American Journal of Plant Sciences, 2012, 3, 1619-1624
http://dx.doi.org/10.4236/ajps.2012.311196 Published Online November 2012 (http://www.SciRP.org/journal/ajps)
1619
Stimulation of Root Growth Induced by Aluminum in
Quercus serrata Thunb. Is Related to Activity of Nitrate
Reductase and Maintenance of IAA Concentration in
Roots
Rie Tomioka1, Chisato Takenaka1, Masayoshi Maeshima1, Takafumi Tezuka1, Mikiko Kojima2,
Hitoshi Sakakibara2
1Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya, Japan; 2RIKEN Plant Science Center, Yokohama, Japan.
Email: tomiokar@agr.nagoya-u.ac.jp
Received August 10th, 2012; revised September 24th, 2012; accepted October 16th, 2012
ABSTRACT
Aluminum (Al) is the most abundant metal in the earth’s crust. Excess Al3+ released by soil acidification in soil solution
is thought to be a growth limiting factor to many cultivated plant species, but it has been reported to stimulate plant
growth in some crop and tree species in certain concentration of Al3+. Previously, we had reported that Al treatment
enhanced root development, uptake from growth media and in vivo nitrate reductase (NR) activity of roots. NR
is one of the key enzymes in nitrogen metabolism and acts at the first step of nitrate assimilation in plants. In this study,
we investigated the process of Al-induced root development in an early stage, focusing on the change in in vitro NR
activity, and indole-3-acetic acid (IAA) and cytokinins concentration in roots of Quercus serrata seedlings, which were
treated for 1 h with Al or Ca. In Al-treated roots, NR activity increased and IAA concentration was maintained at the
same level as pretreatment, and indole-3-acetyl-L-aspartic acid (IA-Asp), which is a metabolic intermediate of IAA
degradation, was not detected in roots. In Ca-treated roots, NR activity increased, but IAA concentration decreased as
IA-Asp concentration increased. Thus, the maintenance of IAA concentration in Al-treated roots seems to result from
suppression in the process of IAA decomposition. Al treatment increased the length and number of second lateral roots
but Ca treatment did not. We concluded that root development induced by Al in the early stage was related to NR activ-
ity and maintenance of IAA concentration.
3
NO
Keywords: Aluminum; Root; Development; NR; IAA; Quercus serrata
1. Introduction
Aluminum (Al), a component of primary and clay miner-
als, is the most abundant metal element on the planet,
comprising about 7% by mass of the earth’s crust. Al is
released from the solid phase by soil acidification, and
exchangeable Al increases when the pH of soil solution
falls below 5.0. At a pH of less than 4.0, Al exists pre-
dominantly as Al3+. Excess Al3+ in soil solution is con-
sidered to be toxic to cultivated plant species and is a
limiting factor for plant growth in acidic soil. The pH of
rhizospheric soil around the roots is lower than that of
the bulk soil due to release of H+ and organic anions
from the roots, accompanied by the uptake of cations and
respiration. Under these conditions, the concentration of
Al3+ around the roots is thought to be higher than that of
the average of the bulk soil [1-4]. Therefore, most plant
roots are thought to be exposed to high concentrations of
Al3+. Although there are many reports about negative
effects of Al on plant growth in both crop and tree spe-
cies, enhancement of growth by Al treatment was re-
ported much less than that and only a few in both crops
and trees [5-9], and there seems to be an optimum con-
centration of Al for each plant species. Although much
information on the mechanism of Al toxicity and Al tol-
erance in plants has been published [10,11], few reports
have focused on the role of Al in plant growth.
