First Record of Lactarius atlanticus (Russulaceae, Basidiomycetes) from Turkey in the Subgenus Russularia

Abstract

In this study, Lactarius atlanticus is reported for the first time from Turkey based on the evaluation of both molecular and morphological approaches.

Full text

FIRST RECORD OF Lactarius atlanticus (Russulaceae, Basidiomycetes) FROM TURKEY IN
THE SUBGENUS Russularia
Oğuzhan KAYGUSUZ
- 125 -
chapter
8
FIRST RECORD OF Lactarius atlanticus
(Russulaceae, Basidiomycetes) FROM
TURKEY IN THE SUBGENUS Russularia
Oğuzhan KAYGUSUZ1
1
https://orcid.org/0000-0003-3455-2965. Isparta University of Applied Sciences,
Atabey Vocational School, Department of Plant and Animal Production, Isparta, Turkey
to cite this chapter:
Kaygusuz, O. (2022). First Record of Lactarius atlanticus (Russulaceae, Basidiomycetes)
from Turkey in the Subgenus Russularia. R. C. Beram (Ed.), Interdisciplinary Basic
Science Research and Approaches (p. 125-144). Lithuania: SRA Academic Publishing

FIRST RECORD OF Lactarius atlanticus (Russulaceae, Basidiomycetes) FROM TURKEY IN
THE SUBGENUS Russularia
Oğuzhan KAYGUSUZ
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FIRST RECORD OF Lactarius atlanticus (Russulaceae, Basidiomycetes) FROM TURKEY IN
THE SUBGENUS Russularia
Oğuzhan KAYGUSUZ
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Introduction
The genus Lactarius Pers. (Russulaceae) is recognized as a worldwide
group of ectomycorrhizal fungi with more than 583 temperate species
(Kirk et al. 2008, Wang et al. 2018, Lee et al. 2019). The members of the
genus are characterized by milk-caps originated from the milky fluid
(latex) which is derived when the species are cut or damaged (Persoon
1797, Singer 1986). Molecular phylogenetic established that the milk-caps
are specific to a paraphyletic genus, which also lead to the segregation of
the genera Lactifluus (Pers.) Roussel and Multifurca Buyck & V. Hofst. from
Lactarius (Buyck et al. 2008, 2010). Lactarius consists of subgenera as
Lactarius subgenus Lactarius Pers., L. subg. Russularia (Fr. ex Burl.)
Kauffman and L. subg. Plinthogalus (Burl.) Hesler & A.H. Sm (Verbeken &
Nuytinck 2013, Wisitrassameewong et al. 2014a).
The biodiversity of one of major subgenera Lactarius subg. Russularia was
previously studied in Europe and in North America (Hesler & Smith 1979,
Heilmann-Clausen et al. 1998, Basso 1999) and some described species
have been reported from Southeast Asia (Verbeken 2001, Verbeken et al.
2014, Wisitrassameewong et al. 2014a, 2014b, 2015, 2016).
In Europe, L. sect. Olentes (Bataille) Basso (L. subg. Russularia) is
represented by L. atlanticus Bon, L. serifluus (DC.: Fr.) Fr., L. subumbonatus
Lindgr., L. camphoratus (Bull.: Fr.) Fr. and L. rostratus Heilm.-Claus. (= L.
cremor sensu Basso) (Basso 1999, Heilmann-Clausen et al. 1998). Lactarius
atlanticus described from France (Bon 1975) is characterized by smooth,
rusty red, reddish orange to orange fawn pileus, the watery, transparent
latex and a spicy smell (Triantafyllou et al. 2015) and by association with
evergreen Quercus L. species (Basso 1999, Briffa 2002, Triantafyllou et al.
2015).
In this study, Lactarius atlanticus is reported for the first time from Turkey
based on the evaluation of both molecular and morphological approaches.

