Characterization of the edible red alga Meristotheca papulosa (Solieriaceae, Gigartinales) from Japan


Faye, E.J.; Shimada, S.; Kawaguchi, S.; Masuda, M.

Phycological Research 53(3): 234-245

2005


The vegetative and reproductive morphology of the edible red alga Meristotheca papulosa (Montagne) J. Agardh (Solieriaceae) was reexamined based on material collected from various localities in Japan. Although the habit of the blades is variable according to the length and width of the axes, the frequency of branching and the abundance of proliferations, rbcL sequence analyses indicate their conspecificity. M. papulosa displays four distinctive reproductive features (presence of an auxiliary cell complex, occurrence of cystocarps on marginal proliferations and the blade surface (although very rare) in addition to the margins of axes, frequent production of spinose outgrowths on the pericarp and tetrasporangial initials typically basally attached to their parental cells) that have not been reported for M. papulosa from other areas. Although these features might warrant recognition of the Japanese entity as a separate species, a better understanding of their possible taxonomic value requires comparisons with M. papulosa from other geographic regions, including the type locality.

Phycological
Research
2005;
53:
234-245
Characterization
of
the
edible
red
alga
Meristotheca
papulosa
(Solieriaceae,
Gigartinales)
from
Japan
Etienne
Jean
Faye,'
Satoshi
Shimada,
2
Shigeo
Kawaguchi'
and
Michio Masuda
l
*
'Division
of
Biological
Sciences,
Graduate
School
of
Science,
Hokkaido
University,
Sapporo
060-0810,
'Center
for
Advanced
Science
and
Technology,
Hokkaido
University,
Sapporo
001-0021,
and
3
Division
of
Animal
and
Marine
Bioresource
Sciences,
Faculty
of
Agriculture,
Kyushu
University,
Fukuoka
812-8581
Japan
SUMMARY
The
vegetative
and
reproductive
morphology
of
the
edible
red
alga
Meristotheca
papulosa
(Montagne)
J.
Agardh
(Solieriaceae)
was
reexamined
based
on
material
collected
from
various
localities
in
Japan.
Although
the
habit
of
the
blades
is
variable
according
to
the
length
and
width
of
the
axes,
the
frequency
of
branching
and
the
abundance
of
proliferations,
rbcL
sequence
analyses
indicate
their
conspecificity.
M.
papulosa
displays
four
distinctive
reproductive
features
(presence
of
an
auxiliary
cell
complex,
occurrence
of
cystocarps
on
marginal
proliferations
and
the
blade
surface
(although
very
rare)
in
addition
to
the
margins
of
axes,
frequent
production
of
spinose
outgrowths
on
the
pericarp
and
tetrasporangial
initials
typically
basally
attached
to
their
parental
cells)
that
have
not
been
reported
for
M.
papulosa
from
other
areas.
Although
these
features
might
warrant
recognition
of
the
Japanese
entity
as
a
separate
species,
a
better
under-
standing
of
their
possible
taxonomic
value
requires
comparisons
with
M.
papulosa
from
other
geographic
regions,
including
the
type
locality.
Key
words:
Meristotheca
papulosa,
rbcL,
Rhodophyta,
Solieriaceae,
taxonomy.
INTRODUCTION
The
red
alga
Meristotheca
papulosa
(Montagne)
J.
Agardh
(1872)
(Solieriaceae,
Gigartinales),
the
gen-
eritype,
was
first
described
as
Kallymenia
papulosa
Montagne
(1850;
as
Callymenia)
on
the
basis
of
mate-
rial
from
Yemen,
in
the
Red
Sea.
Since
then,
it
has
been
reported
from
various
countries
in
the
Indo-Pacific
region:
Pakistan
(Borgesen
1934),
India
(Krishnamur-
thy
&
Joshi
1970),
Sri
Lanka
(Durairatnam
1961),
South
Africa
(Norris
1988),
Madagascar
(Bornet
1885),
Somalia
(Lawson
1980),
Australia
(Gabrielson
&
Kraft
1984),
Indonesia
(Weber-van
Bosse
1928),
Philippines
(Silva
et
al.
1987),
China
(Xia
&
Zhang
1999)
and
Japan
(Yoshida
1998).
However,
its
repro-
ductive
structures
are
insufficiently
known.
Monoecism
or
dioecism
of
gametophytes
and
postfertilization
stages,
including
the
origin
of
connecting
filaments,
the
diploidization
of
an
auxiliary
cell
and
the
origin
of
gonimoblasts,
should
be
elucidated
in
order
to
better
circumscribe
the
alga.
In
Japan,
the
alga
in
question
is
used
for
food
and
was
first
tentatively
treated
as
M.
papulosa
(Yendo
1911)
before
being
transferred
to
Eucheuma
as
E.
papulosa
(Montagne)
Cotton
et
Yendo
(in
Cotton
1914).
Kylin
(1932),
however,
subsequently
returned
it
to
Meristotheca
and
described
it
as
Meristotheca
japonica
Kylin,
which
currently
is
considered
a
synonym
of
M.
papulosa
(Okamura
1936;
Yoshida
1998).
It
is
widely
distributed
along
the
Pacific
coasts
of
central
to
southern
Japan
(Yoshida
1998),
and
its
gross
morphol-
ogy
has
been
reported
to
be
extremely
variable
accord-
ing
to
the
age
and
mode
of
branching
(Cotton
1914).
However,
the
taxonomic
significance
of
such
variability
is
unresolved.
Only
a
few
taxonomic
studies
were
pub-
lished
on
the
Japanese
M.
papulosa
(Yendo
1911;
Cot-
ton
1914;
Okamura
1926),
and
they
did
not
adequately
characterize
the
alga.
Accordingly,
the
purpose
of
the
present
study
is
to
document
the
vegetative
and
repro-
ductive
features
of
this
economically
important
sea-
weed
on
the
basis
of
recent
collections
across
Japan.
Moreover,
rbcL
gene
sequences
of
our
material
are
reported
as
well
to
assess
the
taxonomic
significance
of
the
gross
morphological
variability
and
to
allow
future
comparisons
with
M.
papulosa
plants
from
other
regions,
including
the
type
locality.
