PERSOONIA
Published
Volume
Significance
in
the
by
Rijksherbarium, Leiden
Part
4,
of
the
2,
pp.
the
Sao
Botdnica",
Plates
Paulo, SP, Brazil
6-9)
of this
peculiar
higher Basidiomycetes
The
data
cytogenetic
the
reviewed
available
but the
basidiomycetous species,
among
were
of
type
septum in
the classification of
from the literature
restricted
are
and
small
a
to
and
formation
cytogenetic phenomena affecting clamp-connection
the interpretation
the
clamp-connection
Furtado
"Instituto de
(With
The
(1966)
Basidiomycetes
João+S.
Cryptogamic Section,
125-144
discussed.
number
formation of clamp-connection
of
is included
major phenomena whose genetic control is generalized
for the
Basidiomycetes.
formation in
Clamp-connection
the
factors affecting
heterothallic species
sexuality. Simple
septa
the
bearing species when (1)
clamp-connection
hyphal growth
of the
duction and further
only
of
one
appears
kind
dikaryon.
of the
Genetic
of apomictic
The
monokaryotic hyphae
also show
that
are
spores
(3)
or
B,
or
Therefore,
the
or
clamped
and
genetically
and
when
at
are
formed
species
formation
there
invariably simple-septate.
in successful
appear
crosses
homo-
time, incompatibility factors.
In
is
are
homothallic species
well known,
not
masked
by
the
dikaryotic
the
In
are
control
clamp-
but whenever
nuclear pairings.
clamp-connections follows
of
but
heterothallic species,
same
distinct.
formation
connections
the
there
splitting
simple-septate hyphae of the Basidiomycetes
cytologically
of clamp-connection
the
both
even
pro-
containing
monokaryons of tetrapolar heterothallic species carrying
A
is
when there
(asexual)
simple septa
of
from
without subsequent
(2)
dikaryon,
of the
hyphae
of monokaryotic hyphal growth caused by the
experiments
between
allelic
development
nuclear components
the
any
or
recovered monokaryon,
newly
controlled by
the
septa result
simple
independent nuclear division of the dikaryon, with
is
in
appear
pseudohomothallic
the
of
pattern
nature
of the
the
basidio-
spores.
The
taxonomic interpretation
divergent.
condition
necessity
before
In
of
the
of the
any
cases
many
hyphae
the
to
hypothesis
the
clamp-connection
did
formulate
evaluation
proper
of
authors
not
their
of the
is
somewhat
investigate the cytogenetic
hypothesis.
pattern
of
This
septation
shows
of the
the
hyphae
is formulated.
Introduction
The
of its
clamp-connection
inconspicuousness
especially
the
peculiar type
culture of
in
is
a
and
Polyporales
irregular
and
of septum is
basidiocarp
character of
questioned
pattern of
Agaricales.
both
In
prominent
tissues of many
contrast to
125
significance
in many
because
Basidiomycetes,
this erratic occurrence, this
and abundant in
species
nature.
taxonomic
occurrence
in which the
mycelia
septation
derived from
is
not
evident
PERSOONIA
126
The
careful
recently by
of
a
of the
study
few
are
on
polypores
literature. I
hope
Basidiomycetes,
the
used
the
emphasizing
The
Part
1966
2,
has
Basidiomycetes
cytologic
studies
is
manuscript
paper
necessity
been stressed
many
review
a
paper.
of the taxonomic
all
were
only
the formation
involving
essentially
and
data
cytogenetic
between
gap
the
4,
illustrate this
to
original.
are
bridge
to
This
advanced.
cytologic preparations
studies
in the
septation
mycologists, although
clamp-connections
The
Vol.
taken
from the
of the
taxonomy and modern genetics
define
to
the
septation
of the
species
properly.
Material and methods
for nuclear demonstration
Cytologic preparations
technique
&
(Ward
Ciuryzek,
Polyporus pseudoboletus
of
species
polypores)
and immediate
in
medium
plastic "Abopon"
herbarium
included
specimens
toluidine blue,
dried
&
HCl-Giemsa
specimens
polypore,
several
(of
of
ig62a)
Beneke,
made with
sampling
Permanent
ig62).
the
of the
use
water-
Additional technique used
1962).
with 0.5
and
the
of unstained material were made
were
Harder,
water
by
wood-rotting
technique {1936,
mounts
staining
with distilled
washing
&
(Hrushovetz
made
were
tropical
(Alexopoulos
of stained and unstained preparations
soluble
for
Teixeira's
by
mounting. Semipermanent
blue
the
of fresh and
studies
Hyphal
made
were
lactophenol-cotton
mounts
or
Speg.
with
1962 )
percent aqueous solution of
in either distilled
mounting
water
"Abopon".
Photographies
bright-field,
high
made with 35
were
and
dark-field,
Kodabromide
contrast
F4
and
Nomenclature of the
Homokaryotic
the
hyphal segments
1953)
and
ization
are
claimed
(1)
the
of
Derx
perplexans
cleate,
of the
but
presence
ex
of
reported
and
life-cycle
mycelium.
by
genetic
of the
The
1-5).
&
(Figs.
from culture of
of the
hyphae
6-7).
(Olive,
In
species
basidiocarp
Dodge,
cases
terms
The
in the
the
mycelium
to
this
ex
the
corresponding
mycelium
in the
and (2J
1933),
Itersonilia
on.
diploid-equivalent
taxonomic
are
of septa
mycelium
of
Fries, respectively
term
usually
simple-septate
types
(Olive,
general-
will be discussed later
to
of
The
primary mycelium
1928; Raper,
and either
or
haploid
multinucleate
or
(Batsch)
applied
with both
tissues,
on
primary mycelium.
primary mycelium of
secondary
1953),
the
is
Two contradictions
in the
Both
genetic
for
term
narcoticus
Coprinus
( 1932).
are
film under
made
components
uninucleate
are
Basidiomycetes.
also multinucleate
terms
taxonomic
(Gäumann
Olive
dikaryotic
and its
clamp-connections
true
Fries and
and Brunswik
clamp-connections
mycelia
are
corresponding
KB-14
were
papers.
incomplete clamp-connections
Heterokaryotic
secondary
6
primary mycelium
(Willd.)
by Kniep
presence
phase
of the
Agfa
mycelium
monokaryotic
the
illuminations. Prints
invariably simple-septate (Figs.
