Journal of Threatened Taxa |
www.threatenedtaxa.org | 26 May 2022 | 14(5): 21076–21083
ISSN 0974-7907
(Online) | ISSN 0974-7893 (Print)
https://doi.org/10.11609/jott.6721.14.5.21076-21083
#6721 | Received 17
September 2020 | Final received 09 March 2022 | Finally accepted 01 April 2022
Two new varieties of Russula Pers. (Basidiomycota: Russulaceae) from Sal forests of Shiwaliks,
India
Jitender Kumar 1 & Narender Singh Atri
2
1 Department of Botany, Rajiv
Gandhi Govt. College, Chaura Maidan, Shimla, Himachal
Pradesh 171004, India.
2 Department of Botany, Punjabi
University, Patiala, Punjab 147002, India.
1 jitenderthakur2010@gmail.com
(corresponding author), 2 narinderatri04@gmail.com
Editor: Richard Mibey,
Nairobi, Kenya. Date of publication: 26 May 2022
(online & print)
Citation: Kumar, J. & N.S. Atri (2022). Two new
varieties of Russula Pers. (Basidiomycota: Russulaceae) from Sal forests of Shiwaliks,
India. Journal of Threatened Taxa 14(5): 21076–21083. https://doi.org/10.11609/jott.6721.14.5.21076-21083
Copyright: © Kumar & Atri 2022. Creative
Commons Attribution 4.0 International License.
JoTT allows unrestricted use, reproduction,
and distribution of this article in any medium by providing adequate credit to
the author(s) and the source of publication.
Funding: This study was
supported by Council of Scientific and Industrial
Research, New Delhi, India (Grant number 09/140
(0159) 2014-EMR-1).
Competing interests: The authors
declare no competing interests.
Author details: Dr.
Jitender Kumar is currently working as assistant professor at Department
of Botany, Rajiv Gandhi Govt. Degree College Chaura
Maidan, Shimla. Dr. N.S. Atri is a mycologist and
retired professor from Department of Botany, Punjabi University, Punjab.
Author contributions: Both the authors carried out the
research work. The first draft of the manuscript was written by Jitender Kumar
and Narender Singh Atri commented on previous
versions of the manuscript. Both the authors read and approved the final
manuscript.
Acknowledgements: We would like to express our
sincere gratitude to the Head, Department of Botany, Punjabi University,
Patiala for providing laboratory facilities and to the Council of Scientific
and Industrial Research (CSIR), New Delhi, India for financial assistance under
CSIR-JRF fellowship scheme. To UGC, DST and DBT we are indebted for financial
assistance under different schemes to the Department during the course of the
present work.
Abstract: This paper deals with two new
varieties of Russula species, R. camarophylla var. reticulospora
var. nov. and R. aurea
var. minuta var. nov. These were collected from the Shiwalik
range of northwestern India, in association with Shorea robusta. Russula aurea var. minuta differs from R. aurea
in having small sized sporophores, dentate to wavy
gill edges with golden or yellow deposition instead of smooth and much smaller
spores. Whereas, mushroom R. camarophylla var.
reticulospora is close to Russula
camarophylla except for the
larger carpophores that have white cream pileus surface and larger spores.
In basidiospores warts are connected to form mostly complete reticulum instead
of mostly isolated warts reported in Russula
camarophylla. In view of the presence of some
unique varied features in the presently examined collections two new varieties
of Russula has been proposed.
Keywords: Diversity, Ectomycorrhiza, R.
camarophylla var. reticulospora
var. nov., R. aurea var.
minuta var. nov.,
scanning electron microscopy, taxonomy.
INTRODUCTION
Genus Russula is one of the dominant basidiomycetous fungi
genus which grow in a wide variety of habitats. These are mostly found in
mycorrhizal association with variety of plants including trees (Corrales et al.