MATERIALS
AND
METHODS
Morphological
observations
Material
examined
was
collected
from
eight
localities
in
Japan
(Table
1),
fixed
in
10%
formalin/seawater
or
pressed,
and
deposited
in
the
Herbarium
of
the
*To
whom
correspondence
should
be
addressed.
Email:
mmasuda@sci.hokudai.ac.jp
Communicating
editor:
G.
C.
Zuccarello
Received
13
December
2004;
accepted
8
April
2005.
Meristotheca
papulosa
Table
1.
List
of
specimens
of
Meristotheca
papulosa
used
in
the
present
study
235
Collection
site,
date
and
collector
SAP
Reproductive
Sample
Gen
Bank
numbert
state
codet
numbert
Sokodo
(33°09'07"N,
139°49'17"E),
Hachijo
Island,
Tokyo,
096692
Tetrasporangial
Japan,
12
July
2003,
M.
Masuda
096693
Tetrasporangial
096694
Tetrasporangial
096695
Tetrasporangial
096696
Cystocarpic
M29
AB195310
096697
Cystocarpic
Ookataura
(33°06'12"N,
139°45'38"E),
Hachijo
Island,
Japan,
096698
Tetrasporangial
13
July
2003,
M.
Masuda
096699
Tetrasporangial
M37
AB195311
096700
Spermatangial
Ishijirogawa
(34°19'23"N,
139°13'20"E),
Shikine
Island,
096701
Tetrasporangial
Tokyo,
Japan,
26
August
2003,
M.
Masuda
096702
Spermatangial
M54
AB195312
096703
Cystocarpic
Nakanoura
(34°19'43"N,
139°12'22"E),
Shikine
Island,
Tokyo,
096704
Tetrasporangial
M52
AB195313
Japan,
27
August
2003,
M.
Masuda
096705
Spermatangial
096706
Cystocarpic
096707
Cystocarpic
Chojagasaki
(35°15'04"N,
139°34'38"E),
Hayama,
Kanagawa
096708
Cystocarpic
M38
AB195314
Prefecture,
Japan,
15
July
2003,
M.
Masuda
Okinoshima
(34°59'13"N,
139°49'40"E),
Tateyama,
Chiba
096709
Tetrasporangial
Prefecture,
Japan,
16
July
2003,
M.
Tani
096710
Cystocarpic
096711
Cystocarpic
M40
AB195315
Tajiri
(31°00'20"N,
130°40'19"E),
Sata-cho,
Kagoshima
096712
Tetrasporangial
M10
AB195316
Prefecture,
Japan,
26
June
2002,
S.
Kawaguchi
Oodomari
(31°01'12"N,
130°41'07"E),
Sata-cho,
Kagoshima
096713
Spermatangial
M2
AB195317
Prefecture,
Japan,
25
June
2002,
S.
Kawaguchi
Oodomari,
Sata-cho,
Kagoshima
Prefecture,
Japan,
20
June
097367
Cystocarpic
M91
AB195318
2004,
E.
J.
Faye
097368
Cystocarpic
097369
Cystocarpic
tVoucher
specimen
deposited
in
the
Herbarium
of
the
Graduate
School
of
Science,
Hokkaido
University,
Sapporo
(SAP);
tApplicable
to
only
specimens
used
for
rbcL
analysis.
Graduate
School
of
Science,
Hokkaido
University,
Sap-
poro.
Anatomical
observations
were
made
on
10%
for-
mal
in/seawater-preserved
specimens.
Material
was
sectioned
on
a
freezing
microtome
at
40
gm
or
by
hand,
stained
with
0.5%
(w/v)
cotton
blue
solution
(lactic
acid/phenol/glycerol/water
(1:1:1:1)
(v/v)),
and
mounted
in
50%
glycerol/seawater
or
30%
Karo.
rbcL
analyses
Total
DNA
was
extracted
from
nine
samples
of
M.
papulosa
(Table
1)
using
the
DNeasy
Plant
Mini
Kit
(QIAGEN,
Valencia,
CA,
USA)
following
the
manufac-
turer's
protocol.
Polymerase
chain
reaction
amplifica-
tion
and
sequencing
of
the
chloroplast-encoded
rbcL
gene
were
performed
as
in
Faye
et
al.
(2004).
The
rbcL
sequences
were
aligned
manually
and
no
insertion—
deletion
mutations
were
detected.
Sequences
of
25
species
of
the
Solieriaceae
were
downloaded
from
Gen-
Bank
and
included
in
the
alignment
(Table
2).
Two
species
of
the
Caulacanthaceae,
Caulacanthus
ustula-
tus
(Turner)
Kilitzing
and
Heringia
mirabilis
(C.
Agardh)
J.
Agardh
and
a
species
of
Areschougiaceae,
Areschou-
gia
ligulata
Harvey
ex
J.
Agardh
(AF099683),
were
used
as
outgroups
for
the
phylogenetic
analysis
follow-
ing
Fredericq
et
al.
(1999).
The
alignment
is
available
from
the
second
author
upon
request.
The
maximum
parsimony
(MP)
and
maximum
likeli-
hood
(ML)
methods
were
used
to
construct
phyloge-
netic
trees.
Parsimony
analysis
was
performed
with
PAUP
4.0b10
(Swofford
2002).
All
sites
were
treated
as
unordered
and
equally
weighted.
Heuristic
search
option
with
random
addition
of
sequences
(100
repli-
cates)
and
tree-bisection-reconnection
branch
swap-
ping
algorithm
(TBR)
was
used
for
tree
searching.
Bootstrap
analysis
based
on
2000
re-samplings
of
the
236
E.
J.
Faye
et
al.
Table
2.
List
of
taxa
for
which
rbcL
sequences
were
extracted
RESULTS
from
GenBank
for
the
analysis
Habitat
and
vegetative
structures
Taxon
GenBank
number
Agardhiella
ramosissima
(Harvey)
Kylin
AF099680
Agardhiella
subulata
(C.
Agardh)
Kraft
et
Wynne
U04176
Agardhiella
sp.
AF099681
Anatheca
montagnei
Schmitz
AB122014
Areschougia
ligulata
Harvey
ex
J.
