Ribeiro Et Al. (1976) - The Influence of Qualitative and Quantitative Radiation On Reproduction

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Mycological Society of America
The Influence of Qualitative and Quantitative Radiation on Reproduction and Spore Germination
of Four Phytophthora Species
Author(s): O. K. Ribeiro, G. A. Zentmyer and D. C. Erwin
Source: Mycologia, Vol. 68, No. 6 (Nov. - Dec., 1976), pp. 1162-1173
Published by: Mycological Society of America
Stable URL: http://www.jstor.org/stable/3758748
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THE 1NFLUENCE OF
QUALITATIVE
AND
QUANTITATIVE
RADIATION ON
REPRODUCTION AND SPORE
GERMINATION OF FOUR
PHYTOPHTHORA SPECIES
O.
K.
RIBEIRO,
G. A.
ZENTMYER,
AND D. C. ERWIN
Department of
Plant
Pathology, University of California,
Riverside, California
92502
SUMMARY
The influence of visible and near-visible radiation on the
reproduction
and
spore germination
of
Phytophthora capsici,
P.
cinnamomi,
P.
mega-
sperma
var.
sojae
and several isolates of P.
palmivora,
was
investigated
utilizing
a
synthetic
medium and a 12 h
light/12
h dark
cycle.
In
general,
near-UV radiation
(8
to 100 uW
cm-2), significantly
enhanced asexual
sporulation
in P.
capsici
and P.
palmivora. Phytophthora
cinnamomi and
P.
megasperma
var.
sojae,
when
exposed
to
light,
failed to
produce
sporangia.
Differentiation of
zoospores
from
sporangia produced
under
specific regions
of the visible and near-visible
spectrum
differed
among
isolates.
Significantly
fewer
sporangia produced
under near-UV radiation
differentiated and released
zoospores. Oospore production
was
significantly
higher
in the far-red
wavelengths
at 8 ,W cm-'. At 100 /,W
cm-2, oospore
production
was less than that obtained in darkness. Germination of
oospores appeared
to be
independent
of the
quality
and
quantity
of radia-
tion received
during gametogenesis.
The influences of
light
on
fungi
are
many
and varied
(9, 19, 23).
In
the
genus Phytophthora, investigations
on the effect of visible and near-
visible radiation on
sporulation
have indicated that the
response
to
light
differs with the
species (1,
5, 10, 11, 15, 17, 22, 28, 36). Sporangium
production
is abundant in some
species
in
response
to
light (1,
7, 11, 12,
16, 22, 30, 31),
while other
species
are either inhibited
(10),
or fail to
respond (1,
11, 34).
It is also known that
light
inhibits the formation
of
oospores
of
Phytophthora spp. (11,
13, 14, 15, 17, 22, 24).
More
recent
investigations
with P.
palmivora (15, 16),
indicate that short
wavelengths (450 nm)
inhibit
oospore production
and enhance forma-
tion of
sporangia,
while
longer wavelengths (700 nm),
enhance
oospore
production. Reports (2, 5, 8, 15, 28),
also indicate that
greater
num-
bers of mature
oospores germinate
when
exposed
to blue
(400-450 nm)
and/or
far-red
(700-750 nm) regions
of the
spectrum.
The
majority
of these studies have
investigated only
one
phase
of the life
cycle
of
1162
RIBEIRO ET AL.: RADIATION AND PHYTOPHTHORA
Phytophthora using
continuous
light
and either natural
agar
media or
natural substrates. We have
attempted
to
approximate
field conditions
more
closely by employing
