Plant Physiol. (1973) 52, 105-110
Polarity and Rate of Transport of Cyclic Adenosine 3',5'Monophosphate in the Coleoptile1
Received for publication February 2, 1973
S. A. GORDON, E. CAMERON, AND J. SHEN-MILLER
Division of Biological and Medical Research, Argonne National Laboratory, Argonne, Illinois, 60439
ABSTRACT
Transport of tritiated cyclic AMP in the coleoptile of oats
(Avena sativa) and corn (Zea mays) is polar, with basipetal to
acropetal ratios of 4.0 and 3.2, respectively. The rate of transport is approximately that of indoleacetic acid. The linear
velocity of transport, however, is at least five times that of
auxin. A loss in transport polarity of the nucleotide occurs in
subapical tissues within several hours after decapitation of the
coleoptile, accompanied by a decrease in transport rate. The
loss in polarity is not reversed by exogenous auxin, but the
reduction in transport is. Auxin also inhibits the uptake of
cyclic AMP. Exogenous cyclic AMP is metabolized rapidly by
coleoptile tissues. If cyclic AMP does have a cellular function in
the coleoptile, its transport behavior is compatible with that
of a hormone.
Cyclic 3', 5'-adenosine monophosphate is believed to act as
a "second" messenger in mammalian cells. Specifically, a hormone, released or produced by a stimulus, travels to an effector cell and there causes an increase in the concentration of
cAMP2 (28). The rise in level of cAMP, in turn, alters the
rates of a diverse array of enzyme and physiological activities.
Cyclic AMP has also been shown to act as a "primary" hormone, as in the aggregation of the amoeboid stage of a slime
mold in response to a pulsed output of the nucleotide from an
initiator cell (2, 18). Assignment of either a primary or second
messenger function for cAMP in higher plants cannot be done
as yet, and even normal function of the nucleotide in physiological processes is conjectural.
Certainly, most of the experiments with higher plants have
been consistent with a second messenger role of exogenous
cAMP. It has been proposed that cAMP is involved in the
induction of amylase, protease, acid phosphatase, and ATPase
by barley half-seeds treated with GA (4-6, 25), although the
nucleotide alone is essentially inactive. It has also been noted
that labeled adenine is converted to cAMP in barley, and that
this conversion is enhanced by GA (27). The promotive effect
of 2,4-D on cell expansion in Jerusalem artichokes has been
found to be synergistically enhanced by cAMP (15), the nucleotide alone being without effect. Furthermore, it has been
'This work was supported by the United States Atomic Energy
Commission and the National Aeronautics and Space Administration Grant W12792.
'Abbreviation: cAMP: cyclic AMP.
105
reported that cAMP mimics the effect of IAA in stimulating
the de novo synthesis of tryptophan oxygenase in chick peas
(Azhar and Murti, unpublished), and that IAA stimulates
2-fold the conversion of labeled adenine into cAMP (1). Cyclic
AMP has been isolated from lettuce seeds (24), where it occurs at a concentration of 0.1 nmole/g of dry seeds, about
one-tenth that of mammalian tissue.
Salomon and Mascarenhas (30) have demonstrated an auxininduced synthesis of cAMP in oat coleoptiles. They find that
the nucleotide concentration is increased within 30 min by
pretreatment of subapical coleoptile sections with IAA and
report a low but positive growth-stimulating effect of cAMP in
coleoptile sections (about 20% increase). Their thesis is that
the plant tissues are similar to those of the animal in that the
nucleotide performs a mediating role in the response to a hormone, in this instance IAA.
However, none of the observations noted above are incompatible with cAMP function as a hormone in the correlative
sense, as it does in the slime mold. We will show that cAMP is
polarly transported in corn and oat coleoptiles, that it has a
velocity of transport at least several times that of IAA, and
that IAA, although it enhances both basipetal and acropetal
transport of cAMP in corn and oat tissues, does not determine
the polarity of movement of the nucleotide.
MATERIALS AND METHODS
Corn (Zea mays cv. Wisconsin 64A X 22R) and oat (A vena
sativa cv. Victory I) seeds were rinsed twice in tap water at
45 C and soaked for 2 hr in tap water initially at the same
temperature. They were drained, covered with foil, and kept in
the dark at 2 C for 18 to 20 hr. The corn was spread on moist
Kimpax tissue, the oats on moist filter paper on lucite racks
angled at 450 from the horizontal, and both were exposed 24
hr to red light (G. E. Ruby Red, 10 w, fluence rate 400
,uw cm') at 25 C to suppress elongation of the mesocotyl.
They were then allowed to grow in the dark at 25 C for an
additional 48 hr.