Agardh
AF099683
Betaphycus
philippinensis
Doty
AF099684
Betaphycus
speciosum
(Sonder)
Doty
AF099685
Caulacanthus
ustulatus
(Turner)
KOtzing
AF099687
Eucheuma
arnoldii
Weber-van
Bosse
AF099690
Eucheuma
denticulatum
(Burman)
Collins
et
Hervey
U04177
Eucheuma
isiforme
(C.
Agardh)
J.
Agardh
AF099691
Eucheuma
serra
(J.
Agardh)
J.
Agardh
AF099692
Heringia
mirabilis
(C.
Agardh)
J.
Agardh
U21601
Kappaphycus
alvarezii
(Doty)
Doty
ex
Silva
AF099694
Kappaphycus
cottonii
(Weber-van
Bosse)
Doty
ex
AF099695
Silva
Kappaphycus
striatum
(Schmitz)
Doty
ex
Silva
AF099696
Kappaphycus
sp.
AF481500
Meristotheca
dakarensis
Faye
et
Masuda
AB159224
Meristotheca
gelidium
(J.
Agardh)
Faye
et
Masuda
AF099697
(as
Meristiella
gelidium
(J.
Agardh)
Cheney
et
Gabrielson)
Meristotheca
gelidium
(as
Meristiella
gelidium)
AF099698
Meristotheca
procumbens
Gabrielson
et
Kraft
AF099701
Meristotheca
procumbens
AF099702
Sarcodiotheca
furcata
(Setchell
et
Gardner)
Kylin
AF099706
Sarcodiotheca
gaudichaudii
(Montagne)
Gabrielson
U04184
Sarcodiotheca
gaudichaudii
AF099707
Sarconema
filiforme
(Sonder)
Kylin
AF099708
Solieria
chordalis
(C.
Agardh)
J.
Agardh
AF099709
Solieria
filiformis
(KOtzing)
Gabrielson
U04185
Solieria
pacifica
(Yamada)
Yoshida
AF099710
Solieria
robusta
(Greville)
Kylin
AF099711
Solieria
sp.
AF099712
dataset
(Felsenstein
1985)
was
calculated
(10
random
additions,
TBR,
full
heuristic
search
option).
The
ML
analysis
was
also
implemented
with
PAUP
4.0b10.
The
ML
parameters
were
estimated
using
the
ML
ratio
test.
The
program
Modeltest
version
3.06
(Posada
&
Crandall
1998)
was
used
to
find
the
model
of
sequence
evolution
that
best
fitted
each
dataset
by
a
hierarchical
likelihood
ratio
test
(a
=
0.01).
When
the
best
sequence
evolution
model
was
determined,
ML
tree
search
was
performed
using
the
estimated
parameters
with
the
following
options:
starting
tree
option
=
obtained
by
neighbor
joining,
and
branch
swapping
algorithm
=
TBR.
We
obtained
the
starting
tree
by
the
neighbor
joining
method
for
the
ML
bootstrap
analyses.
Bootstrap
analysis
based
on
100
re-samplings
of
the
dataset
(Felsenstein
1985)
was
calculated
(TBR,
full
heuristic
search
option).
Individual
thalli
grow
subtidally
at
1-20
m
depth
on
bedrock,
rocks
and
boulders
in
both
wave-exposed
and
sheltered
places.
They
are
fleshy,
deep
rose-red
to
dark
red.
Each
thallus
has
a
single
or
a
few
erect
blades
arising
from
a
discoid
holdfast;
however,
lower
portions
of
blades
are
sometimes
attached
to
the
substratum
by
secondary
attachment
discs
that
develop
from
their
margins.
Each
erect
blade
has
an
irregularly
to
subdichoto-
mously
divided
axis
that
is
terete
only
near
the
hold-
fast
and
become
flattened
upwards.
The
habit
of
the
blades
varies
greatly
in
individual
thalli.
Some
thalli
consist
of
elongated
and
narrow
axes
(18-26
cm
high
and
up
to
6
mm
wide)
that
profusely
branch
up
to
15
orders
and
usually
lack
marginal
proliferations
(Fig.
1).
Others
are
less
branched
(from
4
to
9
orders)
and
have
short
to
elongated
and
wide
axes
(9-22
cm
high
and
10-25
mm
wide)
that
might
or
might
not
bear
numerous
proliferations
(Fig.
2).
Inter-
mediate
forms
between
these
two
extremes
are
also
observed
(Figs
3,4).
Surface
maculae
are
present
in
some
specimens
(Figs
2,4).
Marginal
proliferations
are
simple
or
subdichotomously
ramified
one
to
three
times
and
bear
reproductive
structures.
Small
prolif-
erations
are
also
(but
very
rarely)
produced
on
the
surface
of
axes.
Young
germlings,
consisting
of
one
to
several
blade-
lets,
are
attached
to
various
parts
of
some
female,
male
(Fig.
4)
and
tetrasporangial
blades
in
our
August
col-
lections
from
Shikine
Island,
which
included
many
old
blades.
These
germlings
are
distinguished
from
prolif-
erations
by
the
presence
of
the
basal
attachment
disc.
They
are
similar
in
structure
to
younger
parts
of
M.
papulosa
and,
therefore,
might
be
derived
from
tet-
raspores
or
carpospores
of
this
alga
after
release
of
spores.
In
the
basal
regions,
the
blades
are
900-1000
p.m
thick
and
become
gradually
thinner
upwards
and
are
500-700
gm
in
the
median
part
and
200-400
gm
near
the
apex.
Blades
are
multiaxial
and
consist
of
a
pseudoparen-
chymatous
cortex
and
a
filamentous
medulla.
The
cor-
tex
is
composed
of
up
to
12
cells
separable
into
two
layers.
The
outer
cortex
consists
of
4-8
layers
of
small,
subspherical
to
elongate,
compact
and
darkly
staining
cells.
This
layer
is
connected
to
an
inner
cortex
of
3
or
4
layers
of
large,
irregular
to
stellate
or
rounded
cells
that
are
unpigmented
to
lightly
pigmented
and
laterally
connected
by
secondary
pit-connections.
The
medulla
is
composed
of
axial
and
adventitious
filaments
and,
from
the
younger
to
the
older
portions,
it
occupies
about
one-eighth
to
one-third
of
the
blade
thickness.