an alternate 12 h
light/12
h dark
cycle,
selected
wavelengths
in the visible and near-visible
spectrum,
and radia-
tion
approximating average
intensities recorded over a
period
of one
year
in an avocado
grove
in southern California.
MATERIALS AND METHODS
The fluorescent
lamps
and filters used to
generate
radiant flux
density
within
specific regions
of the visible and near-visible
spectrum
have been
described in detail
(36).
Radiation at 8 ,W
cm-2,
in the
blue,
red and
far-red
regions
of the
spectrum
utilized a
system
described
by
Ribeiro
et al.
(28).
The intensities of all
lamps
were monitored
frequently
throughout
the duration of
experiments
and
adjusted
to maintain
equal
radiant flux densities for each
spectral region throughout
the visible and
near-visible
spectrum.
A diurnal
light cycle (12
h
light/12
h
dark),
at 25
-
1 C was used in this
study.
The culture medium used for
growth
and irradiation of the
fungus
has been described
(27). Eight
ml of the
synthetic agar
medium was
dispensed
into each 60-mm
plastic petri
dish. Each dish was inoculated
with a
cylindrical
5-mm-diam
plug
taken from 5-da-old cultures
growing
on the
synthetic
medium
(two plugs
of
opposite compatibility types
placed
2 cm
apart
for heterothallic
species,
a
single plug
in the center
of the dish for homothallic
species).
Inoculated dishes were
immediately
placed
under the different
light
sources. The
petri
dish lids transmitted
all
wavelengths greater
than 293 nm. Dark controls were
placed
in a
blackened 1.3 cm thick wooden
box,
wrapped
with two
layers
of
heavy
duty
aluminum foil.
All
experiments
were terminated at 10 da and observations made
immediately
thereafter. Numbers of
sporangia
and
oospores
were counted
with the aid of a
microscope
in 5 random fields of 1.5
mm2,
for each
petri
dish.
Oospore germination
tests were conducted after 30 da
incubation
by
the method of Ribeiro et al.
(28).
Indirect
germination
of
sporangia
was observed
by flooding
cultures with 6 ml sterile
deionized distilled water and
chilling
at 9 C for 40 min. Each treat-
ment was
repeated.
The
Phytophthora spp.
used in this
study
were as follows:
Phytoph-
thora
capsici
Leonian
(P504
Al, [ATCC
32067],
and P505s A2 [ATCC
32068],
from
pepper [Capsicum sp.])
; Phytophthora
cinnamomi Rands
(Pc97
A1,
from Camellia
sp.,
and Pc 40
A2,
from avocado
[Persea
americana
Mill.]) ;
Phytophthora megasperma
Drechs. var.
sojae
1163
MYCOLOGIA,
VOL.
68,
1976
A. A. Hildb.
(P174,
from
soybean [Glycine
max
(L.) Merr.]);
Phytophthora palmivora
(Butl.)
Butl.
(P253 A1,
P255
A2,
P376
A2,
P611
A1,
P613
A1,
P622
A1,
P623 A2, P794 A1 and P795 A2, all
from cacao
(Theobroma
cacao
L.)
and isolate P377
A1,
from Durio
zibethinus Murr. Number
designations
refer to the
Phytophthora
stock
culture collection maintained in the
Department
of Plant
Pathology,
University
of
California,
Riverside.
RESULTS
Sporangial production
of P.
palmivora,
in
general,
was
significantly
stimulated
(P
=
0.01) by
radiation in the near-UV and blue
regions
of the
spectrum (FIGS.
1-4 and
9).
There
was, also,
an
apparent
relationship
between the
intensity
of radiation and
production
of
sporangia; increasing