For transport studies, a 7-mm section cut 3 mm below the
tip was excised with a double-blade cutter, and the foliage
leaf was pushed out. The sections were maintained in normal
orientation to avoid geotropic effects on transport (23). Each
section was placed on a donor block (2.7 X 2.8 X 1.5 mm) of
1.5% agar. A receiver block, 4 mm in diameter and 1.5 mm
thick, was placed on top of the section. For basipetal transport,
the positions of the donor and receiver blocks were reversed.
Donor blocks contained about 0.02 ,tc of cAMP, 8-3H
(Schwarz-Mann, 16.3 c/mmole), or G-3H (New England Nuclear, 4.4 c/mmole). The concentrations of cAMP were such
that if completely absorbed it would yield a concentration in
the tissues about the same as that observed in lettuce seeds,
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106
-
GORDON, CAMERON, AND SHEN-MILLER
0.1 nmole/g dry seed. All donor blocks contained sucrose at a
concentration of 2%; the sucrose was added to reduce the
likelihood of carbohydrate limitation of transport. A small
plastic holder was used to keep the oat coleoptile sections in
position; no holder was necessary with the corn sections. Transport assemblies were maintained at 25 C in a water-saturated
atmosphere in the dark. All manipulations were performed
under a green safelight (33).
For the depletion of endogenous auxin, 2 mm of the coleoptile tip was removed from the seedling. Two hours later a thin
slice (1 mm) was taken from the stump and replaced by a
block of agar containing 2% sucrose with IAA at a concentration of 5 mg/l, or without IAA. The block was allowed to
remain for an additional 2 hr, and then the apical 7-mm segment was cut from the coleoptile. The tissues taken for test of
transport were thus from the same location as those undepleted. To the depleted coleoptile segments, pretreated or not
pretreated with IAA, donor blocks containing cAMP and 2%
sucrose, respectively, with or without 5 mg/l of IAA, were then
applied.
After various periods of transport, receiver blocks were
dropped into 15 ml of Scintisol and allowed to remain for at
least 12 hr at room temperature. The extracts were then
counted in a Beckman LS-250 liquid scintillation counter.
Blank donor assemblies were made in an identical fashion as
the test assemblies, and run for identical transport periods,
except that they contained cold cAMP. Unless otherwise noted,
every datum is the mean of eight replicate samples, corrected
for the mean counts of two blank assemblies.
To measure tissue activities, each section was placed on a
small circle of Whatman No. 1 filter paper and allowed to dry
overnight. The tissue and filter paper were oxidized in a Packard 305 sample oxidizer and counted in Scintisol in the LS-250
system. The coleoptile tissues were not washed, as no significant difference in counts was found between sections rinsed
and unrinsed.
To determine if cAMP was transported as such, basipetal
transport assemblies of corn, similar to those described above,
with the donor blocks containing about 0.02,uc of 8-3H cAMP
and 2% sucrose, were left for 0.5, 1, and 2 hr. Ninety receiver
blocks were dropped into 15 ml 95% ethanol, and then washed
five times each with 10 ml of 95% ethanol. All extractions were
pooled. The combined extracts were taken to near dryness in
a flash evaporator and then taken up in a small quantity of
95% ethanol. They were filtered through Whatman No. 50
paper to remove the insoluble material that deposited during
evaporation of the alcohol. This filtrate was again reduced in
volume in the flash evaporator and then spotted on a Whatman
No. 1 filter paper strip. Cold cAMP and 5'-AMP, approximately, 0.05,umole of each, were added as carriers. The paper
strip, after equilibration for 5 hr over isopropanol-NH,OH-H2O,
70:10:30 (v/v/v) was then developed in the same solvent
system for 18 hr by ascending chromatography. The cAMP
and AMP spots were located under UV light. The first half of
the strip (origin to RF 0.5) was cut into 10 equal sections, and
the second half into5 equal sections, which were then oxidized
and counted in Packard Permafluor II.
To indicate the stability of cAMP in the donor blocks, 10
used and 10 unused donor blocks were also extracted in the
same manner. These extracts were chromatographed. All
counts were found at the RF of cAMP. Analysis of variance
was used to assess significance of differences.
Plant Physiol. Vol.
