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Submitted 29 June 2019, Accepted 7 October 2019, Published 25 November 2019
Corresponding Author: Rajnish K. Verma – e-mail – vermarajnish1985@gmail.com 230
Two new additions to mycoflora (Hyphomycetes) of India
Verma RK1, 2, Prasher IB2, Sushma2, 3 and Gautam AK4
1Department of Botany, Dolphin PG College of science and Agriculture Chunni Kalan, Fatehgarh Sahib, Punjab,
140307, India
2Department of Botany, Mycology and Plant Pathology Laboratory, Panjab University Chandigarh, 160014, India
3Department of Botany, Govt. PG College for Girls Sector- 42, Chandigarh, India
4School of Agriculture, Faculty of Science, Abhilashi University, Mandi- Himachal Pradesh, 175028, India
Verma RK, Prasher IB, Sushma, Gautam AK 2019 – Two new additions to mycoflora
(Hyphomycetes) of India. Studies in Fungi 4(1), 230–243, Doi 10.5943/sif/4/1/25
Abstract
Hyphomycetes are abundant and highly diverse in tropical areas such as India due to its
climate and geographical landscape. However, several regions of the country remained unexplored
or underexplored and many species remained undiscovered in the country. During mycological
forays from the forests of Himachal Pradesh, two hyphomycetous fungi were collected. After
detailed analysis of mycological characters like oval to oblong–ellipsoidal, muriform conidia with
transverse, longitudinal, and oblique septa rounded or irregular at the ends and often with a
protruding hilum, singly on short, unbranched conidiophores or sessile, in sporodochial
conidiomata, it was found that these taxa belongs to the genus Berkleasmium. The further
evaluation of morphological and microscopic characters revealed the identity of these fungi as B.
pandani and B. typhae. Review of literature reveals that both are new records for India. Synoptic
table of all the accepted species (both asexual morph and sexual morph) along with checklist of
Berkleasmium from India is also provided.
Key words – Anamorphic fungi – biodiversity – taxonomy
Introduction
Himachal Pradesh is a state of Indian union situated between 30°22′40′′ to 33°12′40′′ along
North latitudes and 75°45′ 55′′ to 79°04′ 20′′ along East longitudes. The altitude varies from 350
meters to 6975 meters above mean sea level. Terrestrial fungi play an important role in nutrient
cycling and are important part of forest ecosystem of Himalayan region. Most of the studies of
fungal diversity in the region are restricted mainly to Agaricomycetes (Prasher & Ashok 2013,
Ashok & Prasher 2014a, b, Prasher 2015). There are sporadic reports of hyphomycetes primarily
pertaining to the plant pathogenic fungi affecting the crops of this area (Bilgrami et al. 1991,
Jamaluddin et al. 2004). India is an active centre of research of fungal biodiversity, with a high
proportion of genera and species first described in this country (Subramanian 1971, Bilgrami et al.
1991, Jamaluddin et al. 2004). In spite of this intensive research, new species and records of
hyphomycetes are still discovered in India (Kumar & Singh 2018, Kumar et al. 2018, Rajeshkumar
et al. 2018, Verma et al. 2019).
The genus Berkleasmium was established by Zobel in 1854 with B. cordaeanum Zobel as the
type species. Hughes (1958) considered B. cordaeanum as a synonym of Sporidesmium concinnum
Berkeley and proposed it as Berkleasmium concinnum (Berk.) S. Hughes.
Studies in Fungi 4(1): 230–243 (2019) www.studiesinfungi.org ISSN 2465-4973
Article
Doi 10.5943/sif/4/1/25
231
Asexual morph
There are two main morphological types have been reported by Lu et al. (2018)
1. Forming sporodochia, having short or flexuous conidiophores and producing muriform,
ellipsoidal conidia broad-cylindrical, multicellular, with large and fairly regular cells, fuscous,
borne on short conidiophores which become obscure with maturity (Moore 1958, Ellis 1971, Lu et
al. 2018).