Stereum hirsutum
the
and
Basidiomycetes;
black-and-white Adox
mm
phase-contrast
or
(either
of the
is
binu-
bearing
in
the
basidiocarp
FURTADO:
in
the
nature),
simple-septa
never
On
clamp-connections
in
appear
127
of
hyphal segments
consti-
dikaryotic
tution.
Context,
dissepiment,
classification.
A
new
trama,
and
hymenium,
terminology
has
microstructural criteria in classification. The
such
structures
termed
could
hypha
definitionof the
logically
hyphae
the
1962b).
In
and
hyphae
the
in which
structures
having
a
Contemporary
lose
and
in
processes
and
sexuality;
nuclear
The
and
(3)
io
first
percent
of the
It does
indicate,
species
species
tetrapolarity,
1949a)
was
a
with
the
however,
including
species,
mycelial
(Buller,
for the
secondary mycelium
association
the
are
surveyed.
between the
relationship
formation in the
i960 )
genetic
Basidiomycetes.
characterized
are
and
heterothallic
and
growth
such
nuclei
of
a
1938; Boidin,
genetically
thing
can
in
is
by (1)
a
tetrapolar
patterns
fusion followed
of
by
and
the
still
of heterothallism
In
later
the
entire
and,
only
35 percent
is
selected
on
a
biased
for
within
study.
this,
of
the
and
The
the
be
"per
by
hyphae
hyphae
use
now
of the
species
possessing
show
term
paired
dikaryon
misleading because, although
mating system,
established
se".
the entire life-
homothallic
clamped,
1963).
can
life-cycle
completes
characterized
(except
species)
90 percent,
are
the
among
analysed,
heterothallic. This
of the homothallic species is
nuclei
sexuality
sample
Basidiomycetes.
usually
appear
diverse
the
remaining
were
1958; Berthier,
homothallic
perform
in
haploid basidiospore
meiosis.
of
patterns
that,
tetrapolar
predominance
single,
a
karyogamy
the initial
percent
attribute of the
particular
homothallic
these
showed
clamp-connections
nuclei
no
are
hyphae
formation
secondary
homothallic. Of the
simple septa. Clamp-connections
is
the
and
should be
copulation by hyphal
distribution of
heterothallic and 55
since
studied,
the
(Whitehouse,
sample
cycle,
mechanism of somatic
of
survey
bipolar
In
or
1956,
hyphae,
division
(a) homothallic, (b) bipolar
a
binding
and
generative
species
of the
migration.
Basidiomycetes
was
a
strict
fungi (Raper,
pseudohomothallic
(c)
or
a
clamp-connection
generally haplo-dikaryotic life-cycle; (2)
heterothallic,
of the
septation
cell
the
morpho-
Teixeira
generative
the
Therefore,
skeletal
any
species.
constituent
1963;
for
capacity
clamp-connection
this class of
the
are
limited
elements of the
1954,
of the
nature
definition,
ig62b)
only
new
hyphal types
differentiate into
particularly
their
growth.
of
the
are
elements
Cunningham,
research has demonstrated
controlling sexuality
The sexual
hyphae
totipotent
the pattern
(1962a,
in
of the
divide and form
original
totipotent dikaryotic
generative
limited
Sexuality
factors
the
binding
by
the
1933;
to
characterized
Teixeira
distinct structures,
contrast
the addition
can
its
1932b). By
1932a,
to
the
1932b,
1932a,
that
hyphae
generative.
generative
others,
functionally
and
skeletal
true
In
context.
(Corner,
1962a,
called
generative hyphae
Basidiomycetes
many
basidiocarp
(Corner,
be
with
currently
used
terms
are
on,
setae, and any other modified
cystidia,
generative hyphae
dividing
In
basidia,
as
so
introduced
been
Olive
because
there
(hybridization),
( 1933) proposed
all
the
PERSOONIA
128
distinguishing
thallic
heterothallism in
the
the
Basidiomycetes
heterothallic Mucorales and
preted
for
"homodikaryon"
term
4,
Part
1966
2,
secondary
mycelium
of the
follows
analogous
A,
homo-
Basidiomycetes.
Bipolar
the
Vol.
the
as
Ascomycetes.
of the addition of
consequence
the
factor, #,
a new
system of
a
heterothallism is
Tetrapolar
located
inter-
different
a
on
chromosome.
To the classical
l 94 r
>
concept of compound
is
Tetrapolarity
factors
for
incompatibility
interpreted
now
at
least
from the individual
of the subunits
one
and
the total
and
1958;
i960;
Day,
Takemaru,
A and
spontaneous and
by
1961;
each
form
&
the
Parag
1963;
Raper,
Day,
a
B,
at
affected;
by crossing-
&
&
i960;
or
change
factor
Baxter
(Raper,
of
either A
combinations
new
Ellingboe,
&
incompatibility
allelic
any
of
the
added.
composed
factor,
(4)
expression
mutations
B
subunit is
subunit;
of
and
Buller,
1933)
has been
1951)
of each
expression
B factors
Finchan
1962;
each
(2)
change
induced
Baxter
Raper,
Parag,
entire
an
1950,
both the A
(1)
1933, 1935',
1958; Raper,
(Papazian,
subunits;
composition of
to
the subunits of both
(5)
over
leads
follows;
as
two
multiple allelomorphic series; (3)
results
tetrapolarity (Quintanilha,
1949b; Papazian,
1949a,
loci
formed of
are
of
interpretation
Whitehouse,
1 95
Middleton,
i960;
Raper,
1963;
&
Raper
Esser, 1964).
According
A,
homoallelic B
others
at
heterokaryon
(common-i),
refer
usually
simply
as
loci,
into
its
may
fruit like the
heterokaryon
heterokaryosis.
