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Soil Science and Plant Nutrition

ISSN: 0038-0768 (Print) 1747-0765 (Online) Journal homepage: https://www.tandfonline.com/loi/tssp20

Further evidence for gaseous CO2 transport in relation to root uptake of CO2

in rice plant

Toshihiko Higuchi,Karin Yoda & Kiyoshi Tensho

To cite this article: Toshihiko Higuchi , Karin Yoda & Kiyoshi Tensho (1984) Further evidence
for gaseous CO2 transport in relation to root uptake of CO2 in rice plant, Soil Science and Plant
Nutrition, 30:2, 125-136, DOI: 10.1080/00380768.1984.10434676

To link to this article: https://doi.org/10.1080/00380768.1984.10434676

Published online: 14 May 2012.

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Soil Sci. Plant Nutr., 30 (2), 125-136, 1984

FURTHER EVIDENCE FOR GASEOUS CO2 TRANSPORT

IN RELATION TO ROOT UPTAKE OF CO2
IN RICE PLANT

Toshihiko HIGUCHI, Karin YODA,* and Kiyoshi TENSHO*

Laboratory of Agriculture. Faculty of Education. Tokyo Gakugei University.
Koganei. Tokyo. 184 Japan
• Radioisotope and Nue/ ear Engineering School. Japan Atomic Energy
Research Institute. Bunkyo-ku. Tokyo. 113 Japan

Received June 25, 1983

In order to make clear the mechanism of transport of CO. absorbed by rice roots, several
experiments were carried out. The amount of COl derived from root uptake in rice seedlings was
significantly larger than that in wheat seedlings. As CO. concentration in the culture solution increased,
the predominate uptake by rice roots became more obvious. 2,4-Dinitro phenol and sodium azide
constantly inhibited dark CO. fixation in roots of rice and wheat, while their effects on the CO. transport
to the shoots were not significant. In the case of mannitol treatment, CO. transport from roots to shoots
in wheat decreased by 50%, while no strong inhibition was observed in rice. CO. gas analysis in roots
indicated that the CO. enrichment in the culture solution led to the increase of CO. gas content in rice
roots. The volume of the gas phase in rice roots was ten times as large as that in wheat roots and CO.
gas contents in rice roots were by far higher than those in wheat roots. These results as well as other
experimental data may suggest that a large part of CO. absorbed by rice roots moves to the shoots in
the gaseous state. Further, it can be postulated that the principal gasifica tion site in rice plants is located
in the root cortex where Iysigenous intercellular spaces are present.

Key Words: lowland rice, root uptake of CO .. ventilation system, gas movement.

Numerous studies have demonstrated that plants are capable of absorbing CO2
through the roots (1-4). Some of these studies showed that the amount of CO2 ab
sorbed by the roots does not exceed 1 % of that assimilated by the leaves, and it was
eventually concluded that root uptake of CO2 is of no importance from the view point of
crop production. These studies, however, still leave an open question concerning the
following problems for estimating the actual amounts of CO2 taken up through the roots.

1) Root uptake of CO2 has been considered only from the view point of bio
synthesis leading to the formation of organic compounds in roots.
2) Plant materials used did not include aquatic plants.
3) In the tracer experiments, CO2 concentration in the culture solution was very
low.
125
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126 T.HIGUCHI, K.YODA , and K.TENSHO

It is well known that CO2 absorbed by the roots is reduced to organic compounds
in roots, and that these compounds are transported to the shoots through the xylem
(5). On the other hand, tracer experiment with rice seedlings revealed the existence of
a leakage of gaseous CO2 derived from the root uptake through the leaf sheath within
a short time (6). This fact suggests that the carbon transported to the shoots is not only
in organic forms but also in inorganic ones.
It has been previously observed in tracer experiments using soil that rice grown
under submerged conditions absorbed far more CO2 through the roots than wheat and
upland rice grown under upland conditions (7, 8). This phenomenon has been ascribed
to the high concentration of CO2 dissolved in the soil solution under sub merged
conditions (9). Meanwhile, in other experiments with water culture it was found that rice
absorbed more CO2 through the roots than wheat even when the CO2 concentration
in the root medium was identical (6, 10). The peculiarity of root uptake of CO2 in rice
is ascribed to the intrinsic characteristics of the plant.
Studies conducted on Lobelia dortmanna and Littorella uniflora grown in lakes
suggested that CO2 fixed by the photosynthetic activity leaves was mostly derived
from the lake sediments through root uptake (11-13). Rice as well as these plants is a
typical hydrophyte and undoubtedly these hydrophytes absorb more CO2 through roots
than non-aquatic plants.
These experiments (6, 10-13) have again prompted studies on root uptake of CO2
from the view point of the peculiarity of rice plant.
More recently, a hypothesis on the mechanism of the transport of CO2 absorbed
by roots has been proposed by one of the authors (14). On the basis of this hypo
thesis, the peculiarity of rice with regard to CO2 uptake can be ascribed to the differ
ences in the development of the aerenchyma between rice and upland plants.
The study on the transport of CO2 absorbed by rice roots seems to be still insuffi
cient. For the estimation of the contribution of CO2 absorbed by rice roots to dry matter
production, information on CO2 transport from roots to shoots is essential.
The purpose of the research work presented here is to clarify the transport mechanism
of CO2 absorbed by rice roots and analyze the unique properties of rice plant in rela
tion to the CO2 uptake-transport through roots.