2. Effuse, helicosporous, gregarious, mycelium partly immersed, partly superficial, brown, septate,
branched hyphae, with masses of crowded, glistering conidia; conidiophores erect, arising as lateral
branches from creeping hyphae, macronematous, mononematous, 0–3-septate, brown, smooth-
walled; conidiogenous cells holoblastic, mono- to polyblastic, integrated, sympodial, terminal,
cylindrical, truncate at apex, brown, smooth-walled; conidia acrogenous, helicoid, tapering to apex
and base, solitary, coiled 1–3 times, with elongated basal cell, rounded at tip, septate, slightly
constricted at septa (Lu et al. 2018).
Sexual Morph
Ascomata superficial, seated on a subiculum, scattered, solitary, subglobose to globose, dark
brown to black, with ostiole. Ascomata covered by setae. Setae multi-septate, thick-walled, brown
to black, straight or slightly curved. Peridium composed of textura angularis. Hamathecium
comprising, branched, filiform, septate, pseudoparaphyses. Asci bitunicate, cylindrical, pedicellate,
apically with 8 ascospores. Ascospores biseriate, fusiform, hyaline, smooth-walled, tapering
towards the ends, slightly curved, guttulate, multi-septate, not constricted at septa (Lu et al. 2017,
2018).
During the survey of saprophytic conidial fungi, two interesting hyphomycetes were
collected. Morphological analysis confirmed that these taxa are Berkleasmium pandani McKenzie
and B. typhae Somrithipol & E.B.G. Jones were collected. This is the first report of both taxa from
India (Bilgrami et al. 1991, Jamaluddin et al. 2004). Moreover, this communication is in
continuation with our earlier reports on hyphomycetes (Prasher & Verma 2014a, b, 2015a, b, c,
2016, Adamčik et al. 2015, Buyck et al. 2017, Verma et al. 2019).
Materials & Methods
Decaying culms, twigs and dead wood and bark were collected and kept in paper bags. Then
the specimens were brought to the laboratory. The specimens were mounted in 4 % KOH,
lactophenol and cotton blue 0.01 % in lactophenol (Kirk et al. 2008), and were examined for
microscopic characters using a Matrix stereo trinocular microscope (VL-Z60) and transmission
microscope (VRS-2f) for macroscopic and microscopic characters. All measurements were taken
with the help of Pro MED software. The scanning electron microscopic studies were conducted
with a JSM-6100 (JEOL Ltd.) microscope. The material was vacuum-dried in an oven for 24 hours,
mounted and sputtered with gold for 60 seconds, and photographed. The specimens were deposited
in the herbarium of the Department of Botany, Panjab University, Chandigarh, India (PAN)
Results
Berkleasmium pandani McKenzie, Mycotaxon 104: 24 (2008) Figs 1, 2
Index Fungorum: IF511285
Colonies on natural substratum forming black punctiform scattered, pulvinate, shiny or
glistening, more or less circular sporodochia. Mycelium mainly immersed in the substratum.
Stroma none. Setae and hyphopodia absent. Conidiophores reduced to conidiogenous cell,
differentiated, single, aseptate, hyaline, thin–walled, smooth. Conidiogenous cell holoblastic,
determinate, 12–20 × 8–19 µm. Conidia solitary, dry, acrogenous, brown, smooth, oval to oblong–
ellipsoidal, muriforrn with transverse, longitudinal, and oblique septa, sometimes slightly
constricted at the median septa and other septa, 26–35 × 18–22.5 µm. Conidiogenous cell usually
remaining attached to base of conidium at maturity.
232
Material examined – India, Himachal Pradesh, Near Kandaghat (Solan), on bark of
Eucalyptus tereticornis, 5 April 2014, Rajnish Kumar Verma, PAN (32722).