',
the
In
some
in
'95
Swiezynski
Esser,
1964; Raper
grow
insufficiently
&
cases
only
the
the
of
the
as
types
of
heteroallelic
(common-d#).
and
dikaryon,
are
clamped, tetrapolar species
if the
homokaryons
homoallelic
formed
In
is
rare
the
the
Day,
1960a;
Raper,
to
reach
fusing
instances,
the
(Quintanilha,
&
San
Takemaru,
In the
eventual
it,
or
to
the
the
to some
terminal cells
of the
hyphae.
The
nuclear
are
the
1935;
Genetic
has
simple
Fulton,
by
in
transfering
A locus has
a
&
1969;
a
the
Raper,
Raper
&
the hook may
touch
the
hyphal
sub-
branch.
complementary
heterokaryon
specific
incomplete,
Papazian,
may
as
septa
to
(un-
Parag
1962,
independently
eventual
investiga-
1950;
1954;
cell,
resolving
heterokaryons
migration leading
replaced
Antonio,
paired,
incompatibility
often
unstable,
Raper, 1964).
penultimate
may grow
Therefore,
both
however,
are
different alleles
pseudoclamp-connections
fails
penultimate
carry
at
1961; Parag,
cell.
to
or
heterokaryon
pseudoclamp-connection
nucleus
&
extensive
clamp-connections
1964).
with
at one
limited and
common-/?
1963; Raper
1953,
&
terminal cell without
of
four
heteroallelic B
A,
heterokaryon
heterokaryon
controlls
B factor
others
Raper,
i960;
hook
homoallelic
(3)
dikaryon (Raper, 1963; Raper
'95°>
The
mates
pseudoclamp-connections
8
of
mycelia
formed
eventually
that
whereas
damped)
or
type
homokaryotic components.
indicate
false
are
and B loci. If the
the
tions
the first
loci,
heterokaryon, (2)
homoallelic AB
(4)
(homokaryotic)
clamp-connections
both A
to
(common-#),
and
incompatibility
heteroallelic AB
heterokaryons.
When primary
true
constitution of the
recognized: (1)
be
can
heterokaryon
Geneticists
allelic
the
to
heterokaryons
is
control
restricted
on
clamp-
FURTADO:
connection formation: in common-J
pseudoclamp-connections
clamp-connections
true
are
are
clamp-connections
On
ever
neither
heterokaryons
formed.
when
Only
129
nor
factor is heteroallelic
formed
pseudoclamp-connections
or
clamp-connections
the A
&
(Finchan
Day,
'963) ■
A
influence upon
cytoplasmic
(Papazian,
He
1938).
subterminal element and
considerable
cell.
Harder's
(.1952)
who
claims
'neohaplonts',
The
of
problem
reconsidered
The
in
i.e.,
the
mimics
homokaryon
mimics
homokaryon
mimics
connections and
there
only
is
one
incompatibility
homokaryon
or
the common-d
the
one
nucleus
per
with
Dodge,
&
pseudoclamp-connections
The
nature.
factors in
dependence
Schizophyllum
data
unpublished
here with
his
Although
mentioned the
opposite
kindly
claims
of
on
given
by
Dr.
mutant-/? modified-d
forms
are not
of
clamped
The natural
pseudoclamp-
formed because
genetically
two
primary
of
occurrence
be
1932) might
the
the mutant-i?
the modified-d
or
in heterothallic species raises
tentatively
mechanism of
mycelia
homokaryons
assumed
incompatibility
as
R.
John
(provisional,
1
Harvard
Raper,
the
control in
proper allelic constitution of the A
Fries is shown in Table
commune
species
of
the
homokaryon
possibility
mating
questioned,
are
type,
behaving
homokaryon
segregate
out
into
carried
a
the
still
in the
but
remains
Papazian
Papazian
be
"might
carrying
their
influencing
of the
and B
tentative and
University,
used
explained.
homokaryon
A
and
a
primary mycelium
termed
by
spontaneous
Raper
spores
extra
that
the
( 1933)
carrying
unquestionable
stated, however,
extra
the
be
to
claimed
(1931)
( 1958 )
separate nucleus and produce
without
hyphae
special phenomenon
of contamination of the
spontaneous dikaryotization.
be
disrupt
septation
the
participation
necessary
the reports of clamp-connections
dikaryotization
to
The
Brunswik's
the mechanism of the
mutant-type
clamp-connections
1953).
was
permission).
of heterothallic
the
of
latter
clamp-connections
(Olive,
consequence of mutations that
and
heterokaryon;
true
1928; Raper,
in the
formation
circumstances,
the mutant-d
cell.
and
Kniep's
disrupt
Under these
true
Aschan
formation is also revealed
clamp-connection
The
dikaryon.
&
dikaryotic dividing hyphae.
clamp-connection
on
heterokaryon;
common-5
the
and Fries
(1964).
mutations that
1963).
eventually fruits, but
concerning
(Gäumann
more
(Raper,
distinct nuclei for formation of
doubts
influence
Raper
control of
genetic
homokaryons carrying
control of
&
Raper
{1952)
during
dicytoplasmic
pseudoclamp-connections
nor
obtained from the
dicytoplasmic
ofthe
specificity
Harder
by
formed
were
homokaryotic,
Aschan
by
clamp-connections
homokaryons
by
recently
clamp-connections
true
confirmed
not
were
the
that
newly-formed subterminal,
neither
reported
claimed
the terminal cell and its hook before fusion with the
reported
of the
growth
formation was
clamp-connection
destroyed
cases
normally
# factors which
dikaryon,
but
incompatibility
they
of
later
would have
phenotype
which
is
incongruous."
Lange
mation
( 1932)
introduced the
of 'homothallic' and
basidiocarp. Lange's reports,
term
'amphithallism'
'heterothallic'
as
well
as
mycelia
the results
for the
from the
presented by
phenomenon
spores
of for-
of the
same
French authors who
Persoonia
130
Vol. 4, Part
Mod.
7-3
Nor.
