| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
|
Plant Physiol. (1998) 118: 1105-1110
Update on Development
Michigan State University-Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, Michigan 48824-1312
Semiaquatic
plants grow mostly in flood plains and along river beds and are adapted
to survive partial submergence during periods of flooding (Blom and
Voesenek, 1996 Rice (Oryza sativa L.) is a semiaquatic plant whose growth,
at both the seedling and adult stages, is well investigated. It is
cultivated in five ecosystems where the source of water supply and the
degree of flooding are the major environmental determinants. The rice
types corresponding to these ecosystems are rain-fed low- and upland
rice, rice grown under controlled irrigated conditions, deepwater rice,
and rice in tidal wetlands. Rice grown in the deepwater ecosystem
distinguishes itself from most modern rice varieties by its ability to
survive in water depths of more than 50 cm for at least 1 month
(Catling, 1992 Figure 1A illustrates the growth habit of
deepwater rice. Seedlings are allowed to establish themselves before
the onset of flooding. The potential for submergence-induced rapid
internodal elongation develops with the differentiation of internodes
(Métraux and Kende, 1983
Deepwater rice is a subsistence crop for about 100 million people in
areas of Southeast Asia, where severe flooding occurs during the
monsoon season. Whereas yields of modern rice cultivars average 6 tons/ha, the average yield of deepwater rice is only 2 tons/ha (Vergara
et al., 1976 The genetic basis for submergence-promoted internodal elongation of
deepwater rice has received relatively little attention. It appears
that this trait is controlled by a number of minor and perhaps as few
as two major genes (Catling, 1992 In addition to its importance as a crop plant, deepwater rice is also
excellent for studying basic aspects of plant growth. The growth
response is induced by an environmental signal and is mediated by at
least three interacting hormones, namely ethylene, ABA, and GA.
Internodal elongation is based on increased cell-division activity and
enhanced cell elongation in well-delineated zones of the internode.
This allows one to study both processes of growth in an integrated
manner. Also, the unusually high growth rates magnify growth-related
cellular, physiological, biochemical, and molecular processes, thereby
facilitating their analysis. In addition to yielding fundamental
insights into the growth process, studies of internodal elongation in
deepwater rice may ultimately help to identify genes that could confer
at least limited elongation capacity onto modern, high-yielding
cultivars.
The original growth experiments with rice were carried out
with coleoptiles, which were found to elongate under water or at low
partial pressures of O2 at a faster rate than in
air. This feature helps coleoptiles to emerge from shallow waters and
to act like a snorkel for the aeration of the growing seedling (for review, see Jackson, 1985
Based on [3H]thymidine incorporation
(Métraux and Kende, 1984
Progression of cells in the IM through the cell cycle has been
followed by measuring [3H]thymidine
incorporation, by flow cytometry and by determining the expression of
genes whose products regulate the entry of cells into mitosis and the S
phase (Sauter and Kende, 1992a Cell elongation is driven by uptake of water into the central
vacuole. Flow of water into the cell is a function of the osmotic potential of the cell, the wall pressure potential or turgor, and the
hydraulic conductivity. Elongation of internodal cells in deepwater
rice is not the result of decreased osmotic potential or increased
hydraulic conductance. However, the cell walls of rapidly growing
internodes exhibit increased plastic and elastic extensibility
(Kutschera and Kende, 1988
GA is the growth hormone that ultimately promotes elongation of
deepwater rice internodes. Because of the magnitude of this response,
it is likely that GA regulates, directly or indirectly, the expression
of growth-related genes. Such genes were identified principally by a
targeted approach, e.g. genes encoding cyclins and expansins, and by
differential display of mRNA. Three genes whose function in growth is
unknown but that appear to be of particular interest encode a
Leu-rich-repeat receptor-like protein kinase (Os-TMK), a
putative type 1a plasma membrane receptor (Os-DD3), and a
putative transcription factor or activator (Os-DD4) (Van der
Knaap, 1998 The mechanism by which environmental factors and hormones induce
growth is largely unknown. The results obtained with deepwater rice
illuminate some of the questions that need to be answered. First, there
is the sensory pathway that connects influences from the environment
with the activity of the hormone(s) regulating growth. Next is the mode
of action of the respective hormone(s). Does a growth hormone such as
GA activate one key reaction via one signal transduction pathway, or
are there several GA response pathways that control different aspects
of growth? In intact plants growth consists of the production of new
cells in the meristems and of subsequent elongation of these cells. Are
these two processes interconnected or are they separately controlled?
