Effects of phosphate fertilization, lime amendments and inoculation with VA-mycorrhizal fungi on soybeans in an acid soil


Maddox, J.; Soileau, J.

Developments in Plant and Soil Sciences 134(1): 83-93

1991


Soybeans [Glycine max (L.) Merr. cv. Essex] were grown in nonsterile acid (pH. 5.2) infertile Wynnville silt loam (Glossic Fragiudult) in a glasshouse. The effects of P fertilization and lime were determined by inoculation with two VAM-fungi (VAMF): Glomus fasciculatum (Gf) and Glomus etunicatum (Ge). An important factor affected by the interaction between applied lime (soil acidity), applied P, and VAMF inoculation was the soil Al. Five application rates of P as KH2PO4 and three rates of lime were tested. Potassium was equalized with KCl (muriate of potash). P-efficiency (g seed/mg P kg-1 soil) by vesicular-arbuscular mycorrhiza (VAM) was maximal at 20 mg P kg-1 soil at all lime and VAMF treatments. VAMF inoculation increased plant survival and protected the soybeans from leaf scorch, thereby substituting for the effects of lime and P. The Ge inoculum was superior in ameliorating leaf scorch in the nonlimed soil. The Gf inoculum required more lime and P than the Ge inoculum to increase seed yield relative to the noninoculated controls containing only native VAMF. Both inocula increased root Al uptake and extractable soil Al in the acid soil without apparent adverse effects on root or shoot. The ability of the VAMF inocula to enhance the efficiency of applied P and decrease seed Cl concentration was increased by lime. Seed yield (Y) was negatively related to seed Cl concentration (X) where Y = aX-b. Both VAMF inoculation and lime application reduced this negative relationship and may have increased the tolerance to both Cl and soil Al.

Plant
and
Soil
134:
83-93,
1991.
©
1991
Kluwer
Academic
Publishers.
Printed
in
the
Netherlands.
PLSO
AS23
Effects
of
phosphate
fertilization,
lime
amendments
and
inoculation
with
VA-mycorrhizal
fungi
on
soybeans
in
an
acid
soil
J.J.
MADDOX
and
J.M.
SOILEAU
National
Fertilizer
and
Environmental
Research
Center,
Tennessee
Valley
Authority,
NFE
2K-M,
Muscle
Shoals,
AL
35660,
USA
Key
words:
aluminium,
chloride,
Glomus
etunicatum,
Glomus
fasciculatum,
Glycine
max,
lime,
potassium
phosphate,
soil
pH
Abstract
Soybeans
[Glycine
max
(L.)
Merr.
cv.
Essex]
were
grown
in
nonsterile
acid
(pH.
5.2)
infertile
Wynnville
silt
loam
(Glossic
Fragiudult)
in
a
glasshouse.
The
effects
of
P
fertilization
and
lime
were
determined
by
inoculation
with
two
VAM-fungi
(VAMF):
Glomus
fasciculatum
(Gf)
and
Glomus
etunicatum
(Ge).
An
important
factor
affected
by
the
interaction
between
applied
lime
(soil
acidity),
applied
P,
and
VAMF
inoculation
was
the
soil
Al.
Five
application
rates
of
P
as
KH
2
PO
4
and
three
rates
of
lime
were
tested.
Potassium
was
equalized
with
KC1
(muriate
of
potash).
P-efficiency
(g
seed/mg
P
kg
-1
soil)
by
vesicular-arbuscular
mycorrhiza
(VAM)
was
maximal
at
20
mg
P
kg
-1
soil
at
all
lime
and
VAMF
treatments.
VAMF
inoculation
increased
plant
survival
and
protected
the
soybeans
from
leaf
scorch,
thereby
substituting
for
the
effects
of
lime
and
P.
The
Ge
inoculum
was
superior
in
ameliorating
leaf
scorch
in
the
nonlimed
soil.
The
Gf
inoculum
required
more
lime
and
P
than
the
Ge
inoculum
to
increase
seed
yield
relative
to
the
noninoculated
controls
containing
only
native
VAMF.
Both
inocula
increased
root
Al
uptake
and
extractable
soil
Al
in
the
acid
soil
without
apparent
adverse
effects
on
root
or
shoot.
The
ability
of
the
VAMF
inocula
to
enhance
the
efficiency
of
applied
P
and
decrease
seed
Cl
concentration
was
increased
by
lime.
Seed
yield
(Y)
was
negatively
related
to
seed
Cl
concentration
(X)
where
Y
=
aX
-b
.
Both
VAMF
inoculation
and
lime
application
reduced
this
negative
relationship
and
may
have
increased
the
tolerance
to
both
Cl
and
soil
Al.
Introduction
A
primary
reason
for
liming
acid
soils
is
to
increase
phosphate
availability
to
plants
(Haynes,
1982).
However,
conflicting
reports
and
variable
results
may
be
attributed
to
differ-
ences
in
the
amount
of
exchangeable
Al-ions
in
the
soils
used.
The
phosphate
adsorbing
surfaces
offered
by
precipitated
insoluble
polymeric
hy-
droxy-Al
cation
species
can
reduce
P
availability.
Wetting
and
drying
of
limed
soil
influences
the
formation
and
surface
characteristics
of
such
ad-
sorption
sites
in
the
soil.
Adding
P
fertilizer
to
a
freshly
limed
acid
soil
can
fail
to
increase
P
availability
if
the
soil
is
not
first
subjected
to
drying
cycles
(Haynes,
1982).
The
implication
of
this
fact
is
obvious
for
greenhouse
studies
as
well
as
for
the
correct
timing
of
lime
and
P
amend-
ments
to
certain
field
soils
when
the
right
soil
moisture
conditions
are
present.
The
benefits
of
lime
in
highly
weathered
acid
soils
are
largely
related
to
the
reduction
of
soluble
and
exchange-
able
Al
and
Mn
by
precipitation
which
alleviates
phytotoxic
levels
and
enhances
the
availability
of
P.
