Micromorphological characteristics of the species of Pholiota (Strophariaceae, Basidiomycota) in pure culture
The article presents results of the research on micromorphology of vegetative mycelia of eight species of the genus Pholiota from the IBK Mushroom Culture Collection of the M.G. Kholodny Institute of Botany, National Academy of Sciences of Ukraine. Using scanning electron microscopy and light micr...
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Інститут ботаніки ім. М.Г. Холодного НАН України
2019
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irk-123456789-1767582021-02-08T01:26:50Z Micromorphological characteristics of the species of Pholiota (Strophariaceae, Basidiomycota) in pure culture Regeda, L.V. Bisko, N.A. Гриби і грибоподібні організми The article presents results of the research on micromorphology of vegetative mycelia of eight species of the genus Pholiota from the IBK Mushroom Culture Collection of the M.G. Kholodny Institute of Botany, National Academy of Sciences of Ukraine. Using scanning electron microscopy and light microscopy, the micromorphological structures specific to these species were studied in order to enable their identification in pure culture. New data on micromorphology of Pholiota species are given. A set of micromorphological structures was observed for this genus, namely clamp connections, chlamydospores, arthrospores, anastomoses, crystals on hyphae, hyphal rings, rhizomorphs, pellicle spots, hyphae ornamentation, and secretory hyphae. For the first time a detailed study of microstructures of P. alnicola, P. limonella, P. nameko, P. populnea, and P. subochracea was conducted. Secretory hyphae and vacuolized mycelia in pure culture were noticed only for P. populnea. For P. subochracea, various hyphae ornamentation on vegetative mycelium was demonstrated. New information about the presence of hyphal rings for three Pholiota species, P. alnicola, P. limonella, and P. subochracea, is presented. Представлені результати досліджень мікроморфології вегетативного міцелію восьми видів роду Pholiota з Колекції культур шапинкових грибів Інституту ботаніки ім. М.Г. Холодного НАН України (ІВК). За допомогою світлової мікроскопії та сканувальної електронної мікроскопії були вивчені мікроморфологічні структури, специфічні для цих видів та необхідні для їхньої ідентифікації в чистій культурі. Наведено нові дані з мікроморфології видів роду Pholiota. Відмічено сукупність мікроморфологічних структур, а саме: пряжки, хламідоспори, артроспори, анастомози, кристали на гіфах, гіфальні кільця, ризоморфи, міцеліальні плівки, секреторні гіфи на вегетативному міцелії, орнаментація гіф. В нашому дослідженні вперше проведено детальне вивчення мікроструктур P. alnicola, P. limonella, P. nameko, P. populnea та P. subochracea для уточнення морфологічних характеристик та надійної ідентифікації цих видів у чистій культурі. Лише для P. populnea було відмічено існування секреторних гіф і вакуолізованого міцелію. Для P. subochracea отримана інформація щодо орнаментації гіф на вегетативному міцелії. Гіфальні кільця вперше виявлені у трьох видів – P. alnicola, P. limonella і P. subochracea. 2019 Article Micromorphological characteristics of the species of Pholiota (Strophariaceae, Basidiomycota) in pure culture / L.V. Regeda, N.A. Bisko // Український ботанічний журнал. — 2019. — Т. 76, № 2. — С. 114-120. — Бібліогр.: 27 назв. — англ. 0372-4123 DOI: https://doi.org/10.15407/ukrbotj76.02.114 http://dspace.nbuv.gov.ua/handle/123456789/176758 en Український ботанічний журнал Інститут ботаніки ім. М.Г. Холодного НАН України |
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Digital Library of Periodicals of National Academy of Sciences of Ukraine |
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Гриби і грибоподібні організми Гриби і грибоподібні організми |
| spellingShingle |
