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Neonothopanus gardneri: A new combination for a bioluminescent agaric from Brazil

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Mycologia
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The bioluminescent agaric, Agaricus gardneri Berk., was rediscovered recently in central Brazil. The new combination, Neonothopanus gardneri, is proposed for this long-forgotten taxon supported by morphological and molecular data.
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Neonothopanus gardneri
: a new combination
for a bioluminescent agaric from Brazil
Marina Capelari
1
Nu´ cleo de Pesquisa em Micologia, Instituto de Botaˆnica,
Caixa Postal 3005, 01031-970 Sa˜o Paulo, SP, Brazil
Dennis E. Desjardin
Department of Biology, San Francisco State University,
San Francisco, California 94132
Brian A. Perry
Department of Biology, University of Hawaii at Hilo,
Hilo, Hawaii 96720
Tatiane Asai
Nu´ cleo de Pesquisa em Micologia, Instituto de Botaˆnica,
Caixa Postal 3005, 01031-970 Sa˜o Paulo, SP, Brazil
Cassius V. Stevani
Departamento de Quı
´
mica Fundamental, Instituto de
Quı
´
mica, Universidade de Sa˜o Paulo, Caixa Postal
26077, 05599-970 Sa˜o Paulo, SP, Brazil
Abstract
: The bioluminescent agaric,
Agaricus gard-
neri
Berk., was rediscovered recently in central Brazil.
The new combination,
Neonothopanus gardneri
,is
proposed for this long-forgotten taxon supported by
morphological and molecular data.
Key words:
Agaricales, Basidiomycota, biolumi-
nescence, omphalotoid clade, taxonomy
INTRODUCTION
In 1840 George Gardner published a short paper
titled ‘‘Description of a new phosphorescent species
of
Agaricus
’’ wherein he recounted observing boys
amusing themselves with a luminous object in the
streets of Vila de Natividade, Goia´s State, Brazil
(Gardner 1840). Gardner at first thought the object
was some sort of large firefly, but on closer inspection
he recognized it as a species of
Agaricus
belonging to
tribe
Pleurotus
of Fries. The locals called it ‘‘flor-de-
coco’’ and noted that it grew abundantly on decaying
fronds of a dwarf palm that they called ‘‘pindoba’’.
Gardner sent a brief description and drawing of the
luminous agaric to M.J. Berkeley at Kew and indicated
that if the species was new he intended to name it
Agaricus phosphorescens
. Berkeley responded that the
species indeed was new and was referable to Fries’
new genus
Panus
(accommodating
Agaricus
tribe
Pleurotus
species with coriaceous texture) but that he
(Berkeley) thought
A. phosphorescens
was not an
appropriate epithet because phosphorescence (lumi-
nescence) was not unique to the new species.
Berkeley suggested that the taxon should be named
after the collector. Hence in Gardner’s paper
(Gardner 1840) the new luminescent agaric was
described formally as
Agaricus gardneri
Berk. ex
Gardner. Three years later Berkeley (1843) reported
the species as
Agaricus
(
Omphalia
)
gardneri
in his
‘‘Notices of some Brazilian fungi’’. Saccardo (1887)
transferred it as
Pleurotus gardneri
(Berk. ex Gardner)
Sacc., repeating the Latin diagnosis of Gardner and
reporting the species from Brazil as well as from
Queensland, Australia. Saccardo was undoubtedly
following Berkeley and Broome (1879) who reported
A. gardneri
from Brisbane, although the latter was a
misapplied name for
Omphalotus nidiformis
, a com-
monly encountered luminescent agaric in Queens-
land (cf. May and Wood 1997).
Pegler (1988) provided a revised description of the
species based on his examination of type material
labeled by Berkeley as
A. gardneri
(K), and noted that
‘‘the overall caespitose habit, the woody substratum,
spore form and the properties of luminescence are
also typical of
Omphalotus olearius
.’’
Pegler added that distinguishing
A. gardneri
as a
distinct species or as a yellow, geographical variant of
O. olearius
would require examination of fresh
material, unavailable at the time. Ample fresh
material of this long-forgotten luminescent species
was collected recently from Piauı´ and Tocantins
states, Brazil, allowing a re-evaluation of its taxonomic
affinities. We herein transfer
A. gardneri
to the genus
Neonothopanus
based on a combination of morpho-
logical and molecular data.
MATERIAL AND METHODS
Morphological study.—
Microscopic analyses were made
from dried material rehydrated in 70% ethanol followed
by 5% KOH and stained with Melzer’s reagent. Q
m
represents the mean length/width quotient of all spores
measured. Colors notations correspond to those of Ku¨ppers
(1979). All specimens are deposited in the Herba´rio do
Instituto de Botaˆnica (SP).