2016). Studies on taxonomy and diversity of genus Russula
are inviting more attention now a days primarily because of their importance in
human welfare, ecosystem functioning and stability. These macro-fungi are
important source of food, medicine, nutraceuticals and also play a pivotal role
in ecosystem strengthening and maintenance as mycorrhizal associates (Manoharachary et al. 2005). It is reported that Russula spp. can form EcM
with many temperate and tropical plant families, including Leguminosae, Fagaceae, Cistaceae,
Dipterocarpaceae, Salicaceae, Betulaceae, Nothofagaceae,
Myrtaceae, and Pinaceae
(Tedersoo et al. 2010; Wang et al. 2017). The compounds derived from these mushrooms
are reported to boost up immune system and avert diseases thereby improving
human health (Wasser 2002). Different species of Russula
are known to possess anti-inflammatory, antiviral, antibacterial,
antiparasitic, antioxidant, hepatoprotective, anticancer, and antidiabetic
properties (Wasser 2011).
To date,
approximately 1,100 Russula species have been
reported worldwide (Kirk 2014) and distributed across a wide range of habitats
from the tropics to arctic zones (Riviére et al.
2007; Ba et al. 2012). Russula is one of the
dominant ectomycorrhizal genera in Indian Himalaya (Saini & Atri 1984, 1989; Atri & Saini
1986; Atri et al. 1994; Kumar & Atri 2016, 2019; Sharma et al. 2016) and is represented by
ca. 158 taxa from India (Sharma et al. 2017). While investigating the EcM diversity of Sal forest, two varieties of R. camarophylla Romagn. and
R. aurea Pers. were documented, which upon
investigation were found to be new to science based on detailed macro- and
micro-morphological examination. In the present study sporocarps and their EcM colonised roots were
collected by tracing the hyphal or rhizomorphs connections in association with Shorea robusta from
pure Sal forests. These species are fully illustrated and described in this
paper.
MATERIALS AND METHODS
Study area
Area
selected for the present investigation is Sal forests of Shiwalik
mountain range of northwestern India (Figure 1), which represent the
geologically lowest and youngest mountain range of Himalaya. The study area is
located between 30.316N, 78.032E.
Elevation range of the area is 400–1500 m and vegetation of the area is
typical of tropical moist deciduous type (Champion & Seth 1968).
Sampling,
identification and characterization
Sporocarps
were collected from different localities of pure Sal forests, during the rainy
season of 2013–2015. Macromorphological features were recorded from fresh
collections in the field and colour codes used are
that of Kornerup & Wanscher
(1978). After noting down morphological characters on the field key (Atri et al. 2005) some pieces of sporocarps from cap and
stipe were preserved in liquid preservative (25 ml rectified alcohol (95%) + 5
ml formalin (37%) + 70 ml distilled water) for studying the microscopic
characters. By adopting the standard procedures spore deposit was taken after
bringing the specimens to the temporary laboratory setup. Sporocarps were air
dried at 40–45 0C in a drier specially designed for drying mushroom
specimens (Atri et al. 2005) which were finally
packed in a cellophane paper packet for permanent preservation in Punjabi
University Herbarium under PUN. The cross section of pileus and longitudinal
section of stipe were stained in congo red for
examination, drawn under a compound microscope and photographed under digital
microscope (Leica DM4000 B LED). Observation of basidia, cystidia, and elements
of pileipellis and stipitipellis
were recorded for further use in taxonomic categorization. Melzer’s reagent was
used to observe the amyloidy in basidiospore
ornamentation. The microscopic details were worked out as per standard
methodology (Singer 1986; Atri et al. 2000, 2017).
Scanning
electron microscopy
Scanning
electron microscopic (SEM) studies of basidiospores were carried out with
JSM6610LV GEOL scanning electron microscope. For SEM examination basidiospores
from spore print and lamellae tissue were mounted on a double-sided adhesive
tape pasted on a metallic specimen holder or stub. The material was scanned at
different magnification ranging 3,000–15,000 X in high vacuum mode to observe
pattern of spore ornamentation.
TAXONOMY
Russula aurea Pers. var. minuta
var. nov.
(Image 1a–h,
Figure 2A–G)
MycoBank number:
MB834095
Diagnosis: Russula aurea Pers. var. minuta var. nov. is
characterised by small golden to brightly yellow
pileus with more darker brownish-yellow centre;
dentate to wavy gill edges with golden deposition instead of smooth; sour taste
, much smaller spores size and presence of pilocystidia.
Etymology: The variety
name is based on the smaller size of sporophore and
basidiospore as compared to Russula aurea.