Гриби і грибоподібні організми Гриби і грибоподібні організми Regeda, L.V. Bisko, N.A. Micromorphological characteristics of the species of Pholiota (Strophariaceae, Basidiomycota) in pure culture Український ботанічний журнал |
| description |
The article presents results of the research on micromorphology of vegetative mycelia of eight species of the genus
Pholiota from the IBK Mushroom Culture Collection of the M.G. Kholodny Institute of Botany, National Academy of Sciences
of Ukraine. Using scanning electron microscopy and light microscopy, the micromorphological structures specific to these
species were studied in order to enable their identification in pure culture. New data on micromorphology of Pholiota species
are given. A set of micromorphological structures was observed for this genus, namely clamp connections, chlamydospores,
arthrospores, anastomoses, crystals on hyphae, hyphal rings, rhizomorphs, pellicle spots, hyphae ornamentation, and
secretory hyphae. For the first time a detailed study of microstructures of P. alnicola, P. limonella, P. nameko, P. populnea,
and P. subochracea was conducted. Secretory hyphae and vacuolized mycelia in pure culture were noticed only for
P. populnea. For P. subochracea, various hyphae ornamentation on vegetative mycelium was demonstrated. New information
about the presence of hyphal rings for three Pholiota species, P. alnicola, P. limonella, and P. subochracea, is presented. |
| format |
Article |
| author |
Regeda, L.V. Bisko, N.A. |
| author_facet |
Regeda, L.V. Bisko, N.A. |
| author_sort |
Regeda, L.V. |
| title |
Micromorphological characteristics of the species of Pholiota (Strophariaceae, Basidiomycota) in pure culture |
| title_short |
Micromorphological characteristics of the species of Pholiota (Strophariaceae, Basidiomycota) in pure culture |
| title_full |
Micromorphological characteristics of the species of Pholiota (Strophariaceae, Basidiomycota) in pure culture |
| title_fullStr |
Micromorphological characteristics of the species of Pholiota (Strophariaceae, Basidiomycota) in pure culture |
| title_full_unstemmed |
Micromorphological characteristics of the species of Pholiota (Strophariaceae, Basidiomycota) in pure culture |
| title_sort |
micromorphological characteristics of the species of pholiota (strophariaceae, basidiomycota) in pure culture |
| publisher |
Інститут ботаніки ім. М.Г. Холодного НАН України |
| publishDate |
2019 |
| topic_facet |
Гриби і грибоподібні організми |
| url |
http://dspace.nbuv.gov.ua/handle/123456789/176758 |
| citation_txt |
Micromorphological characteristics of the species of Pholiota (Strophariaceae, Basidiomycota) in pure culture / L.V. Regeda, N.A. Bisko // Український ботанічний журнал. — 2019. — Т. 76, № 2. — С. 114-120. — Бібліогр.: 27 назв. — англ. |
| series |
Український ботанічний журнал |
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AT regedalv micromorphologicalcharacteristicsofthespeciesofpholiotastrophariaceaebasidiomycotainpureculture AT biskona micromorphologicalcharacteristicsofthespeciesofpholiotastrophariaceaebasidiomycotainpureculture |
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2025-07-15T14:39:12Z |
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2025-07-15T14:39:12Z |
| _version_ |
1837724186522419200 |
| fulltext |
114 Ukrainian Botanical Journal, 2019, 76(2)
https://doi.org/10.15407/ukrbotj76.02.114
Micromorphological characteristics of the species of Pholiota
(Strophariaceae, Basidiomycota) in pure culture
Liubov V. REGEDA, Nina A. BISKO
M.G. Kholodny Institute of Botany, National Academy of Sciences of Ukraine
2 Tereschenkivska Str., Kyiv 01004, Ukraine
regeda.lyubov@gmail.com
Regeda L.V., Bisko N.A. 2019. Micromorphological characteristics of the species of Pholiota (Strophariaceae, Basidiomycota) in
pure culture. Ukrainian Botanical Journal, 76(3): 114–120.