4
-
E
Meristotheca
papulosa
237
I
2
A
d
s
4
1
:1
Alb
I
n.
3
4
44
f
4
o
rs
41
0
Figs
1
-
4.
Representative
voucher
herbarium
specimens
of
Meristotheca
papulosa,
used
for morphological
observations
and
molecular
phylogenetic
analysis
(Graduate
School
of
Science,
Hokkaido
University,
Sapporo
(SAP)
number/sample
code).
1.
Tetrasporangial
thallus
with
elongated
and
narrow
axis
that
is
profusely
branched
and
lacks
marginal
proliferations
(Nakanoura,
SAP
096704/M52).
2.
Tetrasporangial
blade
with
short
and
wide
axis
provided
with
numerous
marginal
proliferations
(Tajiri,
SAP
096712/M10).
3,4.
Intermediate
forms
between
blades
shown
in
Figures
1
and
2.
3.
Cystocarpic
thallus
with
numerous
marginal
cystocarpic
protuberances
(Sokodo,
SAP
096696/M29).
4.
Spermatangial
blade
on
which
numerous
young
germlings
that
might
be
derived
from
released
spores
from
cystocarpic
or
tetrasporophytic
plants
of
this
alga
are
attached
(Ishijirogawa,
SAP
096702/M54).
E
Axial
filaments
are
parallel
to
the
longitudinal
plane
of
the
blade
(Fig.
5)
and
bear
periaxial
cells
from
each
cell.
These
periaxial
cells
subsequently
cut
off
lateral
filaments
that
later
develop
into
the
cortex.
Adjacent
axial
filaments
are
frequently
linked
by
secondary
pit-
connections
(Fig.
6).
Interconnecting
cells
or
filaments
between
axial
filaments
are
absent.
Abundant
adventi-
tious
medullary
filaments
are
produced
from
axial
and
inner
cortical
cells.
Some
of
those
that
are
produced
from
inner
cortical
cells
traverse
the
blade
and
form
secondary
pit-connections
with
inner
cortical
cells
on
the
opposite
side
(Fig.
7).
.4
14
r
.
f
no.
U)
238
E.
J.
Faye
et
al.
Figs
5-7.
Vegetative
structures
of
Meristotheca
papulosa.
Longitudinal
sections
stained
with
cotton
blue.
5.
Axial
filaments
(arrow)
that
lie
parallel
to
the
longitudinal
plane
of
the
blade
and
bear
periaxial
cells
(arrowheads)
(near
apex,
Ishijirogawa).
6.
Secondary
pit-
connections
(arrowheads)
between
adjacent
medullary
cells
(Ishijirogawa).
7.
Adventitious
medullary
filament
(arrow)
traversing
the
blade
and
connecting
two
inner
cortical
cells
(Ookataura).
Reproductive
structures
Sexual
thalli
are
dioecious.
Spermatangia
are
produced
on
all
surfaces
of
male
blades
except
at
the
base.
One
or
two
spermatangia
are
cut
off
obliquely
or
trans-
versally
from
elongated
outermost
cortical
cells
that
function
as
spermatangial
parental
cells.
Mature
sper-
matangia
are
ellipsoidal,
5-6
gm
long
and
3-4
gm
in
diameter
(Fig.
8).
Carpogonial
branches
and
auxiliary
cells
are
borne
on
separate
cortical
filaments
located
in
fertile
mar-
ginal
regions
(Fig.
9)
of
distal
segments
of
female
blades
or
proliferations.
Carpogonial
branches
develop
from
inner-
or
mid-cortical
cells,
are
directed
inwardly
and
terminated
with
a
long,
outwardly
reflexed
trichogyne.
Each
carpogonial
branch
is
typically
three-celled
(Fig.
10),
occasionally
four-celled
(Fig.
11)
and
con-
sists
of
a
conical
carpogonium,
4-7
gm
in
diameter,
a
hypogenous
cell,
6-10
gm
in
diameter
and
one
or
two
basal
cells
that
are
subcircular
to
ellipsoidal,
10-
15
gm
in
diameter.
Auxiliary
cells
are
noticeable
by
the
presence
of
a
single,
large,
darkly
staining
nucleus.
Before
diploidiza-
tion,
the
auxiliary
cell
stains
more
deeply
together
with
two
distal
cortical
cells
(Fig.
12)
and
these
cells
con-
stitute
the
auxiliary
cell
complex.
Mature
auxiliary
cells
are
15-25
gm
long
and
8-15
gm
in
diameter,
and
the
two
associated
cells
of
the
complex
are
15-35
gm
long
and
10-30
gm
in
diameter.
Presumed
fertilization
of
the
carpogonium
results
in
the
issue
of
a
single,
unbranched,
non-septate,
con-
necting
filament
(Fig.
13),
which
fuses
with
only
one
auxiliary
cell.
After
diploidization,
the
auxiliary
cell
slightly
elongates
(Fig.
14)
and
its
surrounding
inner
cortical
cells
initiate
active
divisions
to
form
nutritive
cell
clusters.
Subsequently,
a
single
gonimoblast
initial
is
cut
off
from
the
auxiliary
cell
laterally
(Fig.
15)
and
rapidly
divides
to
give
rise
to
darkly
staining
gonimo-
blast
cells
(Fig.
16)
that
constitute
the
carposporo-
phyte.
As
the
carposporophyte
develops,
the
nutritive
cell
clusters
grow
into
a
distinct
envelope
of
sterile
tissue
(Fig.
17).
At
the
same
time,
surface
cells
above
the
diploidized
auxiliary
cell
actively
divide
to
form
a
protuberance
in
which
the
developing
carposporophyte
is
included.
Further
development
of
the
carposporo-
phyte
results
in
a
centrally
placentate
cystocarp
(Fig.
18).
At
various
stages
of
cystocarp
development,
tubular
gonimoblast
cells
that
fuse
or
connect
with
cells
of
the
enveloping
tissue
are
observed.
Each
cystocarp
consists
of
a
centrally
placentate
carposporophyte
with
peripherally
arranged
carposporangia
(Fig.
19),
inner
enveloping
tissue
and
a
surrounding
ostiolate
pericarp.