MATERIALS AND METHODS

Tracer experiment with 14c. Seedlings of rice (Oryza sativa L., variety Nihonbare)
and wheat (Triticum spp., variety Norin No. 61) were raised in a phytotron under water
culture conditions for 28 and 14 days after sowing, respectively.
Two levels of CO2 concentration in the uptake solution were prepared for the
experiments. Low CO2 level was 0.3 mM solution of sodium bicarbonate and the pH
was carefully adjusted to 6.0 with 0.1 M HCI before the uptake treatments were initi
ated. High CO2 level solution was prepared by mixing 25 volume of 7 mM solution of
sodium bicarbonate with 8 volume of CO2 saturated water. Its concentration was
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Root Uptake of COa in Rice 127

10-15 mM and the pH was usually maintained at 6.0. Changes in pH during the uptake
periods were below 0.1 unit.
The uptake solution was labeled with NaHl4COa (radioactive concentration: 3- 10 pCi
per liter). One hundred ml of the solution thus prepared was put in a 125 ml Erlenmeyer
flask. Roots of five plants were dipped in the solution to absorb l4C02, while the basal
parts of the shoots were supported with a plastic sponge to hold the plants in the flask.
After the completion of the uptake treatment at a light intensity of 10,000 Ix and
temperature of 25°C, the roots were immediately washed with water and the seedlings
were separated into three parts, i.e., leaf blade, leaf sheath, and root, which were then
dried at 70°C throughout the night for the determination of dry weights.

Using an auto-combustion system (Aloka, model ASC-113), l4C of dry samples of

five plants was oxidized to l4C02 in a lump, and the radioactivity was measured with a
liquid scintillation counter (Packard, model 300).
The amount of CO2 fixed into each part of plant was calculated from the specific
activity in the uptake solution and expressed on the basis of dry weight of root. Val ues
obtained with the tracer experiments were the mean values of two experiments.
Additional information on the treatment in the respective experiments is as fol lows.

1) The distribution of CO2 derived from root uptake in the seedlings was examined
for an uptake period of 4 h.
2) The time-course of root uptake of CO2 was examined for a high CO2 level for uptake
periods from 30 to 240 min.
3) The effects of such respiratory inhibitors as 2,4-dinitrophenol and sodium azide on the
root uptake of CO2 were evaluated for both high and low CO2 levels. Con centrations
of 2,4-dinitrophenol and sodium azide were 10-' M, respectively.
Furthermore, as mannitol inhibits water absorption by plant (15), the effect of mannitol
on the root uptake of CO2 was also studied (concentration: 190 mM).
In addition to the above tracer experiments for mannitol, preliminary separate
experiment on water absorption by rice seedlings was carried out at mannitol
concentrations of 0,55, 165, and 275 mM.
Gas collection from roots and CO2 gas analysis. In order to collect the gas in the
roots directly, a modification of YAMADA'S method was devised (16, 17). Roots of rice
and wheat grown in water culture were treated with distilled or CO2 saturated water for 2
h. After the treatments, plant roots were washed once with distilled water and the gas in
the roots was collected immediately. As shown in Fig. 1, whole plants were soaked in
water and roots were cut off at the vicinity of the node beneath the apparatus for gas
collection. Excised roots were pressed manually to have the gas, which was collected
into the apparatus.
The volume of gas collected ranged from 0.8 to 2.0 mI. An aliquot of 250 pI of gas
was sampled with a micro-syringe from the apparatus and was analyzed by gas
chromatography. The successive steps of the operation of gas collection were com-
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128 T.HIGUCHI, K.YODA, and K.TENSHO

syringe

Fig. 1. Method for gas collection from plant roots.