0.6
2,
1966
18.4 1.4 24-3 14.0
7-3
.0
1.4
»4-7
136
—
168
'•3 i-3
i-3
158
2.6 3-5
—
16
1
1
Dikaryon
OF
98.2
—
—
— 0.6
0.6 —
—
MYCELIA
MODIFED
Raper)
AND
Hetrokayns
IN
CLAMP-ONETIS
AND
SEPTAION
COMPARTIVE
Nor.
2.6 —
39-5 0.7 12.0 8.8
11.2
4-38.6 67.2
1
John
Dr.
by
TABLE
20.3
R.
NORMAL PERCNTAGE
I
Com on-5
—
Mod.
COM UNE
SCHIZOPYLUM
obtained
Com on-zl
Mod.
7-3
Nor.
97-2
—
IOO
—
39-3 2-5 21.3 18.0
i-5 6.0 0.7 3-3
150
1.1 0.6
—
—
—
—
—
—
183
—
—
—
—
—
—
—
149
data
unp blished Homkaryon
Be
—
—
Ax
(Provisonal,
clamp-onectispseudoclamps
septa
Simple True Septal
nucleate
nucleate pseudoclamps
nucleate
nucleate
Non-septaeNon-septae, SeptateSeptate,InterseptalNon-septae Non-septae,SeptateSeptate, Sample
FURTADO:
have
the
accepted
the
species
do
form
and
{194.1),
Skolko
consequences of the
cultures
typical
genetics
The
the
in
deciding
on
fruiting
the
referred
to
is of
progeny
be
the
of
validity
the
bodies,
as
Both
primary
and
hyphae
mitotic,
by
{1964)
and
can
ascospores
by
called
was
that is used
used
term
the
in
of
single
by
'secondary
Alexopoulos'
contemporary review of
for
both
encompassing
'amphithallism'
the
not
take
clamps
as
a
because
the
of
should be
haploid
the
of
'haploid
some
it is
species
fruiting',
is
some-
fructification the
it may be
that
generally accepted
Before
haploid fruiting specimen.
characteristic for the identification
haploid
appears
of the
extent
the
basidium,
significant
criteria
cytogenetic
as
parental type. Although
in the
place
interpretation
In
parthenogenesis.
have
versus
to
condition
dikaryotic
have caused
taxonomic
no
in
haploid fruiting phenomenon
in
is
Ciuryzek
staining
for
as
&
amitotic,
Ciuryzek
{1961)
(Fig. 8),
inent but difficult
in
by Bakerspigel
{1961),
possibility
of the
at
to
in the
study
nature
(Nobles,
of
and Lu
two or
{1959),
( 1964).
more
truly
as
&
Raper
basic modes of
optical
most
fungi.
often
The
among
the
selection of the
of nuclear division. In addition
microscope.
division appears
(Figs.
used
the
to
that,
the smallness of the chromosomes is under
interphase (Fig. 9).
count
been
demonstration in
indicated that
nuclear
has
technique
nuclear
important
the resolutional limits
the nuclei appears
commonly
general.
procedures
the nuclei
Ward
mycelium
distributed
are
stated that there remains the
technique
Ward &
interpreted
{1953),
of the
of each other. Nuclear divisions in the
vegeta-
independently
been
HCl-Giemsa
cytologic
stability
secondary mycelia
grow
Olive
nuclear divison
proper
suggested
is unknown.
1958b)
The
for the
known
mating type,
Growth and
Esser
the basis
as
established. This situation
securely
the
the
analysed
'pseudohomothallism'
{1964)
alternatively
phenomenon
one
do
problems yet, especially
tive
& Esser's
dikaryotic
& Vasermanis
who
1957)
Basidiomycetes
terminology
a
Raper
Unless
in culture
and meiosis
karyogamy
nature
{1949a),
of
production
nuclei in the
named
was
in the
that sister nuclei fuse in the young
possible
{1927,
diverse
genetically
pseudohomothallism
complicated by
erroneously
Dodge
was
tetrasperma
and
fungi.
which generate
dikaryotic basidiospores
The
1962;
'amphi-
pseudohomothallism.
fruiting ability
basidiospore
must
mycology
by Dodge's
somewhat
of
Whitehouse
by
i960)
The apparent homothallism
Neurospora
heterothallism and
replaced
times
of
textbook of
and
it
of
homologous phenomenon
heterothallism'
sex
but
{1944),
ascospore
{1962)
and
Fichet,
&
show that the so-called
(192g), Quintanilha, Quintanilha
incorporation
tetrasperma Dodge.
and the
Sass
by
Neurospora
Dodge,
1959,
homokaryotic
discussed
was
1957c,
131
Lamoure
(Kiihner,
dikaryotic mycelia respectively.
and
homokaryotic
basidiospores
clamp-connections
'amphithallism'
term
Lamoure, 1955, 1957a, 1957b,
thallic'
On
10-12).
to
Regardless
be very
Chromosomal
rapid
of the
and
small
the
size
majority
bodies, however,
are
of
of
prom-
migration
Nuclear
Basidiomycetes
&
Vol. 4,
PERSOONIA
132
McAlear,
through
the
(1963).
In
of
Buller's
1962),
septal
the
&
contracting through
a
less
septum. No
hyphal
Butler
0.5
n
that
the
entire
been confirmed
( 1964)
pictured
distended
is
remarkably
in
phenomenon
the septal
aperture of
pores
Statement
has
1966
2,
prominent
a
the small
hyphae
Bracher
is
hyphae
{1958)
of the
pore
addition,
solani Kühn
type
through
13-14). Despite
(Figs.
Part
septal
the
nucleus
genetically
nucleus
a
of
pore
migrates
Snider
by
of Rhizoctonia
basidiomycetous-
a
shown
picture
the
(Moore
&
by Giesy
Day
[1965)The
of
events
nuclear
conjugate
connection formation in the
(193°>
I
Olive
95&)> Quintanilha
and
( 1953)
others.
formation:
connection
from the
cell
upper
establishing
the
relationship
(Noble,
lapse
is
Harder
& San Antonio
on
agar
medium,
(1996),
Raper
Da
karyons.
commonly
many
&
into
or
without
special
a
Homokaryotic
division,
(Figs.
