the most easily recognized genus, within the
Marantaceae (Souza and Lorenzi 2008).
Observation of fresh samples of C. longifolia leaves
bearing those necrotic spots revealed the presence of a
dematiaceous hyphomycete constantly associated with such
lesions. The fungus was readily recognized as belonging to
the Dactylaria–Pyricularia complex; however, after more
careful examination, it was concluded that it better fitted
within Pyriculariopsis M.B. Ellis sensu Matsushima
(1975). This paper provides an account on the morphology
and identity of this fungus.
Materials and methods
Samples with foliar spots were collected, examined under a
stereo-microscope and dried in a plant press. Slides with
free-hand sections of infected plant tissues and fungal
structures scraped from the surface were mounted in
lactophenol. Representative specimens of the fungus were
deposited in the herbarium at the Universidade Federal de
Viçosa (Herbarium VIC).
Observations, measurements and line drawings were
prepared using an Olympus BX 50 light microscope fitted
with a drawing tube. Measurements of taxonomically
316
Fig. 1 Pyriculariopsis calatheae leaf spot symptoms on Calathea
longifolia. a General view of the plants in the forest understory
showing leaf spot symptoms. b Close-up view of a severely damaged
leaf. c Close-up view of a leaf spot (adaxial surface). d Close-up view
of a leaf spot (abaxial surface). e,f Result of pathogenicity test 10 (e)
and 20 (f) days after inoculation showing similar leaf spots from those
observed in the field
Mycol Progress (2011) 10:315–321
relevant structures were made at ×1,000 magnification.
Samples were also examined under scanning electronic
microscope (SEM). Small leaf fragments bearing abundant
fungal structures were selected and dried for 7 days in a
dessicator containing silica-gel. The leaf fragments were
then covered with a gold-palladium coat in a sputter
coater (Balzers; FDU 010) and examined under a SEM
(Carl Zeiss; LEO VP 1430) with variable pressure.
The fungus isolation was performed by directly trans-
ferring conidia with a sterile fine-pointed needle from the
lesions onto Petri dishes containing Vegetable Broth Agar
(Pereira et al. 2003). Pure cultures were preserved in silica-
gel (as described in Dhingra and Sinclair 1995), and were
deposited at the culture collection of the Departamento de
Fitopatologia of the Universidade Federal de Viçosa
(accession number: OF 55) and in the reference culture
centre Coleção Brasileira de Microrganismos de Ambiente
e Industria of the UNICAMP (accession number: CBMAI
1060).
Cultures were described based on observations of
colonies produced as follows: 5-mm-diam culture discs,
obtained from the margin of actively growing 7-day-old
cultures, were transferred to the centre of each of a series of
plates contain 15 mL of V8 juice-agar (V8), malt extract
agar (MEA) (2%) and potato dextrose agar (PDA); plates
were sealed with cling film and maintained in a growth
chamber with a temperature of 26±2°C for 7 days with a
12-h light regime (light provided by two white and one
near-UV lamp located 35 cm above the plates).
Three healthy individuals of Calathea longifolia were
used to perform the pathogenicity test. Each individual was
sprayed with a 1.0 x 106 conidia/mL conidial suspension in
0.5% Tween 20. Half of the leaves of each individual plant
were surface-injured with the help of a sterile needle. The
control (non-inoculated) plants with and without injuries
were sprayed with a 0.5% Tween 20 suspension. After
inoculation, the plants were placed in a humid chamber for
48 h and then moved to a greenhouse. The plants were
examined for disease symptoms 10 and 20 days after
inoculation.
DNA was extracted as follows: culture discs taken
from the margin of actively growing colonies on PDA
were transferred to liquid medium (as described in
Alfenas 1998) and incubated during 7 days under 27°C
in the dark. Mycelium was dried in the dark at room
temperature and powdered in liquid nitrogen using a
mortar and pestle. DNA was extracted using the cetyl-
trimethylammonium bromide (CTAB)-based protocol
(Murray and Thompson 1980). The pellet was resus-
pended with 40 μm Tris-EDTA + RNAase at 37°C for 2 h.