intensities from 8
pjW
cm-2 to 100 ,LW cm-2
generally
resulted in
greater sporangia production
in 3 of the 4 isolates
tested. The P.
palmivora
isolates from
Nigeria (FIG. 1),
Cameroon
(FIG. 2), Malaysia (FIG. 3),
Brazil
(FIG. 4),
and Central America
(FIG. 9), represented
a wide
ecological range. Phytophthora capsici
produced
abundant
sporangia
when
exposed
to radiation in the near-
UV-blue
region
of the
spectrum,
and
rarely
in darkness
(FIG. 10).
Phytophthora
cinnamomi and P.
megasperma
var.
sojae did not
produce
sporangia directly
in the
synthetic
medium under
any
condition of
light
quality
and irradiation used in this
study.
Indirect
germination
of
sporangia (i.e. by
differentiation and release of
zoospores),
of P.
pal-
mivora,
varied with the isolate
(FIGS. 5-8).
In
general, significantly
fewer
(P
=
0.01) sporangia produced
under near-UV irradiation
germinated indirectly, except
for the Cameroon isolates
(FIG. 6).
Phytophthora
cinnamomi
produced oospores
in all
regions
of the
visible and near-visible
spectrum
at 8 and 60 uW cm-2
(FIG. 11).
Oospore production
at these intensities were
significantly higher (P
=
0.05)
than that obtained in darkness. At 100 ,uW cm-2,
however,
oospore production
in all
wavelengths
was
significantly
less than in
dark-
ness
(Fig. 11).
At 8 MUW
cm-2,
in the far-red
region
of the
spectrum,
P.
capsici
and P.
palmivora
showed an increase in
oospore production
over that obtained in darkness
(FIGS.
12 and
13),
while P.
megasperma
var.
sojae (FIG. 14), produced
as
many oospores
as in darkness. The
near-UV-blue
regions
of the
spectrum
were
inhibitory
to
oospore
forma-
tion for P.
capsici (FIG. 12),
P.
palmivora
(FIG. 13),
and P.
mega-
sperma
var.
sojae (FIG. 14),
when
compared
to
oospore production
in
darkness.
Oospore production
of P. cinnamomi was
only
inhibited
at
high intensity (100
MtW
cm-2). Percentage germination
of
oospores
1164
RIBEIRO ET AL.: RADIATION AND PHYTOPHTHORA 1165
P. PALMIVORA 8eW cm-2
ISOLATES
6o
c
I
60oW
cm-2
I
IOO0/W
cm-2
200
- -
150
-
b n b
o a
z
100 -
50-
m d
d
c
0
i * * * * * * * 0*
3
c
f
c
200-
-
a
a
J
2
_
150
-
00
b
o
2
50-
cd
*
d
d
d
d
O
E
200-
-|
0.?
50
c
FIGS. 1-4. Effects of the quality and quantity of radiation on sporangia pro-
duction by isolates of P. palmivora. 1. Nigerian isolates (P611 A1, P613 A1).
2. Cameroon isolates (P794 A; P795 A2). 3. Malaysian isolates (P377 A
P374 A2). 4. Brazilian isolates (P622 A1; P623 A2). Bars having the same
letter are not significantly different from each other (P = 0.01).
*
Indicates
that sporangia produced were too numerous to count accurately by the method
employed.
Z
MYCOLOGIA,
VOL.
68,
1976
RED RED
SPECTRAL REGIONS
FIGS. 5-8. Effects of the
quality
and
quantity
of radiation on indirect
germina-
tion of
sporangia by
isolates of P.
palmivora.
5.
Nigerian
isolates. 6. Came-
roon isolates. 7.
Malaysian
isolates. 8. Brazilian isolates. Bars
having
the same
letter are not
significantly
different from each other
(P
=
0.01).
1166
I-
(.
z
0
QL
O3
-J
I-
-4
0
LJ
c_
-I
0
z
co
NEAR BLUI
UV
E
P. PALMIVORA
Jt
T,
'55
t 5
5f
rl
:
r:
,:
)
,
Z f
r
,55:
'''
,1
,
,
,..
f.
r.t
ft
...'
r'.f
r
.Z
,r:r
I
It
,
,
.t.'
,'.'.'
...'