The
stimulatory
effects
of
P
fertilizer
are
not
always
obvious
since
lime
and
P
can
interact
with
each
other
augmenting
plant
growth
without
af-
fecting
tissue
concentrations
of
P.
Both
lime
and
P
could
affect
a
third
soil
factor
influencing
plant
growth
but
the
mechanism
of
this
influence
by
84
Maddox
and
Soileau
lime
could
be
different
from
that
by
P
Raju
et
al.
(1988)
found
vesicular-arbuscular
mycorrhiza
fungi
(VAMF)
development
on
sorghum
cul-
tivars
was
reduced
in
an
acid
soil
with
high
Al,
thereby
probably
reducing
the
VAM
activity.
Angle
and
Heckman
(1986)
found
that
heavy
metal
content
of
municipal
sludge
was
generally
not
related
to
VAM
development
but
was
a
factor
when
applied
to
a
soil
with
a
low
pH.
The
edaphic
effects
of
soil
Al
and
heavy
metal
con-
tent
of
municipal
sludge
are
apparently
examples
of
factors
that
are
not
directly
related
to
VAM
development
or
VAM
activity
unless
the
soil
is
acidic.
Soil
acidity
(pH
<
5.3)
reduced
the
infection
and
development
of
Glomus
sp.
(WUM
16)
in
clover
roots
(Trifolium
subterraneum
L.
cv.
Sea-
ton
Park),
but
soil
pH
had
little
effect
on
Glomus
fasciculatum
(Abbott
and
Robson,
1985).
Skipper
and
Smith
(1979)
found
the
Bos-
sier
soybean
cultivar
responsive
to
inoculation
with
Gigaspora
gigantec
in
nonlimed
soil
(pH
5.1),
but
not
to
inoculation
with
Glomus
mos-
seae.
In
limed
soil
(pH
6.2),
good
plant
re-
sponses
were
obtained
with
Glomus
mosseae.
Different
endophytes
can
vary
enormously
in
their
symbiotic
effectiveness
at
different
soil
pH
(Hayman
and
Tavares,
1985).
Davis
et
al.
(1983)
have
suggested
that
host
plants
should
be
match-
ed
with
VAMF
species
adapted
to
particular
soil
and
climatic
conditions
to
obtain
maximum
ben-
efit
from
a
mycorrhizal
association.Root
coloni-
zation
on
alfalfa
(Medicago
sativa)
by
indigenous
VAMF
was
inhibited
by
high
soil
pH
(7.2-7.5),
but
the
same
soil
pH
stimulated
root
coloniza-
tion
by
inoculated
species
whereas
a
lower
soil
pH
(5.4-6.1)
was
inhibitory
to
the
introduced
species
of
VAMF
(Kucey
and
Diab,
1984).
Root
colonization
can
be
decreased,
be
increased,
or
remain
unchanged
by
the
addition
of
soluble
P
to
a
soil,
depending
on
the
resultant
level
of
avail-
able
soil
P
for
a
given
crop
and
VAMF
species
(Bolan
et
al.,
1984).
It
is
possible
to
achieve
a
plant
response
to
VAMF
inoculation
even
in
the
presence
of
infective
and
active
native
VAMF
(Barea
et
al.,
1980).
Medina
et
al.
(1988)
con-
cluded
that
increases
in
plant
growth
can
be
achieved
over
practical
ranges
of
P
amendments
with
effective
VAMF
inocula.
Soil
characteristics
such
as
P-fixing
capacity,
VAMF
composition,
mineralogy,
and
fertility
level
necessitate
testing
selected
VAMF
species
for
their
efficiency
with
P
fertilization
(Pacovsky
and
Fuller,
1986;
Sainz
and
Arines,
1988)
and
lime
response
(Newbould
and
Rangely,
1984).
Response
of
sweet
sorghum
[Sorghum
bicolor
(L.)
Moench]
and
soybean
[Glycine
max
(L.)
Merr.]
in
field
experiments
conducted
from
1980
through
1982
on
an
acid
infertile
Wynnville
silt
loam
(fine-loamy
siliceous,
thermic
Glossic
Fragiudult)
in
Lawrence
County,
Alabama,
indi-
cated
that
high
rates
of
applied
P
(as
triple
superphosphate)
may
have
neutralized
most
of
the
adverse
effects
of
soil
acidity
(Soileau
and
Bradford,
1985).
The
purpose
of
this
study
was
to
examine
some
of
the
edaphic
effects
(soil
acidity)
and
influence
of
P
fertilization
in
this
nonsterile
Wynnville
soil
on
soybeans
inoculated
with
two
vesicular-arbuscular
mycorrhizal
fungi
(VAMF)
Glomus
etunicatum
and
Glomus
fas-
ciculatum.
Methods
Soil
Wynnville
silt
loam
(Glossic
Fragiudult)
soil
from
the
Ap
horizon
(0-15
cm
depth)
was
used
in
this
experiment.
This
acid
surface
soil
(aver-
age
pH
=
4.9)
is
low
in
cation
exchange
capacity
(CEC
=
4.3
cmol
kg
-1
)
and
organic
matter
(10
g
kg
-1
).
Exchangeable
Ca,
Mg,
K,
and
Mn
(neu-
tral
1
M
NH
4
O
Acetate)
was
0.70,
0.25,
0.16,
and
0.05
cmol
kg
-1
respectively.
Extractable
Al
(1
M
KCl)
and
extractable
P
by
the
Mehlich
1
double
acid
method
(0.5
M
HCl
+
0.013
M
H
2
SO
4
)
was
76
and
4
mg
kg
-1
.
Soil
amendments
The
experiment
was
set
up
in
June
1983
with
three
lime
treatments,
five
P
levels,
two
VAM
inoculants,
and
four
replications
aligned
into
randomized
complete
blocks.
The
experiment
was
conducted
in
an
evaporative
cooled
glass-
house
with
non-draining
plastic
pots
containing
6
kg
of
soil.