Remarks – Our collection morphologically resembles with B. pandani (McKenzie 2008). The
Himalayan collection differs from type in having smaller size of conidiogenous cell i. e 16–26 ×10–
19 in type and 12–20 × 8–19 µm in Himalayan collection, but we considered it as same species.
This is the first record of B. pandani from India.
Berkleasmium typhae Somrithipol & E.B.G. Jones, Fungal diversity 12: 170 (2003). Figs 3, 4
Index Fungorum: IF372008
Colonies on natural substratum forming punctiform, scattered, brown, shiny sporodochia.
Mycelium immersed in the substratum. Stroma none. Setae and hyphopodia absent. Conidiogenous
cells terminal on the conidiophores, holoblastic 10–14 × 8–10 µm. Conidia solitary, oval to
ellipsoidal, muriform, constricted at the septa, often with a dark median septum, pale brown to
brown, smooth, 20–29 × 15.5–18.9 µm. Conidiogenous cell sometimes remaining attached to base
of conidium at maturity.
Material examined – India, Himachal Pradesh, on the way Kuthera to Morshingi (Bilaspur),
on bark of Eucalyptus species, 19 January 2013, Rajnish Kumar Verma, PAN (32723).
Remarks – Our new collection morphologically resembles B. typhae (Somrithipol & Jones
2003). The species is the first report of B. typhae from India (Bilgrami et al. 1991, Jamaluddin et al.
2004).
Discussion
Presently there are 45 accepted species of Berkleasmium (Bussaban et al. 2001, Seifert et al.
2011, Whitton et al. 2012, Qu et al. 2013, Hüseyin et al. 2014, Tanney & Miller 2017, Tibpromma
et al. 2017, Lu et al. 2018). Among these species, B. aquaticum reported as sexual morph while two
species (viz. B. fusiformae and B. thailandicum) are reported with both sexual and asexual morphs.
Of the 44 asexual morphs four species namely B. guangxiense, B. latisporum, B. longisporum and
B. thailandicum are having helicoid conidia rest have dictyoconidia. Table 1 and 2 summarizes
synopsis of Berkleasmium.
Table 1 Synopsis of Berkleasmium species with asexual morph
Species with Dictyoconidia
Sr.
no.
Species
Conidiophores (µm)
Conidia (µm)
Reference
1.
B. ariense
flexuous, unbranched,
2–5
119–238 × 41–60, solitary,
dry or sti
cky, acrogenous,
simple, clavate, ellipsoidal,
oblong or irregular,
muriform, pale to dark
brown or blackish brown,
hilum not protruding;
conidial base 11–15. Young
conidia hyaline or
subhyaline, 56 × 17
Tibpromma et
al. 2017
2.
B. atropicale
–
30–50 × 21–38 broadly
elliptical, sometimes ovoid
or obovoid
Whitton et al.
2012
3.
B. atrovirens
13–16 × 1.5–3.5
Irregularly muriform, 30–37
× 15–17
Zhao & Zhang
2004
4.
B. concinnum
30 × 2–5
60–124 × 24–31, muriform
Hughes 1958
5.
B. conglobatum
–
36.5–99 × 26–47
Moore 1958
233
Table 1 Continued.
Sr.
no.
Species
Conidiophores (µm)
Conidia (µm)
Reference
6.
B. correae
2–5 × 2–2.5
26–44 × 16–24, broadly
ellipsoidal
Yip 1988
7.
B. corticola
–
26.5–34 × 18.5–26,
multicellular, with 1 or 2
subtending cells
Moore 1959
8.
B. crunisia
45–47.5 × 10
muriform, oval to
ellipsoidal, pale brown,
smooth, 35–100 × 17.5–30
Pinnoi et al.
2007
9.
B. daphniphylli
–
16.5–28 × 10–13
Zhang et al.
2009
10.