O-bubble

O
leaf blade

syringe leaf sheath

Fig. 2. Pressurization with air in the medullary cavity of rice.

pleted within 5 min.

The instrument (Shimadzu-3AH) used was equipped with TCD and a stainless column
packed with silica gel (60-80 mesh). The temperature of both detector and column was
80°C, and that of the injector was IOO°C.
Injection of air into the medullary cavity of rice. In the previous study, it was noticed
that a part of CO2 derived from root uptake in rice leaked through the aerial tissues to the
atmosphere (6). In order to determine the site of CO2 leakage, the following experiment
was carried out. The main stem of rice at the heading stage was cut off at the level of a
node and the upper part with leaves was soaked in water. As shown in Fig. 2, air was
injected into the medullary cavity and the leakage of the air through the leaf sheath was
monitored by the appearance of air bubbles.
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Root Uptake of CO. in Rice 129

RESULTS

Differences in CO2 fixation between rice and

wheat CO2 fixation includes both dark CO2 fixation in the roots and CO2 fixed by
photo synthesis after being transported to the shoots in the inorganic state. Therefore,
CO2 fixed in the roots represents the total amount of both dark fixation of CO2 in the
roots and organic carbon transported from the shoots to the roots. CO2 fixed in the
shoots corresponds to the total amount of both carbon transported to shoots after dark
fixa tion of CO2 in roots and photosynthetic carbon in shoots.
As shown in Fig. 3, the total amount of CO2 fixed in rice was roughly equal to that
in wheat for a low CO2 level. In the case of a high CO2 level, however, the fixa tion
was far greater in rice than in wheat, and the CO2 fixed in rice was distributed mostly
in the shoots, resulting in the high value of the shoot/root ratio.
Experiments on the time-course of CO2 fixation confirmed the obvious difference
between rice and wheat. As shown in Fig. 4A, the amount of CO2 fixed in the roots of
both rice and wheat and in wheat shoots increased slowly, while that in the rice shoots
increased rapidly. Moreover, as shown in Fig. 4B, the major part of CO2 derived from
root uptake in rice was fixed in the leaf sheath.
Water absorption by rice and wheat was determined by a parallel experiment.
No significant difference in water absorption between the two plants was observed
(Table 1).

Effect of inhibitors on CO2 fixation

Table 2 shows the effects of 2,4-dinitrophenol, sodium azide, or mannitol in the
culture solution on CO2 fixation by rice and wheat seedlings.

C02 fixation (~mol CO2/9 root)

O 50 100 150 200 250

L !J (2.2)

Rice
L (8.8)
H_

53 _ (0.15)

Wheat
(0.90)

Fig. 3. Effect of CO. level in culture solution of fixation of CO. derived from root uptake. L.low CO. in roots.
CO. level; H, high CO. level. D. CO. in shoots; ., Value in parentheses.
ratio of CO. fixation in shoots to that in roots.
Machine Translated by Google

130 T.HIGUCHI, K.YODA, and K.TENSHO

...

O
It is
THERE

.......
200 • 200
0
C.J
B
______ •

O A .--------
/.
./
AND

~ 100o 100

...

to )( ./ •
/.
_A:::::::::=:;??? 6- ::::~

=:=j;=- ~6 0 0 6
120 240 30 60 120 240
Tlme(million) hour (min)
Fig. 4. Time-course of COs fixation in rice and wheat. A: fixation of CO2 derived from root uptake in the root and shoot.
e, rice shoot; 0, rice root; A, wheat shoot; 6, wheat root.
B: fixation of CO2 derived from root uptake in the leaf blade and leaf sheath. e, rice leaf sheath; 0, rice leaf blade;
A. wheat leaf sheath; 6. wheat leaf blade.

Table 1. Water absorption by rice and wheat.

Weight of water absorbed

(H20 gig root/h)

Rice 7. 18±0. YOU

Wheat 7. 16±0. 38

Both 2,4-dinitrophenol and sodium azide inhibited strongly CO2 fixation in the
roots of the seedlings. This inhibitory effect appeared to be more severe in wheat
than in rice and for a low CO2 level than a high level. However, the remarkable
inhibition observed in the roots was not demonstrated in the shoots except for the
case in wheat treated with a low CO2 level.
Figure 5 shows that the treatment of mannitol at a concentration of 165 mM re
sulted in about a 50% decrease in water absorption by rice seedlings. As shown in
Table 2, when the rice roots were treated with 190 mM mannitol, CO2 fixation in
shoots as well as in roots was not inhibited. In contrast, the fixation of CO2 in wheat
shoots was inhibited by about 50% in both treatments of the low and high CO2 levels,
respec tively.