FIRST RECORD OF Lactarius atlanticus (Russulaceae, Basidiomycetes) FROM TURKEY IN
THE SUBGENUS Russularia
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Materials and Method
Morphological study
A total of four Lactarius specimens were collected during mycological
excursions to the Aegean region (Aydın Province) of Turkey in 2014-2020.
The fruiting bodies of the macrofungi were photographed in their natural
habitat and ecological information was recorded. The materials examined
in this study were dried at 40°C. Macroscopic descriptions were made
based on data obtained from fresh basidiomata. Microscopic features were
described from the dried material mounted in water or 3% KOH, and
stained in 3% Congo red solution or Melzer’s reagent using an a Leica
DM750 light microscope (Wetzlar, Germany) with a magnification of
1000×. Lm, Wm and Qm indicate the average spore length, width and ratio,
respectively. The investigated materials are deposited at the fungarium of
Isparta University of Applied Sciences (IUF), Isparta, Turkey.
Molecular characterization
Genomic DNA extraction was performed from fresh specimens using ZR
Fungal/Bacterial DNA MiniPrep kit (Zymo research, Irvine, California)
following the manufacturer’s guidance. PCR amplification and sequencing
were conducted from the nrITS region of all specimens using the primer
pairs ITS1F/ITS4 (White et al. 1990). PCR condition for the nrITS is
described in Kaygusuz et al. (2019, 2021a, 2021b). In brief, they include
initial denaturation for 5 min at 95°C, followed by 35 cycles of 1 min at
94°C, 45 s at 54°C, and 1 min at 72°C, and a final extension at 72°C for 10
min. The amplified PCR products were sequenced from both ends (Source
Bioscience, Berlin, Germany). The alignment of sequences were checked
and edited using in BioEdit 7.0.5 (Hall 1999). The phylogenetic analysis
was performed with the reference sequences retrieved from GenBank
(Table 1). Phylogenetic tree was produced via Maximum Likelihood (ML)
and Bayesian Inference (BI) methods using an aligned dataset. The ML
analysis was conducted using RAxML v8.2.10 (Stamatakis 2014) and
GTRGAMMA substitution model (1.000 bootstrap replications). The BI
analysis was carried out using MrBayes 3.2.2 (Ronquist et al. 2012) by
Markov chain Monte Carlo (MCMC) algorithm. Six simultaneous Markov
chains were run for one million generations, sampling every 1000th
generation. The similarity/identity matrix between the sequences was
calculated using MatGAT v2.0 (Matrix Global Alignment Tool)
(Campanella et al. 2003) with BLOSUM 50 alignment matrix.

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Table 1. Details of the collections included in the phylogenetic analysis in this study.
Taxon
Specimen/Strain
voucher
Locality
GenBank
Accession
No
References
L. albidigalus
KUN-HKAS 78310
(FL1148)
China
MK253477
Wang 2018
L. alpinihirtipes
KUN-HKAS 86025
China
MG589785
Wang 2017
L. atlanticus
OKA-TR2090
Turkey
OM918237
This study
L. atlanticus
OKA-TR2091
Turkey
OM918238
This study
L. atlanticus
OKA-TR2092
Turkey
OM918239
This study
L. atlanticus
OKA-TR2093
Turkey
OM918240
This study
L. atlanticus
PAL 1 (GV)
Italy
KP420215
Triantafyllou et al.
2015
L. atlanticus
JKLAC13122801
Portugal
KR025611
Wisitrassameewong
et al. 2015
L. atlanticus
1810
Italy
JF908297
Osmundson et al.
2013
L. atlanticus
EP02-A421
Greece
KP420217
Triantafyllou et al.
2015
L. atlanticus
EP05-N296
Greece
KP420216
Triantafyllou et al.
2015
L. atlanticus
AQUI 97–16 (GL)
Italy
KP420219
Triantafyllou et al.
2015
L. atlanticus
LGAM 2503
Greece
KP420218
Triantafyllou et al.
2015
L. atlanticus
AV13_047
Italy
KR025612
Wisitrassameewong
et al. 2015
L. aurantiobrunneus
KUN-HKAS 61365
(XHW2399)
China
MK351921
Wang et al. 2019
L. camphoratus
JMP0039
USA
EU819480
Palmer et al. 2008
L. cf. rufulus
5048615
USA
MH179120
Unpublished
(GenBank)
L. chichuensis
Wang-1236
China
KF475766
Wisitrassameewong
et al. 2014a
L. cinereoroseus
SFC20150819-46
South
Korea
MH984938
Lee et al. 2019
L. cremor
691
Italy
JF908276
Osmundson et al.
2013