B. dudkae
up to 25 long, 1.8–
2.3(–2.9) wide
oval to obovoid, smooth,
regularly muriform, (13–)
14–17(–17.5) × 12.5–15
Hüseyin et al.
2014
11.
B. fusiforme
up to 8 long, 3–5 wide
fusiform, oval to ellipsoidal,
18–29 × 10–14
Qu et al. 2013
12.
B. granulosum
–
29–66 × 16.5–18.5, profile
irregular, multicellular
Moore 1958
13.
B. inflatum
39–80 long, 3–4 wide
at base, 7–19 apex
ellipsoidal, 31.5–49 × 16–26
Holubová-
Jechová 1987
14.
B. juglandis
7–15 × 8–13
20–25 × 14–18
Qu et al. 2013
15.
B. leonense
Up to 25 long, 1–3
wide
20–27 × 15–17 × 6–8,
muriform, broadly elliptical,
flattened, smooth
Ellis 1976
16.
B. lingual
–
65–89.5 × 18.5–24
multicellular, without
subtending cells, cylindrical
to slightly obclavate,
sometimes somewhat
curved, fuscous
Moore 1959
17.
B.
micronesicum
–
30–40 × 13–16, muriform,
cylindrical
Matsushima
1981
18.
B.
minutissimum
Absent
11.5–17 × 8.5–11.5,
subglobose to squarish–
subglobose to oval ellipsoid
Moore 1959
19.
B.
monilicellulare
13–23 × 4–5.2
27–39 × 20–29, broadly
elliptical, pyriform or
sometimes almost spherical.
Whitton et al.
2012
20.
B. moriforme
–
23.5–26.5 × 18.5–22 ,
muriform, pale brown
subtending cells either
numerous, tending to be
amorphous
Moore 1959
21.
B. nigroapicale
Up to 22 high, inflated
to 6.5–10 at the apex
24–27 × 12.5–15 , broadly
clavate, muriform
Bussaban et al.
2001
22.
B. obovoides
17 long, 6 wide
ellipsoidal to obovoid,
regularly muriform, 26–34 ×
19–24
Qu et al. 2013
234
Table 1 Continued.
Sr.
no.
Species
Conidiophores (µm)
Conidia (µm)
Reference
23.
B. opacum
Absent
52–83 × 31–41.5, verrucose,
subglobose to oval–
ellipsoid,
Moore 1959
24.
B. osmaniae
7.2–7.6 × 3.6–7.2
18–75 × 3.6–5.4 at base,
7.2–10.8 at apex, oval–
clavate to cylindrical,
curved or straight, Smooth
Rao & Rao
1964
25.
B. pandani
Reduced to
conidiogenous cell
27–34 × 18–22.5
McKenzie 2008
26.
B. parmelielfae
6–9 × 4–5
40–55 × 22–27, muriform,
clavate to ellipsoidal,
rounded at the ends
Rao & Rao
1964
27.
B. parmeliellae
–
40–45 × 22–27
Etayo &
Diederich 1995
28.
B.
phyllostachydis
–
17–25 × 9–13, muriform,
ellipsiodal to broadly
clavate
Matsushima
1983
29.
B. pulcharum
up to 25 long, 2–5
thick
muriform, brown, smooth,
31–41(–46) × 21–28(–32) ×
13–16, with (3–) 4–5(–7)
transverse and 2
longitudinal thick, dark
septa, basal cell conical,
hyaline to sub-hyaline, 3–5
× 2.5–5.
Holubová-
Jechová &
Mercado
Sierra1984
30.
B. sansevieriae
5–13 × 2.6
15.5–26 × I0.5–15.5,
oblong, muriform
Batista et al.
1962
31.
B. sinense
–
broadly ellipsoidal to
obovoid, brown, paler
towards base,
40–52 × 20–32
Taylor & Hyde
2003
32.
B.
sutheppuiense
15–17.5 × 6–6.5
35–37 × 22.5–25, muriform,
subglobose,
Bussaban et al.