Greenhouse
temperatures
were
maintained
within
2
to
3°C
of
ambient
tempera-
tures,
and
plants
were
watered
daily
with
dis-
tilled/dionized
water
by
weight
to
maintain
18%
Soil
and
fertilizer
effects
on
mycorrhizal
soybean
85
moisture.
Lime
as
4:1
CaCO
3
:MgCO
3
was
added
at
rates
of
0,
1.5,
or
3.0
g
kg
-1
soil
in
bulk,
and
equilibrated
in
two
wetting/drying
cy-
cles
for
two
weeks.
Phosphorus
was
applied
as
KH
2
PO
4
to
6
kg
soil
in
greenhouse
pots
and
mixed
at
rates
of
0,
20,
40,
80,
or
160
mg
P
kg
-1
.
The
soil
pH
before
adding
the
fertilizer
was
5.2,
6.0,
and
7.8.
Sufficient
potassium
was
added
as
KC1
to
403
mg
K
kg
-1
of
soil
within
these
five
P
treatments
by
adding
half
of
the
KC1
at
preplant
and
the
remainder
40
days
after
planting.
A
micronutrient
mix
was
added
to
all
treatments
containing
33
mg
Fe,
18
mg
Zn,
9
mg
Cu,
0.9
mg
B,
1.2
mg
Mo,
and
33
mg
S
pot
1
.
Concentrated
superphosphate
[CSP,
Ca-
(H
2
PO
4
)
2
2H
2
0]
or
potassium
phosphate
[KP,
KH
2
PO
4
]
was
applied
to
another
lime
series
at
a
rate
of
320
mg
P
kg
-1
of
soil.
Pots
with
this
high
rate
of
P
from
CSP
(nonpotassium
source)
re-
ceived
the
same
rate
K
as
the
first
series
as
KC1
(nonphosphate
source)
to
equalize
the
K
(403
mg
K
kg
-1
soil)
with
pots
receiving
KH
2
PO
4
(non-
chloride
source).
Two
sets
of
control
treatments
for
this
PK
fertilizer
rate
in
this
lime
series
re-
ceived
either
no
fertilizer
or
only
KC1
plus
micro-
nutrients.
Inocula
consisted
of
20
g
of
mixed
propagules
reared
on
soybean
(cv.
Essex)
or
soil
from
VAM
free
pot
cultures
from
nurse
pots
which
received
no
VAMF
inoculum.
The
fungi
used
were
Glomus
fasciculatum
(Thaxter
sensu
Gerd.)
Ger-
demann
and
Trappe
purchased
from
Abbott
Laboratories
and
Glomus
etunicatum
Becker
and
Gerdemann
isolated
from
pot
cultures
obtained
from
International
Paper
Company
at
Natchez,
Mississippi.
All
inocula
were
mixed
through
the
soil
with
the
fertilizer
amendments.
Measurements
Soybeans
[Glycine
max
(L.)
Merr.
cv.
Essex]
were
seed
coated
with
a
commercial
inoculum
of
Rhizobium
japonicum
without
Mo
and
planted
with
12
seeds
per
pot.
Plants
were
thinned
to
three
seedlings
per
pot,
watered
daily
to
18%
soil
moisture,
and
grown
to
maturity.
Plant
parts
were
weighted
after
drying
at
70°C
and
ground
in
a
Wiley
mill
(40-mesh
screen).
Plant
P
content
was
determined
by
the
vanadate
P
method
from
dry
ash.
Plant
and
soil
Cl
was
determined
with
an
Orion
specific
ion
electrode
after
extracting
0.6
g
of
plant
tissue
with
50
mL
of
0.5
M
HNO
3
and
5.0
g
of
soil
with
40
mL
of
0.1
M
NaNO
3
(Gaines
et
al.,
1984;
Islam
et
al.,
1983).
Plant
Al
and
soil
Al
were
determined
with
inductively
coupled
emission
spectroscopy
after
extracting
1.0
g
of
plant
tissue
with
25
mL
of
6.0
M
HNO
3
and
1.0
g
of
soil
with
1.0
M
KC1.
Extractable
P
was
determined
by
the
Mehlich
1
(double
acid)
extraction
procedure.
Roots
were
cleared
and
stained
with
trypan
blue
for
microscopic
exami-
nation
(Phillips
and
Hayman,
1970)
for
deter-
mining
the
percentage
of
roots
colonized
(classi-
fication).
One
to
2
g
of
root
were
cut
into
uni-
form
lengths
and
examined
and
counted
using
the
line
intersect
method.
Roots
were
rated
for
intensity
of
the
colonization
as
low
=
1,
medium
=
2,
or
high
=
3.
Pots
were
arranged
in
a
randomized-block
de-
sign
and
rotated
weekly
within
the
blocks
to
minimize
the
positional
effects.
Data
were
sub-
jected
to
analysis
of
variance
and
Duncan's
mul-
tiple
range
test
and
least
significant
difference
to
test
the
difference
between
treatment
means.
Results
General
A
positive
response
to
P
fertilization
through
160
mg
P
kg
-1
at
all
lime
levels
was
apparent
within
2
weeks
after
seedling
emergence.
A
lime
response
was
evident
in
the
zero-P
treatments
after
4
weeks
of
growth.
This
positive
response
to
P
fertilization
and
lime
application
persisted
into
plant
maturity
to
give
significant
increases
in
seed
yield.
Beginning
at
4
weeks
of
growth,
leaf
chlorosis
appeared
in
the
nonlimed,
zero-,
and
low-P
treatments
which
received
KC1
and
mi-
cronutrients.
After
7
weeks
of
growth
these
plants
exhibited
many
scorched
leaves,
with
de-
foliation
evident
in
the
older
leaves;
at
8
weeks
some
plants
in
this
treatment
were
dead.
Lime,
P
fertilization,
and
VAMF
inoculation
all
dimin-
ished
leaf
chlorosis
and
reduced
leaf
scorching.
VAM
inoculation
and
P
fertilization
increased
the
survival
of
soybean
seedlings
in
the
nonlimed
soil.