Abstract. The article presents results of the research on micromorphology of vegetative mycelia of eight species of the genus
Pholiota from the IBK Mushroom Culture Collection of the M.G. Kholodny Institute of Botany, National Academy of Sciences
of Ukraine. Using scanning electron microscopy and light microscopy, the micromorphological structures specific to these
species were studied in order to enable their identification in pure culture. New data on micromorphology of Pholiota species
are given. A set of micromorphological structures was observed for this genus, namely clamp connections, chlamydospores,
arthrospores, anastomoses, crystals on hyphae, hyphal rings, rhizomorphs, pellicle spots, hyphae ornamentation, and
secretory hyphae. For the first time a detailed study of microstructures of P. alnicola, P. limonella, P. nameko, P. populnea,
and P. subochracea was conducted. Secretory hyphae and vacuolized mycelia in pure culture were noticed only for
P. populnea. For P. subochracea, various hyphae ornamentation on vegetative mycelium was demonstrated. New information
about the presence of hyphal rings for three Pholiota species, P. alnicola, P. limonella, and P. subochracea, is presented.
Keywords: light microscopy, macrofungi, micromorphological structures, Pholiota, pure culture, scanning electron microscopy,
vegetative mycelium
Регеда Л.В., Бісько Н.А. 2019. Мікроморфоогічні характеристики видів роду Pholiota (Strophariaceae, Basidiomycota) у
чистій культурі. Український ботанічний журнал, 76(3): 114–120.
Інститут ботаніки ім. М.Г. Холодного НАН України
вул. Терещенківська 2, Київ, 01004, Україна
Резюме. Представлені результати досліджень мікроморфології вегетативного міцелію восьми видів роду Pholiota
з Колекції культур шапинкових грибів Інституту ботаніки ім. М.Г. Холодного НАН України (ІВК). За допомогою
світлової мікроскопії та сканувальної електронної мікроскопії були вивчені мікроморфологічні структури, специфічні
для цих видів та необхідні для їхньої ідентифікації в чистій культурі. Наведено нові дані з мікроморфології видів роду
Pholiota. Відмічено сукупність мікроморфологічних структур, а саме: пряжки, хламідоспори, артроспори, анастомози,
кристали на гіфах, гіфальні кільця, ризоморфи, міцеліальні плівки, секреторні гіфи на вегетативному міцелії,
орнаментація гіф. В нашому дослідженні вперше проведено детальне вивчення мікроструктур P. alnicola, P. limonella,
P. nameko, P. populnea та P. subochracea для уточнення морфологічних характеристик та надійної ідентифікації цих
видів у чистій культурі. Лише для P. populnea було відмічено існування секреторних гіф і вакуолізованого міцелію.
Для P. subochracea отримана інформація щодо орнаментації гіф на вегетативному міцелії. Гіфальні кільця вперше
виявлені у трьох видів – P. alnicola, P. limonella і P. subochracea.
Ключові слова: вегетативний міцелій, макроміцети, мікроморфологічні структури, світлова мікроскопія, сканувальна
електронна мікроскопія, чиста культура, Pholiota
© 2019 L.V. Regeda, N.A. BIsko
Introduction
About 470 species of the genus Pholiota (Fr.) P.Kumm.
are known worldwide (http://www.mycobank.org), 25
of them have been reported for Ukraine (Zerova, 1979;
Dudka et al., 2009). Mushrooms received attention
due to combination of nutritious properties with
health-stimulating and medicinal effects (Kim et al.,
2006). Anticarcinogenic, antioxidant, antimicrobial
and immunomodulating properties of the components
isolated from mycelia and fruit bodies of this genus have
been established (Cho et al., 2003; Kim et al., 2006;
Zhang et al., 2009). Using mushrooms as a source of
preventive and therapeutic agents and their cultivation
in the industrial scale have been realized after many
years of fundamental research of biology of macrofungi,
peculiarities of their growth and development, and
nature and mechanisms of metabolic and enzymatic
activity (Wasser, 2010). Fruit bodies of P. adiposa and
P. nameko are cultivated in the countries of Southeast
Asia in the industrial scale (Pegler, 2003; Gizaw, 2015).