15-16)
(Noble,
or
factory
transfers
may lack
one
a
may
also
vary
simple
a
hook derived
nucleus
cell and
per
(Olive, 1953).
nuclei divide with
the
re-
time
constant
a
con-
Whenever the
has
it
by
in
dikaryon
Kerruish
spontaneous splitting
sorting
apomictic
out
&
of the
experimentally
spores
in
technique.
Da
Miles
Costa
proportion
dikaryon
is
the
by
&
( 1963)
of homoobserved
of the nuclei into uninucleate
produced
are
original
Waring Blender, plated
way, increased the
some
the
growing hyphae.
simple-septate
and
and
micrurgical
a
nuclei
parent
split
induced
been
achieved
( 1962),
is
dikaryon
hyphae,
hyphal
with
or
conidial apparatus.
hyphal
branches
when
the
when the
result
parent
spindle
from
disturbance
nuclei of the
of the
nuclei
dividing
of
conjugate
divide
dikaryon
nuclear
independently
accommodated
are
widely
1937).
Apomictic (asexual)
spore
formation is
of the
oidia, conidiospores,
gasterospores,
the
in
which,
either the
homokaryotic components
been termed
the
recovery
1958)
Kerruish
uninucleate
especially
apart
by
when
dikaryon.
macerated the
the
species
in culture
branches,
This
and selected
used various toxic chemicals
In
the
segments
(Papazian,
(1954)
(2)
number of nuclei
hyphal height
even
during clamp-
the
(3)
Buller
( 1948),
(Fig. 9).
hyphal
Costa
and the
Routien
place
and
phenomena
1948),
same
preserved
recovered.
are
ways.
Raper
is
the
absolute in
not
different
into
homokaryons
several
at
take
clamp-
(1918),
conjugately,
cell and
penultimate
Routien,
formed
in time and
space
Heterokaryosis
separated
the
Bensaude
( 1942),
dividing parent nucleus,
condition. These
1937;
divide
with
relationships
by
phenomena
nuclei
parent
with
heterokaryosis
Nevertheless,
siderable
fuses
dikaryotic
of clamp-connections
out
the
their
(1937), Dodge
three
Basically,
(i)
and
discussed
were
Noble
( 1935),
is formed between each
septum
division
dikaryon
etc.
because
To
name
apomictic
such
major
a
secondary
chlamydospores,
spores
basidiospores
as
The
apomictic
ballistospores,
asexual
are
for recovery of the
source
mycelium.
spores
produced
is
by
not
the
original
spores have
secondary
spores,
absolutely
haploid
satis-
fruiting
specimens.
The asexual
spores
can
be
produced
by
both
primary
and
secondary mycelia.
In
FURTADO:
the spores
cases
many
of the
have been
either in
species,
nature
Nobles,
ig43;
Kiihner, 1346,
&
1947;
Rogers,
Yen,
1959b; Jacquiot,
Genetic and
mycelium
;
(Fig.
1337;
17)
Jackson,
formed
1346,
chains and
arise
by budding (Figs.
released
Usually
singly
germinate, giving
rise
The
secondary
(Nobles,
1935',
1943; Doguet,
The
95&)•
germ
bears
Asexual
mycelium
asexual
are
from
(Figs.
primary
spores
Brodie,
Doguet,
1336;
1956).
These
series of nuclear
a
10-11). They
may also
1935).
(Nobles,
asexual
may function
or
arising
relatively
have also been
in
quantity
as
a
spores
may
dikaryotizing
1963b,
(Corner,
and
more
1950),
clamp-connections
or
to
are not
clamp-connections
not
seen.
commonly
in
reported
the
and
many
simple septa
because
and Teixeira &
the
Rogers
are
situation—the
Agaricaceae.
In
in
in
In
1952;
Bose,
both
Lamoure,
clamped
species
species
some
Heim
1887;
the
&
asexual
in others the asexual spores
so-called
Ptycho-
Basidiomycetes.
nature
many
as
the
than is
species,
actually recognized.
especially
Tremellales
1963).
This may be due
septation,
mixed,
not
or
studied
of
1963a,
other
species
the construction
cases
cases
in the
as
in which
in which septa
septation—is
observed
clamp-connections
carefully.
with
1945),
1962,
binding hyphae
in the
however,
demonstrated that
In
either in those
irregular pattern
cases,
to
those
(Martin,
(Maas Geesteranus,
(Cunningham,
found
were
of a
(3)
or
clamp-connections
easily.
many
specimens
(1955)
spore
formed of skeletal and
of
Olive,
spores
1359a);
1937;
1962);
(Patouillard,
1963).
Hydnaceae
detected
Nobles,
imperfect stage—the
such
irregular pattern
The latter
the
found
Thelephoraceae
basidiocarp, predominantly
Polyporaceae,
of
1937;
Sarkar,
22).
basidiospores;
frequently
are
organization
various
(Fig.
1952;
Fichet,
1949;
nature
Fidalgo,
occurrence
&
dikaryotic
from
with the
Barnett,
of different genera of
clamp-connections
1963c )
O.
Aschan,
Lamoure
start
asexual
homokaryotic,
Kiihner,
characterize the
species
occur
the
reported
1948b;
to
hyphal
an
from
conjunction
various
simple
Clavariaceae
from
only
1935;
Kiihner,
asexual,
Clamp-connections
Conspicuous
not
1934;
the
asexual
'337',
homokaryotic
1947;
tube
produced
in
(i)
1937;
Natural
are
the
Yen,
(Kaufert,
1959;
clamp-connections
gaster-form i—of
the
that
conidial apparatus
special
form:
may
Kiihner &
spores
1928; Jackson,
formed
of the
a
1926; Vandendries,
spores
Malen^on,
are
by
primary mycelium,
1956; McKay,
(Gilmore,
usually
spores
the
or
pairs (Fig. 20),
Brodie, 1936;
(2) only dikaryotic,
T
in
or
to
19)
and
Sarkar,
1353',
(Fig. 21).
agent
kinds
12
1335,
result
divisions without immediate formation of cross-walls
ig34;
1363).
homokaryotic
Maxwell,
1330;
in
Bulat,
1952;
Fidalgo,
Nobles,
1333;
recognition
Chow,
1348] Kühner, Romagnesi
the asexual spores show
Kaufert,
usually
O.