G.
etunicatum
was
more
effective
than
G.
fasciculatum
in
ameliorating
foliar
damage.
Glomus
etunicatum
Glomus
fasciculatum
0
None
Lime
=
0
NS
NS
NS
NS
NS
1p
S
r
S
$
Lime
=
1.5
g
kg
-1
NS
A
Lime
=
3.0
g
kg
-1
NS
AB
B
NS
I
S
NO
BB
A
B
A
NS
s
P
NS
p
g
s
NS
p
NO
0
20
40
80
160
86
Maddox
and
Soileau
Yield
Seed
yield
was
not
significantly
increased
by
VAMF
inoculation
in
the
nonlimed
soil
within
any
given
rate
of
P
but
was
generally
increased
over
all
rates
of
P
(Fig.
1).
In
the
medium
pH
soil
and
at
the
highest
P
rate
(160
mg
P
G.
etunicatum
inoculum
increased
seed
yield
over
the
noninoculated
soil
by
27%,
but
its
effect
was
not
significantly
different
from
that
of
G.
fasciculatum.
Similarly,
in
the
high
pH
soil
with
less
applied
P
(80
mg
P
kg
-1
),
G.
etunicatum
increased
seed
yield
over
the
noninoculated
soil
by
33%,
but
again
the
effects
of
two
inocula
were
not
significantly
different.
In
the
high
pH
soil
with
the
highest
rate
of
applied
P,
however,
inoculation
with
G.
fasciculatum
did
increase
seed
yield
approximately
20%
compared
to
other
inoculation
treatments.
G.
fasciculatum
in
the
latter
treatment
also
increased
the
seed
yield
17%
over
the
comparable
high
P
treatment
in
the
medium
soil
pH.
G.
fasciculatum
is
apparent-
ly
more
basophilic
at
high
rates
of
P
than
G.
etunicatum.
With
the
high
lime
treatment,
G.
etunicatum
inoculation
increased
seed
yield
by
40
••••••
1
5
0
0.
40
173
.
42)
20
(1)
0
co
60
40
20
P
Rate
(
mg
ke
Fig.
1.
Effect
of
lime,
P
fertilization,
and
VAMF
inoculation
on
seed
yield.
Letters
denote
significance
(P
=
0.05)
within
the
lime
and
P
treatment.
NS
=
nonsignificant.
273%
without
any
fertilizer
P.
G.
etunicatum
apparently
requires
less
available
P
to
produce
a
significant
increase
in
seed
yield
over
the
noninoculated
controls
(with
indigenous
native
VAMF-spp.)
in
an
alkaline
soil
pH.
Chloride
Leaf
chloride
was
not
analyzed
but
electrical
conductivity
in
the
soil
(EC)
was
below
1.5
dS
m
1
and
was
well
below
what
is
considered
to
be
the
safe
range
of
salinity
EC
values.
Seed
Cl
concentrations
indicate
that
Cl
was
the
probable
cause
of
leaf
scorch
in
nonlined
soil
without
VAMF
inoculation
and
applied
P.
Seed
yield
and
concentration
of
Cl
in
the
seed
were
negatively
related
(Fig.
2)
by
the
function
Y
=
aX
-b
where
Y
=
yield
(g
pot
-1
)
and
X
=
seed
Cl
(mg
b
is
the
change
in
yield
relative
to
the
change
in
seed
Cl,
and
a
is
the
factor
that
expresses
the
scale
of
the
relationship
of
seed
yield
to
seed
Cl.
Both
the
VAM
inoculation
and
lime
reduced
the
negative
correlation
by
reducing
the
a
and
b
terms
of
this
relationship.
The
critical
threshold
of
this
relationship,
where
seed
yield
is
no
longer
negatively
correlated
with
seed
Cl,
is
shifted
to
a
lower
concentration
of
seed
Cl
by
the
use
of
lime
and
VAMF
inoculum.
Phosphorus
The
efficiency
of
fertilizer
P
was
calculated
as
g
of
seed
yield
(pot
basis)
mg
-1
of
P
applied
per
kg
of
soil
(Fig.
3).
The
efficiency
of
fertilizer
P
declines
with
increasing
P
rates
to
values
be-
tween
(0.2-0.4)
at
the
highest
level
of
applied
P
used
(160
mg
kg
-1
)
regardless
of
the
lime
level.
The
main
effect
of
lime
was
to
increase
the
efficiency
of
applied
P
at
the
lower
P
rates,
but
too
much
potential
yield
must
be
sacrificed
at
these
rates
of
P
fertilization.
Inoculation
with
mycorrhizal
fungi
increased
the
efficiency
of
inherent
soil
P
and
applied
P
at
all
lime
and
P
rates
tested
in
this
study
(Fig.
3).
VAMF
colonization
No
significant
effect
of
P
rate
or
P
rate
x
lime
were
detected
in
this
study
on
the
percentage
of
roots
colonized
by
VAMF
or
VAM
development
as
measured
by
the
intensity
of
VAMF
root
colonization.
A
significantly
higher
percentage
of
roots
were
colonized
when
inoculated
with
G.
60
O
30
a.
I
10
-a
>••
50
a)
co
30
Lime=3.0
(
g
kg
)
LSD
(
P
=
0.05
)
I
S
-------
............
..
I
I I
1.2
0.8
0.4
CD
0.8
a)
O
0.4
a
0
50
100
150
0
50
100
150
-••••*--
-
Glomusiasciculatum
•••••••••None
0
0
Lime=0
LSD
(
P
=
0.05
)
I
I I
0
50
100
150
0
0.8
0.4
1.2
Lime=1.5
(
g
kg
-1
)
LSD
(
P
=
0.05
)
I
Inoculum:
•-•••••••
Glomus
etunicatum
Soil
and
fertilizer
effects
on
mycorrhizal
soybean
87
50
Noninoculated
-b
Y-
,
aX
,
where
a>0
R
2
a
a
Soil
pH
Range:
-•--
5.3
-
5.1
(Low)
0.87
98489
1.448
-'-•---
7.1
-
5.8
(Med)
0.82
64395
1.509
7.8-
6.7
(High)
0.84
21013
1.248
..