Does the increase in cell size trigger the entry of meristematic cells
into the cell-division cycle? What biochemical reactions control cell
wall loosening? Does wall extension cause accelerated synthesis and deposition of new cell wall material? Work with deepwater rice has
contributed to identifying pieces of the puzzle, but much more needs to
be done to complete the picture. As pointed out at the beginning of
this Update, deepwater rice is not only a "model system"
for studying growth, the remarkable growth response of submerged plants
is also the process that needs to be understood in order to introduce
elongation capacity into high-yielding rice cultivars. The resulting
increased rice production in deepwater areas would elevate the living
standards of some of the poorest farming populations of Southeast Asia.
INTRODUCTION
Top
Introduction
References
). Among their adaptive features are the development of
internal air channels (aerenchyma) that facilitate aeration of
submerged organs and the capacity for rapid elongation when the plants
become partially covered by floodwaters. Submergence-induced growth
enables semiaquatic plants to keep part of their foliage above the
rising waters and to avoid drowning.
). Among the deepwater rice types, the so-called floating
rices exhibit extreme elongation capacity. They can grow at rates of 20 to 25 cm/d when partially submerged and can reach a length of up to
7 m in water depths of up to 4 m (for a detailed description
of the deepwater rice ecosystem, see Vergara et al. [1976]; Catling
[1992]).
). As the floodwaters rise, the
internodes elongate and adventitious roots are formed at the nodes.
When the waters recede, the rice plant sinks to the ground and
gravitropic stimulation causes the top of the stem and the panicle to
grow upward. Figure 1B illustrates the growth response of one internode
during 2 d of submergence.
View larger version (19K):
[in a new window]
Figure 1.
A, The growth cycle of a deepwater rice plant.
Young plants are allowed to establish themselves before the annual
flood arrives. As the floodwaters rise, rapid internodal growth permits
the plants to maintain part of their foliage above the water.
Adventitious roots develop at the submerged nodes. After the flood
recedes, the upper internodes show gravitropic sensitivity and grow
upward (modified with permission from Catling, 1992 ). B, Youngest
internode of an air-grown (left) and a submerged plant (right). The
upper and lower arrows indicate the positions of the highest and second
highest node, respectively. The whitish tissue of the internode on the
right corresponds to about 10 cm of new growth during 2 d of
submergence.
; Catling, 1992). Efforts to improve yield and grain
quality of deepwater rice have been met with limited success. Increases
in yield and retention of floating ability have not yet been combined
in one single cultivar. Since deepwater rice is the only crop that can
be grown in many flood-prone areas of Southeast Asia, developing
cultivars with increased yield and growth potential is of major
agronomic importance.
). Suge (1987) proposed that
elongation during submergence is based on the capacity of an internode
to elongate, as well as the degree of elongation, and identified one
gene with incomplete dominance that determined elongation ability.
Deepwater rice is of the Indica type and can be crossed with
Japonica rice. It can be transformed (Alam et al., 1998), and
investigating its unique biological properties such as the signal
transduction pathways leading to accelerated internodal growth is
greatly aided by the rapidly expanding genetic database of rice.
INTERNODAL ELONGATION IN DEEPWATER RICE IS REGULATED BY
ENVIRONMENTAL AND HORMONAL FACTORS
). In 1970, Ku et al. discovered that growth
of rice coleoptiles is stimulated by ethylene. The growth-promoting activity of ethylene was subsequently found in a number of other semiaquatic plants (Jackson, 1985). The response of semiaquatic plants
to ethylene is the opposite of that observed with most terrestrial
plants, in which growth is inhibited by ethylene.
