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

Abstract

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.

Full text

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).
LITERATURE CITED
Berkeley MJ. 1843. Notices of some Brazilian fungi. Lond J
Bot 2:629–643.
———, Broome CE. 1879. List of fungi from Brisbane,
Queensland; with descriptions of new species. Trans
Linn Soc London Bot Ser 2 1:399–408, doi:10.1111/
j.1095-8339.1879.tb00140.x
Corner EJH. 1981. The agaric genera
Lentinus
,
Panus
and
Pleurotus
. Beih Nova Hedwig 69:1–169.
Ewing B, Green P. 1998. Basecalling of automated
sequencer traces using phred II. Error probabilities.
Genome Res 8:186–194.
———, Hillier L, Wendl M, Green P. 1998. Basecalling of
automated sequencer traces using phred I. Accuracy
assessment. Genome Res 8:175–185.
Felsenstein J. 1985. Confidence limits on phylogenies—an
approach using the bootstrap. Evolution 39:783–791,
doi:10.2307/2408678
Ferreira ME, Grattapaglia D. 1995. Introduc¸a˜o ao uso de
marcadores moleculares em ana´lise gene´tica. Brası´lia,
Brazil: EMBRAPA-CENARGEN.
Gardner G. 1840. Description of a new phosphorescent
species of
Agaricus
, with remarks upon it by the Rev.
M.J. Berkeley. Hooker J Bot 2:426–428.
Gardes M, Bruns TD. 1993. ITS primers with enhanced
specificity for Basidiomycetes: application to the
identification of mycorrhizae and rusts. Mol Ecol 2:
113–118, doi:10.1111/j.1365-294X.1993.tb00005.x
Gordon D, Abajian C, Green P. 1998. Consed: a graphi-
cal tool for sequence finishing. Genome Res 8:195–
202.
Horak E. 1968. Synopsis generum Agaricalium. Beitr
Kryptogamenflora Schweiz 13.
Huelsenbeck JP, Ronquist F. 2001. MrBayes: Bayesian
inference of phylogeny. Bioinformatics 17:754–755,
doi:10.1093/bioinformatics/17.8.754
Ku¨ppers H. 1979. Atlas de los colores. Barcelona, Spain:
Editorial Blume.
Maddison DR, Maddison WP. 2000. MacClade 4: analyses of
phylogeny and character evolution. Sunderland, Mas-
sachusetts: Sinauer Associates.
May TW, Wood AE. 1997. Fungi of Australia. Vol. 2A.
Catalogue and bibliography of Australian Macrofungi
1. Basidiomycota p.p. Canberra, Australia: Australian
Biological Resources Study. 348 p.
Moncalvo J-M, Lutzoni FM, Rehner SA, Johnson J, Vilgalys
R. 2000. Phylogenetic relationships of agaric fungi
based on nuclear large subunit ribosomal DNA
sequences. Syst Biol 49:278–305, doi:10.1093/sysbio/
49.2.278
———, Vilgalys R, Redhead SA, Johnson JE, James TY, Aime
MC, Hofstetter V, Verduin SJW, Larsson E, Baroni TJ,
Thorn G, Jacobsson S, Cle´menc¸on H, Miller OK Jr.
CAPELARI ET AL.:
N
EONOTHOPANUS GARDNERI
COMB. NOV. 1439

2002. One hundred seventeen clades of euagarics. Mol
Phylogenet Evol 23:357–400, doi:10.1016/S1055-7903
(02)00027-1
Oliveira AG, Stevani CV. 2009. The enzymatic nature of
fungal bioluminescence. Photochem Photobiol Sci 8:
1416–1421, doi:10.1039/b908982a
Pegler DN. 1988. Agaricales of Brazil described by M.J.
Berkeley. Kew Bull 43:453–473, doi:10.2307/4118978
Petersen RH, Krisai-Greilhuber I. 1999. Type specimens
studies in
Pleurotus
. Persoonia 17:201–219.
Posada D, Crandall KA. 1998. Modeltest: testing the model
of DNA substitution. Bioinformatics 14:817–818,
doi:10.1093/bioinformatics/14.9.817
Ronquist F, Huelsenbeck JP. 2003. MrBayes 3: Bayesian
phylogenetic inference under mixed models. Bioinfor-
matics 19:1572–1574, doi:10.1093/bioinformatics/
btg180
Saccardo PA. 1887. Sylloge Fungorum omnium hucusque
cognitorum 5:1–1146.
Shimomura O. 1989. Chemiluminescence of panal (a
sesquiterpene) isolated from the luminous fungus
Panellus stipticus
. Photochem Photobiol 49:355–360.
———. 1992. The role of superoxide dismutase in
regulating the light emission of luminescent fungi. J
Exp Bot 43:1519–1525, doi:10.1093/jxb/43.11.1519
Singer R. 1944. New genera of fungi. Mycologia 36:358–368,
doi:10.2307/3754752
Spegazzini C. 1883. Fungi Guaranitici. Pugillus I. An Soc
Cient Argent 16:242–248.
Swofford DL. 2003. PAUP* 4.0b10: phylogenetic analysis
using parsimony (*and other methods). Sunderland,
Massachusetts: Sinauer Associates.
White TJ, Bruns T, Lee S, Taylor J. 1990. Amplification
and direct sequencing of fungal ribosomal RNA genes
for phylogenetics. In: Innis MA, Gelfand DH, Sninsky
JJ, White TJ, eds. PCR protocols: a guide to methods
and applications. San Diego: Academic Press. p 315–
322.
Zwickl DJ. 2006. Genetic algorithm approaches for the
phylogenetic analysis of large biological sequence
datasets under the maximum likelihood criterion
[doctoral dissertation]. Austin: Univ Texas Press.
115 p. (Software available at: http://code.google.
com/p/garli/).
1440 MYCOLOGIA