Although
cystocarps
are
produced
singly
or
in
clusters
all
along
the
edges
of
the
axes
(except
at
their
base),
they
are
also
formed
on
the
lateral
proliferations,
espe-
cially
in
plants
with
wide
and
proliferous
axes
(Fig.
20).
Only
the
Oodomari
collection
in
June
included
some
individuals
producing
cystocarps
both
on
the
surfaces
of
their
blades
and
along
the
margins
(Fig.
21).
Mature
cystocarps
prominently
protrude
and
have
peripherally
radiating,
unbranched
to
occasionally
branched
chains
of
3-12,
ellipsoidal
or
obovoid
car-
posporangia,
18-48
gm
long
and
13-20
gm
in
diam-
eter
(Fig.
19).
They
are
1500-1950
gm
high
and
1375-2000
gm
in
diameter
(including
enveloping
tis-
sue
90-100
gm
thick
except
an
ostiolate
pericarp).
Cystocarps
are
sometimes
provided
with
one
to
seven
spinous
outgrowths
(Fig.
22)
that
develop
from
the
sur-
face
cortical
layer
and
are
up
to
2.4
mm
long.
110
.1
4
11
101m
4o-
'5
0
1
4
i•V
Meristotheca
papulosa
239
10
Pm
C
4
it
a
ac
-
ac
ti
1
0
Pm
1
0
14m
Air
15
17
'1
A
.;,!;••
'
4
!"
:•ir
r
xf
••••,_
J
10P
I
.
50
Pm
Figs
8-17.
Reproductive
structures
of
Meristotheca
papulosa.
Transverse
sections
of
Okinoshima
material
stained
with
cotton
blue.
8.
Spermatangia
produced
from
the
outermost
cortical
cells.
9.
Marginal
fertile
portion
containing
a
carpogonial
branch
and
an
auxiliary
cell:
arrowhead
indicates
the
supporting
cell
of
a
carpogonial
branch;
arrow
shows
the
supporting
cell
of
an
auxiliary
cell.
10.
Three-
celled
carpogonial
branch:
arrowhead
indicates
the
supporting
cell.
11.
Four-celled
carpogonial
branch:
arrowhead
indicates
the
supporting
cell.
12.
Auxiliary
cell
complex
(ac,
auxiliary
cell).
13.
Connecting
filament
(cf)
developing
from
a
carpogonium:
arrowhead
indicating
the
remnant
of
a
trichogyne.
14.
Fusion
between
a
connecting
filament
(cf)
and
the
auxiliary
cell
(ac).
15.
Gonimoblast
initial
(arrowhead)
cut
off
from
a
diploidized
auxiliary
cell
(ac)
(connecting
filament
being
out
of
focus).
16,17.
Early
development
of
carposporophytes:
arrowheads
indicate
gonimoblasts;
arrows
show
enveloping
tissue.
r
4
.
,
4'
4
200Prn
da_
240
E.
J.
Faye
et
al.
18
a
19
I
4
0
Lf)
4111141
FIQuas..
20
21
4,
.
.
10
'
4
.
10
23
0
ipric
hv
10
prn
24
E
10Pm
25
1111111
14
P
rn
IV
8Ir
i
Figs
18
-
25.
Reproductive
structures
of
Meristotheca
papulosa.
Transverse
sections
stained
with
cotton
blue
unless
otherwise
indicated.
18.
Placentate
cystocarp
with
ostiole
(Nakanoura).
19.
Branched
chains
of
carposporangia
(Nakanoura).
20.
Numerous
lateral
proliferations,
each
of
which
is
branched
and
bears
one
or
several
cystocarps:
arrowhead
indicates
surface
proliferation
(surface
view
of
Chojagasaki
specimen).
21.
Portion
of
segment
bearing
marginal
and
surface
cystocarps
(Oodomari).
22.
Spinose
cystocarp
(arrowhead)
(Okinoshima).
23.
Young
tetrasporangium
basally
pit-connected
(arrow)
to
its
parental
cell
(Okinoshima).
24.
Zonately
divided
tetrasporangium
with
basal
pit-connection
(arrow)
with
the
bearing
cell
(Okinoshima).
25.
Young
tetrasporangium
laterally
pit-
connected
(arrow)
to
its
parental
cell
(Okinoshima).
,
Meristotheca
papulosa
241
Tetrasporangia
are
scattered
among
cortical
cells
over
the
entire
tetrasporophytic
blade
except
the
low-
ermost
part.
Typically,
tetrasporangial
initials
are
basally
atached
to
their
parental
cortical
cells
(Fig.
23),
and
basal
pit-connections
remain
in
mature
tetraspo-
rangia
(Fig.
24).
In
a
few
cases,
however,
tetrasporan-
gial
initials
appear
laterally
pit-connected
to
their
parental
cell
(Fig.
25).
Tetrasporangia
are
zonately
divided
and
measure
30-60
p.m
long
and
15-25
p.m
in
diameter
at
maturity.
rbcL
analysis
Nine
samples
of
M.
papulosa
collected
at
eight
differ-
ent
localities
and
showing
various
gross
morphologies
(Figs
1-4)
were
sequenced
for
the
rbcL
gene
analyses.
Because
sequences
were
incomplete
at
the
5'
and
3'
ends,
1295
bp
corresponding
to
positions
110-1404
of
the
rbcL
sequence
of
Chondrus
crispus
Stackhouse
Fig.
26.
Strict
consensus
tree
of
seven
equally
parsimonious
trees
(1135
steps,
CI
=
0.505,
RI
=
0.583,
RC
=
0.294)
of
the
Solieri-
aceae
inferred
from
partial
rbcL
gene
sequences
(1295
bp).
Caulacanthus
ustulatus,
Heringia
mirabilis
and
Areschougia
ligulata
were
used
as
outgroups.
All
sites
were
treated
as
unordered
and
equally
weighted;
only
values
above
50%
bootstrap
support
(2000
replicates,
full
heu-
ristic
search
with
TBR
method)
are
shown.
Each
of
V,
G,
F
and
P,
follow-
ing
the
labels
Meristotheca
gelidium
and
Meristotheca
procumbens
indi-
cates
the
region
where
material
was
collected:
Virgingor,
Guadeloupe,
Fiji
and
Philippines,
respectively.