). The ethylene concentration inside submerged internodes
increases 50-fold, from approximately 0.02 to 1 µL
L
1 (Fig. 2C), and ethylene applied to
nonsubmerged plants promotes internodal growth (Fig. 2D). The
accumulation of ethylene in submerged tissues of rice is the result of
two processes. Ethylene is physically trapped because its diffusion
coefficient in water is 10,000 times lower than in air (Jackson, 1985).
In addition, ethylene synthesis is enhanced in submerged internodes
(Raskin and Kende, 1984a). Isolated stem sections containing the
highest internode respond to submergence just as intact plants do
(Raskin and Kende, 1984a). When such sections are exposed to the same
gas atmosphere that prevails in submerged internodes
namely 3%
O2, 6% CO2, and 1 µL L1 ethylene in N2the
submergence response is fully mimicked. Therefore, deepwater rice
plants respond to submergence by sensing the altered composition of
their internal gas atmosphere. Lowered O2 and
increased CO2 tensions promote ethylene synthesis
and also enhance the growth-promoting effect of ethylene (Raskin and
Kende, 1984a).
View larger version (24K):
[in a new window]
Figure 2.
Promotion of growth by submergence and ethylene in
deepwater rice. A, Regime of submergence. The plants were partially
submerged in a 1-m-high tank so that one-third of their foliage was
above the water. They were lowered progressively into the tank to
compensate for growth. B, Total internodal length in submerged ( 
)
and air-grown (
) plants. C, Ethylene content in the internodal
cavity of submerged () and air-grown () plants. D, Total
internodal length of plants treated with 0.4 µL L1
ethylene () and of air-grown plants (). After Métraux and
Kende (1983).
with the semiaquatic plant
Callitriche platycarpa showed that submergence-induced
elongation was mediated by an interaction of ethylene and GA. Thus, GA
was the prime candidate for the hormone that would ultimately promote
elongation of deepwater rice internodes. Indeed, when air-grown plants
were treated with GA, their growth was greatly enhanced, and
submergence- and ethylene-induced growth were inhibited when plants
were treated with GA-biosynthesis inhibitors (Raskin and Kende, 1984b;
Suge, 1985). The requirement of GA for internodal growth of deepwater
rice was also demonstrated genetically by Suge (1987), who examined the
growth habit of F2 plants derived from a cross
between a deepwater rice and a rice mutant deficient in GA
biosynthesis.
). This
indicates that ethylene increases the responsiveness of the internode
to GA. How is this achieved? ABA is a potent antagonist of GA action in
rice internodes, and both applied ethylene and submergence reduced
endogenous ABA levels in internodes by 75% within 3 h
(Hoffmann-Benning and Kende, 1992). At the same time, there was also a
4-fold increase in the endogenous content of GA1.
Submergence- and ethylene-mediated reduction of ABA levels in deepwater
rice has also been described by Azuma et al. (1995). Thus, rapid
internodal growth of deepwater rice may result from an
ethylene-mediated increase in the ratio of an endogenous growth
promoter (GA) and a growth inhibitor (ABA). The proposed chain of
events connecting submergence and GA-stimulated internodal elongation
is shown in Figure 3.
View larger version (20K):
[in a new window]
Figure 3.
The proposed sequence of events connecting
submergence and enhanced internodal elongation.
INTERNODAL ELONGATION IS BASED ON INCREASED CELL DIVISION ACTIVITY
AND ENHANCED CELL ELONGATION
) and anatomical studies (Bleecker et
al., 1986), the rice internode can be divided into three regions (Fig.
4). At the base of the internode is the
IM, where cell divisions generate new internodal cells. These cells are
displaced into the EZ, where they reach their final length, and growth
ceases in the DZ, where secondary wall and xylem formation take place.
The transition from one zone to the other is reflected in cell size
measurements (Fig. 5). The IM is about 2 mm above the node and is characterized by small, brick-like cells (Fig.
4). Cell sizes increase above the IM in the EZ and stay constant in the
DZ (Fig. 5). The rate at which new cells are produced in the IM
increases 3-fold in response to submergence, the EZ expands about 3- to
5-fold, and the cells attain a 3- to 5-fold greater final length (Fig.