Molecular study.—
To elucidate the relationships of
Neo-
nothopanus gardneri
to members of the omphalotoid clade
(Moncalvo et al. 2000, 2002) ITS and nLSU sequence data
were generated from recently collected material and
analyzed within a phylogenetic framework.
Submitted 28 Mar 2011; accepted for publication 3 May 2011.
1
Corresponding author. E-mail: mcapelariibot@yahoo.com
Mycologia,
103(6), 2011, pp. 1433–1440. DOI: 10.3852/11-097
#
2011 by The Mycological Society of America, Lawrence, KS 66044-8897
1433
DNA extraction followed an adapted protocol of Ferreira
and Grattapaglia (1995) using lyophilized basidiomata
ground to a fine powder in liquid nitrogen. The sample
was resuspended in 50
mL TE, incubated at 37 C for 30 min
after the addition of RNase A (0.01 mg/
mL) and stored at
220 C. The ITS and nLSU regions were amplified
respectively with the primer set ITS1F/ITS4 and LR0R/
LR5 (White et al. 1990, Gardes and Bruns 1993, Moncalvo et
al. 2000). PCR reactions contained these concentrations in
100
mL final volume: 2.0 U PlatinumH Taq DNA Polymerase
(Invitrogen), 0.2 mM of each dNTP, 1.5 mM MgCl
2
and
0.2
mM of each primer. PCR protocols consisted of a 5 min
denaturation step at 94 C, followed by 40 cycles of 40 s at
94 C, 30 s at 55 C and 60 s at 72 C, and final extension step
of 72 C for 5 min. Resulting PCR product was purified with
PureLink PCR Purification Kit (Invitrogen). DNA sequenc-
ing reactions were performed with the DYEnamic ET dye
terminator Cycle Sequencing Kit on a MegaBACE 1000
DNA sequencer (Molecular Dynamics) according to the
manufacturer’s instructions. Consensus sequences were
generated with the Phred/Phrap/Consed package (Ewing
et al. 1998, Ewing and Green 1998, Gordon et al. 1998).
Edited ITS and nLSU sequences of
N. gardneri
were
deposited in GenBank (T
ABLE I).
Sequences of
N. gardneri
were aligned manually to
other sequences of the omphalotoid clade (T
ABLE I) with
MacClade 4 (Maddison and Maddison 2000). Phylogenetic
analyses were performed with parsimony, maximum
likelihood and Bayesian methods. Parsimony searches
were performed in PAUP* 4.0 (Swofford 2003), using a
branch-and-bound algorithm with furthest sequence addi-
tion, M
ULTREES on, collapse of zero length branches and
equal weighting of all characters. Support of individual
clades was assessed by bootstrap (BS) analyses (Felsenstein
1985), using 500 branch-and-bound replicates with the
same parameter settings as above. Maximum likelihood
(ML) searches also were conducted in PAUP*, under a
GTR + I + G model of sequence evolution determined
with the Akaike information criterion as calculated in
Modeltest 3.7 (Posada and Crandall 1998), with starting
trees obtained via neighbor joining, TBR branch swap-
ping, M
ULTREES on, and all parameter values estimated by
the program. Clade support was assessed by nonparamet-
ric ML bootstrap (BS) analyses as implemented in Garli
(Zwickl 2006) and consisted of 1000 replicates run under
the same model of sequence evolution as the ML search,
with all parameters estimated by the program. Bayesian
analyses to obtain posterior probabilities (PP) were
performed with MCMCMC methods as implemented in
MrBayes 3.1.2 (Huelsenbeck and Ronquist 2001, Ronquist
and Huelsenbeck 2003) using the same model as the ML
analyses. Bayesian analyses consisted of two parallel
searches, run 2 000 000 generations and initiated with
random starting trees. Chains were sampled from the
posterior distribution every 200 generations for a total of
10 000 trees each. All trees sampled before the distribu-
tion reaching a spit deviation frequency of 0.01 were
discarded as the burn-in, while the remaining trees were
used to calculate posterior probabilities (PP) of the
individual clades. The default settings were used in
MrBayes to set the incremental heating scheme, uncon-
strained branch lengths and uninformative topology
priors. Sequence alignment was submitted to TreeBASE
(submission number 11243).
