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Acta
Neerlandica
Botanica
347-379
(1960)
9
The
Exobasidium
Parasitism
japonicum
W.
(Phytopathological
of
Shir.
Azalea
on
Graafland
“
Laboratory
(received
Willie
Commelin Schölten ”,
August 4th,
Baarn)
1960)
CONTENTS
CHAPTER
I.
CHAPTER
II.
CHAPTER
III.
CHAPTER
IV.
TAXONOMY
CHAPTER
CHAPTER
V.
VI.
VII.
VIII.
CHAPTER
347
AND
OCCURRENCE
THE
CULTIVATION
OF
THE
4.1.
Review
Description
MATERIAL
of
the
USED
5.1.
The
plant
5.2.
The
isolation
galls
FOR
X.
6.1.
Literature .
Experiments
XI.
Azalea
354
355
and
355
cultivation
of Exobasidium japonicum
OF
355
357
357
358
Exobasidium
359
species
7.1.
Literature
7.2.
Experiments
360
INOCULATIONS
363
CROSS
359
Cross inoculations
with
from
different
Cross
inoculations
DEVELOPMENTAL
with
CHAPTER
353
EXPERIMENTS
on
THE
Azalea
on
material
6.2.
CYCLE
352
fungus
EXPERIMENTS
INOCULATION
LIFE
the
of
Azalea
STAGES
OF
THE
spores
originating
spores
originating
363
Exobasidium
closely related
OF
Exobasidium japonicum
CONTROL
Exobasidium
cultivars
with
from different less
CHAPTER
351
DISEASE
of literature
Anatomy
THE
8.2.
IX.
349
AZALEAS
352
4.2.
8.1.
CHAPTER
OF
FUNGUS
4.3.
CHAPTER
page
INTRODUCTION
THE
is
BUD
AT
host
369
Control by
10.3.
Experiments
with fungicides
in vitro
10.4.
Experiments
with
in
Ustilago,
.
366
10.2.
dium,
.
possible
Hygienic
OF
364
.
INFECTION
DISEASE
10.1.
DISCUSSION
plants
WHICH
369
measures
THE
fungicides
369
.
fungicides
RELATIONS
Tilletia
.
AND
BETWEEN
370
vivo
THE
371
GENERA
Exobasi-
374
Taphrina
SUMMARY
.
376
378
REFERENCES
CHAPTER
I
INTRODUCTION
The
growing
cultural
Ghent
centres
in
of
of
Belgium,
Azaleas
Western
and
s
an
Europe,
Boskoop
in
347
important part in many hortisuch
the
as
Dresden in
Netherlands.
Germany,
Every
year
348
W.
Dutch
growers
plants,
from the
plants
sold.
are
The
which,
ziekte”
like
shaped
ears.
be
recognized,
(Plate
be
disease is
The
Shir, and
the
cells,
the basidia form
the
cells,
they
basidia.
numbers,
to
who
disease
of this
of
spaces
century.
Japan,
for
Shirai
(1896).
The
Thus,
After
first
and
galls
they give
lacking:
a
cient
to
cubation
is
an
question
period
infection,
be
to
varies
preventive
measures
out
with
applied before and after
This kind of
scale
be
in
the
research,
a
is
it
small
how
the
This
at the
turn
plants from
that
country
by
known.
paper,
of the para-
questions
still
was
does the
parasite
basidiospore
suffi-
heterothallic?
the
conditions.
length
of the
The presence
inof
but
the
moment of infection
is difficult
for
the growers
observed,
have
of
with
nature
one
fungus
was
different
is over,
owner
Europe
following
the
answered
under
easily
can
is
frequently
described in this
circumstances;
or
are
healthy plant.
a
stage of the development of the plant
produce
carried
the
that stage.
only incompletely
concerning
to
The
at
of the
described
experiments
answer
yet unknown. Therefore,
when
were
An
fungus.
symptoms
as
purpose
they
as
a
produced
are
flowering period
imported
Azalea is
on
of
epidermal
the
reddish
to
surprise
was
already
of the
and under which
Another
the
possible
the
consists
velvety appearance.
time in Western
that it
japonicum
produces
and
the latter
as
possession of
the first
was
the
to
himself in
fungus
at what
penetrate
hypertrophic
tissue,
through
becomes white
obtain better information
sitism of this
these
epidermis,
breaking
the
lifecycle of Exobasidium
the
to
was
the
because
no
mycelium of the fungus
leaf
the
under the
suddenly,
appear
thought
It is
can
Exobasidium
as
The
basidiospores,
observed for
was
are
longer
misshapes reminded
article
galls develop gradually, often unobserved,
Azalea,
leaves
and crooked
of the leaves
hidden under flowers and leaves. When the
seem
“oortjes
as
deformed
convex
fungus known
a
colour of the diseased
parts
The
Rhododendron group.
greatly enlarged and thicker
are
Basidiomycetes.
develops
of
enormous
by
the
to
layer
in
the
In this
B).
be
to
names
galls.
intercellular
which
hymenium,
the
to
that
becoming
and
A
caused
belonging
in
present
1,
called
ready
are
grown
young
under the
disease known in Dutch
original shape
The
mostly
nurseries these
of cultivars
great variety
a
and it is understandable that these
ears
will
organs
belong
a
indicating
the leafblades
normal,
irregular growth.
people of
suffer from
and
flower,
to
The diseased leaves
of
Azaleas,
In the Dutch
consists of
all
speaking,
plants
buying
of Azaleas that is
obtusa,
“ezelsoren”,
or
begin
they
assortment
botanically
Often these
for
sums
horticulturists.
until
grown
large
large
Belgian
indica and Azalea
Azalea
than
spend
GRAAFLAND
to
be
carried
number
the Azaleas
were
of
out.
Some
fungicides,
which
inoculated with the
however, will have
to
be
to
know
experiments
continued
were
parasite.
in
large-
cultures.
In this
paper
the Azalea
some
parasite.
Exobasidium
on
attention is
Shirai
also
(1896)
the ‘Indian Azalea’.
has
paid
to
the nomenclature of
been the first
American
to
describe
mycologists
an
described
THE
parasites
Ericaceae
PARASITISM
OF
EXOBASIDIUM
wild Rhododendron
on
family
still
genus Exobasidium. It is
distinct,
are
described
be
to
by Woronin
that
distinction
host
of different
their host
on
their
has
of
plants.
parasites
should
species
authors
Many
as
the
prove
of
are
morphological
no
living
to
the
answer
on
different
question whether
they show specialization
whether
or
collection of host
a
The
however, restricted
paper were,
and
vaccinii named and
parasites
to
us
To that purpose
indispensable.
is
the
Shirai
by
inoculations with Exobasidium spores
cross
fully identical,
are
priority.
between
found
species of the
new
described
conspecific,
are
origin would enable
parasites
as
question whether all these species
1867. If the various
actually
349
AZALEA
other members of the
on
America
parasites
name
The results
plants.
these
be
can
in
this
they
open
ON
identical with Exobasidium
are
conspecific,
opinion
the
whether
or
American authors
an
and
species
in North
occurring
SHIR.
JAPONICUM
plants with
described in
experiments
this
inoculations with Exobasidium
cross
originating from Azalea and from Vaccinium vitis idaea. This Vaccinium
and
Azalea cultivars
some
The
purpose
aforesaid
used
were
investigation
and
whether
investigate
to
that described
by Woronin. Finally,
the
of Exobasidium spp.
parasitism
belonging
the
to
Ascomycetes,
TAXONOMY AND
Linnaeus described in his
the
which
he
plants.
obtain
will
About
an
to
answer
described
in
1851.
later
More
well
as
fungus is identical with
similarity between
striking
be
by
Taphrina
II
OF
AZALEAS
Species Plantarum (1753)
ferrugineum.
the red
This,
Alpine
therefore,
Hooker’s
as
species
expedition
species
new
to
Western
to
hardy
The latter
between
retain
The
more
Azalea
latter
Anthodendron.
bearing
subgenus
species,
is
which shed
placed
were
and
Indo-
China, Japan, Burma,
as
can
a
leathery
divided
the
in
All
However,
leaves
which
arc
practice
placed
are
experiments
were
not
shed
about
called
performed
900
non-
as
justified
to
Eurhododendron and
will
As
the
In
the
soft-leaved
name
Azalea
be used in this
with Rhododendron
to
species
winter.
non-hardy,
Azalea.
type. The Japanese Azaleas may be assigned
hybridization
not
Rhododendron
during
70
name
is
sunk into Rhododendron.
the
assigned
are
it
easy,
subgenera;
two
are
generally used by the growers, the
too.
is
species
into
former
Anthodendron
which
hardy
to
under unfavourable conditions.
distinct genus. It should be
be
To
their leaves
in the genus Azalea.
less
were
Europe
called Rhododendron and
ones,
known, including hardy
ones,
is
Himalayas
Europe, which
introduced into
were
from Western
the
China, Malaya and other Asiatic countries. At present about 800
are
spp.,
discussed.
CULTIVATION
Rhododendron
new
from America
species
the
Rhododendron.
genus
century
a
45
this
and that shown
named Rhododendron
of the
type
brought
to
the
CHAPTER
Rose,
host
as
was
questions concerning the life cycle of the Exobasidium parasite
Azalea,
on
of this
paper
plants of this
the ‘Tsutsutsi’ section
350
GRAAFLAND
W.
of the
subgenus Anthodendron. They
Rhododendron obtusum Planch,
Rhododendron
other
kaempferi,
Japanese species.
small-
and
Other
cultivars
‘Galestin’
and
group,
originating
from
The
W.
grower
cultivar
pink-flowered
indica. A
obtusum
var.
nurseries
For
the
cultivation
woods of the
The
plants
old,
the
the
age
is the cultivar
amoenum
“Campine”,
a
“baby Azaleas”
of
trimming the plants
can
either
beds has
rooting
to
be
value
into
be
of
the
Dutch
the
indica
Netherlands
guilders
in
indica and Azalea
obtusa
plants
the
to
plants
greenhouse.
under
exposure
be kept in the
brought
time of the
ture
In all
are
too
high,
greenhouses
cases
of the soil
16°
a
are
the time the
are
at
during the
or
which
plants
start
and
1.2
million
according
Guide),
to
the
540.000 Azalea
conditions.
climatological
greenhouses
till the
they have
and winter
they
to
their
beginning
(Van Raalte,
open
autumn
The
Luxembourg
about
at
have
flowering,
firms.
Belgian
year,
1955).
They
be returned
exposed
are
C, which may be raised gradually
may
opened
in
occur
order
in
at
plants
are
a
blowing
means
to
the
doors
temperature.
high moisture
of mist
content
the
sprayers,
plants
during
as
well as during the time they are
spraying and the opening of the glass-
outside
This
through
the
spread easily from diseased
the
spores
are
glasshouses.
organisms, including spores of pathogens such
dity of the air keeps
the
good development. Therefore,
sprayed, often by
the
early spring,
lower
to
house doors in order to lower the
temperature
be
at
by
the Dutch auctions.
high humidity of the air and
kept in the glasshouses.
can
and
obtained
night frosts is still necessary.
autumn
which
conditions for
continuously
air-currents
months
development of the flower buds. However, if the tempera-
becomes
the
During
fir
Belgium.
night frost by shedding
into the
late
and
leaves,
are
they
from
that
our
to
an
against
of about
i.e.
before
estimated
In
of
humidity of the air in the
plants,
sold
were
8
to
cuttings
Horticultural
(Dutch
to
are
protection
temperature
of
was
Belgian
When 8
September,
to
growers
densely planted in the beds. In
are
a
they have
May, when they
However,
on
of 6
The
year
1960).
in
the oak
cuttings.
imports from Belgium
hardy
not
are
Most varieties react
leaves. Thus
Young
1957
grown
used from
The
second
a
(Vandendael,
“Tuinbouwgids”,
The
August
April.