t.
:t.
t.
..'
.'.
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15S'

t..
r

..5
t..
555
rr

r
r

(
I
...
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:...
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...
:.:.-
!!ii
::-:-
JC C
- ---
.'..
.'..
..5
.t.
(

rf;
"-'
"-'
(

'-"
"-'
.55
5'.
Z
t.

t.
.
Sf

..

..'
55

..5

.5.
.'.'.

.55

...

.'.'.

.'.'.

JC
a
K..
*--
..
i,
I
~'.*.'
1K$
;.,;

.5.
y^:
g3 8 iW cm-2
LI 60/zW cm-2
I
I
100, W
cm-2
*
a
.'.'.

.t.
...
55
r.t.
2..
.' .

.'.'.

.'.'.
,

r'Z

r'.'.

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i.
..'.

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r
f.
55
,

)
)
(
)
)
L
)
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)
,'.'.'
;'.'.'
C..'
rt

C
b
al
I
I.'
:.:.
:--:
::.::
i
C
d
I
...
I- *:.
: :
.: .
.'

I
.S

e
10
P. CAPSICI
b
C c
:
...
c
c
r7'
NEAR
UV
c
BLUE DAY-
LIGHT
RED FAR INFRA DARK
RED RED
SPECTRAL REGIONS
FIGS. 9 and 10.
Comparative
effects of the
quality
and
quantity
of radiation
on two
Phytophthora species.
9. P.
palmivora (Central
American isolates P253
A' and P255
A2).
10. P.
capsici (P504
A' and P505s
A2).
Bars
having
the same
letter are not
significantly
(P
=
0.01).
*
Indicates that
sporangia produced
were too numerous to count
accurately by
the method
employed.
200 -
9
-J
I
w
L.
a. 0
0
o
0
u
2
150 -
100 -
50-
CM
E
E
1)
200
-
CD
0
Z
150
<:
n
03
100
z
50-
.,. I
... M, ... Ii ,. . . [I-I- JI J
1167
b
e
e
_
MYCOLOGIA,
VOL.
68, 1976
0
-J
w
0
LL
0
E
o
E
10
0
o
a
0
o
2
SPECTRAL REGIONS
quality
and
quantity
of radiation on
oospore pro-
duction of four
Phytophthora
species. 11. P. cinnamomi
(Pc97
A1 X Pc40
A2).
12. P.
palmivora (P254
A1 X P255
A2).
14. P.
megasperma
var.
sojae (P174).
Bars
having
the same letter are not
significantly
(P
=
0.05).
*
Indicates that
oospores produced
were too numerous to count
accurately
by
the method
employed.
1168
RIBEIRO ET AL.: RADIATION AND PHYTOPHTHORA 1169
0o-
P. CINNAMOMI
8W
15
90
-
80 -
|i 60,iW
cm-2
70 - 0
IOO W cm-2
60 -
50-
40- a
20-
bc bc
b bc
10- b cAfl bbb
bc
1oo-
16
o00- P. CAPSICI
16
90
-
80-
70
-
s 60-
50-
z
O
40-
a
- 30
-
<
20- b
c
bc
b
b
bc
bc b
R 11L B \ [^ M \ FB c
100o- P.
PALMIVORA
17
90 -
LU
80-
EC
70-
0