Holoype: PUN 9112, Male, 27 July 2013, Rajban, Dehradun, Uttrakhand,
India, 30.316N, 78.032E, 800 m, coll. J. Kumar.
Paratype:
PUN 9113, 1 ex., Male, 21 August 2015, Kalsi, Dehradun, Uttrakhand,
India, 30.316N, 78.032E, 1,190 m, coll.
J. Kumar.
Taxonomic
description
Sporophores 2.0–2.5 cm in height. Pileus 1.3-2.0 cm broad,
convex to hemispherical when young, flattened depressed at maturity; centre umbonate when young, golden (6C7) to brightly yellow
with more darker brownish-yellow centre; margin
regular to slightly irregular, nonsplitting at
maturity, moist, unchanging, apex depressed at maturity with slight umbo;
cuticle half peeling; flesh 0.1 cm thick in the centre,
almost absent along the margin, white (1A1), changes to light brown on bruising
and cutting, brittle; taste sour, odour mild. Lamellae adnexed to
slightly adnate, equal, moderately broad (2–3 mm), crowded (12–16 gills/cm),
white with golden edges; gill edges not smooth, eroded or wavy. Stipe central,
1.5–2.0 cm in length, 0.3–0.5 cm broad, cylindrical to slightly tapering
downward, white (1A1) in the upper half, yellowish to pale white in the lower
half, unchanging, first solid, than hollow, smooth. Spore deposit deep ochre.
Basidiopores 5.0–6.5 (7.5) × 4.0–5.0 (6.0) µm (excluding
ornamentation), broadly ellipsoidal to ellipsoid (Q =1.2–1.3), warty; warts up
to 0.8 µm high, mostly connected by thick and thin lines to form partial to
complete reticulum, ornamentation type IIIa, IIIb,
IV, amyloid; plage hyaline, indistinct; apiculate, apiculus up to 1.6 µm long. Basidia 19.5–32.6 × 6.5–9.0 µm,
clavate, bisporic to tetrasporic,
hyaline, abundant; sterigmata up to 3.5 µm long; pleurocystidia 26.0–40.9 ×
6.5–9.8 µm, clavate to ventricose granulated;
cheilocystidia 22.5–37.4 × 4.1–13.1 µm, similar to pleurocystidia. Pileus
cuticle clearly differentiated, epicutis gelatinised, heteromerous,
palisade having interwoven projecting septate 3–5 µm broad hyphae mixed with
5–10 µm broad sphaerocyst and dermatocystidia,
cuticle hyphae and cellular mass having dark yellow content throughout; pilocystidia 24.0–40.8 × 4.9–8.2 µm, thin walled, clavate,
fusiform to fusoid ventricose
with acute to blunt end; context heteromerous having multiseptate 3.0–6.5 µm broad hyphae intermingled with
8.0–36.0 × 8.0–32.6 µm rosettes of sphaerocysts. Hymenophoral trama
16–100 µm, heteromerous with up to 3.3–5.0 µm broad
hyphae intermingled with 8.0–36.0 × 8.0–32.6 µm sphaerocysts.
Stipe cuticle gelatinised with more or less parallel
arranged 1.6–6.5 µm broad septate hyphae having yellowish content; context made
up of 12–28 × 12–24 µm sized rosettes of sphaerocysts
and 4–6 µm broad septate hyphae in alternate manner. Clamp connections
absent.
Chemical colour reaction: Stipe
surface pinkish with FeSO4, Gills turns carmine red in Sulphovanillin.
Habitat: Sporophores directly attached to the roots at the base of Shorea robusta
tree.
Collections
examined: Uttrakhand: Dehradun, Rajban (800 m), in groups in Sal forest in association with
Shorea robusta.
Jitender Kumar, PUN 9112, 27 July 2013. Dehradun, Kalsi (1,190 m), solitary in
Sal forest in association with S. robusta
tree. Jitender Kumar PUN 9113, 21 August 2015.
Remarks: The overall
diagnostic characters of the presently examined collection are in agreement
with Russula aurea
(Rayner 1970; Romagnesi 1967; Das & Marstad 2014) except that the carpophores are much smaller
in size (2.0–2.5 cm instead of 4–9 cm), gill edges not smooth (dentate to wavy
with golden or yellow deposition instead of smooth), much smaller spores size
(5–7.5 × 4–6 µm instead of 7.5–10 × 6–8
µm) and presence of pilocystidia which are absent in
case of Russula aurea.