5). Similar observations have been made in GA- and ethylene-treated
internodes (Métraux and Kende, 1984; Raskin and Kende, 1984b;
Sauter and Kende, 1992a; Sauter et al., 1993). From these results it is
apparent that both the regulation of cell division in the IM and the
regulation of cell elongation in the EZ must be studied to gain an
understanding of internodal growth in deepwater rice.
View larger version (78K):
[in a new window]
Figure 4.
Rice stem containing the uppermost elongating
internode. The insets show scanning electron micrographs of cells in
the IM, in the EZ, and at the base of the DZ. After Sauter and Kende
(1992a) .
View larger version (17K):
[in a new window]
Figure 5.
The size of cells in the growing internode of
submerged ( ) and air-grown () plants. The IM corresponds to the
region with the smallest cell size 2 to 5 mm above the second highest
node. The EZ is between 5 and 10 mm in air-grown plants and 5 and 25 mm
in submerged plants. From Bleecker et al. (1986).
GA ACTIVATES THE CELL CYCLE IN THE IM
; Sauter et al., 1995; Lorbiecke and
Sauter, 1998). The activation of the cell cycle by GA and submergence
was reflected in increased expression of a gene encoding a
p34cdc2-like histone H1 kinase
(cdc2Os-2) and of the corresponding enzymatic activity
(Sauter et al., 1995; Lorbiecke and Sauter, 1998). Similarly, the
transcript levels of two cyclin genes, cycOs1 and
cycOs2, increased in GA-treated and submerged internodes
during the G2 phase, indicating that the corresponding cyclins control
entry into the M phase (Sauter et al., 1995; Lorbiecke and Sauter,
1998). In a screen for GA-regulated genes using differential display of
mRNA, two genes were identified whose products function in the cell
cycle. GA promoted the expression of a gene encoding a histone H3,
which is a marker for the S phase (Van der Knaap and Kende, 1995), and
the expression of RPA1, a gene encoding one of the subunits
of replication protein A (Van der Knaap et al., 1997). RPA is a
heterotrimeric protein that functions in DNA replication,
recombination, and repair, and may also be involved in the regulation
of transcription.
.
GA ALSO ENHANCES CELL ELONGATION
). Therefore, work aimed at understanding the
mechanism of cell elongation in deepwater rice has focused on chemical
and structural features of the growing cell wall and on the action of
wall-loosening proteins, the expansins.
3),(14)-
-D-glucan accumulates transiently in
growing cell walls of graminaceous monocotyledons and is thought to
play a role in wall expansion (Carpita, 1996). The content of
-D-glucan correlates well with cell elongation in
deepwater rice internodes (Sauter and Kende, 1992b). Its level reaches
a maximum in the EZ and decreases toward the DZ. In rapidly growing
internodes, the EZ and the region of high -D-glucan
content expand in parallel, and lignification of internodal cell walls is delayed. Azuma et al. (1996) determined the cell wall composition of
deepwater rice internodes and found that the pattern characteristic of
the IM mainly the relatively low ratio of cellulosic to noncellulosic materialexpanded with the EZ in rapidly elongating internodes.
; Sauter et al., 1993). Cells that
have been displaced from the IM before the start of GA treatment do not
respond to the hormone by further elongation. Responsiveness to GA may
be determined by the orientation of CMFs. In the epidermal walls of the
IM, CMFs are oriented perpendicularly to the direction of growth (Fig.
6). Such transverse orientation of CMFs
permits cell elongation. In slowly growing control internodes, the
orientation of CMFs in epidermal cells above the IM changed to oblique,
a configuration that impedes growth. In rapidly growing GA-treated
internodes, the reorientation of CMFs from transverse to oblique was
gradual and extended over the entire EZ (Fig. 6). Thus, there was a
close correlation between the rate of growth along the internode and
the orientation of CMFs. At least in rice internodes, GA does not
reorient the direction in which CMFs are deposited and enhances only
elongation of cells with CMFs that are still in transverse orientation.
Herein may lie one of the basic differences between GA and auxin
action. Auxin is known to change the deposition of CMFs from the
oblique/longitudinal to the transverse and to promote elongation of
cells that have stopped growing (Bergfeld et al., 1988). GA action
usually requires the presence of a meristem in which cells still have
transversely oriented CMFs.