Volume and CO2 content of gas collected from

roots The results are shown in Table 3. The volumes of gas collected from rice
roots were 1.68 and 0.88 ml per gram of dry root for distilled and CO2 saturated
water, respectively. The values for wheat were 0.124 and 0.096 mI. Therefore, it was
evi dent that rice roots contained more gas than wheat roots. The CO2 contents in
the gas collected from rice roots were 100 and 1,280 nmol per gram of dry root for distilled
Machine Translated by Google

Root Uptake of COa in Rice 131

Table 2. Effect of 2,4-dinitrophenol, sodium azide, and mannitol on CO2 fixation by rice and wheat.

% Inhibition
Treatment
Top Root Total

2,4-DNP Rice L 1.8 84.1 27. 3

H 8.3 66. 1 14.5

Wheat L 36.1 94.9 87.4

H 1.7 74.3 40.2

NaNa Rice L 12.0 61. 7 27.9

H -15.4 40.5 -9.7

Wheat L 31. 88.6 81. 3

H 1 -11. 6 61.1 26. 8
Mannitol Rice L 4.4 -14.9 -1.8
H -3.2 -16.1 -4.5
Wheat L 54.4 3.3 9.9

H 49.5 12.6 30.0

L, low CO2 'level; H, high CO2 level. Percentages of inhibition were calculated from the equation: % inhibition=(1-Ft/Fc) x 100, where Fc is the amount of
COl fixed in the control plant and Ft is the amount of CO2 fixed in the treated plant.

c o
...

Jl

100 0 100 200 300

Mannitol cone. (mM)

Fig. 5. Effect of mannitol on water absorption by rice.

Table 3. Volume and CO2 content of gas collected from roots.

CO2 content
Volume
Treatment
(ml/g root) In gas On a root basis (nmol/
(%) g root)

Distilled water Rice 1. 68 0.138 100

Wheat 0.124 0.05 2.8
CO. saturated water Rice 0.88 3.27 1,280
Wheat 0.096 0.21 8.9

Results are expressed as the mean values of two experiments.

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132 T.HIGUCHI, K.YODA , and K.TENSHO

and CO2 saturated water, respectively. Accordingly, it was evident that CO2 enrich
ment in the culture solution enhanced CO2 gas content in roots.

Injection of air into the medullary cavity

As a result of the injection, small bubbles appearing in the adaxial epidermis of the
leaf sheath were observed, as shown in Fig. 2.

DISCUSSION

Form of carbon transported to rice shoots. It has been well documented that plant
roots possess an enzyme system for assimilating CO2 • As phosphoenolpyruvate
carboxylase appears to be the primary enzyme responsible for CO2 fixation in roots
(18, 19), metabolic energy is required for the reaction of carbon reduction. In the study
presented here, it was demonstrated that CO2 fixation in plant roots was mark edly
inhibited by treatments with such respiratory inhibitors as 2,4-dinitrophenol and sodium
azide. These phenomena suggest that CO2 fixation in the roots of rice and wheat
requires metabolic energy.
It was reported that CO2 absorbed by potato roots was transported to leaves in
the form of organic components fixed in the roots as well as in the form of CO2 dis
solved in the xylem sap (5). From the data in Table 2 concerning the inhibition of CO2
fixation by the treatments with respiratory inhibitors in wheat shoots at a low CO2 level,
it was speculated that the decrease in the production of organic compounds such as
malate in roots suppressed the transport of 14C to the shoots.
Meanwhile, the degree of inhibition in shoots was smaller than in roots. If the
carbon transport requires metabolic energy in roots, the degree of inhibition of 14C
fixation in shoots should be the same as that in roots. Nevertheless, the degree of
inhibition in wheat shoots for a low CO2 level was half to one-third of those in its roots.
This finding suggests that a large amount of CO2 absorbed by rice roots is transported
to the shoots in an inorganic form without reduction process of carbon.
Previous study has already pointed out that the inorganic form was thought to be
the principal form for the transport of carbon to the shoots (6). This assumption has
been supported by experiments of 14C analysis in organic and inorganic fractions of
bleeding sap, more recently (20).
It may therefore be concluded that the predominant form of transport to rice
shoots must be the inorganic form.
Route of CO2 transport. As for the route of CO2 transport to the shoots of rice, it
is important to elucidate the causes of the peculiarity of rice in root uptake of CO2,
which is illustrated in Fig. 3. Rice fixed 3 to 5 times more than wheat the amount of
CO2 contained in the medium. In the study presented here, since only CO2 fixation
was studied, the total amount of CO2 absorbed by plant roots can not be estimated
accurately. But some of the authors have measured the amount of CO2 exhausted
and estimated the total amount of CO2 absorbed by the roots (6). The results demon-
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Root Uptake of CO. in Rice 133