Sequence of the ITS region were amplified by PCR using
the reverse primer ITS4 and the forward primer ITS5 (White
et al. 1990). The amplification reaction were performed in a
Mycol Progress (2011) 10:315–321
50-μl reaction volume [PCR conditions: 1 μl each primer,
1 μl DNTPs, 1 μl DNA, 0.7 μl Taq (phoneutria), 3.75 μl
buffer, 1.25 μl MgCl2, 40.3 μl H2O]. After electrophoresis in
0.8% agarose gel stained with ethidium bromide, DNA was
purified using the High Pure PCR Product Purification Kit
(Roche Mannheim, Germany).
The purified product was sequenced using Big Dye
Terminator Cycle Sequencing Kits (v3.1; Applied Bio-
systems, Foster City, CA, USA) with the same primers as
used for amplification on the MegaBACETM1000 DNA
Sequencing System. The sequence was edited by the
Staden Package, ver. 1.6.0 (Staden 1996) to generate a
consensus sequence.
Taxonomy
Pyriculariopsis calatheae D.J. Soares, F.B. Rocha & R.W.
Barreto sp. nov. (Figs 1, 2 and 3)
MycoBank: 512390
GenBank: GU294490
Affinis Pyriculariopsis parasitica sed conidiophoribus
brevioribus (36–170 μm) et conidiibus minoribus (18–36×
5–7 μm), 1–2 septatis differt.
Teleomorph: not seen
Etymology: based on the host genus
Holotype: Brazil, Minas Gerais, Viçosa, ‘Mata do Seu
Nico’ on Calathea longifolia (Marantaceae), December of
2003, D.J. Soares (VIC 30699; ex-type culture CBMAI
1060).
Lesions on living leaves amphigenous, starting as small
yellow dots becoming circular to elliptic, pale-brown to
brown, sometimes with a darker centre and with concentric
haloes, the external halo dark-brown, surrounded by a large
dark-yellow border fading into irregular paler and indistinct
margins, 0.5–11×0.5–7.5 cm, sometimes coalescing and
leading to the necrosis of significant portions of leaves; on
petioles elliptic, similar in colour to the foliar lesions, but
smaller and with a narrow yellow border; conidiophores
macronematous, isolate, straight, cylindrical, 36–170×4–
5.5 μm, usually inflated at the base reaching 9.0 μm diam.,
0–7 septate, chestnut to dark brown, darker and thicker-
walled at the base, paler toward the apex, smooth;
conidiogenous cells polyblastic terminal, becoming inter-
calary, cylindrical, proliferating sympodially, denticulate,
22.5–70×3.5–5.5 μm, pale brown to subhyaline, smooth;
denticles conic-truncated, not separated by septa, 0.5–
1.5 μm long, conidia acropleurogenous, cylindrical-
fusiform to obclavate, 18–36×5–7 μm, 1–2-septate, often
with a rostrate apical cell, 3–12×2–4 μm, pale brown to
subhyaline, basal cell paler and supra-basal cell darker,
smooth, hila protuberant, sometimes somewhat dark;
conidial secession schizolytic.
317
Colonies on PDA, MEA and V8 are very similar,
initially white becoming greyish with age, lanose at the
centre velvety at the edges, with uneven margin and with
concentric diurnal zonation (less conspicuous on V8), dry,
but with inconspicuous formation of small droplets appear-
ing over the mycelium with age; reaching 14 mm diam. on
PDA, 16 mm diam. on MEA and 20 mm diam. on V8 after
7 days; sporulating on all media (abundantly in older
cultures) under the growth conditions provided.
Notes A literature search for fungi reported as associated to
Calathea spp. and other genera of the Marantaceae yielded
no species of Pyriculariopsis. The new species was
compared with the eight accepted species in the genus
Pyriculasiopsis following the key provided by Iturriaga
et al. (2008), and had a morphology that was distinct from
all of those species. It is of significance that a Pyricularia
leaf-spot (viz. P. guarumaicola F.C. Albuquerque & M.L.