1362;
for
1929, ig32;
1347,
multinucleate
or
Olive,
1343;
(Cartwright,
ig48a; McKeen,
ig6i,
involving
1933;
133
additional characteristics
as
Olive,
1947;
studies
Bose,
are
or
uninucleate
Vandendries,
Vandendries,
spores
form
used
clamp-connections
in culture
Pantidou,
cytologic
may
&
(Martens
ig47;
ig6o
On
Teixeira
clamp-connections
were
were
( i960)
present
in
which had been
species
has
ig62b)
is
the
Disregarding
caused
are
often
not
by
for
made
toluidine blue aqueous
I95
6,
for
by
basidium,
solutions.
inconspicous
hymenial
hyphae
and
handicap
well
as
The
1965).
cystidium,
structures
useless. This
division. Cell
generative
the
as
of
sampling
blue
methylene
detection of the
addition,
septal analysis
on
conditions
optic
with
of the
collected
generative hyphae.
many mistakes
Optimum
staining
the proper
septa
hyphae.
exactly along
formed
by
be
can
with
or
for
hyphae
proper
basidiocarp (Teixeira,
originally
results
from the
primitive
more
hook.
angle
at
from the
so
affect
by
septa
or
usually
cell
7a,
without
contiguous
branching immediately
at
one
the
portion
end
septum
the
hyphal growth:
bulge
This
from the
The
the
same
of
two
growth
the basal part
truncation which
division inside
form
clamp-connection
The
the
termina-
apical
septa
primitive
form
now
a
of observation indicate
directed backward and
always
direction
or
even
segments
the fusion of the
cell,
therefore
opposing
sometimes obscured
clamp-connection (Fig. 7b)
and reversion of
wholly
originally
and
be
cell
of the
contiguous
principles
can
for
segments
Since the hook
subterminal
statement
breadth,
ability
be determined
of lateral
by
(Furtado,
in
modified
(Fig. 7a).
cell,
hook is
indicates the
general
is
of the
formed
bulge
subterminal
25).
their
formed from nuclear
original septa
a
of
practice
a
cover
changes
penultimate cell,
kind
of the terminal cell
cell has
with
a
pileus
can
clamp-connection.
two
make such
alternating
or
clamp-connection
by
such
The absence
on.
losing
clamp-connections
recognized
15, 23 and
of the lateral
the direction of growth.
of the
undergo
of
inclined
penultimate
direction of
the presence
less
is
Furthermore,
upper
however,
the
of the
so
septation,
structures
the presence of modified generative
structures
on,
of
pattern
hymenial
and
generative hyphae. Separation
two
the basal
angle (Figs.
original
segment
and
The presence
terminal cell
tion of the eventual
concave
special
basidia,
for
hyphae
Consequently,
of
irregular
base of the
the terminal cell fuses with the eventual
of the
a convex
of
generative
the
an
the
of the
compensated
may
with
at
pseudoparaphyses,
autolysis
presence
23-24).
or
usually
wall, coloration,
separated segments
the
In
setae,
be
modification
partially (Figs.
occurs
the
can
modified
of the
thickness
hook
( 1962a,
manner
basidiocarp
inconspicuous
taxonomists,
illuminationand
usually requires
with
species
the
the
with
species
some
examination of the
septa is made
in
the
to
i962a)-
In
as
examination of the
devices of low resolution.
phase-contrast
observation of septa
Teixeira
lacking clamps.
as
descriptions pertaining
microscopic
satisfactory
errors
optical
achieved with
errors
1966
2,
polypores.
The regular procedure
nature
in
Part
4,
previously reported
additional
reported
in various
septation
in
Vol.
PERSOONIA
134
or
(Figs.
15
e.g.
by
detachment of the
by
and
23),
the
latter
in need of further observation.
Another,
in
but
uncommon,
species whose hymenial
irregularity.
spaces
The
of the
source
of
surface is
generative hyphae
hymenial
surface.
The
hyphae
tubular,
can
for
analysis
plicate,
have
generative
of
folded,
localized
hyphae
septation
or
can
provided
growth
and
that occlude
be
with
occlude
those
seen
any
the
spaces
Furtado:
should be
the
by
or
The
of simple
results, therefore,
of wall
septa
(i)
(pseudoseptum),
(cleavage
the
of nuclear division
of the
true
characterize
whereas
of nuclear
or
conidial apparatus
bearing clamp-connections
the
7c).
the
of the
generative
localized
by
followed
cytoplasm
of surface tension and further
These
be
not
disturbance
stage of the life-cycle
(haploid)
formed without nuclear division
septa
deposit
types of septum should
septa derived from
simple
homokaryotic
the
either
division,
by breakage
properties
features
general
there is
of the
with the
gradually
are
not
be
can
Several attempts
at
scopic
1954)',
an
to
were
the
other groups of
(Patouillard,
igoo)
was
;
Basidiomycetes
Martin,
Heim,
Cunningham,
Teixeira,
Wakefield,
1934;
1962a;
1946;
Bondartzev,
Lowe,
1963).
state
1946;
higher
Basidiomycetes
based
primarily
(Ames,
Cooke,
1913;
1949;
the
Nevertheless,
subject
is
taxa,
espeof
well.
as
been
Nobles, 1938b; Kotlaba,
1933;
been
of classification
various
made;
in
classification
upon
and many discussions and
been made for different groups of
19431
chaotic
additional features
as
has
criteria in classification. But
of classification have
introduced
traditionally
emphasis
delimitation of
the
on
entire system of classification
characteristics
The
basidiocarps.
remarks
natural system
types of modified hyphae
(Lentz,
(ig62a)
applied
a
have been based
Basidiomycetes
prominent
general disagreement concerning
Polyporaceae
clamp-connection
addition of microstructural
the genera. Teixeira's
cially
of the
meaning
of classification for the
systems
the
shifted
the
the
by
septa.