Dutch
bought by
Azalea
1960
of
high.
kept in the nursery for
frequently
are
to
in
and
period between February
by
1959).
from
sold.
called
Rhododendron
a
in the northern part
or
be
The Indian
and is
species and
are
‘Kurume’
the
Azalea obtusa.
possession
in
are
they
18 months
seed
seed.
Japanese
to
frequently
is
soil
region
grown from
are
‘Hexe’
with
plains,
obtained the
horticulture
of
ancestor,
1954; Encke,
of Azaleas
from
belong
as
as
of this
hybrid
(Grootendorst,
Japanese
centre
growers
Azalea has Rhododendron simsii Planch,
the growers Azalea
crossing of the hardy
a
Koppcschaar
They all
designated by the
are
F.
Boskoop
the
at
grown
by
the
‘Esmeralda’
‘Moederkensdag’.
and
also called ‘Kurume’ Azaleas.
are
obtained
was
to
as
the
In
and favours
The
of
way
Exobasidium
healthy plants.
viable
cause
this
heavy
micro-
japonicum,
high humi-
infection.
THE
PARASITISM
OF
EXOBASIDIUM
JAPONICUM
CHAPTER
In
the
of
centra
tible
the
varieties, such
plant
same
somewhat
covered
An
to
seem
the
among
period is
the
finished, but
this may be
the
their
resuming
plants
whithering
plants have been moved
clear from
may
these facts
the
as
appear
as
to
well
buds
the
start
as
By hypertrophic growth they
into
turn
colour and
a
the
lating,
and the colour
clusters
The
may
of the
spores,
blastospores
diseased tissues
come
as
of these
name
brown and
attack all
well
caused
which
usually
sharply
will
fall
parts,
parasite.
from
separated
still
in
a
the observation
leaves.
The
dormant
of
of the
more
always
as
the
galls gets
green
to
will
plant except
a
light
starts
covered
the
a
activity
appearance
of
the
was
state.
assumed that
This
galls
appear
in
after,
galls shrivel,
The
occur
on
be-
parasite
hypertrophic
The
with
leaves
growth
the
hypertrophic
leaves,
part
is
healthy leaf tissue.
pathogen.
galls
here
velvety aspect.
are
a
bud
can
never
present
simultaneously
a
on
with
developing
This would also
plants
be infected
hypothesis is in agreement with
fully developed
the
which
were
expanding
bud. The
growth by the dormant bud would coincide with
of the
account
from the basidio-
expounded
however,
attacked.
are
powdery aspect,
becomes
show
green
sporu-
root tissue. Stems and
may
galls,
young
conspicuous.
snow-white. On
be
galls
basidiospores
a
sprouting
disintegrate:
therefore,
that young
galls
and
spores
rapidly
the
to
after
become
the
on
spots
shape, and with
of the young but still folded leaves of
tion
galls
young
used; this gives them
Most
begin
weeks
all sorts of
saprophytes.
prey to
From these observations it
when
The
subsequently
only partially
are
plants
flowering,
buds
some
become
soon
of the
which,
be
of the
parts
the
by
galls
for
then
soon
flower
as
after
observations that
own
cuticle,
changes from light
the surface
spores,
the
the
rupture
development of secondary
of the
our
irregular
that time the surface
some-
time the
axillary
translucent
swollen,
an
and
1952). One gets
smooth, shining surface. When the fungus
basidia
formed. At
of
galls
galls
flowering
greenhouses.
open,
occurs
occurs
unfold.
to
leaves.
They
somewhat
the
certain
outside, i.e. in June. It has become
from
as
the
the
at
This
flowers
visible
small,
appear
growth also
vegetative
in
kept
(Welvaert,
too
galls
this time the
at
plants in the
on
in
revealed that
growers
vegetative development.
Renewed
develop.
of the
that
extent
an
optimum
an
still
are
September
most
underneath the
when
the
in
so
that
impression
are
has
Belgian
During June galls may be frequent
to such
are
the many big galls
Though the galls appear
spores.
formation
gall
year,
of
disease,
frequently. Suscep-
latter
The
ones.
Exobasidium
its normal red flowers also
frequent during March and April;
most
times
the
occurs
besides
carry
351
AZALEA
DISEASE
cultivation
century still
amounts
enormous
inquiry
a
THE
‘Hexe’, may be diseased
as
may
the
throughout
are
Azalea
half
deformed white
with
months.
the
over
ON
III
OCCURRENCE OF
already known for
SHIR.
explain
a
resumprenewal
the sudden
apparently
healthy
352
W.
when
imported.
with
that
GRAAFLAND
This mode of
be
development would
in
agreement
'
camelliae
described
gracilis
var.
Wolf
by
Shirai
and
Wolf
THE
Review
The
he
of
Exobasidium
IV
FUNGUS
literature
genus Exobasidium
described
for
Camellia sasanqua.
on
CHAPTER
4.1.
(1952)
the
fungus
Exobasidium vaccinii.
by Woronin (1867),
proposed
was
causing
disease
a
in
Though Fugkel (1861)
Vaccinium
vitis
had observed
when
idaea
the
as
fungus
already
at an earlier
date, this author did not give a good description
pathogen, which he mistook for a Fusidium. After the appearance
of the
of Woronin’s
scribed.
publication,
Usually
they
other
many
Exobasidium
the
named after
were
species
host
they occurred, but knowledge of their pathogenicity
first
Exobasidium
occurring
was
described
on a
North American wild
have
by
In
country.
Both
this
authors
14-15 /i.
a
In
Belgian
a
Laubert
the
disease
Japan,
validity
a
of many
of
on
could prove
several
siders
parasite
the
was
Exobasidium
hosts,
between these
ces
names
that
of the
of
the
last
often
both parasites
Andromeda
on
to
prove
Exobasidium
as
be
discoideum
species
first
one
Ellis
and
could be
be
found.
species
be
impossible
to
of
latter.
cause
similar
respect
(1877)
azaleae
con-
Peck
as
morphological differen-
According
are
the
to
this author
superfluous,
and
only
retained.
Naumann
(1909) was cautious in his
identity of the Exobasidia occurring in
to
no
the
account
identical with
to
Farlow
Exobasidium
as
about
on
morphological
indistinguishable.
mentioned
should
In
Exobasidium
as
was
Germany
Ragiborski
after
able
by
im-
Exobasidium
doubt
called
1900.
been
In
1909).
in
were
ligus trina.
with
created
species
and
had
flavum
already
attack
in
mentioned
Shir.
(Naumann,
as
parasite
an
report
fi.
Shirai
Japan
nursery
was
either
Rhododendron
in
same
15-20
of this
probably
pentasporium
1906
on
to
indica
which
idcntical with Exobasidium vaccinii Won,
the
first
Dutch
a
identical
(1896)
different
the
that Exobasidium andromedae Peck
symptoms
species
in
the
is
indica
basidiospores
in
in
growing
Azalea
Azalea
Exobasidium
Exobasidium vaccinii
Won,
disease
of
be
would
Richards
Ellis.
their presence
attack
discovered
was
was
observed
Exobasidium,
with
determined
(1909)
discoideum
He
This
or
(1901)
It occurred
basidiospores
shape of the galls.
on
of the
length
Bos
an
nursery
Shir,
occurring
Peck
azaleae
(1909).
from
ported
japonicum
The
Its
basidiospores
the
to
The
genus Rhododendron
(1874) described Exo-
nudiflora
of the
which
on
lacking.
was
discoideum.
Peck
year
Azalea
length
parasite
Ritzema
Exobasidium
by
same
much attention
paid
Exobasidium japonicum.
was
Exobasidium
as
wild
the
species
described
(1896)
the
the
the
species, viz. Azalea viscosa.
In
fi.
from
of
species
a
(1874)
Ellis
length of 20
a
basidium azaleae
on
de-
were
plants
identify the parasites
conclusion
Germany.
on
concerning
He
the
considers
the base of their
it
morpho-
THE
logy
PARASITISM
alone.
Many
differences
and
Wor.
belonging
species
to
(1929)
on
1925;
occurring
Exobasidium
author,
latter
Exobasidium
azaleae
the
Laubert
(
1909
and
Exobasidium
name
clear.
This also
according
to
this
~
good
species.
Exobasidium
the
to
that
on
of
of them
them
different host
question
whether
inoculations
Azalea and
4.2.
Description
depends
a
on
Fig.
1.
of
in
Europe,
may
be
Basidia
Cramer,
regarded
exists
were
is
of
seems
is
It
a
the
is
not
parasite
However,
or
~
the
fungus
intercellular.
on
been
not
forms
a
occurs
another
~**.*^».**~*
of many
described
as
new
excluded,
however,
speciales
occurring
can
give
an
not.
In
this
the
to
answer
investigation
originating
idaea.
azalea
The width of
the
spaces. The
developing basidiospores (bs)
basidiospores
~
parasites belonging
performed with Exobasidium spp.
vitis
be
morphology
formae
as
to
~
layer. The apices of the hyphae,
(b)
that
by Woronin
hirsutum.
several
erroneously
identical.
from Vaccinium
this
and
Azalea
on
remarks
7
the
studied
opinion that
have
are
1
who
galls
to
Ellis
parasite
he
that described
the width of the intercellular
subepidermal
the
Rhododendron
not
specialization
cross
mycelium
for
plants. Only experiments
from
The
(1959),
is also
Exobasidium
Several
some
Japan but
Savxle
species,
genus
species.
of
cause
According
discoideum
though
X.
<
1915;
Marghionatto
author, Exobasidium pentasporium Shir., which
in
as
Exobasidium
identical with Exobasidium vaccinii
Shir.,
and
all
the
Exobasidium rhododendri
jerrugineum
indica
Azalea
on
to
Wor.
Argentina.
retains
and
species
applies
Rhododendron
on
are
1932)
described
were
1959).
Exobasidium
Peck,
japonicum
difference between this
in
vaccinii
1913; Burt,
(Lind,
the
that
be considered
to
comprise
Savile,
vaccinii
cultivated
Exobasidium rhododendri Cramer
Wor.
species
and
1928;
Farlow
that
species
would
353
AZALEA
of Exobasidium
parasites have
Rhododendron
Azaleas
on
Exobasidium
the
Miles,
considers
too
the
species;
one
occurring
Laubert,
of
ON
with
agree
basidiospores
small that these
so
SHIR.
JAPONICUM
however,
between the
of several
are
EXOBASIDIUM
authors,
in size
afterwards
OF
blastospore
on
hyphae,
the future
sterigmata (s).
(bl)
in
±
1
n,
mycelium forms
situ.
basidia.
One
of
the
354
GRAAFLAND
W.
stretch
in
direction
a
perpendicular
the
to
thus
epidermis,
the
hymenium. By further growth the basidia find their
the
epidermal cells and rupture the cuticle.
24-30
cal,
5
on
one
(Fig.
5-8
X
[x.
basidium.
to
Mix
products, which reminds
Among
In this
be
case
called
4.3.
but
Fig.
is
of
seen
paper the
between
the basi-
produce
may
for these
“blastospores”
outgrowths formed by yeast cells.
many
forms
produce
are
occur,
new
called
e.g.
spores
“sporidia”
the
smut
by budding.