Taxonomic features of macrofungi can be used for
their identification in pure culture, therefore research
mailto:regeda.lyubov@gmail.com
115Український ботанічний журнал, 2019, 76(2)
on their micromorphological structures is important.
Micromorphological characteristics of Basidiomycetes
include a set of microscopic features such as presence
of clamp connections or pseudo-clamp connections,
width and types of hyphae according to the traditional
classification by Stalpers (1978), presence of
anastomoses and various structures formed during
differentiation of the hyphae in culture (hyphal rings,
rhizomorphs, inlaid hyphae, crystals on hyphae,
etc.), presence of asexual reproduction structures
(Mykhaylova, 2014).
This study was focused on micromorphological
structures of eight species of the genus Pholiota preserved
in the IBK Mushroom Culture Collection.
The study of microstructures of the Pholiota species
was traditionally conducted based on fruiting bodies
collected in natural habitats (Sawyer, 1917; Hesler,
1968; Farr et al., 1977; Farr, 1985; Smith, Adamcik
et al., 2006; Kirk et al., 2008; Chang, Hayes, 2013).
In contrast, in pure culture these species were poorly
studied. Microstructures only of few species from the
genus Pholiota were investigated, P. adiposa, P. aurivella,
P. lenta, P. nameko, and P. squarrosa (Yoshinori et al.,
1999; Buchalo, Didukh, 2005; Buchalo et al., 2009,
2011; Dyakov et al., 2011). Our research was aimed at
studying microstructures of some of these and other
species of the genus.
Materials and methods
Eight strains of Pholiota species from the IBK
Mushroom Culture Collection of the M.G. Kholodny
Institute of Botany, National Academy of Sciences of
the Ukraine were investigated (Bisko et al., 2016). Some
of these strains were obtained in 2017–2018 (Table 1).
Mushroom cultures were grown on glucose peptone
yeast agar media; g/l: glucose – 25; peptone – 3; yeast
extract – 3; MgSO
4
– 0.25; KH
2
PO
4
– 1; K
2
HPO
4
– 1;
agar-agar – 22; pH – 6.0) in Petri dishes at temperature
26 ± 1 ºC. Mycelia were taken from the cultures in
the phase of active growth (3–10 days) and from the
long-term cultivation of Pholiota species (2 months).
Vegetative mycelium microstructures were studied
using Zeiss light microscope (LM) and scanning
electron microscopy (SEM). Samples were prepared
for light microscopy using distilled water, 10% KOH
or preparative mixture (glycerin: ethanol: water = 1:
1: 1) (Bilay, 1982). Samples were prepared for SEM
using the modified method of Quattelbaum and Carner
(Quattelbaum, Carner, 1980). Four sterilized square 4×4
mm pieces of the cover glass were placed 1–3 cm away
from inoculum into Petri dishes. The cover glasses were
removed from the agar media, when mycelia overgrew
the surface, and then transferred to a microscopic slide.
The slide was then placed into a sealed glass vessel fixed
with osmium tetroxide vapor (1% solution) for 8 hours.
On fixation, the slides were transferred to an empty
Petri dish to dry out for 72 hours. After drying out,
samples were covered with gold in the vacuum spray
gun JII-4X with rotation (Buchalo, Didukh, 2005). The
specimens were examined using the Jeon JSM-6060 LA
Scanning Electron Microscope (Japan) and studied at a
magnification ×1000 – 10000.