The
yet
the
septum; Fig.
Taxonomic
on
to
clamp-connection:
Basidiomycetes,
of species
mycelium
of wall material
with
compared
in
septa regardless
material
either
fungi,
disturbance of conjugate nuclear division in the
immediate restoration due
by
135
reactions.
formation of
(2)
deposition
from
clamp-connections
contaminant
distinguishing staining
appearance
hyphae;
from
distinguished
On
the microhave
proposals
Donk,
1933,
1964;
Pinto-Lopes,
1932;
1961; Singer,
1962;
still
open
to
many
questions.
The
of the
study
basidiocarp
from
has
nature
been
introduction of microstructural criteria in classification
1
and
953)
(1936,
developed
the
basidiocarp,
both
1962b)
1962a,
important
habitually;
simply
position
of the
hypotheses
absence
there
are
taken
is
on
the
( 1954
of
Among
the
clamp-connections
septa
who
to
enhanced
Corner
especially
by
has
a
emphasize
no
the
Teixeira
microstructures
position
search for the pattern of
be of
by
(1932a,
of the
that
is
septation
taxonomic value. Between
the
septation
only
in
species
hyphae.
the
taxonomic
generally governed
origin
and
1963 )
,
(1964).
mycologists
the
mycologists
clamp-connection
on
Fidalgo
consider
prominent generative
The
O.
or
presence
clamp-connections
origin
Cunningham
and contested. Some
others
these extremes,
with
by
and
greatly
proposed by
significance
by
and of the
of the
the
species
Basidiomycetes
of the presence
investigator's
with
are
of absence
interpretation
simple-septate hyphae.
simply
speculative
and
of
of the
The
devoid
PERSOONIA
136
of fossil documentation. It is
of the
Basidiomycetes
1936;
1934,
(1994,
Linder,
hyphae.
Jackson
derived from
unless
sion
the
that
the
through
that
of
of
propagation
of formation of
suggested
Singer (1962)
evolutionary
of
process
in
species
the
clamp-connections
here and
(Agaricaceae)
there
In its pure taxonomic
is
be
significant
taxonomic rank
by
others.
in their
clamp-connections
septation
be of
Nobles
1962b)
of
septation
Hesler
value
absence
the
hyphae.
larger
&
In
only
K.
Fidalgo
the
in
one
and
clamped
It
clampless hyphae
appears,
condition of
the
however,
was
like
from the
connections
neglected
and
the
made
obtained
study
of the
the characteristics of the
reported
are
the
species
and
some
of
dikaryon.
that
cover
the
(1938)
of the
cytogenetic
in which
found
the
mixed
mycelia.
a
the basis
are
The
of the
have
been
are
formed
of the
coexistence
cytological
with
clamp-
simple-septate,
Coprinus
the
hyphae
with
hair-
clamp-
mycologists
and
of
collected in
and
others
of
circumstances,
can
Teixeira
(1969).
genetical
Otherwise,
clamp-connections
on
basidiocarps
with
species
condition of the
Under these
and
simple-septate hyphae
often in
of
larger
Fidalgo (1938-1964),
who cultured the
pileus
in the
for
Polyporaceae
clamp-connections
only study of
hyphae
homokaryotic
septation.
O.
pattern of
that,
used
of view
counterparts.
reported
be
higher
at
value of the
said
(1932)
and Furtado
The
homokaryotic
and
the
that the
in the
points
Fidalgo (1939-1961),
the
can
separated
Teixeira's
(1962b),
(1963)
Hygrophorus
species.
authors,
Pinto-Lopes
be
of
out
un-
absence of clamp-connections
septation
can
groups
and
unnecessary
dropped
in the
agarics
Hesler & Smith
and stressed
experimentally,
by Papazian
upper
of
but
level,
has been
simple-septate
connections
hyphae
studied
invariably,
are,
pattern
Teixeira
1963),
species
specific heterokaryon,
dikaryon
clamped
nature.
(1962,
clamped
an
clamp-connections
Pinto-Lopes'
confirmed in taxonomic studies of K.
O.
as
( 1963) de-emphasized
Hygrophorus
of
species
mentioned that
the
of
by
also
of similar ancestral forms.
species level; Singer (1962), however,
or
at
level
Nobles
mycelium.
organ.
or
have
the suppres-
through
relationships
to
(1998b)
might
homokaryotic counterparts
or
have
to
presence
species
& Smith
treatment
the
specific
regard
the
stated that the
(1938b)
significant
(1962a,
at
the presence
Agaricales,
groups.
be used
can
the
at
be
to
heterothallic
polypores
or
lines
confusing,
Nobles
has been abandoned in
seem
without
interpretation,
to
considered
in the
dikaryotic
simple-septate
clamped
presented by
clamp-connection
a
Savile
simple-septate
is somewhat
from
was
appear
economical way of cell division, except for
mentioned that
derived
clamp-connection
losing
proposal
clamp-connections,
the
with
species
'homothallic',
This
the
(Rogers,
although
1991),
homokaryotic generation
of modern heterothallic species with
said that the
of the
origin
hypothesis
clamp-connection
clamp-connection
Ascomycetes
the idea.
clamp-connections
simple-septate
some
that the
of the
Arnaud,
;
idea of
lines
homokaryotic
the absence
to
species.
A similar but better formulated
suggested
arisen
the
explain
to
1961
contrary
are
'heterothallic', clamped
meant
1966
2,
the crozier
1942,
proposed
(1948b)
Jackson
species.