“second-
or
spores of Exobasidium will
yeast-like
the
galls
between
on
azalea
(p. 351), but also microscopically
the
transverse
found in
Transverse section
palissade parenchyma (p)
the
sections. There is
part,
uniform
through
and
a
sharp
healthy and the diseased tissue, when
mesophyll of the hypertrophic
sparingly
2.
this
“conidia”
Taphrina and
far that both
name
to
number of
as
exists
analogy
an
4
2.5-5.5 [i
X
large
a
designated
genus
so
13-18
“blastospores”.
gall is studied in
in the
too
basidiospores
only macroscopically
boundary
of the
one
newly formed spores
In
Anatomy
Not
a
the
sporidia”.
the
in
the
uses
Protobasidiomycetes
in which
fungi,
ary
the
of the
is
cylindri-
are
sterigmata,
on
produce
are
(1949),
Exobasidium,
by budding.
spores
Mix
ascospores
of the genus
diospores
basidiospores
They
/x.
The basidia
develop
basidiospores
2-4
X
According
the behaviour of the
new
the
measuring 9-13
Woronin.
basidiospores
The size of the
budding
1). By
spores,
by
The
forming
between
way
an
spongy
a
lack of differentiation
and tracheal elements
tissue.
In
comparison
infected leaf, showing
parenchyma (s),
hypertrophic
cells
(h).
and
a
a
healthy
with
are
the
part with
diseased part
with
W.
GRAAFLAND:
The
parasitism
of
Exobasidium
japonicum
Shir,
on
Azalea
PLATE
B
A
U
C
E
F
Plate
1.
Shir.
B.
A.
Azalea oblusa,
Azalea
indica,
G
cultivar ‘Esmeralda’, with
C-G. Development of’ axillary
tation
of the
D-G; further
shoot.
C:
‘Hexe’,
cultivar
just
developmental
in
with
galls
galls
japonicum
Shir.
buds of Azalea indica, cultivar ‘Hexe’, after decapi-
after
decapitation; length of the buds about 2
of the buds in D: 4
E: 6.5
mm; in
stages; length
F;
of Exobasidium japonicum
of Exobasidium
9
mm
and
in
G:
12
mm.
mm.
mm;
THE
normal
both
The
epidermal
is
layer
white
the
on
Azaleas
‘Esmeralda’,
and
flowers
red
in
frequently
‘Hexe’
the
gathered in
The Azaleas
those observed
to
V
THE
still
growing
double
mold,
in the
in
grown
growth
vitis
and
nature
length
glasshouse,
The
flowering,
and
of
use
The
for
idaea,
in
to
the
stable
the shoots
were
cut
manure
buds. Small
suitable for
they
cuttings
soil
was
1/3
April, while the plants
cut in
composed of
sand.
July
Roots
The
were
as
isolation
early
been added.
the
the
obtained with 3
formation
culture
by sprouting.
grow the
were
was
obtained
humidity high.
some
soil
mixture
weeks
the
after
tips
of
unfolding of the axillary
to
4 branches which
as
and
the
cultivation
germination
of
1867. Under humid
of
were
in
a
liquid
Richards
fungus
medium,
conditions
(1896),
in pure
in
which
had failed.
of Exobasidium
they
sprouted
grew the
the
however, reported
culture,
japonicum
[Exobasidium
basidiospores
yeast-like way, forming “conidia”. Brefeld (1889)
in pure
1/3 leaf
in 4-6 weeks.
root
same
After
in
the
of
under
experiments.
Woronin observed
vaccinii
had
in
potted
were
while
August,
mixture
a
developed
stimulate
to
or
kept in the glasshouse
were
removed, resulting
plants
the
disease.
inoculation tests
cross
garden of the laboratory.
either in
were
growth substance
cuttings
were
grown
characteristic,
the Exobasidium
in
use
clay seedpans and by keeping
rooted
pink,
Because
variety is
favourable conditions for rooting
necessary. Very
by the
were
with
(Belgium).
this
An unfavourable
grown
or
and
moss
treatment with
cultivars
‘Moederkensdag’,
multiplied by cuttings. Young, recently hardened
cm
glass-cover.
1/3 peat
three
Boskoop
and
nurseries.
of doors. The
out
EXPERIMENTS
obtained from Ghent
Belgian
were
shoots of about 8
to
similar
are
respectively.
was
of Vaccinium
Specimens
a
healthy appearance
differentiation of the tissues
stems,
however, is the susceptibility of this variety
5.2.
their
though
the basidia.
by
‘Galestin’
vegetative
of its excellent
some
1929 and
material
Japanese
The cultivar
not
have
by several other
enlarged,
their
They keep
burst
The anatomical features
plant
used, viz.
A
size
2).
Marchionatto,
not
are
MATERIAL USED FOR
The
Of the
were
their
(Fig.
leaf.
THE
were
355
AZALEA
as
occur
observed
been
CHAPTER
5.1.
ON
well
as
1909;
however,
increased.
abnormally
lacking.
in the
has
Naumann,
galls which develop
also
cells
hypertrophy
picture
cells,
epidermal
the
In
is
of
and
SHIR.
JAPONICUM
1932).
number is
until
1907;
(Petri,
Laubert,
number
hyperplasy
anatomical
same
authors
EXOBASIDIUM
OF
the
mesophyll,
increased:
This
PARASITISM
cells
in
fungus
multiplied
that his
attempts
Lockhart
(1958)
356
obtained
of
a
pure
culture of this Exobasidium
basidiospores
on
Marghionatto
basidium
Graafland
Exobasidium
rhododendri
hirsutum ;
be
culture.
pure
to
the
report
The
growth of Exo-
“conidia”
grew Exobasidium
developed
on
japonicum from Rhododenfrom
vexans
Thea sinensis
succeeded in
vaccinii
Wor.
from
Exobasidium
from
from
Vaccinium
Rhododendron
Shir,
japonicum
vitis
idaea:
Exobasidium
and
Rhododendron
ferrugineum
from
Azalea
Exobasidium
indica;
Thea sinensis.
following method
the
growing 4 species of Exobasidium
viz.:
Cramer
Massee
The
the first
was
(1955)
(1953)
culture,
pure
vexans
in
kaempferi and Exobasidium
var.
suspension
out a
culture.
pure
in
(1929)
Ezuka
dron obtusum
by pouring
agar.
japonicum
potato-agar.
in
GRAAFLAND
W.
to grow the
suitable
fungus in pure culture appeared
Young, newly sporulating galls were
gathered from the host plants. They were placed in sterile petri dishes,
to
where
most
humidity
wool. The
leaves
by
one:
kept high by the presence of
was
well
galls keep
used, the galls
are
wrapping the
in
this
be
can
surface
cut
way.
kept fresh for
of the shoot in
sporulating surfaces of the galls have
towards
the bottom of the
expelled
Even
nating.
they
be
can
taken
6
After
agar.
formed with
which
and
is
within 24
so
a
many
small,
possible
allow
the
forcibly
they
start
germi-
blastospores
needle and
typical of Exobasidium colonies,
Malt
surface
The
growth.
wrinkled like
and becomes
and
fungi
malt-saleb
It is
and
possible
is
to
i.e.
of the
with
colonies
of
a
favourable
most
are
of
every
grow
two
sunken
a
mycelial
the surface
temperature
in
beyond
the solution.
cells
of
irregular
brain. On
yellow
the
to
shape.
13 to 30
hyphae is
1-2
fi,
/u.
form, in which
galls
crooked
in old
of
the
with
in
A
a
growth of
optimal.
is
The
japonicum, Exobasidium vaccinii
on
agar.
development of the fungus does
fungal
finely
malt
most
brown.
mycelial
particles
divided
solution is
mat. With
suspension
most
good
throughout
sprout
consisting
favourable for
of
ob-
culture.
a
Microscopically
from
the
the
centre
gradually
mat
for
20-22° C
the formation of the
culture
This results
such
taining
shake
a
are
months.
Exobasidium
otherwise
necessary,
proceed
that
nutrient
a
Exobasidium rhododendri in nutrient solutions instead of
aeration
the
A
subcultured
also
Shaking
not
agar
cultures.
were
to
glassy
of the nutrient media used the colour darkens from
Exobasidium
formed
are
transferred
hemi-spherical,
The
as
much
as
to
longer time
even
cotton wool.
where
glass,
cotton
hypertrophic
shiny surface. Gradually they develop the appearance
a
peripheral
shrivels
days
8
to
hours
off with
the
on
an
be turned
to
plug of wet
with
wet
petri dish, in order
fall
to
basidiospores
a
If shoots
a
cultures,
the
length
depending
Their
case
knob
are
The
on
threads
hyphae grown on agar varies
the nutrients used. The width of the
shape is irregular, but part of them
they
plants.
of the
on
one
are
similar
to
particles
or
both
formed,
the
may
ends.
blastospores
also
be
are
fusi-
formed
rectangular
Sometimes,
though the latter
can
on
or
especially
never
be
THE
considered
each
to
PARASITISM
be
to
real
(Fig.
other
OF
EXOBASIDIUM
hyphae,
threads
to
the
typical
3.
the cells
found.
ever
are
ON
357
AZALEA
only loosely attached
are
shaped.
uniform; cells cohering
(bs),
formed
are
the
on
their
length
is
forming
hyphae
and
Especially
Germinating basidiospore
more
Though the cells
Exobasidium-blastospores
irregularly
more
Fig.
hardly
are
the cells
as
SHIR.
3).
In the nutrient solutions
in
JAPONICUM
CHAPTER
comparable
galls,
they
are
variable.
more
blastospores
(bl).
VI
INOCULATION EXPERIMENTS
6.1.
Literature
Inoculations
galls
in
with
infecting
already
healthy plants
result
Lockhart
with
(1958)
leaves of shoots
angustifolium,
basidiospores
information is
with
developing
three months
basidiospores.
out
observed
Graafland
(1953)
of Exobasidium
available with
basidiospores
disease
these
regard
from
(1896)
and
on
and
of basi-
obtained
Gaylussaccia
myrtilloides
plants
succeeded
means
symptoms
inoculated
vexans,
taken
and
ligustrina
Vaccinium
after
by
Richards
ones.
typical
on
idaea
sporulating
who
(1867),
of Vaccinium vitis
Andromeda
from
directly
by Woronin
diospores obtained from diseased
similar
taken
basidiospores
performed
were
the
on
a
resinosa.
young
Vaccinium
had been treated with
young
obtained
tea
good
plants
results.
with
No
to inoculations of Azalea carried
the
galls.
358
W.
Inoculations
with
that the spores
those
Vaccinium
Similar
results
of the
spores
obtained
6.2.
the
and
As
by
para-
after inocuwith
angustifolium
blasto-
difference between the results
no
of
means
buds
the
galls
basidiospores
originating
grown in pure culture.
the
two
ends
were
removed.
As,
After
expand.
to
buds
had
not
the
terminal
than
bud
inoculating
broken.
than 4
more
axillary
4
point surrounded by only
The
bud-scales.
different
were
present,
of
means
small
buds
covered
and
glass
with
the filter
after
about 3
much
at
when
the
period
the
was
weeks,
at
When
sometimes
plants
diminutive
covered
by
It
not
diseased
Then
paper.
the
if the
nights
could
much
be
longer
leaves,
achieve
plants
low
4
inoculate
are
were
had
in
if
by
to
were
opened,
visible
were
not
i.e.
C,
for 24
inside
symptoms
cool,
ones
kept
the
on
these
blastospores,
were
0°-5°
difficult
growing
a
of which
chambers
as
fallen
too
September
the incubation
weeks.
than 3
than
decapitated
of
healthy
to
temperatures
were
10 of these leaves
also
which
been
stems
began
decapitated,
more
to
easy
and
The first
had
as
was
about
the
be
to
galls obtained after inoculation
were
however,
to
shoot
per
consists
plants
inoculated
removed.
least
performed
was
without
much
this
larger
treatment.
1).
(Table
Table
Number
is
Basidiospores
The
filter
temperature
was
latter
inoculation-chambers,
paper
The number of
when
brush.
moist
night.
6
from
the
are
uppermost buds
5
this
although
stages.
organs.
transferred
moist
a
hours in
to
be
order
In
small
too
were
The
one.
terminal bud is
developmental
tightly packed
plants
inoculated,
was
an
to
for
leaves
inoculation,
the
expand after the removal of the tip, only the
treated with inoculum. If the
the
inoculated, and the tips of the
were
usually,
be
to
used
were
when
clear that inoculation had
axillary buds
these
cuttings
visible
already
are
was
began
of
dormancy
growing
vigorously
the
length it
in
mm
before
30
on
results
Experiments
few
in
and
effects
good
by Lockhart (1958)
was
by
culture
culture of the
pure
and those obtained with cells
plants
inoculations.
to
a
were
clearly,
very
similar
have
Vaccinium
fungus. There
inoculations
Well-rooted
a
and
not
obtained
(1953)
obtained
were
myrtilloides
same
with
from the
Graafland
culture
pure
obtained in pure
plant with cells taken from
Vaccinium
lating
vaccinii
in
though
states,
basidiospores
sprouting
idaea.
this
inoculating
site.
by
vitis
He
(1889).
of Exobasidium
formed
obtained
blastospores
Brefeld
performed by
GRAAFLAND
of
galls
on
groups
tation,
of
and
5
plants
1
inoculated with basidiospores after
inoculated without
number
Azalea
cultivars
shoots
decapitated
‘Esmeralda’
‘Galestin’
decapi-
decapitation.
of
galls
shoots
not
decapitated
4
0
14
3
THE
PARASITISM
Thus the
able for
EXOBASIDIUM
development of the symptoms.
lation
was
could
successfully
greatly simplified when it
suspensions
from
the
was
shaking
the
be
inoculum
a
shake culture.
suspended
the cultivars
gall,
plants
sink
to
it
brushing
the number of
a
ON
the
‘Esmeralda’
14
of
the
were
flask.
After
used
was
the
For
plants.
and ‘Galestin’
with
days old,
give the cell
to
bottom of the
inoculated with
were
favour-
of inocu-
especially
was
night in order
the
buds
be
to
technique
cultures,
pure
one
to
359
AZALEA
fluid, the viscose suspension
on
and the others
The
When the culture
during
oppertunity
by
experiment
SHIR.
discovered that inoculations
was
with
performed
discarding the supernatant
from
JAPONICUM
development of the axillary buds appeared
the
material
OF
used.
were
as
first
Half
basidiospores originating
treated with
suspension of the pure
a
culture.
number of
The
with
which
galls
developed
the
on
larger than the number that developed
even
basidiospores
(Table
galls
of
that
developed
basidiospores and
with
group
was
treated
plants
2).
2
Table
Number
latter
the
on
on
of 5
groups
suspensions
of
treated respectively with
plants
cells
in
grown
a
culture.
pure
inoculated
with
Azalea cultivars
basidiospores
cell suspension
a
‘Esmeralda’
4
5
‘Galestin’
7
9
After
such favourable
all further
experiments
results had
were
been obtained with suspensions,
performed with material grown in shake
cultures.
Cultures
in
of Exobasidium
and Exobasidium
japonicum
1952 have remained virulent
up
to
now,
vaccinii
isolated
inoculation host
become infected.
plants
CHAPTER
THE
7.1.
after
as
LIFE
CYCLE OF
VII
EXOBASIDIUM SPECIES
Literature
The mode of infection
brilliant
minate
on
“conidia”
formed
the leaves
developed
into
myrtilloides
to
and
In
a
vitis
penetrated
intercellular
systemic,
attention
idaea.
Vaccinium
occurs
and
revealed
Sometimes
via
the
the
has been
(1956)
angustifolium,
stomata
the
spaces
network within 48 hours after
Hilborn & Hyland
of
was
by the
basidiospores proved
to
ger-
secundary
by budding, but usually the spores themselves
the
by Exobasidium vaccinii
becomes
Vaccinium
which
tubes,
cells.
According
of
formed
were
germ
epidermal
Much
of Exobasidium vaccinii
observations of Woronin. The
the
the
way
the
hyphae
the infection.
“lowbush
stem.
mycelium is perennial
to
via
the infection of Vaccinium
via the cuticle of the
paid
or
branching
blueberry”,
The infection
in
the
rhizomes.
in which
the
tea
plant
360
becomes infected
&
GRAAFLAND
W.
1950; Loos,
by Exobasidium
1949 and
1948,
Loos,
This
1951).
leaf reckoned from the
1950;
parasite
tube. From
the
do
parasite
cell
epidermal
outer
form
not
and Marghionatto
leaves
the
on
species
extensively.
basidia of
of Paris.
sidium
discoideum
these
in the
it
nuclei
After
one.
of
4
the
was
not
this
grown
Shir.
Exoba-
from
their
According
to
Also
dicaryotic.
are
rise
vicinity
be
to
monocaryotic,
are
fuse
which
present,
gives
the latter
and the
the
especially
fungus
are
in
fungus
mycelium
distinct nuclei
divisions
known in what
stage
of which
condition of the
the
first
of all
fusion outside the host
basidiospores,
a
appeared
fusion
the 4
to
several
poles,
which
side, resulting
each
bearing
each
a
to
a
haploid
the
ring,
on
by
nor
glass slide
a
4
also
the
cell
a
the
a
to
of the
possibility
chamber
moist
a
allowed
out
The
5).
in
glued
was
were
haematoxylin.
developed
and
studied
was
with
question
possibility of
stained with
(Fig.
the latter
this
and
investigated. For that purpose
were
gall
diploidi-
dicaryotic
the
answer
the
blastospores
spores
in
the bottom of the
sporulating
directed
side
had been
drop of malt agar
% agar). By keeping the moist chamber upside
we
basidiospores collected
germinated, which could be observed
obtained that the
spore
contents
germination
terminal
neither
other,
be
of
the
of
spores
the
spores
in the formation either of 2
became divided
observed:
as
mature
on
every
The
microscopically.
after
1
hours,
Nearly
a
glass
slip;
placed (5 % malt in
the agar.
these
the
cover
to
gall caught
uninucleate
piece of
inside
towards the
down for
be
had
the
cycle
basidiospores,
Secondly,
the nuclei
well
as
to
between
culture. A small
chamber
of the life
recognizable
whether the
plant
a mature
germinate, after which
The
is
uninucleate.
are
basidiospores from
former,
result
mycelium found in the leaves. To
had to know
blastospores really
on
Azaleas
basidiospores.
yet
zation occurs,
of
young
Experiments
It
to
are
(1925)
the
mycelium,
the
japonicum
of
basidiospores
two
germ
of Exobasidium
cytology
concluded,
of the intercellular
the cells
a
penetrate
may
Marghal
to
considered this
be
can
the
spores,
on
Exobasidium
young basidia two
diploid
we
occurring
was
the
authors,
whereas
it
According
studied
authors
Ellis,
that
illustrations,
7.2.
these
develop
the way in which Azaleas
studied the
They
Though
they
hypha
a
the buds.
(1927)
Exobasidium
an
the 4th
or
the germ tubes penetrate into
(1929)
Kharbush
&
but
cuticle
to
japonicum.
during the unfolding of
Eftimiu
the 3rd
even
wall.
Exobasidium
by
1949 and
Emden,
developing bud. The basidiospores
a
Only little is known with regard
infected
1947; Gadd
(Tubbs,
van
attack
can
blastospores,
appressorium
an
&
tip of the stem, i.e. the leaf which is just fully
developed, and also the leaves of
of this
Massee
vexans
Reitsma
blastospore.
one or
were
more
took
towards
place
blastospores
or
on
of 2
the
2
either
hyphae
In the meantime the spore itself
septae.
basidiospores
moved
No
lying
blastospores originating
sign of cell fusion
in the
from
was
ever
neighbourhood
of
different basidiospores
THE
Fig.
4.
PARASITISM
Basidiospores
OF
EXOBASIDIUM
with
nuclei
JAPONICUM
stained
SHIR.
ON
361
AZALEA
with
haematoxylin.
Fig.
Fig.
Fig.
5.
6.
Blastospores
a\
developed
a
shake
Two germinating basidiospores
dium, forming hyphae
of
in
hyphae
of
a,
and
after
5,
blastospores
10, 29
and
culture,
stained
with
haematoxylin.
(bsj and bs 2 ) originated from
(bl). b,
45
c,
d
and
e:
Blastospores
hours, respectively.
5
one
basi-
and tips
362
W.
ever
conjugating
seen
other
by
only
though they
even
small
a
GRAAFLAND
distance.
against each other without making
chamber cultures
probably
it
existed,
basidiospores
from
fusion
no
the
found in
were
basidium.
same
6). In
of 4
groups
If +
attention
observed.
was
spores behave in
similar
a
It
paid
was
and
be
may
concluded
or
5,
spores
—
these cases,
to
grew
many moist
might be expected that both would be represented
Therefore, special
groups.
here
the
originating
blastospores
of
(Fig.
contact
from each
separated
were
colonies
The
in these
but
that in
even
vitro
all
way.
Another
possibility that had to be investigated, is that the dicaryotic
mycelium in the young leaves develops after a union of the spores
of the
or
tration.
tubes either
germ
If the
fungus
be
spore would
were
homothallic,
ment of
of
cultures
contained
only
sticking
the
to
ascertained
on
by
10
of these cultures
colony
caused
concluded
galls
that
derived from
and
the
pene-
one
the
case
—
fungus
developdispose
to
necessary
plants
3
the
to
group
of
fungus
is
a
ability
of 5
group
are
able
agar.
In
2
tested
Five
of them
monospore
Thus it
plants.
one
this way
was
plants,
5
was
After
infection.
because
cul-
may be
cells
sporidial
develop into
to
needle
spore
one
cause
and 3
plants
of 5
one
colony.
a
all
on
shake
a
a
the malt
agar
After it had been
Each
to
homothallic,
single blastospore
a
its
on
on
malt
to
infection
cause
into
obtained.
were
out
on
taken
only
that
develop
of
suspension
drop
placed
was
transferred
as
4 of the
on
a
a
examination
was
to
that
drop
a
cultures
test
proved
caused infection
tures
was
moist chamber culture.
a
allowed to
was
monospore
far
so
Such
slip of
microscopic
the latter
5
group of
a
obtained from
were
cell.
one
cover
weeks the
two
infection. In
would be necessary for
spore
the latter
by diluting
present,
one
an
after
or
+
one
cultures.
Monospore
about
only
accomplish
to
of the leaves
at least
heterothallic,
gall. To investigate this question it
a
monospore
culture
to
required
the surface
on
were
dicaryotic
a
mycelium.
Monobasidiospore
tures
had to
be
of
to
one
cultures
described before
as
obtained in
The time
kept upside down, however,
minutes
two
diospores
were
(p. 360).
appeared
from
separated
each
to
other
colonies into which
they developed did
microscopically.
more
cover
the
slip,
basidiospore
to
isolate
from
was
the
in
which 21
basidia.
In
two
than
suitable
such
34
a
basidiospores
group
In
were
originated
instances it
was
and
5
probably
tested
colonies
were
derived
separately
on
from
obtained
the
Azalea
it
to
grow
a
from
same
5
colony
These
on
only
the
one
colonies
obtained,
to
different
out
same
the
possible
was
were
basidiospores
basidium.
that
separate
cultures
period
controlled
present
basidiospores belonging
possible
A
obtain basi-
was
cases
raise
to
basidiospores which probably originated from the
Once,
to
cultures
many
monobasidiospore
from
short.
distance
a
in others 2 to 5. In three
of such
all
10
by
but
now
most
cul-
chamber
which the chamber
not touch. This
discarded.
was
present,
spores
them. All
among
of 4
If
culture
was
be
moist
during
of each
basidium.
which
cultures
were
were
plants. They all caused infection (Table 3).
THE
PARASITISM
OF
EXOBASIDIUM
JAPONICUM
Table
Number
of plants
number of
each
one
developing galls
after
monospore
cultures;
used
inoculate
was
to
SHIR.
ON
363
AZALEA
3
inoculationwith
cultures
monobasidiospore
numerator:
number
of
plants with
galls
denominator;
plants
5
number
of
9
45/9
X
5
6
24/6
x
5
6
18/6
x
5
10/2
X
5
4/1
x
5
3/1
x
5
2
)
1
/
originating
)
one
the
1
1
)
3
S
2
}
1
basidiospores
basidium
5/1
x
5
12/3
x
5
10/2
X
5
4/1
x
5
6/2
X
5
same
the
>
from
same
2
These
experiments
Monocaryotic
cells,
and,
diospore
wall of the
that Exobasidium
prove
formed
therefore,
be
no
by
a
process
genotypically
is formed
in
difference
CROSS
Cross
from
azalea
The Exobasidium
varieties
which
very
galls
grown
have
in
are
group
caused
by
Morphologically
to
galls
be
on
identical,
culations
were
suspensions
from infected
tin’,
by only
might
performed
shake
shows
that the
on
the
be
infected
‘Hexe’
It
as
could
cultivars,
13-18
occur.
with
with
the
caused
be
found
and the
fungus
latter
Ghent,
to
seem
on a
the
be
these
different
like
the
Belgian
Japanese
versa.
from
on
as
well
shape
proved
physioloino-
cross
as
the other
with
cell
originating
‘Esmeralda’ and ‘Galescultivar
‘Hexe’.
Japanese
‘Esmeralda’.
plants
question,
Azalea could
The
the
too
However,
(i.
this
study
one
between
basidiospores
2.5-5.5
X
To
of the
infections
grown in
uncertain whether
yet
basidiospores
cultures,
from
The
ancestor.
is
Azalea obtusum
Japanese
parasite, causing galls in all cultivars.
Belgian cultivar and vice
easily
originating
parasites, each occurring
one
plants
parasite
spores
the cultivars
on
plants of the Japanese cultivars
and from infected
the dica-
of cells between which there
the
on
as
as
differences
measuring
from
well
simsii
the different
specialization
gical
as
two different
no
the leaf tissue
outer
VIII
found
are
the disease.
or
In
basi-
one
the
penetrate
Exobasidium
with
Boskoop
to
of cultivars
of the
galls
out
of
cultivars
Rhododendron
susceptible
identical,
out
INOCULATIONS
inoculations
different
japonicum is homothallic.
budding
sex.
CHAPTER
8.1.
of
of the
young leaves.
epidermis
ryotic mycelium, therefore,
can
inoculated
plants
of the
Table 4
galls
cause
cultivars
could
parasite
from
The
same
cultivar,
but
364
W.
GRAAFLAND
Table
Number of galls
developing
of
Exobasidium
4
different
number
of
origin
Azalea
after
inoculation
of
number
galls
number
of
plants *)
‘Hexe’
16/6
‘Galestin’
‘Hexe’
25/6
‘Esmeralda’
‘Esmeralda’
37/6
‘Galestin’
‘Esmeralda’
36/6
‘Esmeralda’
control
‘Galestin’
control
‘Hexe’
‘Hexe’
76/20
19
‘Esmeralda’
‘Hexe’
46/20
17
‘Hexe’
‘Esmeralda’
42/20
19
‘Esmeralda’
‘Esmeralda’
31/20
12
‘Hexe’
control
0/20
0
‘Esmeralda’
control
0/20
0
total
numerator:
of
diseased plants
inoculum
‘Esmeralda’
’)
with
origin.
the
Exobasidium
cultivar
cultivars
Azalea
different
on
0/6
0/6
of
number
denominator:
galls;
number
of inoculated
plants.
less
was
the
Though
galls
latter
narrowly
not
the
on
on
8.2.
Cross
different
less
from which it
certain
‘Hexe’,
on
originated.
Exobasidium
occur,
on
on
related
and
(1959)
Azalea
by Woronin.
Exobasidium
with
closely
Savile
to
occurring
described
This
this does
single species,
*J
t
japonicum
Azalea varieties,
as
If
genicity.
be
may
they
from
cross
the
with
to
different
Vaccinium
Pure
mean
if
the
authors,
with
based
even
originating
the
on
they
Exobasidium
Exobasidium
are
vaccinii
morphological
considered
that the Exobasidium strains
and
occur
of
with pure
Azalea
vitis
to
be
occur-
specialized in their patho-
some
Exobasidium
performed with
cultivar
Vaccinium
‘Hexe’,
vitis
of Exobasidium
cultivars
biotypes
To
from
isolates
they
investigate
different
cultures obtained
pure
Dutch
the
Graafland
the
latter
cultivar
(1953)
pre-
by inoculating
vaccinii.
experiments
described in this paper
of Exobasidium
and
or
plants.
from
idaea.
obtaining infections of
cultures
races
different host
japonicum
of Exobasidium
vaccinii
were
obtained from
obtained
from
idaea.
cultures
The brown
be
not
physiological
on
were
Azalea
from
culture
pure
might
Cross inoculations in the
performed
is
opinion
different
character
succeeded in
a
plants
inoculations
Belgian
‘Esmeralda’
viously
are
expected
parasitic
origin,
other
spores
plants
'
X'
different host
on
ring
not
host
identical
are
similarity of these fungi. However,
it
to
seems
Conversely,
infections
cause
the cultivars
specialized
inoculations
According
species
the
to
parasite may attack Azaleas of different genetic composition.
from
a
Japanese cultivars.
able
was
specialization
some
certainly
the
the
higher degree than
to a
even
is
provoke
to
apt
fungus from
of
colonies
both
of
fungi
the
on
former
agar
showed
produced
a
a
different
dark
aspect.
discolouration
THE
PARASITISM
OF
EXOBASIDIUM
SHIR.
JAPONICUM
ON
365
AZALEA
of the
nutrient agar. The light yellow colonies of the latter hardly
changed the colour of the agar. Both parasites also showed a difference
in colour of the nutrient solution when grown in shake cultures.
From
inoculations it
cross
attacked
not
was
Azalea
does
The
results.
function
not
In
Vaccinium.
became
clear
that
Vaccinium
vitis
idaea
by the Exobasidium from Azalea, and that conversely
6
all
results
of
as
of
sets
host
a
plant
experiments
of these sets
one
of
the
to
fungus
all
made,
were
living
on
with similar
experiments
given in
are
table 5.
Table
Number of
plants with
galls resulting
pure
c
origin
ons,n
of
cultures
from
5
Azalea and
of
inoculation
of Exobasidium
of different
origin; 20
.1
plants
,
the
:li'
culture
plants
test
Azalea
Exobasidium japonicum
if
if
if
if
if
if
if
number
of
number of
c
“
diseased
galls
plants
cultivars:
25
25
17
‘Hexe’
‘Hexe’
40
40
19
0
0
0
0
‘Esmeralda’
0
0
0
‘Hexe’
‘Hexe’
0
0
0
22
15
Azalea
vaccinii
vaccinii
idaea
each set.
‘Esmeralda’
‘Esmeralda’
Vaccinium
Vaccinium
if
vitis
in
of
number
"u
pure
pu,c
c
Exobasidium
Vaccinium
test
vitis
vilis
idaea
cultivars:
cultivars;
Vaccinium
Vaccinium
idaea
idaea
vitis
vilis
their
a
there is
difference in
Despite
morphological similarity,
pathogenicity between these fungi. It is possible, therefore, to consider
them
to
physiological
represent
vaccinii Wor.
and the difference in
of
sufficient
for
name
the
fungus
standpoint
that
the
It is
American
Ellis
not
available.
different
ferrugineum
On
malt agar this
wrinkled
was
surface
and
‘Hexe’
galls appeared.
as
parasite
pure
from
from
therefore, is
not
a
culture
of the Swiss
no
complete,
it
be
may
rather
vaccinii
a
than
this pure
opportunity
with Exobasidium from
this Rhododendron must also
Rhodo-
to
and
finely
yellow
or
but
no
culture,
inoculate Rho-
‘Hexe’, and the evidence,
be assumed that the
considered
1953).
Wor.
more
a
were
Rhododen-
(Graafland,
Exobasidium
grey-brown
was
Swiss
specimens of the latter
inoculated with
Though there
dodendron ferrugineum
form.
in
differs
with
was
we assume
Exobasidium
inoculations carried out with
cross
from Azalea and
rhododendri,
obtained
fungus
and
japonicum Shir, in developing colonies with
brown colour.
lized
of
incomplete,
Exobasidium
be
valid
japonicum Shir.
least if
Peck
to
too.
set
originating
remained
fungus
then the
be Exobasidium
at
of the
considered
are
species,
Exobasidium azaleae
that the
dron
Exobasidium
more
Azalea would
species
are
regrettable
species
on
distinguish
to
Exobasidium
species, viz.
one
is taken up in the
present paper,
Exobasidium cultures
dendron
of
of the pure cultures
aspect
importance
This
discoideum
races
If, however, the physiological specialization
as
a
fungus from
physiologically
specia-
366
W.
GRAAFLAND
CHAPTER
DEVELOPMENTAL STAGES
FECTION
Efforts
WITH
were
developmental
infection
OF
made
stages
obtain
to
of
the
For
that
BUD
information
leaves
At
develop.
to
different intervals
removed and
mental
Exobasidium
an
stages
could be
studied
young
1, 2,
0,
after
7,
IN-
POSSIBLE
concerning
are
the
sensitive
to
buds of
axillary
suspension imme-
inoculation the
leaves and the
3, 4, 5,
WHICH
and the buds had started
fixed in Graf’s solution.
of the
which
dormant
purpose
diately after the shoots had been decapitated
were
AT
JAPONICUM IS
more
young
inoculated with
were
THE
EXOBASIDIUM
by this fungus.
Azalea shoots
IX
In
this
of the
progress
axillary buds
the
way
develop-
gall formation
14, 21 and 28 days after the
10,
inoculation.
Microtome
the infected
chyma proved
observed.
leaves
young
differentiation
intercellular
between
to be
spaces,
showed
the
hypertrophy
palissade
are
leaves.
already
spongy
All
paren-
In a few cases hyphae were visible in the
though the process of penetration itself was not
it
However,
sensitive
hyperplasy.
the
lacking.
The small size of the
young
and
and
layer
blastospores
them between the hairs and the scales
the
days after the inoculation
slides revealed that within 4
to
made it
which
became
infection when
clear
they
difficult
the
cover
that
the
to
detect
epidermis of
young
leaves
still enclosed in
are
the
bud.
The aim of the
the
Fig.
period
7.
following experiment
during which
A-D:
development
the
of
b -b
x
3
:
young
an
axillary
leaves.
was
sr s
4
bud
:
study
to
leaves could
still
of Azalea
bud
scales.
the
length
of
be infected. For
indica, cultivar ‘Hexe’.
THE
OF
PARASITISM
EXOBASIDIUM
that purpose in 70 Azalea
in order
after
stimulate the
to
this
the
in
plants
found that leaves
was
next
that
of
stage
were
the laminae
are
of
galls
stages i.e.
number
at
in
galls
of
mm
10
the shoots.
of
of
number
plants
galls
19
3.0
30
25
4.0
17
8
30
6.5
42
10
9
40
8-10
1
1
50
12-15
0
0
development
which
at
in another way.
inoculated with
a
had
not
appeared
time of inoculation
marked.
those
on
galls
were
soon
as
are
this
in
with
length
5
with
to
least
weeks 42
after
developed
and
at
the
the
just large enough
that
of the former
infection in
spread
to
paint,
After
be
to
at
those leaves which
on
agreement
begin
the 4th
the last
being
had
only susceptible
the laminae
infection,
to
Exobasidium;
treatment.
in
mm
of
shoot
which
present
subject
just visible leaves of 40
marked
were
leaves
about 8
is
of the
for
were
This result
culture
pure
tip
small
too
the leaves
experiment:
As
The young
The inoculated leaves
were
leaf is still
a
of
with
plants
group
10
they
stage.
per
developmental
different
10
leaf reckoned from the
be
number
buds
in
decapitation
85
inoculation. Twelve
to
inoculated
the
70
inoculated.
galls
(Table
1.5
of
It
In
and
out,
infection
to
2.5
were
when
spread
to
0
stage
plants
infected.
11
studied also
visible
culture
pure
6
buds
after
moments
axillary
decapitation
The
axillary
length of the
days after
was
of
different
of
a
of inoculations.
1, C-G).
the leaves
on
begin
removed
were
could be
longer susceptible
no
Table
Number
with
set
still
length
mm
development
6; Fig. 7 and Plate
used for each
367
AZALEA
different intervals
the buds. At
inoculated
were
of 8-10
the leaves
stage
buds
ON
tips of the shoots
unfolding of
the
unfolding,
of Exobasidium. Ten
the
plants
SHIR.
JAPONICOM
juvenile
a
infection
out,
is
no
important
to
longer possible.
From
answer
practical
a
the
in dormant buds. In
on
or
be
infected
start
buds is
leaf
was
kept
with
a
marked
below
at
the
it
especially
was
and,
the
An
with
paint.
marked
long
Nine
was
groups,
In
On
leaf
already
before
experiment
culture.
may
galls long before the growers
therefore,
inoculum.
pure
the Azaleas
greenhouses
broken.
administered
inserted
then
of view
spores of Exobasidium
pruning,
or
inoculated
visible
were
the
axillary
artificially
buds
by
cutting
of the
were
point
question how long inoculum of Exobasidium remains viable
each
every
the dormancy
performed with
each
plant
shoot
of
the
the
inoculated.
plants,
5
youngest
4
axillary
plants
high humidity for 30 hours. At different intervals,
were
The
4 weeks after the inoculation, the tips of the shoots were removed
up to
just above the marked leaf to stimulate the development of the buds.
It
appeared
that
even
buds inoculated
4 weeks before
they began
to
368
W.
showed
expand,
experiment
the
development
in
the
tips of the shoots within
inoculation,
longer
inoculation
for
viable,
a
gall
repeated
was
of
galls
after
year
the
experiment
were
dormant
buds
of
the
had
been
with
an
on
treated
Exobasidium
with
the
the
appeared
suspension
be
to
half
(Table
7,
7
begin
in
each
group.
number
of
number of plants
galls
with
galls
expand
0
17
5
2
20
5
3
18
5
5
16
5
9
10
4
12
7
5
18
3
3
23
4
3
30
4
3
14
4
14
24
11
5
28
5
3
35
11
4
56
2
2
91
3
3
119
2
2
182
4
2
2
after
different intervals
the
to
1
shed
experiments
at
suspension; five plants
inoculated buds
light
no
the
on
question
how
fungus
the
during the period between the inoculation and the develop-
behaves
of
the
their
and
gall,
that the
possible
on
the
after
of days
after
ment
4 weeks after
still
fungus
leaves developing
young
Number
These
6
The
months
most
Even
1).
removing
2).
inoculation
experiment
instead of
found in buds that remained dormant for
galls occurring
experiment
experiment
the
at
chosen.
Table
Number
way,
period of
a
7,
but
(Table
same
intervals
were
they
GRAAFLAND
how it
blastospores
and
surface,
that
between the
hairs and
of the
leaves
young
the
the
colonies
scales
the
may
obtains
administered
occur
at
of
the
the buds
formed
thus
the
nutrients.
necessary
to
remain
dormant buds.
time
the buds
It
is
budding
start
viable
Penetration
begin
expand.
to
However, it is also possible that the spores penetrate directly into the
leaves of the dormant
inside
Which
as
the
The
buds
latter
of these
first
rate
which
and
the
is
two
as
pathways
long
development
stimulated
parasite
takes
environmental
of
the
as
is
actually
developmental stages of
of
the symptoms
are
bud, and that the development of the hyphae
delayed
new
place.
growth,
Thus
conditions:
remain
remains
the disease could
the host
plant
of the disease will
to
buds
taken,
a
appear.
parallel
the incubation
if the buds
are
not
determines
dormant.
undecided
be detected.
the
time
If infected
development
period depends
just unfolding
at
at
axillary
of host
on
the
the time
THE
PARASITISM
contamination,
of the
after the infection but
after
OF
the
EXOBASIDIUM
the symptoms
THE
frequently
White,
done
the
been
of
“Tuinbouwgids”
with
Jaenichen,
galls
the
(Dutch
still
Guide)
though it is known that they
are
The
recom-
conclusive
not
1957). This method would be satis-
removed
were
mixture.
i.e.
time,
in
picking
before
of mature
sporulation,
galls promotes
spread of the basidiospores. However, it is impractical to remove
gall bearing leaves sufficiently early from large numbers of densely
Azaleas.
planted
buds
cannot be
control of the
could
It
easily
is
state
For
duced
into other
buds of
and forbid its
10.2
countries,
laws,
by
(1928)
also
which
In
with
spraying
(1925)
consider
(1954)
the removal of the
the
use
as
are
it is
dormant
to
easy
defeat
parasite
dangerous
a
un-
easily be intro-
prefers
a
a
or
Cole
be
to
good
zineb after
(1944)
an
Ciferri
been
pruning;
(1953)
carbamates
had
the
and Thiel
effective
preventive
treatment with
galls. Anonymus (1956)
frequently
of lime after
use
prefer Bordeaux mixture,
(1929)
sulphur.
as
has
fungicides
spray;
mentions
fungicide.
following
good results by spray-
galls had been removed
possible.
mature
control
fungus
plants
apparantly
hidden in
manner
mixture
of lime
Many authors consider insects
from
an
places.
the
once,
may
be
may
mentions lime.
Bordeaux
ing with copperoxychloride
as
it
recommends the
zincethylenebisdithiocarbamate
far
japonicum
this
the
list
and Marchionatto
Thiel recommends
Jaenichen
neighbouring
galls only
fungus
contamination
the time the dormant buds
because
though Marchionatto also
(1951)
new
fungicides
literature
advised. Marchal
Miles
from
continual
a
importation.
Control
the
In
at
Exobasidium
imported Azalea plants.
quarantine
a
imported from Belgium in
galls
reason
in
Thus
Even if the
necessary.
the
infected
expand,
to
ones.
greenhouse,
a
removing
Plants
begin
healthy
blown
spores
after
show
may
that
from
way
from
that
be diseased.
folding.
the
distinguished
occur
healthy
they
from
unfolding buds would be
obvious
may still
before
Moreover,
eradicated in this
were
as
Bordeaux
Horticultural
when the colour is still green, but the
all
with
spraying
1952; Graafland,
the
if
1909; Miles,
1928;
1954). This is sometimes
(Naumann,
out
1951 ;
1960
mends these measures,
factory
THE DISEASE
importance of removing and burning the galls
pointed
combination
(Welvaert,
period.
measures
1933; Stautemas,
in
that
days
longer
or
X
CONTROL OF
In the literature
has
369
AZALEA
appear within twenty
may
if the buds remain dormant for
infection,
Hygienic
ON
they may also be delayed for 6 months
CHAPTER
10.1.
SHIR.
JAPONICUM
of
galls
insects
to
to other parts
is
important
be effective in
of the
plants.
(Stautemas,
transmitting spores
For
1951).
that
Next
reason
to
the
insects
370
W.
mites
be
this
be
might
killed
opinion
and
involved,
(Miles,
Aleurodes
of these
parts
vaporarius
from
galls
In
the
glasshouses
whatever
fungicide
a
and
keeping
x
is
that the
are
the
minating
also
less
of
and become
in
1960
sulphur
as
_
A drawback
sale.
vitro
Horticultural
advised for
out
were
captan,
unattractive for
disastrous.
(Dutch
are
going
more
and
way
well
as
severely damaged by such frequent
fungicides
lime
and
zineb
shaped
spores
is
of use,
Guide)
As these
spraying.
of
some
assayed against
when
used in
fungicides
a
were
the
centrations
in
high
the
the
newer
Exoba-
only
a
the E.D.
small
growth
are
Even
if
would have
different
from
be
to
be
blastospores could
to
1/100 of
they
occurs
could
the
experiof
the
cultures. The
determined
were
those
be
inoculated
concentrations
following fungicides
1/10
as
condensation-water,
basidiospores
the nutrient solution of shake
The
budding.
basidiospores,
thin film of
a
humidity.
of the
culture
used in
the number of ger-
percentage
50 of the
be
suspensions. Budding only
watery
difficulties,
to
mycelium.
varying
shake
a
hardly
can
high numbers of spores needed for
these
added
they
vitro, in which
hundreds of Azaleas
avoid
inhibition of the
weighing
all
obtain the
to
To
ments.
at
assess
as
covered with
are
spores
kept
to
at
assaying,
in order
tests in
in
developing
but
numbers,
counted,
impossible
when the
blastospores
large
germination
germinate
not
i.e.
or
more
irregularly
ordinary
It is
or
period of flowering is
with
be obtained in
can
more
spray
this
_
Septoria azaleae Vogl.
as
in
disease
the Exobasidium
from
regularly,
even
growers
succeed
and
irrigation.
spray
of the buds with
applied
be
to
Some
our
arising
disease.
The
do
are
the
i.e.
compounds,
sidium
free
“Tuinbouwgids”
fungicides
have
compounds,
copper
by
_
compounds
regards
Though it is
by draughts
protection
'X'
Experiments
copper
augmented
pruning.
parasitic fungi, such
during
the
In
after
They shed their leaves,
Spraying
carried
droplets
Fungicides
or
plants
plants
sprayings.
10.3
with
their
(1925)
role in the transfer of Exobasidium
a
aired and
are
before
v_»
from other
water
necessary.
fortnight
every
in
is
to the bodies
spread of the spores.
way contamination occurs,
alone
not
therefore,
healthy parts of the plants, the disease is in
to
opinion mainly spread by
when
Marghal
arthropods.
possible that insects and mites play
spores
should,
too
1929). Marchionatto based
basidiospores attached
the
causing
as
animals
these
and
Marchionatto,
1928;
his observation of
on
mouth
the
GRAAFLAND
used
used in
in
practice:
copperoxychloride;
0.05,
0.10,
0.20
0.50
g/1
lime
0.075,
0.15,
0.30
and 0.75
cc/1
0.025,
0.05,
0.10
and
0.25
g/1
0.02,
0.04,
0.10
and
0.20
g/1
sulphur:
zineb
1
captan
The
)
2
)
experiments
were
carried out in
J
)
zinccthylenebisdithiocarbamate.
2
)
4,
5-
cyclohexene -1, 2- dicarboximide.
erlenmeyer
and
by
con-
flasks
containing
PARASITISM
THE
50
a
of
cc
EXOBASIDIUM
OF
malt solution
a
which known
to
standard solution had been added.
oxychloride
prepared
were
Table
the
of
Composition
media
in
cc
0.1
cc
of
solution in
40
10
0.1
50
30
20
0.2
50
0
50
0.5
nicum shake culture
well
cultures
mycelium
with
latter
110° C
for
the
g/1).
in
even
the
inhibited
fungicide
growth
fungicide
was
concluded
was
sulphur
that
most
were
weeks,
3
as
controls.
quantity
test
a
at
of
temperature
The
weighed.
the
at
growth of
stimulated
at
effect
this
of
(Fig.
captan
was
were
suppressed
concentration
mycelium,
the
be of
to
seem
any
growth. Though captan
in concentrations of 0.2
degree
influence
favourable
the
not
The
105° C-
experiments
highest
the
cc/1. Zineb did
high
a
no
used
cultures
paper.
concentration
a
fungicide
Since
8).
of 0.1
and
that
is
the latter
chosen for
the
g/1,
g/1.
of
now
experiments
It
lime
less
with
plants.