2001
33.
B. taishanense
Up to 10 long
(including
conidiogenous cell)
1.5–2 wide with
bladder like swelling
Ellipsoidal, clavate, ovovate
or pyriform, 22–35 × 15–
18.75
Zhao & Zhang
2004
34.
B. talaumae
Absent
25–51 × 19–28, oblong,
Batista et al.
1964
35.
B. tetraploides
up to 15 long, 3–5 wide
pyriform, smooth, 20–30 ×
12–19
Qu et al. 2013
36.
B. triglochinis
4–6 long
10–18 × 8–14, tuberculate
to more or less scabrid,
broadly oval to spherical or
pyriform,
Moore 1959
37.
B. tropicale
13–16 × 3–4
50–57 × 28–34 , muriform,
flattened, oval
Morris 1972
235
Table 1 Continued.
Sr.
no.
Species
Conidiophores (µm)
Conidia (µm)
Reference
38.
B. typhae
–
23–28.5 × 15–19.5
Somrithipol &
Jones 2003
39.
B. zhejiangense
–
oval to ellipsoidal, 38–76 ×
19–33
Wongsawas et
al. 2009
Species with Helicoid conidia
1.
B. guangxiense
19–37 × 3.5–5, pale
brown,
macronematous, erect,
short, cylindrical,
septate, smooth-walled
90–130 (–144) diam. and
conidial filament 8–10 wide,
405–725 (-800) long, coiled
2½–3½ times when tightly
coiled, basal cell elongated,
rounded at tip, multiseptate,
up to 62– septate
Lu et. al. 2017,
2018
2.
B. latisporum
–
95–120 diam. and conidial
filament 12–14.5 wide, 540-
760 long, coiled 1½–3½
times when tightly coiled,
becoming loosely coiled in
the water, basal cell
elongated, rounded at the
tip, multi-septate, up to 60-
septate
Lu et al. 2017,
2018
3.
B. longisporum
0–3-septate, 15–40 ×
5–7, brown, smooth-
walled.
solitary, acrogenous,
helicoid, basal cell
elongated, rounded at tip,
110–180 diam. and conidial
filament 11–15 wide in the
broadest, tapering to 4.5–5.5
lm wide near apex and base,
1190–1540 long, 100–122
septate, slightly constricted
at septa, coiled 2–3 times,
becoming loosely coiled or
uncoiled in water, brown,
smooth-walled
Lu et al. 2018
4.
B. thailandicum
10–24 × 4–6, pale
brown,
macronematous, erect,
short, cylindrical,
septate
89-155 diam. and conidial
filament 10.5–14 (–15)
wide, 630–950 long, coiled
2–3 times when tightly
coiled, up to 60-septate
Lu et al. 2017
236
Table 2 Synopsis of Berkleasmium species with sexual morph
Sr.
no.
Species
Ascomata (µm)
Setae
(µm)
Peridium
(µm)
Asci
(µm)
Ascospores
(µm)
Reference
1.
B. aquaticum
235–290 high ×
180–225 in diam.
subglobose,
ellipsoidal-ovate
35–65 long,
3.5–6 wide in
the middle, 1-
celled
25–34 wide,
composed
of cells of
textura
angularis
115–175 × (11–)
12.5–16 (–17.5), 8-
spored, bitunicate,
cylindrical, short-
pedicellate, apically
rounded
(45–) 50.5–60 × 4.5–6.5,
overlapping 2–3-seriate,
fusiform, tapering towards
rounded ends, slightly
curved, guttulate, 7–
septate, not constricted at
septa, hyaline, smooth-
walled
Lu et al.
2017, 2018
2.