RESULTS
Molecular analysis.—
After excluding regions
deemed too ambiguous for alignment the ITS
dataset consists of 652 aligned positions for 16
ingroup taxa and contains 207 parsimony informa-
tive positions. The nLSU dataset includes 761
aligned positions for 13 ingroup taxa and contains
58 parsimony informative positions. For both data-
sets a sequence of
Crinipellis
sp. was used as an
outgroup taxon for rooting purposes. Parsimony
analyses of both datasets results in topologically
similar trees. Before combining the ITS and nLSU
data parsimony bootstrap analyses were performed
(as described above) to determine whether either
data partition recovers well supported taxonomic
groupings that conflict with those recovered by the
other partition. Once a lack of taxonomic conflict
was determined the ITS and nLSU data were
combined. Parsimony analyses of the combined data
recovered three trees of 1000 steps (CI 5 0.6780, RI
5 5619), differing only in the placement of several
taxa within a clade corresponding to the genus
Omphalotus
. Maximum likelihood (ML) analyses
recovered a single tree (F
IG.1) (2 ln 5
4596.33572) identical in topology to one of the
trees recovered by parsimony analysis. Bayesian
analyses reached an average standard deviation of
split frequencies below 0.01 after approximately
170 000 generations. The first 2500 trees sampled
were excluded as the burn-in.
Neonothopanus gardneri
is moderately supported as
the sister taxon to
Neonothopanus nambi
in our
analyses (70% ML-BS, 0.91 Bayesian PP). The
Neonothopanus
clade is weakly supported as the sister
clade to a well supported
Omphalotus
(96% BS, 1.0
PP) represented by eight taxa. Both species of
Anthracophyllum
included in the analyses,
A. archeri
and
A. lateritium
, are well supported as sister taxa
(99% BS, 1.0 PP), whereas the two species of
Gymnopus
sampled,
G. contrarius
and
G. dryophilus
,
do not form a monophyletic lineage.
Gymnopus
contrarius
is weakly supported in a position subtend-
ing the
Anthracophyllum
species, and
G. dryophilus
falls out in a well supported clade with
Lentinula
lateritia
and
Rhodocollybia maculata
(100% BS, 0.99
PP).
Neonothopanus gardneri
did not form a mono-
phyletic lineage with
Omphalotus
species in any
analyses; instead it was sister to
N. nambi
with varied
statistical support in all analyses.
1434 M
YCOLOGIA
TAXONOMY
Neonothopanus gardneri (Berk. ex Gardner) Cape-
lari, Desjardin, Perry, Asai & Stevani, comb. nov.
F
IGS.2,3
MycoBank MB519818
Basionym: Agaricus gardneri
Berk. ex Gardner, J. Bot.
(Hooker) 2:427 (1840).
Synonyms: Pleurotus gardneri
(Berk. ex Gardner)
Sacc., Syll. fung. (Abellini) 5:352 (1887).
Dendrosarcus gardneri
(Berk. ex Gardner) Kuntze,
Revis. gen. pl. (Leipzig) 3:464 (1898).
Pileus 10–90 mm diam, convex to applanate with a
small umbo when young, applanate to depressed or
infundibuliform when mature, smooth, glabrous,
hygrophanous; margin irregular, sometimes lacerate
or lobate, striatulate; yellow (N
00
A
40
M
00
) overall when
young, the disk darker yellow (N
00
A
50
M
00
)and
margin paler yellow (N
00
A
30
M
00
), sometimes fading
on the margin to buff or nearly white, sometimes with
small scattered brownish spots. Context fleshy, thick,
cream to pale yellow (N
00
A
40
M
00
). Lamellae deeply
decurrent, distant with 2–3(–5) series of lamellulae,
broad (3–7 mm); edges entire, yellow, concolorous
with pileus margin (N
00
A
30
M
00
), becoming paler with
age. Stipe 30–50 3 8–15 mm, eccentric or sometimes
central, cylindrical to narrowed toward the base, solid,
tough, fibrous, smooth or reticulate near lamellae
ends, light yellow, concolorous with the pileus surface
(N
00
A
30
M
00
–N
00
A
40
M
00
) above, base darker with
brown tones; partial veil absent. Flavor not recorded.
Odor pleasant. Pileus and lamellae strongly lumines-
cent (bright yellowish green; F
IG. 2b, d); mycelium
luminescent (F
IG. 2f).