In view of the presence of some unique varied features in the presently
examined collections in comparison to R. aurea,
a new variety minuta has been named.
Russula camarophylla Romagn. var. reticulospora
var. nov.
(Image 2a–h,
Figure 3A–G)
MycoBank number:
MB834095
Diagnosis: Russula camarophylla Romagn. var. reticulospora
var. nov. is characterised by larger sporophore
with creamish-white pileus surface, distantly spaced
lamellae, very hard and compact flesh and larger spore size. Also in
basidiospores warts are connected to form mostly dense complete reticulum.
Etymology: The variety
name is based on the densely reticulated basidiospores.
Holoype: PUN 9124, Male, 30 August 2013,
Kalsi, Dehradun, Uttarakhand, India, 1,190 m, 30.316N, 78.032E, coll. J.
Kumar.
Taxonomic
description
Sporophore 7.5 cm in height. Pileus 10 cm broad, umblicate with a depressed disc and irregular margin;
pileus surface moist, glabrous, cream white to white (1A1), not peeling; flesh
5 mm thick in the centre, off white to slightly creamish, unchanging. Lamellae unequal broadly adnate to
decurrent, distant (3–4 gills/cm), broad (11 mm at the centre),
creamish-white to orange white (5A2), forked near the
base, lamellulae present, gill edges smooth, normal. Stipe 2 cm long and up to
2 cm broad, central, solid, white, fleshy, concolorous with the pileus,
unchanging on cutting and bruising; flesh taste spicy; odour
fruity, spore deposit yellowish-white.
Basidiospores
6.5–8.0 (9.0) × 5.0–7.0 (7.5) µm, subglobose to
broadly ellipsoid (Q= 1.12–1.33), densely ornamented, warty, warts up to 0.5
µm, connected to form mostly complete reticulum, superahilar
area usually with low ornamentation, ornamentation type IIIa, IIIb; apiculate, apiculus up to
1.6 µm in size. Basidia 35–57 × 5.0–8.5 µm, clavate to subcylindric,
2–4 spored, sterigmata 6.5–9.8 µm long.
Pleurocystidia 39.0–86.5 × 4.8–9.8 µm, clavate, fusiform, fusoid
clavate to fusoid ventricose,
often acute to blunt ended, granulated to hyaline; arising usually from the subhymenium, nonprojecting. Cheilocystidia 35.8–48.9 ×
4.8–9.0 µm, clavate to fusiform, apically acute to blunt, mostly hyaline, gill
edges heteromorphic; subhymenium 31.4–47.2 µm, heteromerous with 3–13 µm broad hyphae interspersed with
3.0–11.5 × 3.0–10.0 µm sphaerocyst; hymenophoral trama 471–942 µm, mostly cellular with 6.5–11.5 µm hyphae
and 6.5–42.5 × 4.9–42.5 µm sphaerocyst. Pileus
cuticle up to 240 µm broad, trichoderm of nongelatinous, 6.5–18.2 µm interwoven septate projecting
hyphae, hyphae ending attenuate or rounded and some ending with inflated or
rounded cells, hyphal cells cylindric to ampullate at
both sides of the septum, septa mostly constricted, some hyphae with large
inflated cells in the intercalary position. Subcutis not clearly
differentiated, made up of interwoven, nongelatinous,
6.5–18.5 µm broad hyphae with a few inflated scattered cells. Stipe composed of
parallel arranged interwoven septate up to 4.9 µm broad hyphae; caulocystidia 21–41 × 3–5 µm, cylindric to clavate, rounded
apically.
Chemical colour reactions: Stipe
surface pinkish with FeSO4, gills turns carmine red in Sulphovanillin.
Collection
examined: Uttarakhand: Kalsi (1,190 m), in association with Shorea
robusta. Jitender Kumar, PUN 9124, 30 August
2013.
Habitat: Solitary on
the ground in monsoon under Shorea robusta tree.