FIRST RECORD OF Lactarius atlanticus (Russulaceae, Basidiomycetes) FROM TURKEY IN
THE SUBGENUS Russularia
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Taxon
Specimen/Strain
voucher
Locality
GenBank
Accession
No
References
L. crenulatulus
KW383
Thailand
KR025604
Wisitrassameewong
et al. 2015
L. fragilis
ANDESF2210_NVE-
BD8
Colombia
MN612773
Unpublished
(GenBank)
L. fulvihirtipes
KUN-HKAS 75498
(QC743)
China
MK253491
Wang et al. 2018
L. furfuraceus
TG146 (KUN-HKAS
86674, KUN)
China
MH447572
Wang et al. 2018
L. fuscomaculatus
KW128
Thailand
KR025601
Wisitrassameewong
et al. 2015
L. gracilis
KW094
Thailand
KT165322
Wisitrassameewong
et al. 2016
L. hirtipes
Wang-1243
China
KF433007
Wisitrassameewong
et al. 2014a
L. ilicis
15035
Italy
JF908317
Osmundson et al.
2013
L. laccarioides
KW336
Thailand
KF432991
Wisitrassameewong
et al. 2014a
L. marasmioides
KUN-HKAS 51465
(XHW1985)
China
MK253496
Wang 2018
L. mitratus
HCCN21924
South
Korea
MH984994
Lee et al. 2019
L. neglectus
KUN-HKAS 104193
(SFS113)
China
MK253506
Wang 2018
L. olivaceofuscus
KUN-HKAS 101923
(XHW4538)
China
MK351929
Wang 2021
L. pasohensis
DS06-245
Malaysia
KF432986
Wisitrassameewong
et al. 2014a
L. perparvus
KW320 (GENT,
MFLU)
Thailand
KJ458981
Wisitrassameewong
et al. 2014b
L. pseudofragilis
KUN-HKAS 89887
China
MG589764
Wang 2017
L. rubrocorrugatus
KW043
Vietnam
KR025589
Wisitrassameewong
et al. 2015
L. rufulus
MO364303
USA
MT551937
Unpublished
(GenBank)
L. strigosipes
nr
Mexico
JN003629
Lamus et al. 2012
L. subatlanticus
KUN-HKAS 89914
(XHW3640)
China
MK253517
Wang 2018
L. subemboratus
EL10-00
Sweden
AF506412
Larsson & Larsson
2003