Basidiospores 9.5–12 3 (8.5–)9–11
mm(x5 10.2 6
0.7 3 9.7 6 0.7
mm, Q 5 1.00–1.18, Q
m
5 1.07 6 0.02,
n 5 25 spores), globose to subglobose with a
prominent hilar appendix, smooth, hyaline, inamy-
loid, thin-walled. Basidia 35–48 3 7.5–12
mm, sub-
cylindrical to clavate, four sterigmata, occasionally
two sterigmata, hyaline, thin-walled, clamped. Basi-
dioles 35–50 3 7–12
mm, cylindrical to clavate,
hyaline, thin-walled. Pleurocystidia absent. Lamella-
edge heteromorphous, with basidia, basidioles and
scattered cystidia. Cheilocystidia 30–50 3 4–8
mm,
TABLE I. Collection data and GenBank accession number of the taxa analyzed
Species
Culture/
herbarium number Origin
GenBank number
LSU ITS
Anthracophyllum archeri
(Berk.) Pegler PBM 2201 AY745709
AFTOL_ID 973
TFB 3511 Australia DQ444308
TENN 50049
A. lateritium
(Berk. & M.A. Curtis) Singer CULTENN 4419 AF261324
TFB 4043 USA DQ444309
TENN 50256
Crinipellis
sp. MCA 1527 Guyana AY916699 AY916701
Gymnopus contrarius
(Peck) Halling AFTOL-ID 1758 USA DQ457670 DQ486708
Gymnopus dryophilus
(Bull.) Murrill AFTOL-ID 559 USA AY640619 DQ241781
Lentinula lateritia
(Berk.) Pegler RV 95-376 AF356164 AF031179
Neonothopanus gardneri
(Berk. ex Gardner)
Capelari et al.
SP 416340 Brazil JF344714 JF344713
N. nambi
(Speg.) R.H. Petersen & Krisai RVPR1308 Puerto Rico AF042577
Watling 193/95 Malaysia DQ444307
Omphalotus illudens
(Schwein.) Bresinsky & Besl TUB 012155 USA DQ071741 AY313271
TENN54507
O. japonicus
(Kawam.) Kirschm. & O.K. Mill. isolate 456 AF042008 AY313286
culture 2305 Japan
O. mexicanus
Guzma´n & V. Mora TENN51283 Mexico AY313274
O. nidiformis
(Berk.) O.K. Mill. T1946.8 AF042621
Vilgalys E5332 Austra´lia AY313275
O. olearius
(DC: Fr.) Singer AFTOL-ID 1718 Slovenia DQ470816
culture 9061b France AY313277
O. olivascens
H.E. Bigelow et al. VT645.7 AF261325
TENN56257 USA AY313279
O. olivascens
var.
indigo
G. Moreno et al. CBS101447 Mexico AF525065
O. subilludens
(Murril) H.E. Bigelow TENN54320 USA AY313283
Rhodocollybia maculata
(Alb. & Schwein.) Singer AFTOL-ID 540 USA AY639880 DQ404383
CAPELARI ET AL.:
N
EONOTHOPANUS GARDNERI
COMB. NOV. 1435
body submerged and difficult to discern, apices
slightly projecting, elongate-fusoid to sinuous-cylin-
drical, hyaline, thin-walled. Pileipellis undifferentiat-
ed from the underlying tramal tissue, composed of
repent hyphae, 2.5–5
mm diam, hyaline or pale
yellowish in KOH, inamyloid, thin-walled, non-gelat-
inous. Pileus and stipe tramal tissues composed of
hyphae 3.5–6.5
mm diam, cylindrical or sometimes
inflated and branched, hyaline, inamyloid, thin- to
slightly thick-walled, with clamp connections. Hyme-
nophoral trama compact, with a subregular to
irregular mediostratum and a more loosely arranged
lateral stratum; hyphae 2.5–5
mmdiam,hyaline,
inamyloid, thin- to slightly thick-walled. Stipitipellis
similar to pileipellis. Clamp connections present in all
tissues.
Habit
,
habitat and known distribution:
Growing at
the base of palm trees (pindoba palm [
Attalea humilis
Mart. ex Spreng.], piac¸ava [
A. funifera
Mart. ex
Spreng.], and babac¸u [
Orbignya phalerata
Mart.]).
Goia´s, Piauı´ and Tocantins States, Brazil.
Specimens examined:
BRAZIL. GOIA
´
S STATE: Vila de
Natividade, Dec 1839,
Gardner s.n
. (HOLOTYPE, K); PIAUI
´
STATE: Gilbue´s City, Fazenda Boa Vista, 91uS and 45uW,
Mar 2006,
D. Fragaszy & P. Izar s.n
. (SP416340); same
location, 27 Feb 2008,
M.G. de Oliveira s.n
. (SP416341);
Teresina City, Fazenda Cana Brava, 5u 5939.50S,
42u23912.820W, 17 May 2008,
I. Dantas s.n
. (SP416342);
TOCANTINS STATE, Itaguatins City, Fazenda Sa˜o Paulo,
FIG. 1. Phylogenetic tree based on maximum likelihood (ML) analysis of the combined ITS + nLSU datasets, rooted with
Crinipellis
sp. Support at the nodes is represented by ML bootstrap/Bayesian posterior probability.
1436 MYCOLOGIA
21 Mar 2008,
C.E.C. Nascimento & L.S. Arau´ jo-Neta s.n
.