(U02984)
were
used
for
the
alignment.
Sequences
of
four
samples
(M2,
M10,
M29,
M91)
were
found
to
be
identical
and
differed
from
the
five
others
(M37,
M38,
M40, M52,
M54)
in
1
bp.
The
phylogenetic
trees
obtained
from
MP
and
ML
analyses
are
presented
in
Figures
26
and
27.
The
iden-
tical
sequences
of
our
alga
were
excluded
from
the
alignment.
In
the
MP
analysis,
seven
most-parsimoni-
ous
trees
(1135
steps,
CI
=
0.505,
RI
=
0.583,
RC
=
0.294)
were
obtained
and
their
consensus
tree
is
presented
in
Figure
26.
For
the
ML
method,
likelihood
settings
from
the
best-fit
model
(GTR
+
I
+
G)
were
selected
by
a
hierarchical
likelihood
ratio
test
in
the
program
Modeltest
version
3.06:
assumed
nucleotide
frequencies
A
=
0.29560,
C
=
0.13820,
G
=
0.20720,
and
T
=
0.35900;
substitution-rate
matrix
with
AC
=
1.126500,
AG
=
7.624500,
AT
=
2.234100,
CG
=
1.539200,
CT
=
17.457200,
and
GT
=
1;
pro-
portion
of
invariable
sites
=
0.3774;
gamma
distribu-
Emboutim
firimihmiabp*
'
,
mi
l
--
St
0.44111.1.1ii
Vet!.
sum
4p/o5r
phhiRpopeemit
by
Sarrrsiirothrixr
An-m.1J
Fur
radii
tlimi
gwollichnxiki
Mr
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Throgrern
yfriirilkero
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ReAdimer
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etherw
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MiSNItherlA
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perp.rarm
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NI2,
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M911
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M3
A14,111,15.152,
M341
A..14
voriort
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tr
r.telk
rirevni
,
'Soliettie.a4toda)
Sz106rosLr'skisl!fleei
pherho
(00,1e..rarA
Worm.
tp.
SePherno
r
ill
Caafgaslluhris
madams
ouirablIE.7
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Swearieow
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plialphkuot
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fififorme
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kuppaploy,
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weirs
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71
A
yardroiriki
Aidm
ban
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rhornligala
reamusissirmi
Agarrilfreiler
dp
Aorafireca
mouipprei
IIXI
Sarroihoutrca
fiorcruo
4iirrouliduhrvo
grididicheakiii
Wr•
Fist°
thisra
gel/0nm
V
PIFVFAION't
1a
1JeihROL111(1
("L
AferW4rOreca
pe-wtooNhew
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kri..q}frirIJOr
Fr
lerrr
fraht•erT
P
100
10ar
Arerinvirera
paparatet
[112,
M110.,
Mr),
NIVI)
hien:500ml
papiavra
{10}7.
1113I.
M40.
M52.,
11x
1
-
OrferiM•rgiwoor
dakotrows
1410,
rihrierid'
vfluirdisni
',50herra
'
ficreifa
-
si
51410r14
trilfimmia
$r+lir'riel
sp,
ripiiektir
SI
242
E.
J.
Faye
et
al.
0.01
substitulionsIsih•
Fig.
27.
Phylogenetic
tree
of
the
Solieriaceae
inferred
from
ML
analy-
sis
of
partial
rbcL
gene
sequences
(1295
bp).
Caulacanthus
ustulatus,
Heringia
mirabilis
and
Areschougia
ligulata
were
used
as
outgroups.
All
sites
were
treated
as
unordered
and
equally
weighted;
only
values
above
50%
bootstrap
support
(100
repli-
cates,
full
heuristic
search
with
TBR
method)
are
shown.
Each
of
V,
G,
F
and
P,
following
the
labels
Meristo-
theca
gelidium
and
Meristotheca
procumbens
indicates
the
region
where
material
was
collected:
Virgin-
gor,
Guadeloupe,
Fiji
and
Philip-
pines,
respectively.
tion
with
shape
parameter
=
0.5491.
Based
on
these
settings,
the
heuristic
search
was
performed
with
the
TBR
branch
swapping
option
(—In
L
=
7392.15703)
after
10
369
rearrangements
(Fig.
27).
The
topologies
of
the
MP
and
ML
trees
were
almost
congruent,
except
for
the
clades
that
were
supported
with
low
bootstrap
values.
Our
alga
forms
a
monophyletic
Glade
with
spe-
cies
of
Meristotheca
(with
relatively
strong
bootstrap
support).
The
pairwise
distances
between
our
alga
and
the
other
species
of
the
same
Glade
range
from
21
to
65
bp
(1.6
to
5.7%).
DISCUSSION
At
present,
the
following
eight
species
other
than
M.
papulosa
are
assigned
to
Meristotheca
and
are
reported
to
occur
in
warm
temperate
and
tropical
seas
around
the
world:
Meristotheca
coacta
Okamura
(1930),
Meristotheca
dakarensis
Faye
et
Masuda
(Faye
et
al.
2004),
Meristotheca
echinocarpa
(Areschoug)
Faye
et
Masuda
(Faye
et
al.
2004),
Meristotheca
fer-
gusonii
Grunow
ex
Mazza
(1920),
Meristotheca
gelid-
ium
(J.
Agardh)
Faye
et
Masuda
(Faye
et
al.
2004),
Meristotheca
procumbens
Gabrielson
et
Kraft
(1984),
Meristotheca
schrammii
(P.
Crouan
et
H.
Crouan)
Faye
et
Masuda
(Faye
et
al.
2004),
and
Meristotheca
tobagensis
Taylor
(1962).
The
status
of
M.
fergusonii
and
M.
tobagensis,
however,
needs
confirmation
because
of
the
absence
of
information
on
generically
important
reproductive
features.
Critical
reproductive
characteristics,
including
the
carpogonial
branches
and
auxiliary
cells
formed
in
marginal
regions,
the
formation
Meristotheca
papulosa
243
of
a
single
connecting
filament
from
each
fertilized
carpogonium,
the
production
of
a
single
gonimoblast
initial
from
the
diploidized
auxiliary
cell,
the
presence
of
placentate
cystocarps
provided
with
enveloping
fila-
ments,
and
conspicuously
developed
cystocarpic
protu-
berances
or
papillae,
which
are
confirmed
in
our
material,
best
agree
with
other
reports
of
Meristotheca
(Gabrielson
&
Kraft
1984;
Gabrielson
&
Cheney
1987;
as
Meristiella,
Guimaraes
&
Oliveira
1996;
Faye
et
al.