Previously, we reported that Al enhanced root growth
in Quercus serrata Thunb. seedlings in experiments with
various Al treatments, and suggested that Al might act as
a trigger to induce root elongation and rooting at 1.0 mM
and 2.5 mM [7]. Then we showed that Al enhancement
of root growth is related to stimulation of 3
NO
uptake
and activation of in vivo nitrate reductase (NR) in roots
Copyright © 2012 SciRes. AJPS
Stimulation of Root Growth Induced by Aluminum in Quercus serrata Thunb. Is Related to
Activity of Nitrate Reductase and Maintenance of IAA Concentration in Roots
1620
[12]. Recently, lateral root development induced by NO
has been reported to be related to auxin signaling and NR
activity for Lycopersicon esculentum [13] and Arabidop-
sis thaliana [14]. Therefore, we considered that NR ac-
tivity and auxin might be a key factor in Al-enhanced
root growth in Q. serrata. In our previous study, stimula-
tion of 3 uptake and an increase in the number of
lateral root primordia were observed in plants 3 days
after Al treatment, but no increase in NR activity in roots
measured by an in vivo system was detected after 3 days
[12]. NR activity could not be detected possibly because
in an in v ivo system NR activity is measured according to
the final amount of 2 after some consumption
through the metabolic processes in root cells.
NO
NO
Phytohormones, especially indole-3-acetic acid (IAA)
and cytokinins, are key factors in the regulation of plant
growth, including root development [15,16]. We hy-
pothesize that Al may act as an activator of NR in root
cells and as a trigger to change the concentration of phy-
tohormones such as auxin and cytokinin, which induce
root development, in roots. Therefore to clarify the proc-
ess/mechanism of Al-induced root development in an
early stage, roots were treated with Al for 1 h to observe
the change of in vitro NR activity, the concentrations of
IAA and cytokinins, and root morphogenesis.
2. Materials and Methods
2.1. Plant Materials
Seeds of Q. serrata were collected from a secondary for-
est at Nagoya University, Japan. Seeds were germinated
in siliceous sand. After root germination, seedlings were
grown hydroponically in a modified version of the 1/10
Hoagland’s No. 2 nutrient solution, containing 0.6 mM
KNO3, 0.4 mM Ca(NO3)2·4H2O, 0.2 mM MgSO4·7H2O,
0.1 mM NH4H2PO4, 45.5 µM MnCl2·4H2O, 8.95 µM
FeCl3·6H2O, 0.4 µM ZnSO4·7H2O, 0.15 µM CuSO4·5H2O,
2.3 µM H3BO3, and 0.25 µM NaMoO4·2H2O in a growth
chamber at 23˚C with 65% relative humidity, in a photo-
period of 14 h/10 h (day/night) and irradiation of 150
µmol·m2·s1 for 8 weeks. The nutrient solution was
changed once a week and the pH of the solution was ad-
justed to 4.0 ± 0.1 with 1 N HCl.
2.2. Al Treatment of Seedlings
Roots of 8-week-old seedlings were exposed to 2.5 mM
AlCl3 (pH 4.0) or 4.2 mM CaCl2 (pH 4.0) solution for 1 h,
which was then replaced with freshly prepared nutrient
solution. Roots were collected from seedlings before
treatment and 1, 2, and 3 days after the 1-h treatment. 15
seedlings were collected in each treatment at each sam-
pling time, and 5 cm from the tip of the first lateral roots
and the whole tissue of the second lateral roots were col-
lected and used for further analyses.
2.3. Enzyme Extraction and Assay of NR
Activity
For preparation of enzyme fractions, all subsequent steps
were carried out at 0˚C to 4˚C. Roots were homogenized
in a mortar with a grinding medium composed of 50 mM
tris(hydroxymethyl)aminomethane (Tris-HCl, pH 7.5),
10 mM Ethylenediaminetetraacetic acid tetrasodium
(Na2-EDTA), 5 mM dithiothreitol (DTT), 1% bovine
serum albumin (v/v), 20 µM p-amidinophenyl methane-
sulfonyl fluoride hydrochloride (p-APSMF), and 50%
[wt/wt] polyvinylpolypyrorolidone (Polyclar AT). The
homogenates were filtered with a layer of Miracloth
(Calibiochem-Novabiochem, San Diego, CA, USA). The
filtrate was centrifuged at 15,000 g for 10 min. The su-
pernatant was applied to a Sephadex-G25 column (GE
Healthcare Bio-Sciences, Uppsala, Sweden; gel volume,
5 ml) equilibrated with 50 mM Tris-HCl (pH 7.5), 1 mM
Na2-EDTA, 5 mM DTT, and 20 µM p-APSMF. The pro-
tein (enzyme)-rich flow through fractions was collected
and used for the NR assay.
NR activity was measured by a modified version of the
method of Hageman & Reed [17] as follows. The reac-
tion mixture (1 ml) containing 23 mM K3PO4 (pH 7.5),
4.5 mM KNO3, 9 µM flavin adenine dinucleotide (FAD),
69 µM nicotinamide adenine dinucleotide reduced
(NADH), and enzyme fraction was incubated at 30˚C for
30 min in the dark. The reaction was stopped by adding
0.1 ml of the 0.5 M zinc acetate. Then the mixture was
centrifuged at 5000 g for 5 min. An aliquot (0.75 ml) of
the supernatant was mixed with 16 µl of 0.15 mM
phenazine methosulfate (PMS) and incubated at 25˚C for
20 min. Then, 0.5 ml of 1% sulfanilamide (in 1.5 M HCl)
and 0.5 ml of 0.02% N-1-naphthyl ethylenediamine di-
hydrochloride were added to the incubated solution. Af-
ter incubation at 25˚C for 20 min, absorbance at 540 nm
of the sample was measured using a spectrophotometer
(model U-3310, Hitachi, Tokyo, Japan). NR activity on a
fresh weight (fw) basis was calculated.
2.4. Extraction and Quantification of
Phyto-Hormones
The roots were collected from 15 seedlings before treat-
ment and 1, 2, and 3 days after the 1-h treatment, as
mentioned above. Plant hormones such as IAA and cyto-
kinins in root tissues were extracted and quantified using
a liquid chromatography-tandem mass chromatography
system (Waters; AQUITY UPLC System/Quattro Ultima
Pt), as described previously [18]. Also, the amount of
indole-3-acetyl-L-alanine (IA-Ala), indole-3-acetyl-L-
Copyright © 2012 SciRes. AJPS
Stimulation of Root Growth Induced by Aluminum in Quercus serrata Thunb. Is Related to
Activity of Nitrate Reductase and Maintenance of IAA Concentration in Roots
Copyright © 2012 SciRes. AJPS
1621
mately 50% 2 days after treatment. As IAA level de-
creased, IA-Asp concentration increased in Ca-treated
roots (Figure 2(b)). Other metabolic intermediate of
degradation of IAA, such as IA-Ala, IA-Ile, IA-Leu,
IA-Trp and IA-Phe, were not detected in both treatments.
aspartic acid (IA-Asp), indole-3-acetyl-L-iso-leucine (IA-
Ile), indole-3-acetyl-L-leucine (IA-Leu) and indole-3-
acetyl-L-phenylalanine (IA-Phe), which are a metabolic
intermediate of degradation of IAA, was determined to
assess turnover of IAA.
We detected 17 cytokinin species (data was not
shown), including active cytkinins such as N6-(2-
isopentenyl)-adenine (iP) and trans-zeatin (tZ) (Figures
2(c) and (d)). There were not clear difference between Al
and Ca treatment in both active cytokinins, but the total
amount of cytokinins in Ca-treated roots gradually in-
creased to approximately 1.79 pmol/g fw at 3 days after
treatment. The total level of active cytokinins in Al-
treated roots was lower than that of Ca-treated roots, es-
pecially on day 3 (Figures 2(c) and (d)).
2.5. Root Morphogenesis
The lengths of the first and second lateral roots were
measured before, 3 and 7 days after the 1-h treatment and
the numbers of second lateral roots were counted 7 days
after the 1-h treatment by LIA 32 software [19].
3. Results
The lengths of first and second lateral roots did not
change 3 days after 1-h treatment with Al or Ca (data not
shown). At 7 days after treatment, the length and number
of Al-treated second lateral roots were significantly in-
creased compared with those of pretreatment and Ca-
treated roots (Table 1).
4. Discussion
To elucidate the stimulatory effect of Al on lateral root
development in an early stage, in this study we focused
on in vitro NR activity and the phytohormones such as
auxin and cytokinins.
The in vitro NR activity gradually increased to 175%
on day 3 after 1-h treatment with both Al and Ca com-
pared with pretreatment levels. However, there was no
obvious difference between treatments (Figure 1).
Previously, we reported that rhizospheric Al enhanced
NR activity measured using an in vivo system and in-
creased lateral root primordia in 2-year-old Q. serrata
seedlings [12]. In the present study, we also confirmed
IAA concentration (87.3 pmol/g fw) in Q. serrata
roots was comparable with that of rice (82.1 pmol/g fw)
[18]. IAA concentration in in vitro cultured shoots of Q.
robur was about 300 to 700 nmol/g dry weight (dw) in
basal area and about 10 to 70 nmol/g dw in apical section
[20]. IAA concentration in roots of Q. serrata was about
82 to 88 pmol/g fw in the present study, so the IAA con-
centration in Q. serrata roots was very low compared
with that of Q. robur shoots. The IAA level in roots
treated with Al remained at the same level as that of the
pretreatment sample until 2 days after 1-h treatment
(Figure 2(a)). In this study, the amount of metabolic
intermediate of degradation of IAA, was also determined
to assess turnover of IAA. IA-Asp was not detected in
the Al-treated roots even after 2 days (Figure 2(b)). IAA
concentration in Ca-treated roots decreased by approxi-
Figure 1. The activity of NR in roots measured by an in
vitro system at 0 (Pre), 1, 2, and 3 days after treatment with
2.5 mM AlCl3 (pH 4.0) (Al) or 4.2 mM CaCl2 (pH 4.0) (Ca)
for 1 h. Vertical bars represent the means ± SE (n = 3).
Table 1. Length of first and second lateral roots and number of second lateral roots at 0 (Pre) and 7 days after treatment.
Roots of 8-week-old seedlings were treated with 2.5 mM AlCl3 (pH 4.0) or 4.2 mM CaCl2 (pH 4.0) solution for 1 h and then
replaced with freshly prepared nutrient solution.
First lateral roots Second lateral roots
Length Length Number
Pre After 7 days Pre After 7 days After 7 days
Treatment
(cm) (cm) (cm) (cm) (number/cm)
Al 25.5 ± 2.1 28.4 ± 3.0 2.62 ± 0.23 4.45 ± 0.33** 2.5 ± 0.3**
Ca 25.4 ± 2.4 27.5 ± 3.0 2.29 ± 0.12 2.58 ± 0.31 1.7 ± 0.2
V
alues are the means ± SE (n = 20). Asterisks indicate significant differences between Al treatment and Ca treatment (p < 0.01) according to the t-test.
Stimulation of Root Growth Induced by Aluminum in Quercus serrata Thunb. Is Related to
Activity of Nitrate Reductase and Maintenance of IAA Concentration in Roots
1622
(a) (b)
(c) (d)
Figure 2. Concentration of phytohormones: IAA (a), IA-
Asp(b), iP(c), and t Z (d) in roots at 0 (Pre), 1, 2, and 3 days
after treatment. Roots of 8-week-old seedlings were treated
with 2.5 mM AlCl3 (pH 4.0) or 4.2 mM CaCl2 (pH 4.0) solu-
tion for 1 h and then replaced with freshly pre- pared nu-
trient solution. Vertical bars represent the means ± SE (n =
3). Asterisks indicate significant differences between Al
treatment and Ca treatment (p < 0.05) according to the
t-test.
that Al treatment enhanced NR activity in roots measured
using an in vitro system and was detected 1 day after 1-h
2.5 mM Al treatment (Figure 1). The activity of NR in
roots treated with 2.5 mM Al was slightly higher than
that of root treated 4.2 mM Ca after a day from 1-h
treatment, however, it did not show clear differences
between Al and Ca treatments after 2 and 3 days (Figure
1). Both Al and Ca are able to reduce the surface poten-
tial and neutralize negative surface charge by binding to
membrane phospholipids [21,22]. In our previous study,
the uptake of 3 by roots from the cultivation me-
dium was enhanced at 3 days after Al treatment, which
was considered to be a result of an increase in positive
charge on root cell membrane [12]. Thus, it is considered
that enhancement of NR activity induced by 1 h treat-
ment with Al or Ca may be involved in an increase in
3 influx, caused by an increase in positive charge on
the cell membrane due to absorption of Al3+ or Ca2+.
Moreover, these observations support our previous hy-
pothesis that enhancement of NR activity in Al-treated
roots may be induced by promotion of 3
NO
NO
NO
uptake
due to a change in the surface polarity of the cell mem-
brane.
The growth hormone auxin has many roles in plant
development [15]. It plays a central role in cell growth,
gravitropism, apical dominance, lateral root initiation,
leaf abscission, vascular differentiation, flower bud for-
mation, and fruit development [15,23]. In this study, we
succeeded in determining the concentrations of IAA and
a metabolic intermediate of degradation of IAA (IA-Asp).
IAA concentration in Al-treated roots was kept at the
same level as in pretreated roots, and IA-Asp was not
detected 1 and 2 days after 1-h Al treatment, whereas
IAA concentration in roots treated with Ca for 1 h de-
creased and a relatively high amount of IA-Asp was de-
tected at all stages (Figure 2(b)). This result indicates
that IAA concentration is maintained at more than 82
pmol/g fw in Al-treated roots because Al may limit irre-
versible inactivation or metabolic degradation of IAA.
The concentration of each active cytokinin species did
not show an obvious tendency to vary between treat-
ments (Figures 2(c) and (d)). The mechanisms of nitro-
gen assimilation and nitrogen acquisition which involves
plant hormones have been shown, and it has reported that
endogenous or exogenous cytokinin took part in process
of NR activation [24]. In this study, there was not clear
relationship between iP or tZ and NR activity in root
after 1-h Al or Ca treatment. At present, the physiologi-
cal role of individual cytokinin species involving NR
activity and root development in an early stage cannot be
explained in Q. serrata.
In general, cytokinins and auxin act antagonistically in
controlling meristem activities [25]. Moreover, the level
of IAA concentration required to promote growth in each
tissue is different [23]. As mentioned above, the IAA in
Al-treated roots was kept at about 80 pmol/g fw for at
least 2 days, in contrast to the decrease in Ca-treated
roots. The ration of IAA to sum of iP and tZ tended to
decrease with time after both 1h-treatments, and the ratio
was higher in Al treatment than in Ca treatment (Figure
3). Enhanced root elongation and increased number of
Figure 3. The ration of IAA to sum of iP and tZ in roots at 0
(Pre), 1, 2, and 3 days after treatment. Roots of 8-week-old
seedlings were treated with 2.5 mM AlCl3 (pH 4.0) or 4.2
mM CaCl2 (pH 4.0) solution for 1 h and then replaced with
freshly prepared nutrient solution. Vertical bars represent
the means ± SE (n = 3). Asterisks indicate significant dif-
ferences between Al treatment and Ca treatment (p < 0.05)
according to the t-test.
Copyright © 2012 SciRes. AJPS
Stimulation of Root Growth Induced by Aluminum in Quercus serrata Thunb. Is Related to
Activity of Nitrate Reductase and Maintenance of IAA Concentration in Roots
1623
second lateral roots induced by Al in the present study
(Table 1) may result in Al maintaining IAA concentra-
tion, and the hormone balance (auxin/cytokinin ratio)
may be essential for efficient lateral root development.
A close relationship between auxin-induced lateral
root formation and NO-induced lateral root development
has been reported recently. Initiation of lateral roots is
accompanied by an increase in NO level, an increase that
is involved with auxin signaling [13]. Furthermore, Kol-
bert et al. [14] reported that lateral root development by
auxin-induced NO production was associated with NR
activity. In the present study, the 1-h Al treatment en-
hanced NR activity in roots and the elongation and de-
velopment of second lateral roots, but 1-h Ca treatment
did not enhance second lateral root growth even though
NR activity increased (Figure 1 and Table 1).
Al-induced enhancement of root growth in Q. serrata
may be caused by stimulation of NR activity in roots and
IAA-induced NO synthesis. Furthermore, these data,
including those on phytohormones, might be useful for
further investigation of tree development.
5. Acknowledgements
This work was supported by Grants-in-Aid for Young
Scientists (B) (20780114) from the Ministry of Education,
Sports, Culture, Science and Technology of Japan, and
The Salt Science Research Foundation.
REFERENCES
[1] G. R. Gobran and S. Clegg, “A Conceptual Model for
Nutrient Availability in the Mineral Soil-Root System,”
Canadian Journal of Soil Science, Vol. 76, No. 2, 1996,
pp. 125-131. doi:10.4141/cjss96-019
[2] A. Göttelin, A. Heim and E. Matzner, “Mobilization of
Aluminium in the Rhizosphere Soil Solution of Growing
Tree Roots in an Acid Soil,” Plant and Soil, Vol. 211, No.
1, 1999, pp. 41-49. doi:10.1023/A:1004332916188
[3] W. H. Smith and A. S. Pooley, “Red Spruce Rhizosphere
Dynamics: Spatial Distribution of Aluminum and Zinc in
the Near-Root Soil Zone,” Forest Science, Vol. 35, No. 4,
1989, pp. 1114-1124.
[4] T. Ohno, “Rhizosphere pH and Aluminum Chemistry of
Red Oak and Honeylocust Seedlings,” Soil Biology and
Biochemistry, Vol. 21, No. 5, 1989, pp. 657-660.
[5] R. B. Clark, “Effect of Aluminium on Growth and Min-
eral Elements of Al-Tolerant and Al-Intolerant Corn,”
Plant and Soil, Vol. 47, No. 3, 1977, pp. 653-662.
doi:10.1007/ BF0001 1034
[6] T. B. Kinraide, “Aluminum Enhancement of Plant Growth
in Acid Rooting Media. A Case of Reciprocal Alleviation
of Toxicity by Two Cations,” Physiologia Plantarum,
Vol. 88, No. 4, 1993, pp. 619-625.
doi:10.1111/j.1399-3054
[7] R. Tomioka, A. Oda and C. Takenaka, “Root Growth
Enhancement by Rhizospheric Aluminum Treatment in
Quercus serrata Thunb Seedlings,” Journal of Forest
Research, Vol. 10, No. 4, 2005, pp. 319-324.
doi:10.1007/s10310-005-0152-0
[8] F. C. Thornton, M. Schaedle and D. J. Ryanal, “Effect of
Aluminum on the Growth of Sugar Maple in Solution
Culture,” Canadian Journal of Forest Research, Vol. 16,
No. 5, 1986, pp. 892-896. doi:10.1139/x86-159
[9] J. Huang and E. P. Bachelard, “Effect of Aluminum on
Growth and Cation Uptake in Seedlings of Eucalyptus
mannifera and Pinus radiate,” Plant and Soil, Vol. 149,
No. 1, 1993, pp. 121-127. doi:10.1007/BF00010769
[10] T. Mossor-Pietraszewska, “Effect of Aluminium on Plant
Growth and Metabolism,” Acta Biochimica Polonica, Vol.
48, No. 3, 2001, pp. 673-686.
[11] L. V. Kochian, O. A. Hoekenga and M. Piñeros, “How
Do Crop Plants Tolerate Acid Soils? Mechanisms of
Aluminum Tolerance and Phosphorous Efficiency,” An-
nual Review of Plant Biology, Vol. 55, 2004, pp. 459-493.
doi:10.1146/annurev.arplant.55.031903.141655
[12] R. Tomioka, A. Uchida, C. Takenaka and T. Tezuka,
“Effect of Aluminum on Nitrate Reductase and Photo-
synthesis Activities in Quercus serrata Seedlings,” Envi-
ronmental Sciences, Vol. 14, No. 3, 2007, pp. 157-165.
[13] N. Correa-Aragunde, M. Graziano and L. Lamattina,
“Nitric Oxide Plays a Central Role in Determining Lateral
Root Deveropment in Tomato,” Planta, Vol. 218, No. 6,
2004, pp. 900-905, doi:10.1007/s00425-003-1172-7
[14] Z. Kolbert, B. Bartha and L. Erdei, “Exogenous Auxin-
Induced NO Synthesis is Nitrate Reductase-Associated in
Arabidopsis thaliana Root Primordial,” Journal of Plant
Physiology, Vol. 165, No. 9, 2008, pp. 96-975.
doi:10.1016/j.jplph.2007.07.019
[15] Y. Zhao, “Auxin Biosynthesis and Its Role in Plant De-
velopment,” Annual Review Plant Biology, Vol. 61, 2010,
pp. 49-64. doi:10.1146/annurev-arplant-042809-112308
[16] H. Sakakibara, “Cytokinins: Activity, Biosynthesis, and
Translocation,” Annual Review Plant Biology, Vol. 57,
2006, pp. 431-449.
doi:10.1146/annurev.arplant.57.032905.105231
[17] R. H. Hageman and A. J. Reed, “Nitrate Reductase from
Higher Plants,” Methods in Enzymology, Vol. 69, 1980,
pp. 270-280.
[18] M. Kojima, T. Kamada-Nobusada, H. Komatsu, K. Takei,
T. Kuroha, M. Mizutani, M. Ashikari, M. Ueguchi-Ta-
naka, M. Matsuoka, K. Suski and H. Sakakibara, “Highly
Sensitive and High-Throughput Analysis of plant Hor-
mones using MS-Probe Modification and Liquid Chro-
matography-Tandem Mass Spectrometry: An Application
for Hormone Profiling in Oryza sativa.,” Plant Cell
Physiology, Vol. 50, No. 7, 2009, pp. 1201-1214.
doi:10.1093/pcp /pcp057
[19] K. Yamamoto, “Estimation of the Canopy-Gap Size Us-
ing Two Photographs Taken at Different Heights,” Eco-
logical Research, Vol. 15, No. 2, pp. 203-208.
doi:10.1046/j.1440– 1703.2000.00341.x
Copyright © 2012 SciRes. AJPS
Stimulation of Root Growth Induced by Aluminum in Quercus serrata Thunb. Is Related to
Activity of Nitrate Reductase and Maintenance of IAA Concentration in Roots
Copyright © 2012 SciRes. AJPS
1624
[20] N. Vida, G. Arellano, M. C. San-Jose, A. M. Vieitez and
A. Ballester, “Developmental Stages during the Rooting
of in-Vitro-Cultured Quercus robur Shoots from Material
of Juvenile and Mature Origin,” Tree Physiology, Vol. 23,
No. 18, 2003, pp. 1247-1254.
doi:10. 1093/treephys/23.18.1247
[21] P. M. Macdonald and J. Seelig, “Calcium Binding to
Mixed Phosphatidylglycerol-Phosphatidylcholine Bilay-
ers as Studied by Deuterium Nuclear Magnetic Reso-
nance,” Biochemistry, Vol. 26, 1987, pp. 1231-1240.
[22] M. A. Akeson, D. N. Munns and R. G. Burau, “Adsorp-
tion of Al3+ to Phosphatidylcholine Vesicle,” Biochimica
et Biophysica Acta (BBA)—Biomembranes, Vol. 986, No.
1, 1989, pp. 33-40.
[23] L. Taiz and E. Zeiger, “Auxin: the Growth Hormone,” In:
L. Taiz and E. Zeiger, Eds., Plant Physiology, Sinauer
Associates Inc., Sunderland, 2006, pp. 467-507.
[24] G. Krouk, S. Ruffel, R. A. Gutiérrez, A. Gojon, N. M.
Crawford, G. M. Coruzzi1 and B. Lacombe, “A Frame-
work Integrating Plant Growth with Hormones and Nu-
trients,” Trends in Plant Science, Vol. 16, No. 4, 2011, pp.
178-182, doi:10.1016/j.tplants.2011.02.004
[25] L. Moubayidin, R. D. Mambro and S. Sabatini, “Cyto-
kinin-Auxin Cross Talk,” Trends in Plant Science, Vol.
14, No. 10, 2009, pp. 557-562.
doi:10.1016/j.tplants.2009.06.010