B. fusiformae
220–290 high ×
240–300,
subglobose to
globose,
40–55 long, 4–
6 wide, 1–3
celled
45–60 thick,
composed
of several
layered cells
of textura
angularis,
100–140 × 14–19, 8-
spored, bitunicate,
cylindrical,
pedicellate,
apically rounded
45–55 × 5–6, biseriate,
fusiform, tapering towards
rounded ends, slightly
curved, guttulate, 6–7-
septate, not constricted at
septa, hyaline, smooth-
walled
Lu et al.
2018
3.
B.
thailandicum
190–275 high ×
175–230 diam.,
subglobose,
ellipsoidal-ovate,
45–85 long,
septate, tapering
to an acute apex
20–28 wide,
composed
cells of
textura
angularis
110–140 × 17–23,
8–spored, bitunicate,
cylindrical, short-
pedicellate, apically
rounded.
95–115 (–128) × 4.5–6.5,
fasciculate, broadly
filiform, cylindrical to long
subfusiform, elongate,
rounded at ends, slightly
curved, guttulate, 12–13-
septate
Lu et al.
2017, 2018
237
Fig. 1 – Berkleasmium pandani A Colonies on natural substratum. B, C Squashed mount of
sporodochium. D Conidia with conidiogenous cell. Scale bars: A, D = 10 µm, C = 20 µm.
238
Fig. 2 – Berkleasmium pandani (Scanning electron micrograph) A, B Conidia. (CC=
Conidiogenous cell, C= Conidium). Scale bar: A, B = 20 µm.
239
Fig. 3 – Berkleasmium typhae A Colonies on natural substratum. B-E Squashed mount of
Sporodochium. Scale bars: B= 10 µm, C-E= 20 µm.
240
Fig. 4 – Berkleasmium typhae (Scanning electron micrograph) A, C Part of sporodochium showing
conidia. B Conidia. Scale bars: A= 10 µm, B= 50 µm, C= 20 µm
Checklist of Berkleasmium from India.
Berkleasmium ariense Rajeshk. & Marathe, in Tibpromma et al., Fungal Diversity 83: 35 (2017).
Distribution: Maharashtra, Tamhini Village, on unidentified stem litter (Tibpromma et al. 2017)
Berkleasmium conglobatum (Cooke & Ellis) R.T. Moore, Mycologia 50(5): 687 (1959) [1958]
≡ Sporidesmium conglobatum Cooke & Ellis, Grevillea 8(no. 45): 11 (1879)
Distribution: On bark of Syzygium fruiticosum New Delhi (Chowdhry 1974)
Berkleasmium corticola (P. Karst.) R.T. Moore, Mycologia 51(5): 735 (1961) [1959]
241
≡ Sporidesmium corticola (P. Karst.) Mussat [as ‘corticolum’], in Saccardo, Syll. fung. (Abellini)
15: 398 (1901)
≡ Sporidesmium moriforme subsp. corticola P. Karst., Meddn Soc. Fauna Flora fenn. 14: 99 (1887)
Distribution: On dead bark of Tectona grandis, Jabalpur Madhya Pradesh (Sharma 1980), on
Syzygium fruiticosum Agra Uttar Pradesh (Sharma et al. 1976)
Berkleasmium leonense M.B. Ellis, More Dematiaceous Hyphomycetes (Kew): 69 (1976)
Dead twigs of Odina wodier, Moonar, kerala (Rao & Varghese 1979, Varghese & Rao 1979);
Distribution: unidentified dead wood, Dehradun, Uttrakhand (Begum et al. 1978);
Berkleasmium osmaniae P. Rag. Rao & D. Rao, Mycopath. Mycol. appl. 22: 314 (1964)
Distribution: Dead culms of gramineae, hydrabad Andhra Pradesh (Rao & Rao 1964)
Acknowledgements
The authors are thankful to Ministry of Environment and Forests, Government of India for
the financial assistance (vide letter no. 14/26/2008–ERS/RE dt. 06.06.2010), UGC (SAP, DRS III)
and Chairperson Department of Botany Panjab University Chandigarh for providing infrastructural
and laboratory facilities.
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