Duarte, recorded as Piricularia guarumeicolae) was
recorded from the Brazilian Amazon on Ischnosiphon
simplex Hub. (Albuquerque and Duarte 1971), and a second
record of a Pyricularia causing leaf-spots on Marantaceae
was made in Greece by Pappas and Paplomatas (1998). The
latter authors recorded Pyricularia oryzae Cavara on
Ctenanthe oppenheimiana (E.Morr.) K. Schum. and C.
setosa Eichl., imported from Brazil, and showed, by
inoculation tests, that isolates from Ctenanthe had a wide
host range within the Marantaceae, including several
Calathea species, but isolates from rice did not cause
infections on marantaceous hosts. In both cases, the correct
generic identity of the fungus is to be regarded as doubtful
since identifications were based mainly in the conidial
morphology and no reference was made to conidial
secession, which is critical for the placement of fungi in
Pyricularia or Pyriculariopsis. Illustrations in both cases
seem to show a schizolytic rather than rhexolytic secession
and the symptoms are highly similar to those described
here. Nevertheless, both P. guarumaicola and P. oryzae
(isolate from Ctenanthe) have conidial sizes which are
clearly distinct from those of P. calatheae. While P.
guarumaicola has conidia 20–28×10–12 μm and P. oryzae
from Ctenanthe has conidia 18–32×7–12 μm; the conidia
in P. calatheae are narrower, 18-36×5–7 μm ,and have a
clearly rostrate apex which is absent or not so pronounced
in the other species.
A fragment of approximately 490 bp was amplified and
the sequence data were submitted to the National Center for
Biotechnology Information, where it was assigned the
accession number GU294490. This was compared by
BLASTn with other entries in Genbank, and the closest
match was Pyricularia costina (GenBank Accession
GQ340561) with 91% of nucleotide homology (over
100% query coverage). Our isolate also shares 89% of
318 Mycol Progress (2011) 10:315–321

Fig. 2 Conidiophores and

conidia of Pyriculariopsis
calatheae. a A conidiophore
with attached conidia. b,c
Apices of conidiophores
showing the paler
conidiogenous cells and the
conic-truncate denticles (note in
c a younger conidium still
attached to a denticle). d A
close-up of the inflated base of
the conidiophore. e–g Conidia
(note: in e the versicolorous
conidium with a paler basal cell;
in f the schizolytic conidial
secession, arrowed; and in g
some darker hila, arrowed).
Scale bars 10 μm, except in (a)
20 μm

identity with Pyricularia zingiberis (GenBank Accession
AB274434) and 88% with Dactylaria junci (GenBank
Accession AY265320). There are no other entries in
Genbank with sequences of ITS rDNA region for Pyricu-
lariopsis isolates available for comparisons.
Ten days after inoculation, the first symptoms were
observed as small spots (∼5 mm diam.) (Fig. 1e) and
20 days after inoculation, typical lesions of P. calatheae
with sporulation were observed (Fig. 1f). Such lesions only
developed on leaves that has previously been injured; intact
leaves that were inoculated remained healthy. Although this
could be interpreted as an indication that P. calatheae is a
secondary, opportunistic pathogen, observations in the field
contradict this. No obvious entrance wounds were seen in
association with the fungus in the field or on samples
brought to the laboratory. Controls did not develop leaf
spots. The fungus was reisolated from the inoculated leaves
fulfilling Koch’s postulates.
Discussion
Pyriculariopsis was erected to accommodate P. parasitica
(Sacc. & Berl.) M.B. Ellis (Syn.: Pyricularia musae S.
Hughes) (Ellis 1971). Ellis recognized it as differing from
Mycol Progress (2011) 10:315–321 319

Fig. 3 Scanning electron

micrographs and line-drawings
of conidia and conidiophores of
Pyriculariopsis calatheae. a,b
Detail of the inflated base of the
conidiophores showing its origin
directly through the host
epidermis. c Detail of the
conic-truncate denticles. d
Rostrate conidia and the
conidiophores with inflated and
darker bases and paler rostrate
apices. Scale bars 10 μm

Pyricularia by the absence of a septum separating its
denticles from the conidiophore. Therefore, Ellis (1971)
interpreted the conidial secession in Pyriculariopsis as
schizolytic whereas in Pyricularia this would be rhexolytic.
Later, Matsushima (1975) also recognized the conidial
secession in Pyriculariopsis as schizolytic rather than
rhexolytic as in Pyricularia. This assumption was followed
in the descriptions of species of Pyriculariopsis by several
authors (Davydkina and Melnik 1989; Matsushima 1989;
Castañeda Ruiz and Kendrick 1990; Reddy et al 2002).