4Or
52, 1973
CORN
3-
30 -
LL
'bBosl /O
9
*
P
|
oAcro
9
-80
a-
10-
QAcro
J
-60
F~~~~~~~~~~~~~~~~~
p<O
001
-40
p<O.OOI
OATS
~~~~~~~~~~-40
I0
Bosi
... Basi 1
d
/
*0..oAcro
,
6
-20
O 4 O s o~~~~~~~~~~~Acr
o
O
0
p<OOOI
p<O.OO5
lI
0
40
80
120
0
40
80
120
MINUTES
FIG. 1. Cyclic AMP transport in corn and oat coleoptile segments. Per cent refers to fraction of the total radioactivity absorbed that is found in the receiver block; cpm represents the total
counts per minute in the receiver block.
segments are shown in Figure 1. Both as a percentage of that
absorbed and as actual counts, the amount transported peaks
at about 30 min and then falls. There is a basipolarity in transport, with a mean basi- to acropetal ratio of 2.5 for the corn
and 3.2 for the oat tissue (Table I).
Table I lists the means of the transport data averaged over
the entire transport duration of 90 min. In the corn (Table I,
column 1). an average of 28% of that absorbed is transported
basipetally, or 149 cpm/receiver block. Acropetally, 11I% of
that absorbed is transported, or about 87 cpm/block. In oats,
an average of 9% of that absorbed is transported basipetally,
or about 34 cpm/block. This represents about one-fourth to
one-third of the transport level of the corn tissues. Acropetal
transport in oats is also less, with 2.7% and 13 cpm. respectively one-fourth and one-sixth of the corn.
The basi- to acropetal ratio of 2.5 and 3.2 for "true' transport (Table I, column 1) associated with polar ratios of 1.7
and 2.6 for actual counts in the receiver blocks for corn and
oats, respectively, suggests that there was a greater uptake of
the cAMP when it was applied to the base of the coleoptile
segment. This is also true for corn as shown in Figure 2 and
TableII, where the basipetal to acropetal uptake ratio is 0.72.
With the oat, the ratio is 0.85, although the difference in uptake is not significant. A similar generalization may be made
for retention of activity by the tissues (Fig. 2). Retention appears to be highly correlated with uptake.
Chromatography of the Transport. The monotonic trends of
the uptake and retention curves (Fig. 2) are in contrast to the
"breaking" of the transport curves near 30 min (Fig. 1). One
RESULTS
explanation could be that degradation of cAMP occurs, alterTransport in Undepleted Tissues. The acropetal and basip- ing its transport properties. The results of chromatography of
etal transport of cAMP in undepleted corn and oat coleoptile the radioactivity in the receiver blocks are consistent with this
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Plant Physiol. Vol.
TRANSPORT OF cAMP
52, 1973
107
Table I. Tranisport of cAMP through Coleoptile Segments
Data are the average values for the 10- to 90-min transport period. Within a column or row, per cent or cpm followed by dissimilar
subscripts differ significantly at the 1%,b level or lower.
Undepleted
Depleted
-IAA
Ratio
%
+IAA
Ratio
cpm
%
Ratio
cpm
%
Ratio
Ratio
cpm
Ratio
Corn
Basipetal
27.50
Acropetal
10.8d
2.5
149l
86.9d
1.7
2.61abb
1.82a
14
19.8b
17.8b
3.2
3.2b
2 6
2.70,,
0.89
19.2a
20.1a
3.18b
|11
3.05b
Oats
Basipetal
Acropetal
2.71,
1200
UPTAKE
8.72b
13.2,,
II
1000
3.04i,
CORN
9.
~~~~~~Id
*
5.67b
I
5.42b364
1.0
1
1 9a
19.2b
35b
0.92
Table II. Uptake of cAMP by Coleoptile Segmenits
Data are average values of the 10- to 90-min transport period.
Within a column or a row, numbers followed by dissimilar subscripts differ significantly at the 5%10 level.
II
RETENT ION
oAcro
0.95
|91
r Basi
Depleted
800
Undepleted
9.&.
-IAA
600
+IAA
cpm
400
Corn
200
Basipetal
Acropetal
Oat
Basipetal
p
< 0.001
o
Acropetal
II
0
588,
821b
850b
1055,
374a
649d
434,
513,a
750b,
755b
655bc
590ae
IOcDO _
OATS
K~~~~~
8C
-Acro
6C
DO
Basi
4CnO _
2CDO _
.
A
Acro
Basi
p>O.I
jff
p>0.2
n.s.
P
p>0.2
_
n.s.
I
-1, 120
0 I,
40 I,60 I, 120
0 , 401, 80
MINUTES
FIG. 2. Uptake and retention of cAMP in corn and oat coleoptile
Ol
tissues.
possibility. Figure 3 shows the chromatograms made after
basipetal transport periods of 0.5, 1 and 2 hr. About 5 to
10% of the cAMP was converted during the transport period
to what we assume to be 5'-AMP. Also, progressively increasing amounts of a labeled product, RF 0.5 to 0.6, appeared.