----
-
-911-
Glomus
etunicatum
Soil
pH
Range
R
2
a
(Low)
0.95
35262
1.137
(Med)
0.93
20115
1.144
(High)
0.42
1166
0.690
10
-
0
0
200
400
600
800
1,000
1,200
Seed
CI
(
mg
kd
l
)
Fig.
2.
Relationship
between
seed
CI
concentration
and
seed
yield
as
affected
by
soil
acidity
mycorrhizal
inoculation.
range
during
the
test
and
P
Rate
(
mg
k6
1
)
Fig.
3.
Efficiency
of
fertilizer
P
and
lime
upon
soybean
seed
yield
with
and
without
inoculation
with
VAMF.
Efficiency
of
applied
P
=
g
seed
yield
(pot
basis)
per
mg
applied
P
in
1
kg
of
soil.
fasciculatum
compared
to
the
controls,
but
there
was
no
significant
difference
in
root
colonization
among
the
two
Glomus
species
(Table
1).
G.
fasciculatum
also
gave
a
62
to
68%
higher
classi-
fication
score
on
root
colonization
compared
to
G.
etunicatum
or
the
noninoculated
controls
in
the
high
pH
soil
(4.2
vs.
2.6
or
2.5).
The
princi-
pal
indigenous
VAMF
spores
identified
in
the
test
soil
were
of
Gigaspora
coralloidea
(37
per
10
g
soil)
in
the
nonlimed
treatment,
but
the
limed
treatment
had
a
minimal
number
of
spores
of
this
species.
Several
unidentified
types
of
VAMF
spores
were
also
found
in
this
soil.
One
unknown
VAMF
species
had
small
red-brown
spores
similar
to
Sclerocytis
rubiformis
(35
per
10
g
soil)
and
was
prevalent
regardless
of
applied
P
or
lime
rate.
Another
unknown
VAMF
species
with
yellow
spores
was
prevalent
only
in
limed
Lime
Intensity
a
Classification
b
(g
kg
1
)
Inoculum
Inoculum
88
Maddox
and
Soileau
Table
1.
Intensity
and
classification
of
root
infection
by
VAMF
as
affected
by
lime
and
the
inoculant
Gf
Ge
None
Gf
Ge
None
0
1.6
a
1.4
a
1.6
a
2.4
a
2.0
a
2.4
a
1.5
2.0
a
2.0
a
1.4
a
3.4
b
3.4
a
2.0
a
3.0
2.6
a
2.0
a
1.6
a
4.2
a
2.6
ab
2.5
a
Avg
2.1
1.8
1.5
3.3
2.7
2.3
P
=
0.5
A
AB
B
A
AB
B
Intensity;
1
=
least,
2
=
average,
3
=
most.
b
Classification;
1
=
0-5%;
2
=
6
-
26%;
3
=
26-50%;
4
=
51-
75%;
5
=
76-100%.
Gf
=
Glomus
fasciculatum;
Ge
=
Glomus
etunicatum.
Lower
case
letters
within
a
column
indicate
significant
differ-
ences
due
to
lime
(P
=
0.05);
capital
letters
within
a
row
of
average
values
indicate
significant
differences
due
to
in-
oculum.
soil
(20
per
10
g
soil).
Recoverable
numbers
of
spores
of
the
inoculated
species
were
not
affect-
ed
by
the
rate
of
applied
P
and
none
were
recovered
from
the
noninoculated
controls.
Ap-
proximately
five
times
more
spores
of
G.
etunicatum
(4
vs.
19
per
10
g
soil)
were
re-
covered
from
the
high
lime
soil
treatment
than
from
the
nonlimed
soil,
but
lime
did
not
affect
the
recoverable
number
of
spores
of
the
G.
fasciculatum
which
averaged
39
per
10
g.
Root
weight
was
increased
by
the
first
incre-
ment
of
applied
P
in
all
lime
treatments
except
for
the
G.
etunicatum
and
noninoculated
treat-
ments
in
the
high
lime
soil
(Table
2).
The
com-
bined
effect
of
each
VAMF
inoculum
with
the
high
lime
treatment
nearly
doubled
the
root
weight
when
P
was
applied.
The
lower
lime
rate
caused
lower
root
weights
than
the
zero-
and
the
highest
lime
rate.
A
small
reduction
in
root
weight
was
observed
when
inoculum
of
G.
etunicatum
was
used
without
lime
and
with
160
mg
P
kg
-1
.
P
and
Al
uptake
Uptake
of
P
and
Al
(Fig.
4)
into
roots
shows
a
pattern
of
increased
uptake
with
the
increasing
P
rate
at
all
lime
levels.
The
uptake
of
both
P
and
Al
was
lowest
in
the
medium
soil
pH.
At
the
20
mg
kg
-1
P
rate
in
nonlimed
soil,
the
noninoculated
treatment
(containing
only
in-
digenous
VAMF
propagules)
had
a
higher
root
P
Table
2.
Effect
of
P
rate,
mycorrhizal
inoculation,
and
lime
on
root
weight
P
rate
(mg
kg
Inoculum
LSD
.
)
Gf
Ge
None
Lime
0
0
2.3b
4.9c
3.2c
NS
20
9.1
a
8.8
b
11.0
b
NS
40
11.0a
10.1
ab
10.7b
NS
80
15.4a
10.2
ab
11.7
ab
NS
160
15.7
a
10.8
a
14.1
a
2.3
Avg
10.7
A
9.0
A
10.1
A
Lime
(1.5
g
kg
-'
)
0
2.8
b
3.3
c
1.7
c
NS
20
6.9
a
7.1
b
6.6
b
NS
40
7.6
a
7.0
b
7.0
ab
NS
80
7.5
a
7.9
b
6.4
b
NS
160
9.2
a
11.4
a
10.1
a
NS
Avg
6.8
A
7.3
A
6.4
A
Lime
(3.0
g
kg
-
')
0
6.1
b
12.4
a
5.1
b
5.0
20
16.9
a
17.6
a
7.4
ab
5.3
40
13.7
ab
17.9
a
9.6
a
4.8
80
19.6
a
16.1
a
7.8
ab
10.2
160
15.9
a
18.9
a
8.2
ab
6.5
Avg
14.4
A
16.5
A
7.6
B
Gf
=
Glomus
fasciculatum;
Ge
=
Glomus
etunicatum.