FIRST RECORD OF Lactarius atlanticus (Russulaceae, Basidiomycetes) FROM TURKEY IN
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Taxon
Specimen/Strain
voucher
Locality
GenBank
Accession
No
References
L. subgracilis
KUN-HKAS 101921
(XHW4533)
China
MK253500
Wang 2018
L. subhirtipes
XHW3682 (KUN-
HKAS 89953, KUN)
China
MH447554
Wang et al. 2018
L. subserifluus
JMP0046
USA
EU819486
Palmer et al. 2008
L. tuberculatus
KUN-HKAS 104202
(XHW4274)
China
MK253520
Wang 2018
Results
Molecular analysis
A phylogenetic tree for Lactarius was produced using nrITS sequence data
to detect the location of the specimens from Turkey. Maximum likelihood
and Bayesian analysis generated similar topology; therefore, only ML tree
with both MLB and BPP values are presented. The nrITS data matrix
consists of sequences from 45 fungal samples representing 34 taxa.
In the nrITS phylogenetic tree the sequences from four Lactarius atlanticus
collections from Turkey nested with eight L. atlanticus sequences from
Greece, Italy and Portugal with high statistical support (MLB = 99%, BPP
= 0.99, Fig. 1). In the phylogenetic analysis, L. atlanticus is placed as a sister
to L. mitratus H. Lee, Wisitr. & Y.W. Lim and L. subhirtipes X.H. Wang.
According to the results of nrITS sequence comparison of 34 taxa, 47.0-
88.3% nucleotide identity and 55.1-98.1% nucleotide similarity were
determined between Lactarius atlanticus from Turkey and other Lactarius
species (Table 2). In MatGAT analysis of L. atlanticus, L. cf. rufulus
(MH179120) was the closest hit with 88.3% sequence identity followed by
L. rufulus Peck (MT551937), L. laccarioides Wisitr. & Verbeken (KF432991)
and L. subserifluus Longyear (EU819486) with 88.1%, 87.2%, 87.1%
sequence identity, respectively. Similarly, the nrITS sequence of L.
atlanticus showed 98.1% similarity with that of L. cf. rufulus (MH179120),
98% similarity with that of L. rufulus (MT551937) and 97% similarity with
that of L. laccarioides (KF432991) (Table 2).

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Figure 1. Phylogenetic tree derived from Maximum Likelihood analysis based on nrITS
sequence dataset. The phylogeny is rooted with Lactarius ilicis Sarnari (JF908317).
Maximum Likelihood bootstrap (MLB) values ≥ 85% and Bayesian
posterior probabilities (BPP) ≥ 0.90 are shown near nodes. Branches of
significant support (MLB ≥ 90% and BPP ≥ 0.95) are thickened. A new
record is indicated in bold.

FIRST RECORD OF Lactarius atlanticus (Russulaceae, Basidiomycetes) FROM TURKEY IN
THE SUBGENUS Russularia
Oğuzhan KAYGUSUZ
Table 2. Nucleic acid identity (blue) and similarity (yellow) matrix between Lactarius atlanticus and other selected Lactarius sequences.

FIRST RECORD OF Lactarius atlanticus (Russulaceae, Basidiomycetes) FROM TURKEY IN
THE SUBGENUS Russularia
Oğuzhan KAYGUSUZ
Taxonomy
Lactarius atlanticus M. Bon Doc. Mycol. 5(17): 23, 1975 (Figs. 2-5)
Synonym: Lactarius atlanticus f. strigipes M. Bon, Doc. Mycol. 7(25): 57, 1975
Pileus 15‒80 mm diam, when young convex to hemispherical with
prominent small and broad umbo, then applanate to plano-convex with a
central depression, surface dry, smooth, reddish brown or brick tinge,
cinnamon to vinaceous brown, a bit darker in the centre, ochre to dark
ochre at margin, old specimens sometimes dark ochre-brown, margin
striate or inflexed. Lamellae somewhat crowded, adnate to narrowly
decurrent, cream to cinnamon, brick to dark brick in mature specimens.
Stipe 20‒90 × 5‒12 mm, cylindric to subcylindric, sometimes tapering
downwards, sometimes slightly widened at the base, reddish brown to
brick tint. Context rather firm, hollow in the stipe, cream beige to flesh-
coloured. Taste and smell not remarkable.
Basidiospores (6.9‒)7.0‒9.6(‒10.0) × (6.5‒)6.6‒8.8(‒9.8) μm, Lm × Wm = 7.9 ×
7.6 μm, Q = 1.0‒1.1(‒1.2), Qm = 1.0, globose to subglobose, ornamentation
forming an almost complete or incomplete reticulum, composed of
irregular ridges; ridges up to 1.0‒1.3 µm high. Basidia 35.0‒55.0 × 8.0‒14.0
μm, clavate, 4- (3-, 2-, 1-) spored, sterigmata 5.0‒9.0 μm. Pleuromacrocystidia
absent. Lamellar edge heterogeneous, paracystidia narrowly clavate to
clavate or cylindrical with terminal cells (16.0‒)20.0‒37.0(‒40.0) × (5.5‒)6.5‒
12.0(‒15.0) μm, thin-walled. Pileipellis a hyphoepithelium; subpellis
composed of globose, ellipsoid, irregular subglobose elements, 10.0‒45.0
µm diam; suprapellis composed of subcylindrical, narrowly utriform,
pyriform terminal elements, 13.0‒42.0 × 4.0‒12.0 µm, thin-walled.
Stipitipellis a trichoderm consisting of parallel cylindrical elements,
rounded at the apex with narrow base, hyphae 8.0‒25.0 µm diam, thin-
walled.
Ecology: Scattered to gregarious on sandy soil in lowlands of temperate
mixed forests dominated by Quercus ilex L., Pinus brutia Ten. and Laurus
nobilis L., which are completely evergreen trees, native to Mediterranean
ecosystems. Specimens were found predominantly in coastal thermophilic
areas.
Specimens examined: Turkey, Aydın Province, Kuşadası district, under
Quercus ilex, 10 m a.s.l., 10 March 2014, leg. & det. O. Kaygusuz, OKA-
TR2090 (GenBank OM918237); ibidem, in mixed forest of Q. ilex, Pinus
brutia and Laurus nobilis, 12 m a.s.l., 27 January 2015, leg. & det. O.
Kaygusuz, OKA-TR2091 (GenBank OM918238); ibidem, in Q. ilex stand
mixed with P. brutia, 13 m a.s.l., 16 March 2018, leg. & det. O. Kaygusuz,
OKA-TR2092 (GenBank OM918239); ibidem, under Q. ilex, 15 m a.s.l., 20
February 2020, leg. & det. O. Kaygusuz, OKA-TR2093 (GenBank