View larger version (17K):
[in a new window]
Figure 6.
The direction of CMFs in the epidermal cell walls
of control internodes and internodes treated with 5 µM
GA3. The lines with double arrows indicate the measured
average angle of CMF deposition in the respective regions of the
internode. After Sauter et al. (1993) .
) is consistent
with a large body of evidence indicating that plant cell elongation is
based on stress relaxation of the cell wall. Stress relaxation is
thought to be regulated, at least in part, by wall-loosening factors. A
family of cell wall-loosening proteins, the expansins, was recently
discovered by Cosgrove and coworkers (for a review, see Cosgrove,
1998). They are thought to mediate cell expansion by disrupting
noncovalent bonds between wall polymers, most likely between CMFs and
hemicelluloses. Cell walls of deepwater rice internodes underwent
long-term extension (creep) when placed under tension in acidic buffers
(Cho and Kende, 1997a). This is indicative for the action of expansin.
The distribution and activity of rice expansin was correlated with
internodal growth (Cho and Kende, 1997b). Acid-induced extension of
native cell walls and reconstituted extension of boiled cell walls were
confined to the growing region of the internode.
). One sequence was identical to that
deduced from the rice expansin cDNA Os-EXP1, and the other
corresponded to the deduced amino acid sequence of Os-EXP4
(Cho and Kende, 1997c). In total, four expansin genes have been
identified in rice (Shcherban et al., 1995; Cho and Kende, 1997c). In
the coleoptile, root, leaf, and internode, there was increased
expression of Os-EXP1, Os-EXP3, and
Os-EXP4 in developmental regions where elongation occurs
(Cho and Kende, 1997c). This pattern of gene expression was also
correlated with acid-induced in vitro cell wall extensibility.
Submergence and treatment with GA induced accumulation of
Os-EXP4 mRNA before the rate of growth started to increase.
Taken together, these results indicate that expansins mediate, at least
in part, the growth response in deepwater rice.
GA INDUCES THE EXPRESSION OF GROWTH-RELATED GENES
). The expression of all three genes is enhanced by GA and
occurs in growing regions of the plant. The kinase domain of Os-TMK
autophosphorylates on Ser and Thr residues and phosphorylates the
kinase interaction domain of a protein phosphatase. Os-DD3 contains a functional signal sequence and has a predicted transmembrane region. However, no homologous proteins were found in the databases.
PROSPECTS
| |
FOOTNOTES |
|---|
Received June 24, 1998;
accepted August 31, 1998.
| |
ABBREVIATIONS |
|---|
Abbreviations: CMF, cellulose microfibril. DZ, differentiation zone. EZ, elongation zone. IM, intercalary meristem.
| |
LITERATURE CITED |
|---|
|
Top
Introduction
References
|
|---|
Alam MF, Datta K, Abrigo E, Vasquez A, Senadhira D, Datta SK (1998) Production of transgenic deepwater indica rice plants expressing a synthetic Bacillus thuringiensis cryIA(b) gene with enhanced resistance to yellow stem borer. Plant Sci 135: 25-30 [CrossRef][ISI]
Azuma T, Hirano T, Deki Y, Uchida N, Yasuda T, Yamaguchi T (1995) Involvement of the decrease in levels of abscisic acid in the internodal elongation of submerged floating rice. J Plant Physiol 146: 323-328 [ISI]
Azuma T, Sumida Y, Kaneda Y, Uchida N, Yasuda T (1996) Change in cell wall polysaccharides in the internodes of submerged floating rice. Plant Growth Regul 19: 183-187 [ISI]
Bergfeld R, Speth V, Schopfer P (1988) Reorientation of microfibrils and microtubules at the outer epidermal wall of maize coleoptiles during auxin-mediated growth. Bot Acta 101: 57-67 [ISI]
Bleecker AB, Schuette JL, Kende H (1986) Anatomical analysis of growth and developmental patterns in the internode of deepwater rice. Planta 169: 490-497 [ISI]
Blom CWPM, Voesenek LACJ (1996) Flooding: the survival strategies of plants. