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Plant Physiol, August 2001, Vol. 126, pp. 1698-1705
Formation of Rhamnogalacturonan II-Borate Dimer in Pectin
Determines Cell Wall Thickness of Pumpkin
Tissue1
Tadashi
Ishii,*
Toshiro
Matsunaga, and
Noriko
Hayashi
Forestry and Forest Products Research Institute, P.O. Box 16, Tsukuba Norin Kenkyu Danchinai, Ibaraki 305-8687, Japan (T.I., N.H.);
and National Agricultural Research Center for Kyushu Okinawa Region,
Nishigoshi, Kumamoto 861-1192, Japan (T.M.)
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ABSTRACT |
Boron (B) deficiency results in inhibition of pumpkin
(Cucurbia moschata Duchesne) growth that is accompanied
by swelling of the cell walls. Monomeric rhamnogalacturonan II (mRG-II)
accounted for 80% to 90% of the total RG-II in B-deficient walls,
whereas the borate ester cross-linked RG-II dimer (dRG-II-B) accounted for more than 80% of the RG-II in control plants. The results of
glycosyl residue and glycosyl linkage composition analyses of the RG-II
from control and B-deficient plants were similar. Thus, B deficiency
does not alter the primary structure of RG-II. The addition of
10B-enriched boric acid to B-deficient plants resulted
within 5 h in the conversion of mRG-II to dRG-II-10B.
The wall thickness of the 10B-treated plants and control
plants was similar. The formation and possible functions of a borate
ester cross-linked RG-II in the cell walls are discussed.
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INTRODUCTION |
The results of numerous studies have
shown that boron (B) deficiency results in changes in cell wall
structure, e.g. swelling of the cell walls and the formation of small,
irregularly shaped cells (Brown and Hu, 1997 ; Matoh, 1997). Cell wall
swelling has also been reported to be accompanied by changes in the
appearance of the middle lamella (Kouchi and Kumazawa, 1976).
Inappropriate swelling of the cell wall also occurs in the irregular
xylem mutant Arabidopsis, irx4 (Turner and Somerville,
1997). However, the effects of B on the macromolecular organization of
the cell wall are poorly understood.
The recent discovery that most of the B in the wall is present as a
borate diol diester that cross-links two chains of rhamnogalacturonan II (RG-II) has led to the suggestion that a physiologically important function of B is to cross-link cell wall pectin (Ishii and Matsunaga, 1996; Kobayashi et al., 1996; O'Neill et al., 1996). Such a
cross-linked pectic network is likely to have a role in regulating the
mechanical and biochemical properties of the wall (Fleischer et al.,
1999). Nevertheless, there is only limited evidence on cultured cells showing that borate ester cross-linking of pectin is required for the
normal growth and development of plants (Fleischer et al., 1999; Matoh
et al., 2000).
We now provide evidence to show that the wall of B-deficient pumpkin
(Cucurbia moschata Duchesne, cv Tokyo-Kabocha) plants is
swollen compared with the tissue of B-sufficient plants. Adding boric
acid to B-deficient plants results in the rapid formation of the
borate ester cross-linked RG-II dimer (dRG-II-B) and decrease in wall thickness.
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RESULTS |
The B Contents of Leaves from Pumpkin Plants Grown in the
Presence or Absence of Boric Acid
Pumpkin seeds were germinated in vermiculite. The seedlings were
then grown for 1 week on Hoagland liquid medium containing 10 µM boric acid. The plants were then transferred to a
B-deficient Hoagland medium with or without 25 µM boric
acid and grown for 7 d. The second, third, and fourth leaves were
smaller than the control due to the B deficiency (Table
I). The second, third, and fourth leaves
from B-deficient plants contained between 2.6 and 4.2 µg B
g 1 dry weight, whereas the corresponding leaves
in control plants contained 32 to 39 µg B g1
dry weight. At least 90% of the B from the B-deficient leaves (second
to fourth) was present in the AIR. In contrast, only 28% to 47% of
the B in control leaves (second to fourth) was present in the AIR
(Table I). These results confirm that all B is localized in cell
walls of squash and tobacco under the B-deficient conditions (Hu and
Brown, 1994). The B present in the cotyledons of the plants prior to
their transfer to B-deficient medium is not available to newly forming
leaves. Such a result is consistent with the notion that B must be
supplied continuously during plant growth (Skok, 1957; Loomis and
Durst, 1992; Hu and Brown, 1994).
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Table I.
Pumpkin growth, distribution of B, and dRG-II-B
ratio in pumpkin plants
Plants were precultured for 7 d in 10 µM B. Seven
days prior to harvest, one-half of the plants were transferred to
B-free solution and the remaining one-half were transferred to 25 µM B. Fresh leaf wt was expressed as means ± SE (n = 8). Alcohol-insoluble residue (AIR)
were isolated from each leaf (details in "Materials and Methods").
B was determined in the leaf and AIR samples by inductively coupled
plasma-mass spectrometry (ICP-MS). Data are means of three replicates
and SE are shown.
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Anatomical Observation
Light microscopic analysis indicated that the cells of the
B-deficient second leaf and petiole are smaller and more irregular than
their B-sufficient counterparts. The B-deficient cells were shorter by
70% and 20% in the longitudinal and transverse directions, respectively, than those supplied with B. Transmission electron microscope examination showed that the B-deficient cell walls were
swollen compared with the thin-walled normal cell (Fig.
1, A and B). When the B-deficient plants
were treated for 5 h with boric acid, the thickness of their cell
walls and control plants were comparable (Fig. 1, A and C). In general,
the cell wall of B-defecient plants had disorganized middle lamellae. A
similar phenomenon was observed of B-deficient root tip of
Lycopersicon escurentum (Kouchi and Kumazawa,
1976).
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Figure 1.
Transmission electron microscope of the
second leaf from pumpkin grown in B-normal, B-deficient, and B-treated
conditions. A, B-normal leaf; B, B-deficient leaf; C, B-deficient and
then B-treated for 5 h leaf. Scale bar is 1 µm. The mid-lamellae
region is easily distinguishable as the very dark staining region in
the center of the walls.
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Characterization of the RG-II from AIR of B-Deficient, B-Grown, and
10B-Treated Pumpkin
We have shown that B-deficient pumpkin petioles and leaves have
swollen cell walls when compared with control plants. The addition of
boric acid to the B-deficient plants results in the appearance of cells
whose wall thickness is comparable to that of control plants. We now
show that this morphological change is correlated with increase in the
proportion of dRG-II-B in the walls.
When B-deficient pumpkin plants were transferred to
10B-enriched boric acid medium, the
10B content and abundance in the third leaf and
the binding of 10B to the cell wall gradually
increased (Fig. 2). The
10B abundance in the leaves increased to 0.6 after 5-h exposure to the 10B boric
acid-containing medium.
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Figure 2.
The binding of B to B-deficient third leaves and
formation of 10B-containing dRG-II-B after the
addition of 10B-enriched boric acid. At the
indicated times the third leaves were harvested (details in
"Materials and Methods"). B content in the leaves and AIR was
determined by ICP-MS. The ratio of dRG-II-B and monomeric RG-II
(mRG-II) was determined by SEC/refractive index detector. A, B content
in the leaf. B, B content in AIR, which was calculated from B content
determined by ICP-MS and the yield of AIR. Ratio of dRG-II-B and mRG-II
was determined by SEC/refractive index detector. Data are means of
three replicates and SE are shown.
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The AIR prepared from the third leaf of B-deficient, B-normal, and
10B-treated for 22 h pumpkin contained 0.3, 1.4, and 1.5 µ 77 B g1, respectively (Table
II). The AIR from these plants had
similar glycosyl residue compositions and contained similar amounts of RG-II (Table II).
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Table II.
Glycosyl residue compositions and RG-II and B
contents of AIR isolated from pumpkin grown in the presence or absence
of boric acid and 10B-treated pumpkin
AIR was isolated from the third leaf. The values given are for those
glycosyl residue that accounted for >1 mol % of the leaves of plants.
The glycosyl residues that are diagnostic of RG-II (2-O-Me
Fuc, 2-O-Me Xyl, and apiose) each accounted for <0.5 mol % of the AIR.
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The AIR from the cotyledons and the leaves of B-deficient and B-normal
pumpkin was saponified and then treated with EPG. The ratio of dRG-II-B
and mRG-II in the EPG-soluble material then was determined by SEC with
RI. The RG-II dimer accounted for >80% of the total RG-II in the
cotyledon and the first to fourth leaves of the control plant (Fig.
3A; Table I). In contrast, mRG-II accounted for between 80% and 90% of the RG-II in the third and fourth leaves of the B-deficient pumpkin (Fig. 3B; Table I). The
proportion of mRG-II decreased to 65%, 12%, and 7% in the second
leaf, the first leaf, and the cotyledon, respectively. This result was
expected because the cotyledon and first leaf were formed during the
period when the plant was grown in the presence of B. Taken together,
these results establish that in the B-deficient tissues RG-II is
present mainly as a monomer and that dRG-II-B is predominant under the
B-sufficient conditions.
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Figure 3.
SEC/RI and SEC/ICP-MS of the EPG-soluble material
from the AIR of pumpkin grown in the presence or absence of boric acid
and treated with 10B-enriched boric acid. AIR was
prepared from the third leaf. A, SEC/RI profile of the AIR from plants
grown in the presence of boric acid (25 µM). B, SEC/RI
profile of the AIR from plants grown in the absence of boric acid. C,
SEC/RI profile of the AIR from growing B-deficient plants that had been
treated for 7 h with 10B-enriched boric acid
(25 µM). The chromatograms A, B, and C were obtained with
the Superdex-75 column. The Superdex-75 column was calibrated with
sugar beet dRG-II-B (approximately 9.4 kD) and sugar beet mRG-II
(approximately 4.7 kD), which have retention times at 21.0 and 23.2 min, respectively. Pullulans of 23.7 and 5.8 kD eluted at 15.8 and 22.4 min, respectively. The inner volume of the column using Glc was
31.8 min. D through F, the 10B and
11B profiles obtained by SEC/ICP-MS analysis of
the 11B-normal, B-deficient, and
10B-treated pumpkin AIR, respectively. The
chromatograms D through F, were obtained with the Diol-120 column
(details in "Materials and Methods"). dRG-II-B and boric acid were
eluted at 8.1 and 13.2 min, respectively. A large peak of boric acid in
chromatogram D was due to the boric acid contaminant in the enzyme
buffer.
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dRG-II-B and mRG-II were isolated from the B-grown pumpkin AIR, and
mRG-II was isolated from the B-deficient plant. The glycosyl composition and glycosyl linkage analyses of these RG-IIs were similar
(Tables III and
IV). The apiosyl residues in mRG-II are 3'-linked, whereas in dRG-II-B they are 3'- and 2, 3, 3'-linked (Table
IV), confirming that 3'-linked apiosyl residues are the site of borate
esterification (O'Neill et al., 1996; Ishii et al., 1999). The mRG-II
from the B-deficient plants was converted to dRG-II-B in vitro by
treatment with boric acid and lead acetate (O'Neill et al., 1996),
showing that all of the mRG-II synthesized by these plants is capable
of forming a dimer.
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Table III.
Glycosyl residue compositions of the mRG-II and
dRG-II-B isolated from pumpkin leaf in the presence or absence of boric
acid and 10B-treated pumpkin
AIR was isolated from the second to the fourth leaves. RG-II was
isolated by SEC from EPG digests of the AIR of pumpkin leaf grown in
the presence (25 µM) or absence of boric acid and
10B-treated leaf. The neutral and acidic glycosyl residues
were determined by gas-liquid chromatography analysis of alditol
acetates and trimethyl silyl derivatives, respectively.
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Table IV.
Glycosyl linkage composition of the mRG-II and
dRG-II-B isolated from pumpkin grown in the presence or absence of
boric acid and 10B-treated pumpkin
AIR was isolated from the second to the fourth leaves. RG-II was
isolated from EPG digest of the AIR of pumpkin leaf grown in the
presence (25 µM) or absence of boric acid and
10B-treated leaf.
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To establish that adding 10B-enriched boric acid
to B-deficient plants results in the formation of
dRG-II-10B in muro, the AIR treated with
10B-enriched boric acid was digested with EPG and
the solubilized material analyzed by SEC/RI and by SEC in
combination with ICP-MS. SEC/ICP-MS analysis showed that the
dRG-II-B isolated from 10B-enriched boric
acid-treated plants was enriched with 10B
(10B abundance = 0.6, Fig. 3F), whereas the
dRG-II-B from pumpkins grown in the presence of
11B boric acid contained B in the expected
natural abundance ratio (10B abundance = 0.2, Fig. 3D). dRG-II-B accounted for approximately 80% of the total
RG-II in 10B-enriched boric acid-treated for
22 h plants (Fig. 2B). dRG-II-10B and mRG-II
isolated from the 10B-treated for 16 h
pumpkin and the RG-II from plants grown continuously in the presence of
B have similar glycosyl residue and glycosl linkage compositions
(Tables III and IV). These results confirm that normal RG-II is
synthesized under B-deficient conditions and that the mRG-II is able to
form dRG-II-B in the B-sufficient conditions in muro.
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DISCUSSION |
mRG-II in B-Deficient Plants Has Similar Glycosyl Residue
Composition with dRG-II-B in B-Normal Plants
We have shown that pumpkin cell walls contain similar amounts of
RG-II, irrespective of whether they are grown in the presence or
absence of B. The RG-IIs isolated from the B-deficient, B-normal, and
10B-treated pumpkin were structurally similar.
However, the relative proportions of dRG-II-B and mRG-II are correlated
with the amount of water-insoluble wall B. We conclude that in muro B
deficiency results in a significant reduction in the borate ester
cross-linking of RG-II.
Our results are consistent with the notion that a primary function of B
is as a structural component of the cell wall (Loomis and Durst, 1992;
Brown and Hu, 1997; Matoh, 1997; Fleischer et al., 1999). Our data
confirm that B-deficient cells and cells grown in the presence of B
have walls with similar glycosyl residue compositions (Goldbach and
Amberger, 1986; Fleischer et al., 1999).
The Relationship between Cell Wall Physical Properties and the
dRG-II-B Formation
The primary wall of dicots and non-graminaeous monocots consists
of a rigid, rod-like cellulose/xyloglucan load-bearing network that is
embedded in and interacts with a compression-resistant pectin network
(Carpita and Gibeaut, 1993). Cross-linking cell wall polymers and
alternation in cell wall compositions are most likely to determine wall
mechanical properties. We have shown that the cell wall thickness of
the leaves is correlated inversely with the dRG-II-B formation of their
walls. The addition of boric acid to the B-deficient plant results in
the binding of B to the cell walls, the formation of dRG-II-B from
mRG-II, and repacking the matrix into a firm, thin wall. The swelling
is due to the lack of cross-linking of borate ester of RG-II, not to
the increase in density of the wall. A similar type of swelling of cell
wall is observed during certain stages of development or in mutants. The classic swelling phenomenon is that of softening fruits, such as
tomato and kiwifruit, which is attributed to the breakage of cross-linking of tightly packed pectins (Redgwell et al., 1997). Inappropriate swelling occurs in the irregular xylem mutant,
irx4 (Turner and Somerville, 1997). In this instance, a
disruption in normal lignin distribution in the tracheary elements
results in the swelling of the cellulosic matrix into the lumen. It
should be emphasized that in contrast to above phenomena, the swelling of wall caused by B deficiency is reversible. When B-deficient pumpkin
plants were transferred to B-sufficient medium, B binding to the cell
occurred over a period of hours. 10B binding to
the cell wall and the formation of dRG-II-10B was
observed within 2.5 h and after 7 h
dRG-II-10B accounted for approximately 60% of
RG-II. B-deficient suspension-cultured Chenopodium album
cells increased in wall pore size (Fleischer et al., 1999). Adding
boric acid to growing B-deficient cells results within 10 min in the
formation of dRG-II-B from mRG-II and a reduction in wall pore size.
The differences in the rate of dimer formation in plant tissue and in
cultured cells are likely to be due to the rate at which B gets to the
wall. B has immediate access to the walls of cultured cells, whereas in
plants B must be taken up by the root and then transported to the
developing leaves. However, the possibility cannot be discounted that
the delay of B binding and formation of dRG-II-B in B-deficient pumpkin is also due to the impairment of growth and development of meristematic tissue kept under B deficiency for a week.
To compensate for loss of negative charged borate ester, B deficiency
would increase in free-charged density of pectin by de-esterification.
One interesting question concerns degree of methyl esterification and
methyl esterase activity due to B deficiency.
In summary, we have shown that the form of RG-II in the walls of
B-deficient pumpkin is mainly mRG-II. The formation in muro of dRG-II-B
from mRG-II following the addition of boric acid is accompanied by wall
condensation. Our data provide additional support for the hypothesis
that B is a structural component of the cell wall and suggest that B is
required for the formation of a covalently cross-linked pectic network
(Ishii and Matsunaga, 2001) and this network has a role in determining
cell wall mechanical properties.
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MATERIALS AND METHODS |
Plant Material and Growth Conditions
Pumpkin (Cucurbia moschata Duchesne cv
Tokyo-Kabocha) seeds were purchased from Sakata Seed company (Yokohama,
Japan). The seeds contain on average 18 µg B g1 and
average seed weight was 200 ± 5 mg (SE,
n = 25). Seeds were sown in washed vermiculite and
grown for 7 d at 22.5°C, 12-h day length. The plants were then
transferred to 4-L plastic containers containing one-quarter-strength
Hoagland solution (Hoagland and Arnon, 1950) supplemented with 10 µM B. After 1 week, the plant roots were rinsed
thoroughly with B-free distilled water and the plants were then
transferred to fresh medium containing 25 µM B or no B
(<0.14 µM B). To avoid boric acid contamination, 2 mL of
the borate-binding ion-exchange resin IRA-743 was added to the
B-deficient medium. Fifteen plants were grown in the container. The
plants were grown for 1 additional week and then harvested. At this
stage, plants had developed four leaves. The leaves from the same
relative positions on each plant were separately collected, immediately frozen in liquid nitrogen, and then freeze dried. The major
veins of the leaves were removed and the remaining leaf blade was cut
into small pieces and then divided into two equal portions, 0.2 to
0.5 g dry weight. One portion was used to determine total B
content, and the second portion was used to prepare the AIR.
Pumpkin grown in B-deficient medium for 1 week was transferred to
10B-enriched boric acid (95 atom %, 25 µM)
containing medium and grown further. At certain periods, the third leaf
was harvested and treated with the same procedures as the normal boric
acid samples for the determination of 10B and formation of
dRG-II-10B. The second to fourth leaves of the pumpkin
grown in 10B-enriched boric acid for 16 h was used for
structural analysis of RG-II.
Preparation of the AIR from Pumpkin Leaves
The dried leaf was suspended in aqueous 80% (v/v) ethanol and
homogenized for 0.5 min at 1,500 rpm using a Polytron blender (Physco-Troller NS-610, Nichion Rikakikai Co, Tokyo). The suspensions were centrifuged at 2,500g for 5 min. The insoluble
residue was then washed with 80% (v/v) ethanol, 95% (v/v) ethanol,
100% (v/v) ethanol, chloroform: methanol (1:1, v/v), and
acetone and then air-dried.
Solubilization of RG-II from AIR of B-Deficient,
10B-Treated, and B-Normal Pumpkin
The AIR was treated for 4 h at 4°C with 0.1 N
sodium hydroxide to saponify the methyl and acetyl esters. The
suspensions were adjusted to pH 5.0 with 10% (v/v) glacial acetic
acid and then treated for 16 h at 30°C with homogeneous
preparation of EPG from Aspergillus niger (2.5 units,
Megazyme, Wicklow, Ireland; 1 unit releases 1 µmol of reducing sugar
min1 from a 1% [w/v] solution of poly-GalUA at pH 5.0 and 25°C). The suspensions were centrifuged and the insoluble
residues washed with water. The EPG-soluble fractions were dialyzed
(1.0-kD cutoff tubing) against deionized water and freeze dried. EPG
treatment solubilized 10% and 15% of the weight of the B-normal and
B-deficient AIR, respectively.
Pumpkin RG-II was purified from the EPG-solubilized material by
SEC on a Sephadex G-75 (2.5 × 90 cm) and Superdex Prep 75 (Amersham Pharmacia Biotech Inc., Uppsala, 1.6 × 38 cm) columns. For structural analysis of RG-II, AIR isolated from the second to the
fourth leaves was used.
Determination of Ratio of the dRG-II-B and mRG-II in
AIR
The AIR (10 mg) was saponified and digested with EPG (2 units).
The suspension was centrifuged. The supernatant was subjected to SEC/RI
with a Superdex 75 column as described below.
Anatomical Determination
A strip of leaf tissue (approximately 1 cm2) was
excised from the second leaf of B-deficient, B-normal, and the
B-deficient plant grown for 5 h in the presence of B boric acid
(25 µM ). Four leaves of each plant were used and eight
strips were cut from each plant. The leaf strips were fixed for 60 min
in 2.5% (w/v) glutaraldehyde in 0.1 M potassium phosphate,
pH 6.8, and then washed with distilled water. The leaf strips were
dehydrated using a graded series of ethanol (30%, 50%, 70%, 80%,
90%, 95%, and 100% [v/v] ethanol) and propylene-oxide and
then embedded in epoxy resin. Ultra-thin sections (0.1-µm thickness)
were cut with a diamond knife and stained with 0.1% (w/v) uranyl
acetate and lead citrate in 0.1 M sodium hydroxide
solution. Stained sections were examined with a transmission electron
microscope (JEOL 2000 EX, JEOL, Tokyo) at 200 kV. Sections (1 or 2 µm
thick) for light microscopy were cut using a glass knife.
Analytical Methods
SEC/RI was performed with an LC-6A system (Shimadzu, Kyoto) with
an RI (Shimadzu model RID-6A) connected to a Superdex-75 HR 10/30
column (Amersham Pharmacia Biotech Inc.) eluted at 0.6 mL
min1 with 50 mM ammonium formate, pH 5.3, as
described (Ishii and Matsunaga, 1996). The mRG-II and dRG-II-B in the
EPG digests was confirmed by comparing their retention time with those
of the authentic mRG-II and dRG-II-B from sugar beet and red wine.
SEC/ICP-MS was performed with a Diol-120 column (8 × 300 mm,
YMC, Kyoto) connected to the ICP source of a mass spectrometer
SII-SPQ9000A (Seiko Instruments Inc, Chiba, Japan). The column was
eluted at 1 mL min1 with 200 mM ammonium
formate, pH 6.5. The mass spectrometer was operated to selectively
detect 10B and 11B. The B content and
10B abundance of the AIR was determined by the
ICP-MS.
Uronic acid was determined by the m-hydroxybiphenyl
method (Blumenkrantz and Asboe-Hansen, 1973). The neutral and acidic
glycosyl residue compositions of the AIR and RG-II were determined by
GC-MS analysis of the alditol acetate derivatives and trimethylsilyl methyl glycoside derivatives, respectively (York et al., 1985). The
glycocyl linkage compositions were determined by a modified Hakomori
procedure method (Ishii et al., 1999).
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ACKNOWLEDGMENTS |
We thank Malcolm A. O'Neill (Complex Carbohydrate Research
Center, University of Georgia, Athens) for critical reading of the
manuscript. Masako Ishikawa (Forestry and Forest Products Research
Institute) is acknowledged for growing the pumpkin plants and preparing
the manuscript.
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FOOTNOTES |
Received February 26, 2001; returned for revision April 20, 2001; accepted May 17, 2001.
1
This work was supported by the Ministry of
Agriculture, Forestry, and Fisheries (Research Grant no.
BDP-01-II-2).
*
Corresponding author; e-mail tishii{at}ffpri.affrc.go.jp; fax
81-298-74-3720.
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ABSTRACT
INTRODUCTION