Means
followed
by
the
same
uppercase
letter
within
a
row
and
lowercase
letter
within
a
column
are
not
significantly
differ-
ent
(P
=
0.05).
uptake
than
that
of
both
inoculated
treatments,
whereas
in
this
nonlimed
soil
fertilized
with
160
mg
P
kg
-1
,
the
G
fasciculatum
inoculum
was
superior.
VAMF
inoculation
did
not
affect
the
root
P
uptake
in
the
medium
limed
soil,
but
in
the
highest
lime
treatment,
it
increased
the
root
P
uptake
at
the
20
and
160
mg
P
kg
-1
rates.
Both
VAMF
inocula
increased
root
Al
uptake
compared
with
indigenous
VAMF
at
all
P
and
lime
rates
(Fig.
4).
However,
there
was
no
vis-
ible
evidence
of
Al
toxicity
due
to
VAMF
inocu-
lation.
In
the
nonlimed
soil
fertilized
with
160
mg
P
kg
-1
,
root
Al
uptake
was
significantly
lower
when
inoculated
with
G.
etunicatum
than
with
G.
fasciculatum.
The
average
root
uptake
of
Al
was
higher
with
G.
etunicatum
than
with
G.
fasciculatum
in
the
limed
soil
and
was
signifi-
cantly
higher
at
the
zero
and
40
mg
P
kg
-1
with
the
high
lime
rate.
Lime
or
applied
P
did
not
affect
the
uptake
of
Al
into
roots
of
the
noninoculated
controls.
7
;
25
Ume=O
............
Ume=1.5
g
kg
Ume=3.0
g
kg
15
I
NS
NS
NS
5
0.-
0
.
15
NS
NS
µs
µs
............
5
.4.0.616
661,66
0
160
80
80
160
1
:
6
15
a.
5
0
0
20
40
20
40
80
1
160
0
20
40
P
Rate
(
mg
kg
)
250
Ume=0
250
O.
150
150
50
=
50
.7
0
0
. '
8
1
0
160
°
Ume=1.5
g
kg
0
20
40
80
160
Ume=3.0
g
ka
l
150
°
0
20
40
80
160
80
60
40
20
0
0
20
40
80
160
Lime
=
0
....
.......
Lime
=
1.5
(
g
kg')
.......
........
0
0
20
40
80
160
0
0
20
40
80
160
P
Rate
(
mg
kg
1
)
120
.................
80
/
Lime=
3.0
(
g
kg
1
)
40
....
A
0
0
20
40
80
160
120
It
80
E
40
4
... ...
Ume
=
0
120
80
40
Soil
and
fertilizer
effects
on
mycorrhizal
soybean
89
Root
P
Uptake
Inoculum:
Glomus
tasciculatum
Glomus
etunicatum
•••••••
None
Root
Al
Uptake
P
Rate
(
mg
kg
1
)
Fig.
4.
Influence
of
lime,
phosphorus
fertilization,
and
VAMF
inoculation
on
total
root
phosphorus
and
aluminium
uptake.
Bars
=
LSD
(P
=
0.05).
Extractable
soil
P
at
the
end
of
the
experiment
was
increased
by
increasing
P
rates
at
all
lime
levels
in
both
inoculated
and
noninoculated
treatments
(Fig.
5).
In
the
medium
lime
rate
at
the
highest
rate
of
P,
extractable
soil
P
was
approximately
35
mg
P
kg
-1
in
both
of
the
inocu-
lated
treatments,
and
78
mg
P
kg
-1
)
in
the
noninoculated
soil.
At
the
end
of
the
experi-
ment,
lime
had
little
effect
on
the
extractable
soil
P
except
in
the
noninoculated
soil.
Compared
with
nonlimed
soil,
extractable
soil
Al
was
reduced
by
a
factor
of
approximately
10
Extractable
Soil
P
CA
E
0.
8o
60
Lime
=
1.5
(
40
20
40
80
160
80
60
40
20
0
0
20
40
0
0
20
80
160
,
Lime
=
3.0
(
gkf
l
)
.............
•••••••i•
P
Rate
(
mg
kg
1
)
Inoculum
Glomus
tascicutatum
-
Glomus
etunicatum
None
Extractable
Soil
Al
X
10
0
X10
1
X10
2
Fig.
5.
Influence
of
lime,
phosphorus
fertilization,
and
mycorrhizae
inoculation
on
soil
extractable
phosphorus
(Melich
I)
and
aluminium
(1.0
N
KC1)
after
cropping.
Extractable
Al
is
graphed
on
different
concentration
scales
between
the
three
lime
treatments.
Soil
Aluminum
I .1
I
KM
L.
a
W.
None
KCI
Caffif04IKCI
KHE0
4
(
mg
kg
1
)
P
P
=
0
P
320
P
320
K=0
K
403
K
403
K
403
CI.
0
CI
=
365
CI
365
CI=
0
90
Maddox
and
Soileau
at
the
medium
lime
level
and
by
a
factor
of
100
at
the
high
lime
level
(Fig.
5).
Both
inoculants
gave
similar
results
in
producing
higher
extract-
able
soil
Al
in
the
nonlimed
soil
and
lower
values
of
extractable
soil
Al
in
the
high
limed
soil
as
compared
to
the
noninoculated
controls.
The
large
effect
of
VAM
inoculation
on
extractable
soil
Al
may
be
relatively
unimportant
in
the
limed
treatments
because
of
the
low
values
of
extractable
soil
Al.