( 1998 )
tried
hypotheses
with
Bessey,
1940;
Part
4,
generally agreed, however,
homologous
and Buller
1999)
Various
who
is
Vol.
simply
have
report
the usual 'aberrations'
found
only
in
special
areas
FURTADO:
of the fructification such
and
agarics,
of
'irregular pattern
The
can
but
accepted
species.
the
homokaryotic components.
the
geneticist
with
offer
to
In
his discussion
fruitbody
a
but
one
could be
the
on
be
formed
or
mycetes
the
of the
one
clamped
Donk
the
by
haploid
a
in
as
others with
to
'diploid'
of
one
mycelium,
(ii)
condition
the second
who
difficulty
the
clamped
septa
or
on
his
groups
The
Polyporaceae
of
of the
are
is
introduced
by
heterothallic—-
the
of
suppression
same
whereas
genera
Fidalgo
of
taxa
in
It is
some
criteria in
treatment
groups
species.
Teixeira
by
of
for classification of the
least
at
three
in
is
the
(i)
al-
two
the
one
but
the
third
data available.
of the Basidio-
assemblage
on
'forms',
perfectly possible,
cytogenetic
light
clamps
factors:
species lacking clamps
occurring
of the
interpretation
clamp-connections
Aphyllophorales
species
have
taxonomic studies
has
not
species
of
large
only
in the
septa
made
classification have
of the
by
also
on
but maintained genera
of
species
(1964),
clamp-connecby
mycologists
shown
such
Cunningham
Thelephoraceae,
coexistence
Donk
clamp-connections,
with both
taxa
with
a
(1963)
the basis
of the
that encompass
different
type
of
been confirmed in the taxonomic studies of the
K.
Fidalgo
( 1939-1961 ),
1963),
Furtado
(unpublished).
(1962b),
( 1962,
proposed
with
distinguishable additionally
The
Basidiomycetes
controlled and the behavior of the
in taxonomy.
the
totally recognized;
some
formed of
clamp-connections,
clampless
& K.
Segregation
recent
genera
absence
and
O.
into
it would be for
already
assumption
of absence of
presence
microstructural
In
within the
1964),
simple-
accepts the traditional system of families of the Basidio-
splitting
some
various
segregated
one
only simple septa,
discrepancy.
presence
of the
recent
that
adopt
bipolar
heterokaryon
complex
through
the
the basis of the
natural groups will throw
simple septa.
and
of the
character
a
The first of Donk's
satisfactorily;
Whether
the
or
under
and
with
common-/!#)
split
ones
genetical
mentioned that "the absence of
(1964)
theoretically,
species
significance
verifies
tions
more
hyphae.
mycetes,
a
the survival of
known that
even
species (dikaryon)—especially
due,
with
supported
taxonomic
by
condition
but the
pseudohomothallic
The selection of characteristics which would allow the
into
limited
general
species,
for the idea
explanation
clamp-connection
clamp-bearing."
investigated
not
clamp-
cases,
are
major phenomenon
indicate how
findings
from the
(Polyporales),
(iii)
or
clampless,
of the
hyphae
may
fruitbody being
together,
of the
clamp-connections.
Aphyllophorales
in
These
tentative
any
origin
simple-septate
formation of
other
basidia
a
it is
Furthermore,
common-#,
as
in
affecting sexuality
(the
of the
the
the volva
stipe,
In
be included under the
septum is difficult because the general tendency is
taxonomists
of the
elsewhere.
small number of
to a
formation is
heterothallic
heterokaryon
context
confined
are
clamp-connection
tetrapolar
the
the
examples
the strict control of the factors
and
septa
137
septation'.
studies
genetical
control of
the base
found
throughout
These
clamp-connections
hymenium,
simple
or
found
are
simple septum.
basal
of
septa
no
connections
the
as
On
on
species
important, however,
the basis
in culture
that both
O.
Fidalgo
of microstructures
are
( 1938-
genetically
modern and efficient tools
conservative
and
modern
taxon-
PERSOONIA
138
omists
take into consideration
of the
necessity
whenever the pattern of
hyphae
the
or
the
Vol.
of any
proposal
4,
Part
1966
2,
the
investigate
to
septation
condition
cytogenetic
decisive for definition of any
is
taxa
hypothesis.
ACKNOWLEDGMENTS
The lectures
on
"Genetics of the
the
University provided
basis and
the
cytogenetic
the
phenomenon
reported
studies
general
Garden, during
Dr. Alma W.
I
am
their
due
was
of Dr.
George
Dr.
Fidalgo,
helped
New
express
manuscript,
my
their
offering
the
preparation
the
to
the
Basidiomycetes,
The
gratitude
to
Dr.
Dr. Alma W.
Kenneth
the
correcting
Sao
Brazil;
the
Bernard
Dr.
subject
S.
and
and
and
unlimited
Rogerson,
Raper.
the
My
"Secretaria
Rio
Pesquisas",
York
New
indebted.
Weadock who
Virginia
de
of this
patience
Dr. Oswaldo
R.
John
given by
was
Nacional
am
Teixeira,
Dr.
offered
kindly
preparation
Dr. Clark T.
Olive,
and Miss
of The
Rogerson
whom I
to
Alcides R.
support
"Conselho
research funds
The
criticism and
Lowy
Mary Fleming
Brazil;
Clark T.
manuscript.
Lindsay
Financial
English.
Paulo,
by
and
Mrs.
to
to
Barksdale,
Dr.
Wells,
Dr.
the
to
facilities.
laboratory
of this
addition
New York Botanical
the
at
out
especially
investigations
cytologic
made in
were
carried
personal interest,
of help is extended
Agricultura",
Janeiro,
in
clamp-connection.
Columbia
at
correlation between
of the
study
septation
S. Olive
Lindsay
those who read and discussed the
is also extended
in
the
Bistis from The New York Botanical Garden
O'Donnell,
gratitude
de
to
especially
Acknowledgment
Dr. Elsa
I
1962-1964.
Barksdale for
suggestions during
paper
of
taxonomy of polypores
grateful
very
for
inspiration
the pattern
illustration of the
in
Dr.
fungi" given by
of formation of
for
here,
basic
Botanical
de
Garden,
U.S.A.
York,
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2000
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X
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Generative
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a
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in
nature
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X
500.
X
and
of the
1000.
PERSOONIA
Vol.
4
Plate
6
PERSOONIA
Vol.
4
Plate
7
PERSOONIA
Vol.
4
Plate
8
PERSOONIA
Vol.
4
Plate
9