Remarks: The
external and internal characters of the presently examined collection are in
agreement with Russula camarophylla
(Romagnesi 1968) except that the carpophores are
larger in size with cream white pileus surface and larger spore size (6.5–9 ×
5–7.5 µm instead of 5–6.2 (7) × 3.6–4.8 µm). In basidiospores warts are
connected to form mostly complete reticulum instead of mostly isolated warts in
case of Russula camarophylla
as documented in literature.
DISCUSSION
During the
present study, R. aurea var. minuta and R. camarophylla
var. reticulospora were found forming
direct organic connection with Shorea robusta. The overall diagnostic characters of the
presently examined collections of R. aurea
var. minuta are in agreement with Russula aurea Pers.
which is commonly known as the gilded brittle gill or golden Russula and is an uncommon species of mushroom found
in deciduous woodland forests. Its specific epithet aurea
has been derived from the Latin word aurum, which means
golden. Unlike many red-capped members of the genus, Russula
aurea is edible and mild-tasting and is
easily characterised in the field by its golden
pileus, free to adnexed broad fairly distant golden
gills, cylindrical smooth light yellow stipe and brittle yellow flesh. Mostly
it is reported to grow solitary or scattered forming mycorrhizal association
with pine trees (Romagnesi 1967; Rayner 1970; Das
& Marstad 2014). Russula
aurea var. minuta
differs from R. aurea except in having small
sized sporophores, dentate to wavy gill edges with
golden or yellow deposition instead of smooth, much smaller spores and presence
of pilocystidia which are absent in case of Russula aurea. In
view of this a new variety Russula aurea var. minuta has
been proposed. Russula aurora probably
appears to be morphologically closest
species to this undescribed taxon from which it
differs in having fairly crowded pale cream lamellae with abundant forkation near the stipe, mild taste, and absence of dermatocystidia in pileipellis
and low warted spores (0.25–0.5 µm) with few
connections (Romagnesi 1967). Another close taxon is Russula aurantiaca
which differs from R. aurea var. minuta in having usually brick-orange, copper
to carmine coloured cap, widely spaced rather thick
bright yellow ochre strongly interveined lamellae and
presence of mild to slightly acrid taste (Romagnesi
1967). Earlier Russula aurea
was known as R. aurata and under this name it
was documented from different localities of northwestern Himalaya from
coniferous and angiospermic forest (Saini & Atri 1984, 1989; Atri & Saini
1986; Atri et al. 1994). The present collection is
found in pure Sal forest in close vicinity to Shorea
robusta tree from Uttarakhand.
Russula camarophylla, a rare
western Mediterranean European representative of section Archaeinae
is characterized by its camarophylloid habit, pale
ochre or creamish sporophores
with distant lamellae, very hard and compact flesh, hygrophoroid basidia and
tiny spores with barely visible ornamentation (Romagnesi
1968). The present collection of R. camarophylla var.
reticulospora is close to Russula
camarophylla (Romagnesi
1968) except that the carpophores are larger in size with white cream pileus
surface and larger spore size. In basidiospores warts are connected to form
mostly complete reticulum instead of mostly isolated warts reported in case of Russula camarophylla
(Romagnesi 1968). In view of this a new variety Russula camarophylla
var. reticulospora has been proposed. The
apical swelling of hyphal terminations in the pileipellis
is an important feature that is very common within Russula
camarophylla (Buyck et
al. 2003) and presently examined collection. R. camarophylla
var. reticulospora also resembles the
recently described Russula capillaris,
by Buyck (in Wang et al. 2019) from
Madagascar. The latter species is not only very similar in the field, but it
also possesses similar apical swellings in the hyphal terminations of pileipellis. Spores, however, are much smaller with
isolated and very low warts (0.1–0.2 µm) in R. capillaris
and, again, the pileocystidia are not septate. Russula camarophylla
is a very rare species and has been found only a few times in France (Buyck et al. 2003), northern Italy (Setti
& Bigoni 1998; Boffelli
2012) and Austria (Pidlich-Aigner & Klofac 2018).
CONCLUSION
Two new
varieties of Russula species, viz. R. camerophylla var. reticulospora
var. nov. and R. aurea
var. minuta var. nov.
have been described based upon detailed macro- and micromorphological
comparison with already existing Russula
species. The newly proposed varieties are putative mycorrhizal associates of
Sal and were found in direct organic connection with Shorea
robusta roots.
For
figures & images - - click here
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