This product comprised about 10% of the total radioactivity
in the receiver block after 0.5 hr of transport, about 20% after
1 hr, and 45% after 2 hr; at 2 hr only 20% was accountable as
cAMP.
Transport in Depleted Tissues. Auxin is known to accelerate
the rate of its own uptake (9), as well as the uptake and transport of other growth substances (8, 9, 19). To determine if
auxin affects the movement of cAMP, uptake and transport
of the nucleotide were measured in auxin-depleted tissues, with
and without subsequent auxin supplement (see "Materials and
Methods"). The results are given in Tables I and II.
In corn, the 4-hr depletion period caused a 10-fold drop in
the percentage of basipetal, and a 6-fold increase in acropetal
transport of cAMP (Table I, compare column 1 with column
3). The reduction is less in the oat, 3-fold basipetally, and a
difference not significant in the acropetal direction. Not only has
there been a decrease in transport, but the polarity of transport
has largely disappeared. The loss of polarity upon depletion
may be attributed to a greater reduction of the basipetal transport than of the acropetal. In corn, supply of auxin to the de-
pleted tissues effects a limited reversal of the depletion-induced
reduction of transport of cAMP, in both transport directions.
In oats, auxin supplement not only completely reversed the reduction of cAMP movement in the basipetal direction resulting
from depletion, but also increased the acropetal movement to a
level higher than in the undepleted tissues.
In the depleted tissues (Table I), addition of auxin, on the
whole, raised the amount of cAMP transport and the actual
counts in the receiver block. This effect was not due to an enhanced uptake from the donor block. Table II shows that
in the depleted tissues the presence of supplemental auxin depressed the uptake in both corn and oats.
However, we must point out that in the undepleted corn
coleoptile a major portion of the transported radioactivity is
cAMP only for the first 0.5 hr. It is possible that the degradation of cAMP is even more rapid in the depleted tissues (29).
With this consideration in mind, we tabulated the uptake and
transport of cAMP for the first 10 min (Table III). The trends
of cAMP uptake and transport during this 10 min, on the
whole, resemble those averaged over the 90-min period (Table
I). The exceptions are that the basi- to acropetal ratios are
higher in the undepleted tissues, and addition of IAA to the
depleted oat coleoptiles raises slightly the polarity of transport
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108
GORDON, CAMERON, AND SHEN-MILLER
Plant Physiol. Vol. 52, 1973
DISCUSSION
In both corn and oat coleoptiles, the transport of cAMP is
polar. The basi- to acropetal ratios of over 3 do not appear to
result from differences in rates of entry from donors into tissues (compare Figs. 1 and 2). It may be suggested that the
polarity and rate of cAMP transport are not intrinsic characteristics of coleoptile tissues, but consequences of some activity or substance in the tip region. Removal of this tip factor
by decapitation results in a decrease in the transport of cAMP
and a disappearance of its transport polarity. The loss in
polarity cannot be explained completely in terms of auxin, as
there was no reversal (Table I) to limited reversal (Table III)
upon supplying auxin after decapitation. However, auxin does
have a role in determining the intensities of cAMP transport,
both in basi- and acropetal directions. In corn, auxin supplement gave rise to a limited reversal of the fall in transport rate
40
due to depletion, and in oats the reversal was complete (Table
I). We therefore suggest that auxin can control the rate of
transport of cAMP, and that transport polarity and transport
intensity are governed by different mechanisms.
Depletion, whose primary purpose was to depress the level
of endogenous auxin (35), yielded in every instance an enhancement in uptake of cAMP. That auxin was the factor
responsible is shown by the inhibition of uptake by depleted
0
60
tissues that had been exposed to auxin (Tables II and III). The
effect of auxin on cAMP uptake is thus unlike its effect on the
uptake of other growth substances but is similar to its sup2.0 hr
pression of adenine uptake by sunflower hypocotyls (20). One
explanation for the suppressive effect of auxin on cAMP up0.2
04
0.8
0
0.6
1.0
take would be a competition between the two substances for a
Rf
common site of uptake.
In the oat coleoptile, basipetal transport of IAA is about
FIG. 3. Chromatographic distribution of radioactivity in re25%
of the total uptake in 4 hr (Fig. 3 in ref. 7). A similar
ceiver blocks under corn segments after basipetal transport periods
transported fraction was found for IAA in the root of Lens
of 0.5, 1.0, and 2.0 hr.