strated that rice absorbed 5 to 7 times more than wheat the amount of CO2 contained
in the medium and this fact has been generally accepted. While rice absorbed larger
amounts of CO2 than wheat, the amount of water absorbed by rice was equal to that by
wheat in this experiment, as shown in Table I. This fact suggests that the predom inate
uptake of CO2 by rice roots is not ascribed to water absorption.
As shown in Table 2, the strong inhibitory effect of mannitol on HC transport to
shoots was observed in wheat. In other words, root uptake of CO2 by wheat was closely
linked with water absorption. In contrast, as shown in Table 2 and Fig. 5, 190 mM
mannitol was little inhibitive in CO2 absorption by rice roots, though water absorption
was decreased by 50%. This observation suggests that the uptake of CO2 by the roots
in rice is not controlled by water absorption alone, and that the CO2 ab sorbed by the
roots is transported to the shoots through organs other than the xylem.
Based on the theory of gaseous CO2 transport (14), much of the CO2 absorbed by
rice roots is assumed to be gasified in the root cortex and transported in the gaseous
state to the shoots via the aerenchyma.
As for the gas transport in hydrophytes, it has been already pointed out that
atmospheric O2 is supplied to the roots through the ventilation system (21-25). It has
also been demonstrated that ethylene applied exogenously passed through the rice
body from the roots to the shoots (26) and that methane in lake sediments flowed out
through the air spaces in water lilies (27). On the basis of mass flow, the fixation of CO2
transported from the rhizome in Nuphar was made public recently (28, 29). Since rice is
a typical hydrophyte, a similar transport system for gaseous CO2 may operate.
Site of CO2 gasification. Since one of gasification sites in the rice organ was
assumed to be the root cortex (14), CO2 contents in the root gas were measured, as
shown in Table 3. The content in rice roots treated with CO2 saturated water was
thirteen times higher than that of roots treated with distilled water. Accordingly, the
gasification of the CO2 dissolved in the root cortex was proved to occur.
The gas volumes in the rice roots were far greater than those in wheat roots.
Therefore, the peculiarity of rice in the uptake of CO2 by the roots may be ascribed to
the well developed air spaces in the root cortex.
Another site of gasification may be considered. CO2 transported by the xylem
tissues may be gasified in the air spaces of shoots. But it appears more likely that the
gasification takes place in the root cortex. When CO2 dissolved in water moves across
the root cortex, it must be transferred through a narrow path similar to the film between
the air spaces. It is likely that the major part of dissolved CO2 is gasified.
Leakage of CO2 absorbed by rice roots to the atmosphere through the leaf sheath.
It has been observed by some of the authors that a part of the CO2 derived from rice
roots was evolved to the atmosphere mainly from the lower portion of the leaf sheath,
especially under dark conditions (6). When the leakage of CO2 absorbed by rice roots
is considered, it is necessary to determine the site of the leakage in the leaf sheath.
Although the site for CO2 leakage is usually assumed to be the stoma, the existence of
another possible site was shown as indicated in Fig. 2. The leakage of small bub-
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134 T.HIGUCHI , K.YODA, and K.TENSHO

leaf blade

adaxial
side

Fig. 6. Hypothetical diagram for the transport of COl absorbed by rice roots.

bles from the adaxial epidermis of the leaf sheath was detected by the injection of air
into the medullary cavity.
Since the barriers preventing CO2 leakage from the lysigenous intercellular spaces
of the leaf sheath to the atmosphere are considered to be the cell layer of the adaxial
epidermis and one or two layers of the parenchyma cells, pressurized air may be re
leased directly through the parenchyma and epidermis.
Based on the considerations mentioned above, a hypothetical diagram for the
pathway of CO2 transport can be proposed as shown in Fig. 6.

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