Results and discussion
An important taxonomic feature for identification
of macrofungi in pure culture is the presence of a
unique structure that occur on the mycelium of many
species of Basidiomycota clamp connections (Stalpers,
1978; Buchalo, Didukh, 2005). Though the clamp
connections are exclusive to this phylum, not all species
possess these structures. Regular clamp connections
were observed for vegetative mycelia in all studied
Table 1. List of the studied Pholiota species and strains
Species IBK strain Origin of culture, year
Pholiota adiposa (Batsch) P.Kumm. 2169 Ukraine, Kyiv, on Populus, 2011
Pholiota alnicola (Fr.) Singer 2406 Ukraine, Ivano-Frankivsk Region, Halych, Halych National Nature Park, 2015
Pholiota aurivella (Batsch) P.Kumm. 2605 Ukraine, Kyiv Region, Vasylkiv, 2018
Pholiota limonella (Peck) Sacc. 2335 Ukraine, Kamianets-Podilskyi, 2013
Pholiota nameko (T.Ito) S.Ito & S.Imai 2154 Obtained from TSAU (AM2), Melitopol, Ukraine, 2011
Pholiota populnea (Pers.) Kuyper & Tjall.-Beuk. 2602 Ukraine, Kyiv, on Populus, 2018
Pholiota squarrosa (Oeder) P.Kumm. 2010 Obtained from MSU (3935), Moscow, Russia, 2009
Pholiota subochracea (A.H.Sm.) A.H.Sm. & Hesler 2535 Ukraine, Kyiv Region, Kyyliv, on soil, 2017
MSU – Moscow State University, Moscow, Russia; TSAU – Tauria State Agrotechnological University, Melitopol, Ukraine
https://www.sciencedirect.com/science/article/pii/S1340354099708715#!
116 Ukrainian Botanical Journal, 2019, 76(2)
species (Fig. 1), which agrees with the literature data
(Buchalo, Didukh, 2005; Buchalo et al., 2009, 2011;
Dyakov et al., 2011).
Vegetative mycelium of Pholiota species in pure
culture consist of the thin-walled, moderately branched,
regularly septated, uncolored hyphae of 1–3 μm in
diameter, with anastomoses formed between hyphae
(Table 2, Fig. 2, A) and pellicle spots on vegetative
mycelium (Table 2, Fig. 2, B). Hyphae fusion is carried
out through anastomoses and pellicle spots on vegetative
mycelium, which is a well-known phenomenon in the
phylum Basidiomycota (Buchalo et al., 2009).
The formation of secretory hyphae and vacuolised
mycelium in old cultures were noticed only in P. populnea
2602 (Fig. 3). Similar secretory hyphae were found for
Fistulina hepatica (Buchalo et al., 2009), Lepista nuda
(Badalyan, Gharibyan, 2017) and vacuolised mycelia for
Coprinopsis strossmayeri, Fomitopsis pinicola (Badalyan,
Gharibyan, 2017) and Ganoderma adspersum (Badalyan
et al., 2019). Hyphae ornamentation that was observed
in P. subochracea cultures and hyphal rings in old
cultures of P. alnicola, P. limonella and P. subochracea
can be used as diagnostic taxonomic characters (Fig. 4).
A B
Fig. 1. Clamp connections of Pholiota populnea 2602 (A) and Pholiota adiposa 2169 (B), SEM (×10000)
A B
Fig. 2. Anastomoses of Pholiota nameko 2154 (A) and pellicle spot on vegetative mycelia of Pholiota squarrosa 2010 (B), SEM
(×2000)
117Український ботанічний журнал, 2019, 76(2)
A B
A B
A B
Fig. 3. Exudate on hyphae (A), SEM (×10000) and vacuolised mycelium (B), LM (×40) of Pholiota populnea 2602
Fig. 4. Hyphae ornamentation (A), SEM (×10000) and hyphal
rings (B), LM (×40) of Pholiota subochracea
Fig. 5. Conidial sporulation of Pholiota aurivella 2605 (A), SEM (×4000), and Pholiota subochracea 2535 (B), LM (×40)
118 Ukrainian Botanical Journal, 2019, 76(2)
Species of macrofungi form different structures
of asexual reproduction (anamorph structures).
Chlamydospores and arthrospores are the most common
asexual reproduction structures of Basidiomycota
(Buchalo, Diduch, 2005; Buchalo et al., 2011).
Anamorphs can be used as a taxonomic criterion at the
species level, or sometimes for taxa of higher taxonomic
ranks, but most macrofungi do not have these structures.
We observed conidial sporulation in all studied cultures
(Fig. 5), except P. adiposa.