(SP416343).
DISCUSSION
Neonothopanus gardneri
is characterized by this
combination of features: omphalotoid basidiomes
with yellow to yellowish white pileus 10–90 mm diam,
deeply decurrent, distant, broad lamellae, a well
developed, eccentric to central stipe, and pale yellow
context tissues; hyaline, inamyloid, smooth, globose
basidiospores with mean 10.2 3 9.7
mm; elongate-
fusoid to sinuous-cylindrical cheilocystidia; cutis-type
pileipellis and stipitipellis tissues with inamyloid, non-
gelatinized hyphae; growth on debris of dwarf palm;
and basidiomes that are strongly luminescent. Our
material undoubtedly represents the species first
reported by Gardner (1840) from basidiomes growing
on pindoba palm fronds in central Brazil. No
micromorphological details were provided in the
FIG. 2. Basidiomes (a–d) and cultures (e–f) of
Neonothophanus gardneri
taken in natural light (left) and in the dark (right).
Bars 5 30 mm.
CAPELARI ET AL.:
N
EONOTHOPANUS GARDNERI
COMB. NOV. 1437
protolog, although a type study was published by
Pegler (1988). Our material matches that analyzed by
Pegler except in basidiospores size, which was
reported by Pegler (1988) as 6–7 3 4.5–5.7
mm(x5
6.5 3 5.5
mm; Q 5 1.18), much smaller than we report
here. We studied the holotype specimen (K) and
found basidiospores in the range that we report from
fresh specimens (9.5–12 3 9–11
mm) and many
collapsed basidiospores in the range reported by
Pegler (1988).
Neonothopanus
was established by Petersen and
Krisai-Greilhuber (1999) as a monotypic genus based
on
Agaricus nambi
Speg. described from Paraguay
(Spegazzini 1883). Singer (1944) recognized
A. nambi
as a member of his new genus
Nothopanus
(type
A.
eugrammus
Mont.). Horak (1968) revised the types of
A. nambi
and
A. eugrammus
, and Petersen and Krisai-
Greilhuber (1999) also revised the type of
A.
eugrammus
and studied representative materials of
A.
nambi
. All authors considered that they were distinct
species and that
Nothopanus
(with type
A. eugrammus)
represented a synonym of
Pleurotus
. For a complete
discussion of the taxonomy and nomenclature of
Nothopanus
and
Neonothopanus
see Petersen and
Krisai-Greilhuber (1999). Our Brazilian species shows
morphological affinities to both
Neonothopanus
and
Omphalotus
(with syn.
Lampteromyces
). Both latter
genera contain species that form luminescent basi-
diomes with decurrent, distant lamellae, eccentric,
solid stipes, smooth, hyaline, inamyloid basidiospores,
and non-gelatinized, inamyloid hyphae with clamp
connections. Indeed the morphological features of
Neonothopanus
and
Omphalotus
are overlapping and
the distinctions subtle, with
Neonothopanus
forming
unpigmented or pale pigmented (white to grayish tan)
marasmielloid to pleurotoid basidiomes and
Omphalo-
FIG. 3. Micromorphlogical features of
Neonothophanus gardneri
(SP416340). a. Basidiospores. b. Basidia. c. Lamella edge
with cheilocystidia. d. Cheilocystidia. Bar 5 10
mm.
1438 MYCOLOGIA
tus
forming more brightly pigmented (yellow to
orange) pleurotoid to clitocyboid basidiomes. Molec-
ular data have informed our decision to accept
A.
gardneri
in
Neonothopanus
rather than in
Omphalotus
.
Neonothopanus gardneri
is moderately supported as the
sister taxon to
N. nambi
in the maximum likelihood
analysis of the combined ITS + nLSU datasets (FIG. 1),
and these taxa did not form a monophyletic lineage
with
Omphalotus
species in any analysis.
Neonothopanus gardneri
differs from
N. nambi
in
basidiome stature, pigmentation and basidiospore
size.
Neonothopanus nambi
forms white to pale grayish
tan basidiomes with reduced, eccentric to lateral stipe
and ellipsoid basidiospores, 4–6.5 3 2.8–4
mm (Pe-
tersen and Krisai-Greilhuber 1999), whereas
N.
gardneri
forms yellow basidiomes with a well devel-
oped, eccentric to central stipe and globose basidio-
spores, 9.5–12 3 9–11
mm.
Neonothopanus nambi
has not been explicitly
reported as bioluminescent, but from the data
provided by Petersen and Krisai-Greilhuber (1999)
and Corner (1981) we infer this to be the case.