Conversely, de Hoog and van Oorschot (1985) noted that
illustrations of the type species of Pyriculariopsis given in
Matsushima (1980) showed the conidial secession to be
rhexolytic instead of schizolytic. Even so these authors
preferred to maintain the genus Pyriculariopsis based on its
short, stout conidiophores and rostrate conidia rather than
on its conidial secession. Although the significance of
conidial secession as a character in the Pyricularia–
Pyriculariopsis remains an unresolved issue, which was
left aside in recent publications dealing with this genus such
as Park and Shing (2009) and Iturriaga et al. (2008). A
recent molecular study (Bussaban et al. 2005) reinforces the
separation between Pyricularia and Pyriculariopsis and
additionally placed Pyriculariopsis outside the Magnapor-
thaceae clade. These authors concluded that the genus
Pyriculariopsis should be maintained based mainly in its
straight or curved, obclavate and rostrate conidia, a trait
also useful to separate Pyriculariopsis from the still
320
polyphyletic genus Dactylaria. The present study on P.
calatheae and observations on other members of Pyricular-
iopsis suggests that an additional feature that appears useful
for the delimitation of Pyriculariopsis, and that apparently
has been overlooked by previous workers, is the presence
of versicolorous conidia which was consistently observed
or illustrated for most species accepted in this genus, as
pointed out by Whitton et al. (2001). Nevertheless,
confirmation of this character-state is still required for
Pyriculariopsis amomi (Z.D. Jiang & P.K. Chi) X.H. Lai &
H.L. Gao (Lai & Gao 1991).
Presently eight species are accepted in Pyriculariopsis
(Iturriaga et al. 2008). These appear to belong to two
distinct ecological groups: one is composed of saprotrophs,
occurring on foliar and stem debris and the other includes
plant pathogens parasitizing monocot hosts belonging to the
Zingiberales. The former includes the following species: P.
appendiculata Matsush., P. breviphora Matsush., P. indica
B.S. Reddy, Manohar., D.K. Agarwal & V. Rao, P. miogae
Matsush., P. formosa R.Fernández, R.F. Castañeda & Iturr.
and P. theobromae R.F. Castañeda & W.B. Kendr. The
latter includes: P. parasitica, P. amomi and the new species
P. calatheae. An additional undetermined Pyriculariopsis
was also recorded causing leaf spots on Heliconia in
Hawaii, but no description of that fungus was provided
(Uchida and Kadooka 1994).
The fact that the BLAST search performed indicated that
isolates belonging to Pyricularia and Dactylaria shared the
highest homology with our isolate is explained by the
absence of sequences of ITS rDNA region for Pyricular-
iopsis in GenBank and the known close relationship of
these two genera with Pyriculariopsis (Bussaban et al.
2005).
The genus Pyricularia was recently confirmed to be
monophyletic (Hirata et al 2007) and it would be of interest,
although outside the scope of the present work, that a
molecular-phylogenetic study is performed for members of
Pyriculariopsis and related taxa, and to test the hypothesis
that pathogenic species of Pyriculariopsis and Pyricularia
have a common ancestor, particularly those which are
pathogens of members of the Zingiberales. This plant order
includes all known hosts of Pyriculariopsis, a likely
indication of evolutionary specialization within this host
order, similar to that conjectured for Pyricularia (Bussaban
et al 2003; 2005) and for the pathogenic species of Cordana
(Soares et al 2005). Such a study may prove that species of
Pyricularia/Pyriculariopsis on Zingiberales are closely
related and distinct from the group of saprotrophic species
in Pyriculariopsis and from those of Pyricularia described
in others monocots hosts. Isolates of Pyricularia guaru-
maicola, P. oryzae (isolate from Ctenanthe), as well as
several others previously described as causing disease on
members of Zingiberales should be included. In view of the
Mycol Progress (2011) 10:315–321
fact that Zingiberales is a sister order with Commelinales
and Poales, the possibility of such a relationship among
these pathogenic species appears even more likely, since
almost all species belonging to Pyricularia have been found
and described on hosts belonging to these orders of
monocots and may have coevolved with their hosts.
Acknowledgements The authors thank the Conselho Nacional de
Desenvolvimento Científico e Tecnológico (CNPq) and the Fundação
de Amparo à Pesquisa de Minas Gerais (FAPEMIG) for financial
support; SEM work was undertaken at the Núcleo de Microscopia e
Microanálises of the Universidade Federal de Viçosa with the
technical support of Claudia A. Vanetti.
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