60-
(n
50- 77
0
o
40-
30 -
20- b
10- b bi i n
b
100-
P. MEGASPERMA VAR. SOJAE
18
90
-
80 -
70
-
60-
a
50-
a
a
a
40 -
30
-bc
20
-
0 -.....
NEAR BLUE DAYLIGHT RED FAR INFRA DARK
UV RED RED
SPECTRAL REGIONS
quality
and
quantity
of radiation on the
percentage
germination
of
oospores
formed in irradiated cultures of four
15. P. cinnamomi. 16. P.
capsici.
17. P.
palmivora.
18. P.
megasperma
var.
sojae.
Bars
having
the same letters are not
significantly
(P
=
0.05).
MYCOLOGIA,
VOL.
68,
1976
produced
under all the
spectral regions
and intensities was low and
appeared
to be
independent
of the
quality
and
intensity
of
light
received
during gametogenesis (FIGS. 15-18). Light,
however,
is
necessary
for
germination
of
oospores produced
and matured in darkness
(2,
5, 15,
17,21,22,25,28).
DISCUSSION
Our data indicate that the
quality
and
quantity
of radiation influence
sporulation
in most
species
of
Phytophthora.
However,
the
response
to radiation is not
universally
the same for all
Even isolates of the same
species
differed in their
response
to irradiation
(FIGS. 1-4,
and
9), suggesting
that
ecological adaptation may
be a factor
in
eliciting specific photoresponses.
The
general findings
that shorter
wavelengths (312
nm-440
nm)
enhance
sporangium production
(FIGS.
1-4, 9,
10),
while
longer wavelengths (750
nm-950
nm)
stimulate
oospore production (FIGS. 11-14), agree
with
previous reports (15, 16).
The
only exception
was P.
cinnamomi,
which exhibited no
photoresponse
for
oospore production
at 8 and 60
/W
cm-2. The
relationship
between
the
quality
and
quantity
of radiation and
sporulation reported by
Binder
and
Lilly
for
Dendrophoma
obscurans
(Ell.
&
Ev.)
Anderson
(6),
and
by
Benedict for
Trichometasphaeria
turcica Luttrell
(3),
also holds
true for the
Phytophthora species
that we have examined.
Sporangium
production
increased with
increasing intensity,
while
oospore production
decreased as the
intensity
increased from 8 to 100 ,W cm-2.
However,
our
analyses
did not include a sufficient
range
of intensities to ascertain
the
validity
of the Bunsen-Roscoe law of
reciprocity
for this
fungus.
Interactions of
light
with the culture
medium,
as
might
be
expected
with
complex
natural media
(32, 35),
are
unlikely
with a
chemically
defined
medium such as the one used in this
investigation.
The
responses
to
irradiation observed can thus be
largely
attributed to the
fungus
rather
than to interactions between the
light,
culture
medium,
and the
fungus.
No
attempt
was made in this
study
to
precisely
define the
specific
wavelengths
of radiation which are involved in
eliciting sporulation,
or
the nature of the
photoreceptor(s).
A few observations,
however, can
be made. It would seem that since asexual and sexual
sporulation
are affected
by
different
regions
of the
spectrum,
more than one
photo-
receptor might
be involved. The stimulation of
sporangium production
by
both P.
palmivora
and P.
capsici
with radiation in the near-UV
region
substantiates similar
findings
with several other
fungi (4,
9, 18,
19, 20, 23, 33).
This would
suggest
a
flavoprotein
as the most
likely
photoreceptor (3, 9).
The
absorption spectra
of flavins
(maxima
at
1170
290
nm,
380
nm,
and 450 nm
(3)),
coincide with the most effective
spectral region
for
sporangia production
of
Phytophthora.
Also,
a
flavin
compound
has
recently
been shown to be the blue
light photo-
receptor
for the
photoreduction
of
cytochrome
b in
Neurospora
crassa
Shear &
Dodge (26).
A similar
system may operate
in
Phytophthora
for asexual
sporulation
since
cytochrome
b is known to be
present
in the
mycelium
of this
fungus (29).
With
oospore production,
on the
other
hand,
the data would
suggest
the
presence
of a
photolabile
com-
pound
since the
higher intensity (100 ,/W cm-2)
inhibits
oospore
formation.
Also,
the lack of
cytochrome
b in
oospores (29),
and the
photoresponse
in the far-red
wavelengths
for sexual
reproduction
would
appear
to
preclude
a mechanism similar to that involved in asexual
reproduction,
as
postulated
for
Pleospora
herbarum
(Fr.)
Rab.
(20).
ACKNOWLEDGMENT
This
study
was
supported
in
part by
National Science Foundation
Grant PCM-7419982.
LITERATURE CITED
1.
Aragaki, M.,
and R. B. Hine. 1963. Effect of radiation on
sporangial pro-
duction of
Phytophthora parasitica
on artificial media and detached
papaya
fruit.
Phytopathology
53: 854-856.
2.
Banihashemi, Z.,
and
J.
E. Mitchell. 1976. Factors
affecting oospore ger-
mination in
Phytophthora cactorum,
the incitant of
apple
collar rot.
Phyto-
pathology
66: 443-448.
3.
Beinert,
H. 1960. Flavin
coenzymes. Pp.
340-416. In P. D.
Boyer,
H.
Lary,
and K.
Myrback,
Eds. The
enzymes,
Vol. 2. Academic
Press,
New
York.
4.
Benedict,
W. G. 1975.
Light-dependent morphogenesis
of conidia of Tricho-
metasphaeria
turcica in vitro. Canad. J. Bot. 54: 552-555.
5.
Berg,
L.
A.,
and M. E.
Gallegly.
1966. Effect of
light
on
oospore germina-
tion in
species
of
Phytophthora. Phytopathology
56: 583
(Abstr.)
6.
Binder,
F.
L.,
and V. G.
Lilly.
1976.
Qualitative
and
quantitative
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Accepted
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publication June 14,
1976
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