10.4
Experiments
was
Captan
of Azalea
day,
shoots
shoots
the
suspension.
a
the inoculation.
buds
day
removed
In
treating
would
exercised
its
fungicides
treated with
were
of Exobasidium.
were
before
with
in
used in concentrations
and after
culture
a
/2
inhibited the
even
to
of
widely used in practice,
test
if
mycelium
sulphur also
japo-
the
used
were
to
It turned out that copperoxychloride
concentrations of 0.15
this
x
covered with filter
dried
was
Exobasidium
an
determined. The
was
and then
days,
of the
Lime
influence;
this
7
three times.
growth
(0.5
mycelium
to
addition
for 2
Buchner filter
a
of
cc
suspensions without fungicides
added. Similar
developed,
to
1
flasks
erlenmeyer
Thus solutions
way.
the solutions that are
similar
a
value
had been shaken
through
3
replicated
the
all
was
which had
filtered
were
prepared in
malt solutions without any
as
all
After
0.05
in nutritional
equal
used. To
normally
of
cc
5
were
g
1
per
50
obtained
in
concentration
45
The other media
as
chloride
a
50
were
copper-
copperoxychloride.
standard
%
and of
water
containing
8
used
quantity
371
AZALEA
table 8.
copperoxy
water
in
in
containing
malt
solution
ON
quantities of
The media
indicated
as
SHIR.
JAPONICUM
on
In
which
one
the
they
was
were
on
inoculated
experiments
The buds
g/1.
1
fungicide before,
of
the
tips
inadvisable to
plants with captan,
develop
g/1 and
their
fungicidal
infections
action.
total of 36 buds. From
were
remove
as
in
before
that
the
In each series 4
4 control
plants
the
the
10
tips
case
plants
tips of
a
the
captan
the
same
pure
fungal
days
after
long time
unfolding
could
were
the
a
tips of the
the
removed
the
with
simultaneously with the application of
second series
It
the
series
vivo
of 2
have
used with
shoots
were
372
Fig.
W.
8.
basidium
d:
Influence
japonicum
of
fungicides
on
in shake cultures,
captan. Dry-weight
of
the
centration
in
GRAAFLAND
the
a:
dry-weight
of
mycelium
copperoxychloride,
mycelium without fungicides
g
or
cc
per
formed
b: lime sulphur,
1; ordinate; weight
0.52
in
g.
g.
by
r.
Exo-
zineb,
Abscis:
con-
PARASITISM
THE
removed
control
OF
EXOBASIDIUM
with
simultaneously
this
plants
The smallest number
of 2
g/1
the
done
was
of
10
with the
after
inoculation
with
on
of
suspension
a
from
4
other
inoculation.
captan suspension
a
also used in
(Table
practice.
9
of 4
groups
373
AZALEA
fungal suspension
that is
one
Table
developing
the
when
galls appeared
9). The concentration of 2 g/1 is the
Number of galls
after
ON
and
inoculation,
days
applied simultaneously
was
SHIR.
JAPONICUM
Azalea plants with 36
and
Exobasidium japonicum
buds in
total,
with
treatment
captan.
of
tips
removed
time of
with
relation
inoculation
to
7
days later
4
controls:
plants
34
4
From
these
when
not
with
the
g/1
tips
the
reach
the
between the
or
one
1
0
8
6
23
13
removed
removed
it
days
became
after
began
clear
killed
was
the
buds,
because
some
minor
solutions
experiments
been
tested
in
lime
plants
The test
were
composed
of 4
main series
the
sprayed
of
10
5
the time of infection. This
to
danger
glasshouses
Instead of
seems
as
be
the captan
were
could
hidden
fungus had already
was
applied.
these
experiments
the
of
where
g/1
after
after
the
inoculation,
and
that treatment. Each series
30
total about
axillary
buds.
The
10.
showed
that
fungicides
provided that they
means
is
sporulating
the
recommendable.
are
that the buds should
infection
spraying frequently,
more
adminis-
cc/1
week
one
control,
keep
protected,
7.5
days
experiments
under
at
those
galls
was
became visible
g/1
with in
table
to
in
fungus
plants
in
2.5
sulphur
decapitated
indicated
buds
used:
were
were
the
case
the latter
the
In
vitro.
24 galls.
performed with the other
were
copperoxychloride
be
inoculation:
when the latter
captan
Perhaps
because
or
in
that,
by captan
inoculum,
unfold.
to
blastospores
zineb
The
9
the
inoculation:
with the inoculum. If
of the
that had
fungicides
is
14
with
simultaneously
10
week after
sprouting
scales
In addition
result
g/1
19
29
into the young leaves before the
captan
penetrated
was
2
g/1
3
fungus
the infected buds
the shoots
1
15
tips
simultaneously
day
one
following
of
20
experiments
dormant,
added
tered
the
days
inoculation
galls
plants
remained
was
with
shoots
10
concentration
14
8
later
day
2
42
simultaneously
the
captan
g/1
before
1
after
captan
1
days
of
tips
removed
of
concentration
time
2
shoots
inoculation
in
with captan
the
simultaneously
treatment
always
galls
application
Discarding
of
able
continuously
present,
occur
are
administered
particularly
frequently.
hygienic
the young
measures
galls before
374
W.
GRAAFLAND
Table
Number
total
of
after
galls developing
on
inoculation with
10
of 4
groups
of
suspension
a
with
Azalea
number
of
zineb
tural
to
the
destroys
Guide). However, it
is also
pruning
infection.
This
“Tuinbouwgids”
difficult
pick
to
when
all young
out
apply
sporulating
galls
Horticul-
galls
the
at
fungicide
a
are
found.
resumed after
growth is
vegetative
has
practice
(Dutch
grower may
when
especially
important
after
or
is
of
source
the
in addition the
Therefore,
infection,
prevent
Spraying
galls
24
plants
recommended in
proper time.
in
treatment
11
sulphur
control
sporulate,
and
8
lime
been
axillary buds
3
copperoxychloride
they
30
fungicides.
fungicides
also
with
plants
Exobasidium japonicum
have been taken.
cuttings
CHAPTER
XI
DISCUSSION ON THE RELATIONS BETWEEN THE GENERA
EXOBASIDIUM,
According
dyana
compose
siders
this
which
the
to
surface
the
cuticle.
only
host
a
are
of
subclass
class
of
lacking
and
this
presence
the
exposed
genera
there is
as
and also
the
formation
sporidia
Ustilago
of
arising
hordei
in
the
colonies;
from
(Pers.)
the
budding
this
smut
Lagerh.
spores
blance between the characters shown
species
when
grown in pure
develop colonies
In
Ustilago
gation of
caries
as
4-
(D.G.)
they
arc
with
species
and
Tul.,
a
culture
wrinkled
the
process
—- sporidia.
conjugation
formed.
In
this
In
Kordyana
(1954),
assigned
to
the
basidiospores
one
of
of
the
the
to
Ustilagi-
is
an
agar
resulting
budding
species,
Ustilago
there
budding
the
in
be
a
striking
and
of
e.g.
by
of
such
are
in
the
as
resem-
Ustilago
medium. Both
fungi
folded surface.
or
occurs
way
authors,
Talbot
by Exobasidium
on
of
some
the
bursting
that the Exobasidiaceae
of their
Moreover,
below
the
resemblance
reminds
hymenium
a
just
e.g.
must
nales. This resemblance is found in the fact
parasites,
of
Exobasidium and
Others,
a
The Exo-
assignable
and
by
character
primitive
Agaricales,
Basidiomycetes.
developed
becomes
Korcon-
order Hymenomy-
is
genus Exobasidium
Hemibasidiomycetes,
the
and
(1952)
the order
to
the
Exobasidiales.
the
Exobasidium
basidiocarps,
hymenium
(1949), assign
that the
of
account
on
this
order:
opinion
forms,
plant
Because
separate
belonging
seven
TAPHRINA
Alexopoulos
synonymous with
Holobasidiomycetes,
basidia;
Viennot-Bourgin
to
of
one
primitive
of
of
be
others is
AND
genera
Exobasidiaceae.
subclass
are
the
(1949),
family
to
Agaricales
consisting
the
family
the
basidiaceae
to
the
according
of
cetes
Gäumann
to
TILLETIA
USTILAGO,
genus
is
followed
Tilletia,
between the
these
e.g.
by conjuin
sporidia
two* genera
a
Tilletia
as
soon
dicaryotic
THE
mycelium
has
is
point
the
in
of
point
who
fungi
eventually,
or,
both
In
the
The
In
the
A
dermis and
the
both
cuticle
of the
the
show
the
of the
kind
same
Laubert
(1932)
genera
of
tomical
picture:
and
spaces
infection
In
the
to
be
n
in
In
coarse
and
Exobasidium japonicum
Taphrina,
genus
exceptional.
In
in
species,
however,
genera exists
of asci
in
mainly
those
was
The
hyphae,
budding
not
hyphae.
He
agrees
Thus,
yeast
depends
the
with
the
by'
in
arc
used
(1949)
infectious.
the
like
but
not
used
cultures
constant,
Mix
do
of
both
cells.
on
cases
Mix’s
term
Exobasidium. On the other hand A Voronin
cells
to
“conidia”.
It
borne
on
spores
seems,
however,
conidiophores,
as
is
latter
between the
former
genus
'are
this
to
family.
cultivating Exobasidium
for
growing
Taphrina
of
consisting
of
these short
of the
for
that
thus
be
to
taken
the
are
budding,
by
restrict
customary
yeast-like
spores
Taphrina
(1867) called
short
hyphae
nutrient solu-
these
these
similar in
preferable
it
of blastospores
or
of
alike,
can
Taphrina
1935). In the
multiplication
arc
“blastospores”
and
members
(1934)
the
seems
—
J
the
composition
development,
found.
contrast
in
is
J
was
in
length
Fitzpatrick
mycelium
genus Exobasidium and
“blastospores”
shape and the infectious character
Exobasidium.
on
are
The
Ericaceae
(1949)
The
the
name
the
(1953)
Mix
hyphae
the
difference
species of
occur
by Graafland
originally
species.
The
J
ascospores
of basidia in the
ana-
spaces.
spores
Sadeb.
The
same
copulation
(1949),
1927; Mix,
rare.
representatives
which
Taphrina,
is
Taphrina.
on
method used
species
tion.
presence
genus
parasites
of
1 he
the
in
the
conjugation
of
—
(Wieben,
the
the
cases
spores;y
Mix
deformans (Berk.) Tul. show copulation of
derived from the ascospores
both
epiphylla
which
occur
with few intercellular
copulation
to
Taphrina
and in
living
fungi
the intercellular
A
1912).
representatives
show
galls
authors
members
Juel,
the
their way of
haploid
according
Only
in
The
no
of
epi-
epidermis.
some
1897;
parenchyma
grow
the
budding.
that
In both genera
chloroplasts.
width,
shape
spaces
group of which the
(Thomas,
brooms.
by
occurs
astonishing
one
by monocaryotic,
occurs
dicaryotic.
of
scarcity
a
0.5-1.0
thin,
uniform,
a
intercellular
analogy between
plants.
galls and also witches’
the
spores
parasitism
the host
on
similar
a
sporulation.
not
to
mentions the
too
by Wo-
similarities:
important
of
a
striking
a
out
underneath the
or
Taphrina and Exobasidium
their influence
cause
galls
it is
belong
to
in
time of
germination of the
genera
show
develops either between
hyphae
at
Though
related from
pointed
galls
cause
myce-
another
brooms.
of
burst
cases
consider both
following
They
is
Ustilaginales.
closely
been
already
the
conjugation
dicaryotic
a
conjugation
not
are
mycelium lives
layer
cuticle is
has
Considering these similarities
is
however,
of
375
AZALEA
cycles of both fungi
parasites;
witches’
cases
tissues.