FIRST RECORD OF Lactarius atlanticus (Russulaceae, Basidiomycetes) FROM TURKEY IN
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OM918240); ibidem, in mixed forest of Q. ilex, P. brutia and L. nobilis, 18
February 2022, leg. & det. O. Kaygusuz, OKA-TR2094.
Figure 2. Fresh basidiomata of Lactarius atlanticus. Bars: 10 mm.

FIRST RECORD OF Lactarius atlanticus (Russulaceae, Basidiomycetes) FROM TURKEY IN
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Figure 3. Microscopic features of Lactarius atlanticus: Basidiospore, in Melzer’s
reagent. Bars: 10 µm.

FIRST RECORD OF Lactarius atlanticus (Russulaceae, Basidiomycetes) FROM TURKEY IN
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Figure 4. Microscopic features of Lactarius atlanticus: (a-d) Basidia; (e-j) Paracystidia;
(k-o) Pileipellis, in Congo red solution. Bars: 10 µm.

FIRST RECORD OF Lactarius atlanticus (Russulaceae, Basidiomycetes) FROM TURKEY IN
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Figure 5. Microscopic features of Lactarius atlanticus: Stipitipellis, in Congo red
solution. Bar: 10 µm.
Discussion
Phylogenetic analyses based on nrITS sequence data (Fig. 1) indicate that
Lactarius atlanticus forms a sister lineage with L. mitratus and L. subhirtipes,
and groups with L. cinereoroseus H. Lee, Wisitr. & Y.W. Lim, L. laccarioides,
L. rufulus, L. strigosipes Montoya & Bandala, L. subatlanticus X.H. Wang
and L. subserifluus. Morphologically Lactarius atlanticus can be
differentiated from other species of Lactarius subg. Russularia. Lactarius
mitratus, originally described from South Korea, differs from L. atlanticus
by the orange yellow to light orange pileus colour, presence of
pleuromacrocystidia, an epithelium pileipellis and habitat preference
associated with Abies D.Don (Lee et al. 2019). Lactarius subhirtipes,
originally described from China, is distinguished from L. atlanticus by the
brownish orange basidiocarp and smaller basidiospores (5.0‒8.0 × 5.0‒7.5
μm) with less reticulate ornamentation (Wang et al. 2018). Lactarius
cinereoroseus, originally reported from South Korea, can be separated from
L. atlanticus by its greyish yellow to greyish red pileus colour, presence of
pleuromacrocystidia and ixotrichoderm pileipellis (Lee et al. 2019).
Lactarius laccarioides, originally reported from Thailand, differs clearly
from L. atlanticus by the smaller basidiospores size (6.7‒8.5 × 6.0‒7.7 μm), a