Petersen and Krisai-Greilhuber convincingly docu-
mented that
N. nambi
is synonymous with
Pleurotus
eugrammus
(Mont.) Dennis sensu Singer (1944), and
they reported that specimens from Malaysia were
conspecific (intercompatible) with those from Puerto
Rico. Corner (1981) reported that Malaysian material
of
P. eugrammus
(following Singer’s concept of the
species) was luminescent. Moreover we have collected
luminescent basidiomes from Micronesia whose
morphology and DNA sequences match those of
N.
nambi
(Desjardin and Perry unpubl).
Neonothopanus
gardneri
has been used recently in research that
verifies the enzymatic nature of fungal biolumines-
cence (Oliveira and Stevani 2009) in contradiction to
the research of Shimomura (1989, 1992) who
reported that the pathway to light emission in fungi
was non-enzymatic.
ACKNOWLEDGMENTS
The authors thank the curator of the Kew Herbarium; Maria
Cecı´lia Tomasi, Instituto de Botaˆnica, for inking the
drawings; Dr Maria Helena P. Fungaro, Universidade
Estadual de Londrina, for DNA sequencing; Dr. Anı´bal
Alves de Carvalho Jr., Jardim Botaˆnico do Rio de Janeiro,
and Dr Tatiana B. Gibertoni, Universidade Federal de
Pernambuco, for helping with bibliography; Dr Michele P.
Verderane, Instituto de Psicologia, Universidade de Sa˜o
Paulo, for permission to publish her photos (F
IG. 2c–d). We
also are indebted to Mr Marino G. de Oliveira and his family
(Gilbue´s, PI), Drs Ismael Dantas (Teresina, PI), Luiz F.
Mendes, Instituto de Quı´mica, Universidade de Sa˜o Paulo,
Dorothy Fragaszy (University of Georgia, USA) and Patrı´cia
Izar, Instituto de Psicologia, Universidade de Sa˜o Paulo, for
the collection of fruiting bodies. This study was supported
by the Fundac¸a˜o de Amparo a` Pesquisa do Estado de Sa˜o
Paulo (Stevani grant, FAPESP 2010/15047-4) and by a
National Science Foundation (USA) grant to Desjardin
(DEB-0542445).
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1440 MYCOLOGIA
... This fact allowed us to conclude that a selfsufficient luminescent system that ensures luminescence in vitro was isolated from this fungal species. (Capelari et al., 2011). ...
... Although the Brazilian flora has already been extensively studied, few ventured into the interior of the country as Gardner did, mainly in the northeast region (Fagg et al., 2015). In 1840, in his work ''Description of a new phosphorescent species of Agaricus'' the naturalist, after observing children playing with a luminous object and performing a careful inspection, first identified an Agaricus species belonging to the required tribe Pleurotus of Fries (Capelari et al., 2011). ...
... Shortly thereafter, in 1887, Saccardo reclassified it as Pleurotus gardneri. However, Pegler (1988), after carrying out an analysis, found that although it had characteristics typical of Omphalotus olearius, it was one of its variants, but to distinguish A. gardneri as a different species, it required to study with fresh material in which it had no access (Capelari et al., 2011). ...
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Neonothopanus gardneri (N. gardneri) is a species of bioluminescent fungus belonging to the order Agaricales (Marasmiaceae) found in South America. Its existence was first reported in 1840 by George Gardner in his travels to Brazil, where it is popularly called "coco flower". Found mainly in decaying leaves and in the trunk of dwarf palm trees called "pindoba" (Attalea oleifera) or babaçu (Orbignya phalerata), recently N. gardneri had some of its bioactives isolated and their respective structures elucidated. Thus, this paper aims to present and discuss the findings of the works produced involving this theme. Thus, for the development of this literature review, books and scientific articles were searched in the following databases: Scopus, PubMed, Science Direct, web of science, Royal Society of Chemistry (RSC) Publishing and Google Scholar (1990-2021). The following keywords were used to filter the productions: "Neonothopanus", "Neonothopanus gardneri", "Bioactivities", "Bioprospecting", "Secondary metabolite", "Endophytic" and "bioluminescence". Finally, it is possible to observe that studies involving this species of bioluminescent fungus have focused on explaining the mechanism of light production and its potential biological activities, among them, antitumor, antioxidant, antimicrobial and antileishmanial effects.
... The species in question is probably Neonothopanus gardneri (Berk.) Capelari, Desjardin, Perry, Asai & Stevani, which occurs in the Cerrado [38], and has also reported by the Kalunga quilombola community for recreational use [10]. ...