(26; but see 17). Cyclic AMP is transported basipetally with
comparable rates as IAA, about 11% in the oat coleoptile and
Table III. Uptake and Transport of cAMP by Coleoptile Segments 31 % in the coleoptile of corn within 10 min. It is clear, howData are the values during the initial 10 min.
ever, that the substance found in the receiver block is mainly
cAMP only for the first 0.5 hr (Fig. 3). Thereafter, metabolic
Uptake
products of cAMP become increasingly prominent, as with
adenine (34) and GA (14), but unlike IAA (7, 13), 2,4-D (22),
Depleted, +IAA
Depleted, -IAA
Undepleted
and kinetin (34). The gradual disappearance of cAMP could be
a result of depletion of auxin in the transport segment. It has
Corn
been reported that IAA maintains the level of cAMP in coleop238 41 14
308 4 17
452 4 72
Basipetal
tile
tissues (29).
348 + 28
467 ± 23
441 :1: 17
Acropetal
The
sharp reduction in transport intensity, both basipetal
Oats
261 z4 17
242
32
166 &"4
Basipetal
and acropetal, of cAMP occurs after transport times of about
444
514 4 60
244 1 18
77
Acropetal
0.5 hr. Similar reductions, but later in time, have been observed with GA3 in shoots (14), with adenine (34), abscisic acid
Transport
(11), and IAA (16, 21, 22) in shoots, and IAA in roots (12,
31). Such changes in rate have been correlated (14) with the
Ratio
Ratio
Ratio
%
%
%
fact that these substances are endogenous; presumably they are
metabolized faster than 2 ,4-D and kinetin, which do not show
Corn
1.5 4 0.1
31.4 a 1.9
2.1 t0.3
Basipetal
breaks of transport rate in similar time periods (34). Consistent
0.4 0.5
9.8
0.5 3.2 1.6:: 0.2 1.3 2.9
Acropetal
with
this interpretation in the present experiments is the corOats
respondence in time, when a major fraction of the cAMP has
0.5 1.4 4.3 E 0.4 2.4
9.5 d 0.7 4.0 3.2
Basipetal
1.8 + 0.3
2.4 dA0.5
2.3 + 0.2
Acropetal
been metabolized, and the decrease of its transport.
In interpreting an actual decline of radioactivity in receiver
blocks when 14C-adenine transport in Coleus was being exduring the initial 10 min (compare Table III with Table I). amined (34), it was suggested that part of the radioactivity in
The new polarity ratios are 3.2 for the corn and 4.0 for the the receiver blocks was taken up again into the tissues. This
oats. These ratios are probably more representative of cAMP explanation seems equally applicable here. We suggest that this
transport than those tabulated in Table 1.
resorption of cAMP is prevented by auxin, as IAA inhibits the
-
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TRANSPORIT OF cAMP
Plant Physiol. Vol. 52, 1973
109
LITERATURE CITED
CORN
Acro
Basi
6
4
O ATS
0
2I
Basi
Acro
8
p<O.025
p >=0.05ns
6~~~~~+IAA
4IAA-
4o-IAA-
2
.,-IAA
p=0.05
0
40
p
0
80
<0.025
40
80
MINUTES
FIG. 4. Cyclic AMP transport in depleted corn and oat coleoptile segments with and without IAA supplement.
uptake of cAMP, irrespective of polarity (Table II, columns
2 and 3). Further, we have observed that the time-dependent
decline of cAMP transport (Fig. 1) can be prevented by addition of auxin, both in the basipetal and acropetal directions
in the depleted tissues (Fig. 4).
Within a 10-min period, the percentage of the radioactivity
appearing in the receiver block reached 0.8 to 0.9 that of the
maximum activity in the receiver. If we assume that the front
of cAMP moves through 7 mm of tissue in 10 min, the transport velocity is 42 mm/hr. It is very probable that the actual
velocity is higher. These velocities may be contrasted with those
of growth substances, which range from 1.7 mm/hr for kinetin
in Coleus (34), 1 to 2 mm/hr for GA (14), 1 mm/hr for 2,4-D
in Phaseolus petioles (21), to that of 2.5 to 18 mm/hr for IAA
in various tissues (13, 21, 23). In corn coleoptiles attached to
the endosperms, the velocity of IAA movement through the
apex is 41 mm/hr (32). Transport of abscisic acid was estimated at 25 to 35 mm/hr in Coleus (3) and 22 mm/hr in cotton petioles (11). The linear velocity of cAMP transport is thus
one of the most rapid of those encountered in this group of
compounds.
The role of cAMP has been associated with intracellular control of cell functions (28). The findings that it moves polarly,
and that its transport through the coleoptiles is extremely rapid,
suggest that cAMP could also have an intercellular function,
i.e. that of a hormone. It may be pertinent to cAMP that compounds having transport characteristics similar to those of
auxin
possess auxin-like action (10).
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