Effect
of
fertilizer
source
In
an
attempt
to
understand
these
results
on
extractable
soil
aluminium,
we
compared
two
sources
of
P
fertilizer:
concentrated
superphos-
phate
or
CSP
[Ca(H
2
1
3
0
4
)
2
2H
2
O]
and
potas-
sium
phosphate
or
KP
[KH
2
PO
4
].
Fertility
prac-
tices
for
soybeans
commonly
include
muriate
of
potash
(KC1)
and
CSP
as
the
K
and
P
sources
Seed
C
Yield
I-
Z
4
e
CI
NS
tli
0
A A
B
NS
/
NS
\
.L
NS
\/
4—de•
AB
A
Seed
NS
Chloride
Lime:
(
g
)
None
0
1.5
0
3.0
Fertilizer
Fig.
6.
Effect
of
P,
K
and
Cl
fertilization
on
soybean
seed
yield,
seed
chloride,
and
extractable
soil
aluminium
(1.0
N
KCI).
Letters
denote
significance
(P
=
0.05)
within
the
lime
and
fertilizer
treatment.
NS
=
nonsignificance.
unless
potash
of
sulfur
(K
2
SO
4
)
is
the
choice
for
both
K
and
S
or
if
one
wants
to
avoid
the
use
of
Cl.
Comparing
CSP
+
KCl
with
the
treatments
re-
ceiving
no
P
or
K
fertilizer
(Fig.
6),
there
was
a
relatively
small
response
in
seed
yield
to
the
added
P
and
a
sizable
increase
in
yield
in
the
highest
lime
treatment.
Extractable
soil
Al
was
higher
in
the
absence
of
lime
in
all
treatments,
but
was
highest
in
the
nonlimed
KP
treatments.
Seed
Cl
concentration
was
reduced
by
both
the
addition
of
lime
and
the
exclusion
of
KC1.
Comparing
the
treatment
receiving
only
KP
with
the
zero-P
control
receiving
only
KCl
at
a
rate
to
equalize
K
and
Cl,
there
was
a
large
increase
in
yield
due
to
P
but
almost
none
due
to
lime
at
this
P
rate
(Fig.
6).
Theoretically,
a
high
rate
of
P
could
obscure
a
response
to
lime
when
extractable
soil
Al
is
relatively
high.
A
high
rate
of
Cl
could
obscure
a
response
to
P
over
a
large
range
of
applied
P.
Discussion
Chloride
VAMF
inoculation
increased
plant
survival
and
protected
plants
from
leaf
scorch
in
this
acid
soil,
thereby
substituting
for
the
effects
of
lime
and
fertilizer
P.
Glomus
etunicatum
was
more
effec-
tive
than
G.
fasciculatum
in
ameliorating
leaf
scorch
in
the
nonlimed
soil.
The
results
of
inocu-
lation
into
sterile
soil
are
not
reported
here
but
parallel
the
findings
in
nonsterile
soil.
In
the
absence
of
leaf
data
on
these
mature
soybeans,
we
studied
the
relationship
of
seed
Cl
to
seed
yield
(Fig.
2).
Inoculation
with
VAMF
increased
the
effectiveness
of
lime
to
reduce
the
seed
concentration
of
Cl.
Parker
et
al.
(1987)
reported
values
of
seed
Cl
to
be
682
µg
g
-1
for
susceptible
cultivars.
Seed
Cl
concentration
was
>650
µg
g
-1
in
the
noninoculated
controls
with-
out
applied
P
and
limed
to
pH
>7
but
inocula-
tion
with
G.
etunicatum
reduced
the
seed
CI
to
377
µg
g
-1
.
Seed
Cl
concentration
was
reduced
to
143
µg
g
I
by
the
combined
effect
of
high
P
and
lime
rates.
Grattan
and
Maas
(1988a)
sug-
gested
that
the
mechanism
of
P
and
Cl
uptake
and
translocation
may
be
independent
of
one
60
40
a
20
0
la)
200
DI
2
400
600
35
25
E
15
0
Soil
and
fertilizer
effects
on
mycorrhizal
soybean
91
another.
They
reported
foliar
injury
and
leaf
Cl
concentration
are
linearly
correlated
with
the
solution
culture
concentration
of
Cl
and
with
the
increase
in
CaC1
2
/NaC1
ratio
(Grattan
and
Maas,
1988a).
Due
to
the
replacement
rate
of
KCl
with
KH
2
PO
4
in
this
soil
study,
the
interpretation
of
these
results
warrant
further
study,
but
demon-
strate
the
ameliorating
effect
of
VAMF
inocu-
lation.
P
x
lime
x
VAMF
interaction
Results
indicate
not
as
much
applied
P
was
required
to
increase
the
seed
yield
with
the
G.
etunicatum
inoculant
as
the
G.
fasciculatum
ino-
culant
if
this
soil
pH
is
sufficiently
high.
A
higher
soil
pH
was
better
for
the
G.
fasciculatum
inocul-
ant
but
required
the
highest
rate
of
applied
P
tested
with
VAMF
inoculation
to
produce
a
sig-
nificant
increase
in
seed
yield
compared
to
the
noninoculated
controls.
However,
the
efficiency
of
applied
P
remained
constant
between
the
two
inocula
in
a
given
soil
pH
at
the
level
of
applied
P
(80-160
mg
kg
-1
)
required
to
maximize
yield.
Role
of
VAMF
in
Al
tolerance
The
large
difference
in
soil
extractable
Al
and
root
Al
uptake
due
to
VAMF
inoculation
is
difficult
to
explain.
The
explanation
must
en-
compass
the
known
soil
chemistry
and
less
known
effects
of
biochemistry
of
mycorrhizae.
Buwalda
et
al.
(1983)
reported
increases
in
anion
uptake
due
to
VAMF
infection
but
not
by
P
additions.