2004),
in
addition
to
vegetative
features,
such
as
the
flattened
thalli,
the
periaxial
cell
arrangement,
and
the
absence
of
interconnecting
cells
(or
filaments)
between
adjacent
axial
filaments.
Furthermore,
our
ML
and
MP
trees
show
that
our
alga
constitutes,
with
relatively
strong
bootstrap
support,
a
monophyletic
Glade
along
with
other
Meristotheca
species.
Pairwise
distances
between
our
alga
and
the
other
species
of
this
Glade
range
from
21
to
65
bp
(1.6
to
5.7%).
Our
alga
can
be
referred
to
M.
papulosa
on
the
basis
of
its
blades
with
repeatedly
irregularly
to
subdichotomously
divided,
thick,
erect
axes and
the
marginal
position
of
cystocarps.
The
gross
morphology
of
the
alga
under
study
is
extremely
variable.
With
respect
to
the
degree
of
elon-
gation
and
widening
of
the
upright
axes,
the
frequency
of
branching
of
the
axes,
the
number
of
the
prolifera-
tions,
and
the
presence
or
absence
of
maculae
on
the
blade
surfaces,
several
different
forms
could
be
distin-
guished.
Thalli
with
elongated
and
narrow
axes and
smooth
margins
(Fig.
1)
look
very
different
from
those
with
short
and
broad
axes and
copious
proliferations
(Fig.
2).
Nevertheless,
our
rbcL
gene
analyses
show
that
these
thallus
forms
represent
a
single
species
as
specimens
with
different
morphologies
present
great
sequences
similarities.
In
the
molecular
trees,
two
groups
of
M.
papulosa
samples
could
be
identified
(Figs
26,27).
They
differ
in
1
bp
in
the
rbcL
sequence,
and
are
not
related
to
differences
in
blade
morphology.
One
of
the
groups
includes
three
samples
(M2,
M10,
M91)
that
were
collected
from
southerly
localities
(Tajiri
and
Oodomari
in
Kagoshima
Prefecture),
whereas
all
five
samples
(M37,
M38, M40, M52,
M54)
of
the
other
group
were
gathered
from
more
northerly
locali-
ties
(Chojagasaki
in
Kanagawa
Prefecture,
Ookataura,
Nakanoura
and
Ishijirogawa
in
Tokyo
and
Okinoshima
in
Chiba
Prefecture).
Therefore,
in
our
molecular
results,
the
segregation
of
Japanese
M.
papulosa
sam-
ples
into
two
groups
can
be
correlated
with
distribution
patterns
rather
than
blade
morphology.
One
sample
(M29),
however,
constitutes
an
exception
because
it
was
associated
with
samples
from
Kagoshima
Prefec-
ture,
although
it
was
collected
at
Sokodo
in
Tokyo.
Although
the
factor
leading
to
these
groups
is
unknown,
morphologically
variable
plants
of
the
two
groups
should
be
regarded
as
conspecific.
Similar
morpho-
logical
variations
are
also
known
for
Australian
M.
papulosa
(Gabrielson
&
Kraft
1984);
however,
rbcL
sequences
of
these
plants
are
not
available.
The
position
of
cystocarps
might
be
an
important
species-specific
criterion
for
this
genus.
In
some
species
cystocarps
are
located
at
the
margins
of
blades,
whereas
in
others
they
are
scattered
over
the
surfaces
of
thalli
(Faye
et
al.
2004).
Type
material
of
M.
papulosa
is
said
to
bear
cystocarps
in
the
thallus
margin
(Gabrielson
&
Kraft
1984).
This
agrees
with
previous
studies
of
this
taxon
(Yendo
1911;
Durairatnam
1961;
Gabrielson
&
Kraft
1984;
Norris
1988).
However,
our
specimens
produce
cystocarps
abundantly
on
their
lateral
prolifer-
ations
(Fig.
20)
and
rarely
on
blade
surfaces
(Fig.
21),
in
addition
to
blade
margins.
Our
material
is
provided
with
spinose
cystocarps,
a
character
that
Gabrielson
and
Cheney
(1987)
consid-
ered
as
one
of
the
diagnostic
features
segregating
Mer-
istiella
Cheney
from
Meristotheca.
However,
now
that
Meristiella
is
reduced
to
synonymy
with
Meristotheca,
the
presence
or
absence
of
such
cystocarpic
structures
might
be
taxonomically
significant
at
the
species
rank
rather
than
the
generic
rank
(Faye
et
al.
2004).
Although
Yendo
(1911)
and,
subsequently,
Cotton
(1914;
as
E.
papulosa)
found
several
small
spines
on
cystocarps
of
the
Japanese
alga,
spinose
cystocarps
have
not
been
reported
for
any
M.
papulosa
specimens
from
the
other
geographic
regions.
Therefore,
the
pres-
ence
of
spinose
structures
on
the
cystocarps
might
represent
one
of
the
important
diagnostic
features
of
the
Japanese
M.
papulosa.
In
some
members
of
the
Solieriaceae,
including
Agardhiella
(Gabrielson
&
Hommersand
1982b),
Anatheca
(Faye
et
al.
2005),
Sarcodiotheca
(Gabriel-
son
1982a,b)
and
Solieria
(Gabrielson
&
Hommersand
1982a;
Gabrielson
&
Kraft
1984),
the
auxiliary
cell
and
adjacent
cortical
cells
stain
darkly
before
dip-
loidization.
Gabrielson
and
Hommersand
(1982a)
call
such
an
association
of
cells
an
auxiliary
cell
complex.
In
the
genus
Meristotheca,
the
presence
or
absence
of
an
auxiliary
cell
complex
is
now
considered
to
be
pos-
sibly
significant
at
the
species
level
taxonomy
(Faye
et
al.
2004).