This
mentions
true
are
Taphrina
the life
view,
resemblance.
(1867),
Both
3.
This lack
plant.
and
ON
it is known that
of difference between Exobasidium and the
ecological
,
SHIR.
JAPONICUM
Exobasidium,
genus
though
the host
genera Exobasidium
ronin
2.
EXOBASIDIUM
the
observed,
present
taxonomic
1.
OF
formed. In
been
never
lium is
PARASITISM
and in
over
for
sprouting
this
name
nowadays.
376
W.
According
Ainsworth
to
should be confined
and
where
Uredinales,
of the
gation
Therefore,
When
genera
differ
used
the
comparing
are
borne
formed in asci.
which
this
the
it
of
of
these
with
group
it is
also
given
Taphrina
well
as
able
to
one
exogenous spore
their host
these
2
living.
for
stops,
genera
with
group
of
blastospores
the
as
infect
to
are
basidiospores
The
more.
Taphrina,
the
they
both may form
By sprouting
once
are
the genera
as
Exobasidium
In
in
the
both
plants.
of the
are
endogenous
formation have
developed.
possible that the similarity in behaviour between
the
taxonomically
mode
important
development of the spores, has been induced by their parasitic
of
by
of
that
concluded
view.
fungi belonging
different in
so
groups,
“blasto-
term
definition
here the difference
similar.
origin, and that, by differentiation,
and another
by conju-
representatives
basidium;
a
genera,
that the
imagine
However,
the
be
must
However,
ascospores
,
same
the
paper
with
point
on
sprout
may
formed in both
can
in
character of
Taphrina,
taxonomic
a
exogenous,
Exobasidium
One
followed
which has been budded off”.
parasitic
the behaviour of these spores is
are
is
budding
accordance
spore
and
from
blastospores,
“sporidia”
term
biologically very similar. This is remarkable,
are
endogenous,
that
of
confusion,
in
“a
Bisby:
Exobasidium
widely
spores
the process
avoid all
been
Ainsworth and
genera
the
(1950),
sporidia.
to
has
spores”
and Bisby
secundary spores formed by the Ustilaginales
the
to
GRAAFLAND
of
way
)
SUMMARY
The
1.
purpose
japonicum Shir.,
host
and
plant
important
to
parasitic
For
2.
of
frequently
(Belgium),
of the soil.
x
a
cell
the time
and
as
well
life
also paid
of
cycle
this
some
as
Woronin
Rhododendron
genus
the cultivar
cultivated
are
to
as
sprayed.
‘Hexe’,
during
The
were
‘Galestin’
Exobasidium
parasite
control
the
to
its
measures
question of
Exobasidium
chosen
and
the
vaccinii,
as
mainly
and
experiments
host
plants.
‘Moederkensdag’,
grown
the greater part of
temperatures, high humidity,
frequently
the
manuscript of this
Gottgens
von
besonderer
of
suspensions
the
length
Exobasidium
Azaleae
Beriicksichtigung
of Daucus
pure
of the
in Ghent
the
high moisture
were
year
in
content
performed
with
cultures.
As
was
E.
und
ready
1960.
seine
Infektion
gallenbildenden
pure
to be
sent to the
Untersuchungen
printer
iiber
die
Wirtspflanzen
der
Wirkstoffe. Phytopath. Z.
cultures of the Azalea
parasite
in
synthetic
basidiospores as well as with
Environmental conditions proved to be of influence
infecting
incubation
Peck
der
the host
period.
activating substances,
carota roots.
paper
appeared (Gottgens,
and succeeded in
filtrates contain
or
was
‘Esmeralda’,
394-426!. This author obtained
media
on
is
viz.
Boskoop,
low
studied,
the
relation of
idaea.
used. Azaleas
Water
Entwicklung
38:
in
The
described by
cultivars of the
at rather
of
study
unter
that
Japanese origin
grown
were
study
to
cuttings.
At
)
study
vilis
was
Azalea.
on
Attention
growers.
with
fungus
were
greenhouses
investigation
of infection
commercial
this
Cultivars
rooted
the mode
Vaccinium
on
this
fungus parasitic
a
of this
identity
of
plant
with
Further Gottgens found
which promote the
growth
that
of
growth stimulating factors probably biotin,
nicotinamide, inositol and pantothenic acid
are
present
in
the
the culture
tissue cultures
nicotinic acid
filtrate.
THE
3.
The
visible leaves
and
enlarged,
are
called
are
with
covered
4.
The
the
(Fig.
the
leaves.
latter produce
of
hyperplasy
of
of the
parts
the
them
give
number
cells
mesophyll
media malt and malt-saleb
also
be
and
more
The
6.
malt
a
less
or
solution
regularly
developed
were
spores
in
grown
in
in
grown
be
to
shake
a
most
this
increase considerably
to
galls
The
cell
In
culture.
could
be
leaf
a
also
was
it
of
tissue
and
culture
could
fungus
short
ways
cells,
hyphae
resembling blasto-
not
well
as
the shoots
the
of
with
as
sus-
of the plants
inoculated axillary
formed
the newly
shoots
appeared
of the inoculum, whether basidiothe
influence
to
seem
of their
become
fungus cells
neither
number
of
of
between
basidiospores
4
nor
In
that
least
at
case
would
be
one
were
that
had
fungus
+ and
and
one
either from
able
5).
between
one
spores
—
cell
fusion
penetrated into
—
basidiospore,
accomplish infection.
to
necessary
originating
single basidiospore
of -+- and
possibility,
the
after
or
presence
The
(Fig. 6).
the leaf
appeared that blastospores
it
investigated.
was
uninucleate (Fig.
basidiospores and blastospores originating from
blastospores,
a
dicaryotic
be
to
sexual differentiation the
a
investigated.
culture or from
shake
the
the surface
galls (Table 3). Thus,
of
on
blastospores appeared
fusion occurred
no
on
combination
However,
of
the
case
expected,
might take place
a
did
culture,
between
basidium, where in
or
both
fusiform
source
fusion could be observed,
Even
blastospores.
the
of galls
The
1).
(Table
which
at
stage
basidiospores and
vitro no
In
The
hypertrophy
cultures. As
pure
inoculated with basidiospores
number
shake
a
which
(Table 2).
7.
The
from
cells
or
spores
both
B).
3).
were
the
treatment
and
basidiospores
favourable. The
pensions obtained from shake cultures. Simultaneously
in order to stimulate the
were decapitated
development
buds. By
five
to
blastospores by budding.
shaped, eventually
(Fig.
dormant buds
were
appeared
agar
become
A
(Fig. 2).
occurs
Colonies of Exobasidium japonicum
5.
of
they
1,
forms basidia,
four
leaves remains undifferentiated;
leaves
these hypertrophic
(Plate
fungus
the
on
even
of the
after ripening
bears
basidium
377
AZALEA
appear
appearance
of the
mycelium
may
crooked;
green,
velvety
a
Each
great
a
are
ON
diseased parts
The
and
convex
stage they
intercellular
dicaryotic,
attacked
become
japonicum
buds.
unfolding
young
which
spores,
The
1).
of the
a
SHIR.
JAPONICUM
Exobasidium
by
of the
blades
In
galls.
rupture the cuticle
EXOBASIDIUM
of attack
first signs
youngest just
parts
OF
PARASITISM
single
a
to induce the
cell
out
development
be concluded that Exobasidium japonicum is homo-
must
thallic.
8.
By
Vaccinium
vitis
(Table 5).
Exobasidium
and
idaea,
This
in
colonies
inoculations it
cross
difference
vitro,
are
japonicum
appeared that Exobasidium japonicum
that
in
Azaleas
Shir, is
accepted
9.
The
after
leaves
the
susceptible
tip
until
C-G and Table
fungus
on
the
10.
by
was
as
to
the valid
in
difference
a
importance,
name
for
attack
not
colour
and for this
the
of the
reason
Azalea parasite.
on
the
two
host
Japanese Azaleas and from the
plants, proved to be identical in
(Table 4).
are
bud. By inoculating
i.e.
specific
did
Exobasidium vaccinii
by
isolated from the
crossinoculated
cultivar ‘Hexe’,
be of
to
attacked
not
added
pathogenicity,
considered
Strains of Exobasidium japonicum
pathogenicity.
were
still
probably susceptible
the
leaves
of the
they
6).
In
shoot
at different
had
6
months,
infection
removed,
length of
while
after the
it
was
8-10
shown
mm
buds treated with
as
after
removal
still
enclosed
buds began
that
(Fig. 7,
a
spore
of the
to
they
in
the
unfold,
remain
A-D; Plate 1,
suspension, the
tip galls appeared
(Table 7).
The dormant buds should
spores.
a
dormant axillary
viable after
unfolding leaves
wind-borne
been
have reached
to
intervals
Of
the
be
protected
by
following fungicides
a
fungicide against infection
different concentrations
were
to a shake
culture: copperoxychloride, lime sulphur, zineb
assayed by adding them
and captan (Table 8). Captan strongly inhibited the growth of the mycelium at
378
a
W.
concentration
of 0.2
GRAAFLAND
Buds
g/1 (Fig. 8).
The
number
and
the fungus inoculum
11.
The
genera
galls appeared
Exobasidium
the
to
the
Taphrina
the
groups,
be
to
after
shoots
reduced
strongly
most
treated
were
inoculation with
a
spore
when
with
this
suspension.
the
fungicide
applied simultaneously (Table 9).
were
between
similarity
Exobasidium and
taxonomic
of
of
Azalea
on
and
fungicide before, simultaneously with,
is
life
and
Basidiomycetes
and
cycle
striking,
Hemibasidiomycetes
ecological
the
though they
the
is
are
behaviour of the
placed
in
quite different
The
Ascomycetes respectively.
also
relation
discussed.
REFERENCES
G.
Ainsworth,
C.
Alexopoulos,
Anonymus.
1956.
O.
Brefeld,
1952.
J.
Diseases
Die
Bisby.
of
Azalea.
of the
1954. A dictionary
Introductory
New
Mycology.
fungi. Kew.
London.
York,
Gaz. New South Wales
Agric.
Unters.
Gattung Exobasidium.
67;
Gesammtgeb.
583-584.
Mykologie
12-18.
1915.
The
Thelephoraceae of
Missouri
Bot.
Card.
A.
R.
Ciferri,
R.
and G.
1889.
8:
E.
Burt,
C.
1953.
anni
Cinque
2:
di
North
IV:
America
Exobasidium.
Ann.
627-658.
esperienze
anticrittogamici
con
sulle
bisditiocarbamato di zinco. Notiz.
Malat. delle
etilen-
base di
a
Pianta
23: (n.s. 2)
3-19.
Cole, J.
R.
P.
Eftimiu,
and
Rev.
B.
Ellis, J.
S.
34;
1874.
F.
Ezuka,
A.
I960.
1955.
Recherches
14:
Agric.
of fungi found
species
in
Pareys
culture
of two
Phyto-
histologiques
sur
les
Exobasidiees.
62-88.
at
Field.
New
N.
J. Bull. Torrey
Blurnengartnerei 2.
of
species
Shirai. Bull. Tea
japonicum
Sc.
Bot.
Aufi.
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