Their
results
suggest
a
hydroxyl
or
bicarbonate
exchange
for
anions,
especially
for
anions
of
Cl,
Br,
NO
3
,
SO
4
,
and
H
2
PO
4
.
Some
ectomycorrhizae
are
known
to
produce
oxalic
acid
and
other
organic
acids
(Lapeyrie
et
al.,
1987).
The
occurrence
of
calcium
oxalate
associ-
ated
with
fungal
hyphae
in
soils
is
widespread
in
different
soil
ecosystems
but
it
is
destroyed
by
the
metabolic
activity
of
many
soil
organisms
(Graustein
et
al.,
1977).
Jurinak
et
al.
(1986)
has
proposed
a
thermodynamic
model
for
predicting
the
role
of
Ca-oxalate
in
regulating
Ca-ion
activi-
ty
at
the
root
interface.
This
model
shows
that
mycorrhizal-induced
oxalate
exudation
could
regulate
the
solubility
of
Al
and
Fe
phosphate
and
is
very
sensitive
to
soil
pH.
Bolan
et
al.
(1987)
found
the
least
soluble
iron
phosphates
were
more
available
to
subterranean
clover
(Tri-
folium
subterraneum
L.)
and
ryegrass
(Lolium
perenne
L.)
when
inoculated
with
G.
fas-
ciculatum.
They
concluded
that
it
was
not
pos-
sible
to
differentiate
between
the
mechanisms
of
(1)
increased
soil
exploitation
by
hyphae
and
(2)
chemical
modification
of
P
availability
from
Fe-
phosphate.
Similarly,
it
would
be
difficult
to
differentiate
between
these
two
mechanisms
if
Al-phosphate
was
prevalent
as
a
potential
source
of
P.
The
effectiveness
of
organic
acid
exudates
to
detoxify
Al
is
related
to
the
form
of
soil
Al
and
pH
(Haynes,
1982).
Many
hypotheses
have
been
put
forth
to
explain
the
mechanism
of
plant
tolerance
to
soil
Al
(Fageria
et
al.,
1988).
We
hypothesize
that
roots
infected
with
effective
VAMF
could
produce
significant
amounts
of
or-
ganic
acids
in
an
acid
soil
resulting
in
an
in-
creased
extractable
soil
Al
positively
correlated
with
the
amount
of
applied
soluble
P.
Precipi-
tation
of
Al
in
root
cells
by
the
organic
acid
complexation
with
Al
would
serve
to
detoxify
Al,
increase
root
Al
uptake,
and
increase
the
extractability
of
soil
Al.
In
more
alkaline
soil,
the
more
likely
CaCO
3
and
MgCO
3
would
re-
duce
the
effectiveness
of
VAM
exudates
and
decrease
the
extractable
Al.
However,
in
the
more
alkaline
soil,
any
increase
in
organic
acid
exudation
due
to
mycorrhizal
activity
and/or
inducement
by
high
potash
fertility
(Kirkby,
1974)
could
coat
the
surface
of
insoluble
precipi-
tates
and
prevent
further
precipitation
of
soluble
P
as
Al
and
Fe
phosphates
(Grossl
and
Inskeep,
1988;
Kucey
et
al.,
1989).
Wright
et
al.
(1989)
reported
Al
3+
ion
specia-
tion
to
be
greatly
increased
by
the
addition
of
Cl
as
CaC1
2
.
In
this
soil,
there
was
no
response
to
lime
unless
KCl
was
used
as
the
K
source
(Fig.
6).
The
response
to
applied
P
was
diminished
by
the
use
of
KC1
regardless
of
the
lime
rate
or
P
rate.
The
application
of
lime
reduced
both
the
extractable
soil
Al
and
the
seed
Cl
concen-
tration.
The
application
of
CSP
+
KC1
in
non-
limed
soil
reduced
extractable
soil
Al
without
obvious
beneficial
plant
effects.
The
use
of
KC1
may
have
altered
the
speciation
of
Al-ions
to
produce
more Al
3+
and
increase
the
formation
of
Al-phosphate
from
P
fertilizer.
The
use
of
KP
may
increase
the
extractable
soil
Al
without
increasing
the
Al
3+
ions
and
increase
the
forma-
92
Maddox
and
Soileau
tion
of
an
Al
precipitant
which
is
extractable
with
KC1.
If
organic
acid
production
in
the
rhizosphere
is
stimulated
by
a
combination
of
edaphic
factors
such
as
soil
acidity,
fertilizer
effects,
and
its
aluminon
speciation
content,
then,
VAM
symbiosis
in
a
soil
rooting
media
with
high
P
fixing
capacity
could
increase
the
availability
of
both
soil
P
and
fertilizer
P.
The
effectiveness
of
VAM
in
increasing
P
uptake
and
tolerance
to
soil
Al
can
be
altered
by
soil
acidity
and
the
application
of
fertilizers
containing
Cl.
Conclusions
Inoculation
with
either
VAMF
inocula
used
in
this
study
increased
soybean
survival
and
re-
duced
the
incidence
of
leaf
scorch
due
to
applica-
tion
of
murate
of
potash
in
this
acid
soil,
thereby
substituting
for
the
effects
of
lime
and
P
fertilizer
when
only
native
VAMF
was
present.
The
Ge
inoculum
was
superior
to
the
Gf
inoculum
in
ameliorating
leaf
scorch
in
this
infertile
acid
soil.
Both
inocula
increased
root
Al
uptake
and
the
extractable
soil
Al
in
this
acid
soil
regardless
of
the
level
of
P
fertilization
but,
reduced
the
root
Al
uptake
in
the
alkaline
limed
soil.
Results
of
this
study
indicate
that
both
lime
and
P
fertiliza-
tion
of
this
acid
soil
increased
the
plant
response
to
available
P
with
little
effect
on
Al
uptake.
The
effect
of
VAMF
inoculation
to
increase
plant
survival
in
the
presence
of
Cl
fertilization
in
acid
soil
may
be
partially
due
to
an
enhanced
toler-
ance
to
soil
Al.
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