With
regard
to
M.
papulosa
specimens
from
Lord
Howe
Island,
New
South
Wales,
Australia,
Gabrielson
and
Kraft
(1984)
state
that:
'Auxiliary
cells
appear
to
be
undifferentiated
inner
cortical
cells
prior
to
diploidization,
as
dense-staining
auxiliary
cell
com-
plexes
comparable
to
Solieria
were
not
seen'.
This
is
not
the
case
of
our
material,
in
which
a
darkly
stain-
ing
auxiliary
cell
complex
is
present
and
clearly
observable
before
fusion
between
a
connecting
fila-
ment
and
the
auxiliary
cell
itself
(Fig.
12).
Other
reports
of
M.
papulosa
did
not
mention
the
auxiliary
cell
complex.
As
its
detection
is
sometimes
difficult
depending
on
the
staining
condition,
further
critical
examinations
of
materials
from
other
geographic
areas
are
needed.
244
E.
J.
Faye
et
al.
The
tetrasporangial
origin
is
referred
to
as
one
of
the
potential
species-specific
taxonomic
features
in
the
Solieriaceae
(Faye
et
al.
2004,
2005).
In
most
of
the
known
species
of
Meristotheca,
including
M.
papulosa
from
Australia
(Gabrielson
&
Kraft
1984)
and
South
Africa
(Norris
1988),
tetrasporangia
are
reported
as
being
laterally
connected
to
their
parental
cells
(Gabri-
elson
&
Cheney
1987;
as
Meristiella,
Guimaraes
&
Oliveira
1996;
as
Meristiella).
In
contrast,
M.
dak-
arensis
from
Senegal,
western
Africa
and
our
material
have
tetrasporangia
that
are
usually
attached
basally.
This
constitutes
another
critical
feature
whereby
the
Japanese
alga
can
be
distinguished
from
the
other
reported
M.
papulosa
species.
It
can
be
noted,
however,
that
the
position
of
such
pit-connections
is
not
speci-
fied
in
some
reports
of
this
taxon.
Accordingly,
if
a
distinct
species
was
to
be
recog-
nized
for
our
material
under
study,
it
could
be
based
on
the
following
four
reproductive
features:
(i)
the
occurrence
of
cystocarps
on
marginal
proliferations
and
the
surface
of
blades
in
addition
to
the
edges
of
axes;
(ii)
the
presence
of
an
auxiliary
cell
complex;
(iii)
the
frequent
presence
of
spinose
outgrowths
on
the
peri-
carp;
and
(iv)
typically
tetrasporangial
initials
basally
attached
to
their
parental
cells
by
a
pit-connection.
In
that
case,
Kyl
in's
(1932)
earlier
published
name
for
the
Japanese
alga,
M.
japonica
Kylin,
which
is
now
consid-
ered
to
be
synonymous
with
M.
papulosa
(Yoshida
1998),
is
available.
Although
Kylin
(1932)
did
not
give
reproductive
details
of
his
new
species,
he
separated
it
from
the
generitype
M.
papulosa
on
the
basis
of
its
thicker
and
more
cartilaginous
blades.
However,
after
comparing
herbarium
specimens
of
M.
japonica
from
Japan
with
those
of
M.
papulosa
from
the
Red
Sea,
Somaliland
and
the
Arabian
Sea
BOrgesen
(1934)
indi-
cated
that
the
vegetative
features
that
were
used
by
Kylin
(1932)
to
distinguish
the
Japanese
alga
were
perhaps
not
of
taxonomic
value
and,
therefore,
he
regarded
M.
japonica
as
morphologically
similar
to
M.
papulosa.
Nevertheless,
he
abstained
from
synony-
mizing
M.
japonica
and
M.
papulosa
until
further
sampling
could
be
undertaken.
One
specimen
from
Pakistan
examined
by
BOrgesen
(1934,
fig.
10)
dis-
plays
a
feature
we
regard
here
as
distinctive
for
the
Japanese
alga:
the
production
of
surface
and
marginal
cystocarps.
Despite
this
similarity,
however,
we
are
unable
to
evaluate
the
taxonomic
value
of
this
repro-
ductive
feature,
or
even
ascertain
the
conspecificity
or
distinctiveness
of
the
Japanese
and
Pakistani
speci-
mens
until
further
comparative
morphological
and
molecular
studies
are
undertaken.
As
in
the
case
of
Grateloupia
turuturu
Yamada
(Haly-
meniaceae),
an
invasive
species
in
the
Atlantic
Ocean
(Gavio
&
Fredericq
2002),
or
with
Polyopes
tosaensis
Kawaguchi
et
Masuda
(Halymeniaceae),
an
alga
long
overlooked
as
small,
depauperate
thalli
of
Polyopes
prolifer
(Hariot)
Kawaguchi
et
Wang
(Kawaguchi
et
al.
2003),
recent
molecular
studies
applying
rbcL
gene
sequence
analysis
have
proved
this
marker
to
be
very
useful
in
identifying
individual
species
or
discovering
cryptic
species.
In
this
regard,
we
sequenced
the
rbcL
gene
of
Japanese
M.
papulosa,
but
the
absence
of
com-
parative
specimens
from
outside
Japan
made
it
impos-
sible
to
assess
the
taxonomic
significance
of
our
alga's
diagnostic
morphological
features.
Therefore,
morpho-
logical
and
molecular
studies
of
M.
papulosa
from
other
locatities,
including
the
type
locality,
are
needed.
We
provisionally
continue
to
use
the
name
M.
papulosa
for
the
Japanese
alga
until
such
critically
important
data
become
available.
ACKNOWLEDGMENTS
We
are
deeply
indebted
to
Masaya
Tani
(Hokkaido
Uni-
versity)
for
providing
some
specimens
of
Meristotheca
papulosa.
This
research
was
supported
in
part
by
a
21st
Century
Center
of
Excellence
(COE)
Program
on
'Neo-
Science
of
Natural
History'
(Program
Leader:
Professor
Hisatake
Okada)
at
Hokkaido
University
financed
by
the
Ministry
of
Education,
Culture,
Sports,
Science
and
Technology,
Japan,
and
in
part
by
a
Grant-in-Aid
for
Scientific
Research
(No.
16570070)
from
the
Japan
Society
for
the
Promotion
of
Science.
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