Single intercalary chlamydospores were observed
for six cultures – P. adiposa, P. alnicola, P. aurivella,
P. limonella, P. nameko, and P. subochracea (Table 2,
Fig. 6).
According to literature data (Buchalo, Didukh, 2005;
Buchalo et al., 2009; Dyakov et al., 2011), vegetative
mycelia of the strains of P. adiposa, P. aurivella, and
P. squarrosa are able to form a structure of asexual
reproduction, mitotic spores (arthrospores). We
observed arthrospores in our experiment only for
P. aurivella, P. adiposa, and P. limonella (Fig. 7).
The ability to form crystals is widely known for many
species of Basidiomycota which sometimes also depends
on the nutrient media and age of the mushroom cultures
(Buchalo et al., 2009; Dyakov et al., 2011). Crystal
formation was observed in almost all investigated
species of Pholiota (Table 2, Fig. 8). The morphology
of the crystals is very different. We observed prismatic,
cubic, hexahedral, sometimes of the undefined shape
crystals. Maximum length of the crystals was 12.2 μm,
minimum – 0.5 μm, width – 0.3–6.1 μm.
Thus, presence of clamp connections, ability to form
anastomoses and pellicle spots on vegetative mycelia,
formation of conidial sporulation, arthrospores and
chlamydospores, ability to secrete crystals different in
shape and size were observed for various investigated
species. Our results confirm some earlier literature
data (Buchalo, Didukh, 2005; Buchalo et al., 2009,
2011; Dyakov et al., 2011). Micromorphological
characteristics of the studied Pholiota species are shown
in Table 2.
Conclusions
The micromorphological features of eight species of
Pholiota from the IBK Mushroom Culture Collection
of the М.G. Kholodny Institute of Botany, National
Academy of Sciences of Ukraine were established.
For the first time we conducted a detailed study of
microstructures of vegetative mycelia of such species
A B
Fig. 6. Chlamydospores of Pholiota limonella 2335 (A), SEM (×4000), and Pholiota alnicola 2406 (B), LM (×40)
Fig. 7. Arthrospores of Pholiota limonella 2335, LM (×40)
119Український ботанічний журнал, 2019, 76(2)
as P. alnicola, P. limonella, P. nameko, P. populnea,
and P. subochracea for morphological characteristics
and identification of these taxa in pure culture. The
presence of all typical for the genus features has been
noted in various studied species.
New data about micromorphological features of
Pholiota species in pure culture were obtained. Only
for P. populnea the existence of secretory hyphae and
vacuolized mycelium and for P. subochracea – the
hyphae ornamentation on vegetative mycelium were
noticed. New information about the presence of hyphal
rings for three Pholiota species, P. alnicola, P limonella
and P. subochracea, is provided.
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A B
Fig. 8. Crystals of Pholiota adiposa 2169 (A), SEM (×3000) and Pholiota alnicola 2406 (B), SEM (×4500)
Table 2. Micromorphological features of vegetative mycelium of Pholiota species
Species, strain
A
n
as
to
m
os
es
A
rt
h
ro
sp
or
es
C
h
la
m
yd
os
po
re
s
C
la
m
p
co
n
n
ec
ti
on
s
C
on
id
ia
l s
po
ru
la
ti
on
C
ry
st
al
s
E
xu
da
te
o
n
h
yp
h
ae
H
yp
h
al
r
in
gs
P
el
lic
le
s
po
ts
o
n
v
eg
et
at
iv
e
m
yc
el
iu
m
Pholiota adiposa 2169 + + + + – + – – –
Pholiota alnicola 2406 – – +* +* +* +* – +* –
Pholiota aurivella 2605 + + + + + – – – +
Pholiota limonella 2335 +* – +* +* +* +* – +* –
Pholiota nameko 2154 +* – +* +* +* +* – – +*
Pholiota populnea 2602 +* – – +* +* +* +* – –
Pholiota squarrosa 2010 +* – – + + – – – +
Pholiota subochracea 2535 +* – +* +* +* +* – +* +*
"+" structures found; "–" structures not found; * new data for this species
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