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The Cerrado is home to a diversity of traditional communities, among which indigenous and quilombola peoples stand out. The Karajá are one of the ethnic groups in this biome, with a rich history and culture that goes back centuries. They mainly inhabit the regions of the Araguaia and Javaés rivers, occupying lands in the states of Goiás, Mato Grosso, Pará and Tocantins. Considering the importance of studies on ethnomycological knowledge in indigenous communities for preserving culture and the environment, especially in relation to fungi, our objective was to investigate the ethnomycological relationships of the Karajá indigenous people who inhabit Bananal Island, located in Tocantins. Data were collected from applying a semi-structured questionnaire and interviews with 140 people who compose the Macaúba (39%), Fontoura (31%) and Santa Isabel do Morro (30%) communities; they had an average age of 33.9 years, and 62% are male. We observed that the Karajá people recognize the fungi of the environment in which they live, showing a clearer perception of typical morphological groups, such as mushrooms and bracket fungi (wood ears). Although fungi are not used as a component of their diet, the Karajá recognize that some species may have this potential. Furthermore, they use fungi as adornments and decorations in festivities in a playful way, and occasionally for medicinal purposes. Therefore, we can state that this ethnic group does not have a total aversion to fungi, being considered partially mycophilic. This study is a pioneer among Cerrado indigenous people, and reinforces the need to expand research to other communities in different regions in order to expand ethnomycological knowledge among different ethnicities. These investigations could contribute to both an appreciation and conservation of the traditions and knowledge of original Brazilian people, as well as the biodiversity in which they are inserted.
... Anthracophyllum exhibits decurrent lamellae, a context encrusted with conspicuous pigment granules, and lacks a garlic odour (Pegler & Young 1989). Neonothopanus possesses decurrent lamellae, typically has an eccentric stipe, and lacks a garlic odour (Capelari et al. 2011, Petersen &Krisai-Greilhuber 1999, Desjardin et al. 2008, Ndong et al. 2011. Omphalotus, famed for bioluminescence, features decurrent lamellae (Berkeley 1944, Bigelow et al. 1976, Liu & Hu 1993, Mora & Guzman 1983, Murrill 1945, Neda 2004, Raithelhuber 1988, Schweinitz 1822, Singer 1986, Spooner 1977, Yang & Feng 2013. ...
... The Airth and Foerster's assay was used again in 2009 to investigate the mechanism of bioluminescence of new species of glowing fungi found in Brazil [69]. The reaction of cold and hot extracts of species found in the Atlantic Forest [70][71][72] and Brazilian Cerrado [73] resulted in light emission; Mycena lucentipes and Gerronema viridilucens were used as source of cold extract and Neonothopanus gardneri (=Pleurotus gardneri) as a source of hot extract [69]. Studies on the kinetics of the luciferin-luciferase reaction in the presence of NADPH showed that the maximum light emission reaches saturation after systematic addition of the hot extract. ...
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More than 125 known species of fungi, all part of the Agaricales order, can spontaneously emit light. This bioluminescence results from the oxidation of a luciferin derived from caffeic acid by oxygen under the action of the enzyme luciferase. The production and regeneration of caffeic acid tie together the Krebs cycle and the Shikimic Acid pathway in both fungi and plants. Therefore, successful genetic manipulation of luciferase has led to the development of bioluminescent reporters and eukaryotic organisms that exhibit self-sustained glow. This review aims to discuss the underlying mechanisms of fungal bioluminescence, with a focus on the biochemical and chemical processes that lead to light emission, along with an elaboration on its extensive biotechnological applications.
... In the outgroup /omphalotaceae, three other luminescent species are Neonothopanus gardneri (Berk.) Capelari, desjardin, B.a. Perry, T. asai & Stevani (2011: 1435, N. nambi (Speg.) r.h. ...
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A luminescent fungus growing on decaying leaves and sticks was collected in terra-firme forest at the upper Cuieiras river, Amazonas, Brazil. Morphological study and phylogenetic analysis (based on ITS+LSU data) confirmed it as a new species of Mycena. Mycena lamprocephala sp. nov. is characterized macroscopically by small, thin, basidiomata with an olivaceous brown pileus and glutinous stipe, and microscopically by diverticulate pleurocystidia, ramose cheilocystidia, and thin, diverticulate and branching pileipellis hyphae. The luminescence of the pileus and of the mycelium in the substrate is typically green and sometimes pulsating. This is the third luminescent species of Mycenaceae described from the Amazon Forest.
... ex Spreng. (piassava) (Capelari et al., 2011;Vieira et al., 2022). Ventura et al. (2021) found that N. gardneri has a predictable bioluminescence and growth pattern and is highly sensitive to Cd(II), 4-nitrophenol, phenol, and Cu(II) compounds. ...