FIRST RECORD OF Lactarius atlanticus (Russulaceae, Basidiomycetes) FROM TURKEY IN
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trichopalisade pileipellis and habitat dominated by Castanopsis sp. and
Lithocarpus sp. (Lee et al. 2019). Lactarius rufulus differs by larger
basidiomata (up to 100 mm broad) with brownish red pileus colour, and
its habitat on rich soils (Peck 1907). Lactarius strigosipes has smaller
basidiospores (6.0‒7.5 × 6.0‒7.5 μm), and pseudoparenchymatous
pileipellis, specific odour in fresh and dry condition, and mesophytic
upland habitat which is associated with Carpinus caroliniana Walter
(Montoya & Bandala 2008). Lactarius subatlanticus has a smaller
basidiomata with a pileus which is 15.0‒40.0 mm broad, smaller
basidiospores (6.0‒8.0 × 5.0‒7.0 μm) (Wang 2018). Lactarius subserifluus has
orange-ferruginous pileus colour and smaller basidiospores (6.0‒7.5 × 6.0‒
7.0 μm) (Longyear 1902, Hesler & Smith 1979).
In Europe, Lactarius sect. Olentes (L. subg. Russularia) is represented by L.
atlanticus, L. camphoratus, L. cremor Fr., L. serifluus and L. subumbonatus. Of
these, Lactarius camphoratus can be differentiated from L. atlanticus by
pileus colour without orange tinges, smaller basidiospores (7.0‒8.5 × 6.0‒
7.5 μm), presence of macrocystidia and a broader ecological amplitude
(Hesler & Smith 1979, Basso 1999, Běťák 2013). Lactarius cremor is
distinguished from L. atlanticus by the smaller basidiomata with a pileus
which is 14.0‒48.0 mm broad, smaller basidiospores (6.0‒8.0 × 6.0‒8.0 μm),
presence of macrocystidia and a pseudoparenchymatous pileipellis (Basso
1999). Lactarius serifluus has smaller basidiomata (up to 45.0 mm broad),
ochraceous-brown pileus colour, subglobose basidiospores, presence of
macrocystidia and habitat that prefers broad-leaved trees, oaks and
chestnuts (Basso 1999). Lactarius subumbonatus has a pileus without orange
colour, subglobose basidiospores and subclavate to subclindrical
paracystidia (Basso 1999, Triantafyllou et al. 2015).
Lactarius atlanticus has been reported up to now from France, Greece, Italy,
Malta, Portugal, Slovenia (Bon 1975, Basso 1999, Zotti & Pautasso 2013,
Triantafyllou et al. 2015, Leonardi et al. 2021) and Turkey (this study). L.
atlanticus, which was reported primarily from the Mediterranean basin, is
regarded as very rare according to the information on fungal Red Lists
(Leonardi et al. 2021). In terms of habitat, it was reported that Lactarius
atlanticus mostly grows under Quercus (e.g., Q. coccifera L., Q. ilex, Q.
ithaburensis Decne., Q. pubescens Brot., Q. robur L.), but also under mixed
forest of Angiosperms (Arbutus andrachne L., A. unedo L., Ceratonia silique
L., Cistus sp., Fagus sp.) and Gymnosperms (Abies cephalonica Link, Pinus
halepensis Mill., P. nigra J.F.Arnold) (Bon 1975, Basso 1999, Zotti & Pautasso
2013, Triantafyllou et al. 2015, Leonardi et al. 2021). In this study L.
atlanticus was presented from the temperate mixed forests dominated by
Quercus ilex, Pinus brutia and Laurus nobilis.

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