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Fungal diseases, especially those that affect the root systems of plants, caused by Rhizoctonia and Macrophomina are limiting factors for achieving high crop yields. Alternatives to controlling fungi with chemical products drive the search for new options for bioactive compounds from plants. Attalea geraensis, a palm tree from the Brazilian Cerrado, is rich in flavonoids with antifungal actions. The objective of this work is to identify the chemical classes present in the ethanolic extract of green leaves of A. geraensis and determine the antifungal potential of the extract against isolates of Macrophomina phaseolina (Tassi) Goid. and Rhizoctonia solani JG Kühn. Phytochemical prospection, flavonoid dereplication, and antifungal activity were carried out of the ethanolic extract of the green leaves of A. geraensis harvested in the Cerrado area of Brazil. Steroids, triterpenes, saponins, and anthraquinones are described here for the first time for the leaves of A. geraensis. The flavonoids quercetin, isorhamnetin, 3,7-dimethylquercetin, quercetin 3-galactoside, 5,7-dihydroxy-2-(4-hydroxy-3-methoxyphenyl)-3-{[3,4,5-trihydroxy-6-(hydroxymethyl)oxan-2-yl]oxy}-4H-chromen-4-one, rhamnazin 3-galactoside, keioside, and rhamnazin 3-rutinoside were identified. Of these, only quercetin and isorhamnetin had already been identified in the leaves of A. geraensis. The results show a fungistatic potential for the species. The diversity of flavonoids present in the leaves of A. geraensis may be the result of a synergistic action between fungus and plant or there could be an antagonistic effect between flavonoids and the other identified chemical classes.
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Bioluminescence is the generation and emission of light by living things. In the present investigation, Mycena chorophos is reported for the first time from the Konkan region of Maharashtra, India. We observed tiny, luminous clumps of Mycena chlorophos on a rotten bamboo substratum. The fungi grow in clusters of one or more individuals.
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Some fungi are capable of bioluminescence. One of the intriguing bioluminescent mushrooms is Neonothopanus . This mushroom has large fruity body and can produce light throughout their entire body. Light is produced by the reaction of luciferase enzyme to its substrate, luciferin. The information of Neonothopanus luciferase gene is still limited. The aim of this study is to characterize Neonothopanus sp . luciferase cDNA. Samples were collected in Pesisir Selatan West Sumatera. Total RNA and LuzF and LuzR primers were used to amplify 830 bp Neonothopanus sp luciferase cDNA. It was found that the query cover of the luciferase cDNA of Neonothopanus sp . to N. nambi is 93%, and 37% for N. gardnery. Neonothopanus sp and N. nambi have different nucleotides at position 320 – 369, while Neonothopanus sp and N. gardnery just have similar nucleotides at position 9 - 322 pb. Phylogenetic analysis shows bootstrap value of Neonothopanus sp cDNA sequences and Neonothopanus nambi 100% and 99.5% with N. gardneri . This suggests that Neonothopanus sp . luciferase cDNA is closely related to Neonothopanus nambi and N. gardneri .
Chapter
Bioluminescence is one of the most fascinating features of basidiomycetes. In this chapter, we have reviewed a total of 105 bioluminescent fungi that have been documented to date. We show that these species are restricted to three major lineages, including mycenoid, Armillaria, and Omphalotus, and display different bioluminescent patterns and geographical distributions. A global phylogeny shows that these species also exhibit patchy phylogenetic placement with their non-bioluminescent relatives. We review previous work on their genomes, which contain the fungal luciferin biosynthetic cluster. The dynamics of this cluster provide an evolutionary scenario since the last common ancestor of the family Mycenaceae and the marasmioid clade of Agaricales. Finally, we discuss potential functions and possible research directions of bioluminescence in these fungi.KeywordsBasidiomycetes, Fungal evolution, Bioluminescence, Luciferase, Mycena
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Omphalotus guepiniiformis, a bioluminescent mushroom species, is a source of the potentially valuable anticancer chemical. To provide genome information, we de novo assembled the high-quality O. guepiniiformis genome using two Next-Generation sequencing techniques, PacBio and Illumina sequencing. Our draft O. guepiniiformis genome comprises 42.5 Mbp of sequence with only 80 contigs and an N50 sequence length of over 1 Mbp. There were 15,554 predicted coding genes, and 7693 genes were functionally annotated with Gene Ontology terms. We performed a genomic study focusing on mushroom bioluminescent pathway cluster genes by comparing 17 luminescent and 23 non-luminescent Agaricales species belonging to 23 genera. Synteny analysis of genomic regions near the luminescent pathway cluster genes inferred that the Omphalotus lineage was genus-specific. In summary, our de novo assembled O. guepiniiformis genome provides significant biological insights into this organism, including the evolution of the luciferase gene block, and forms the basis for future analyses.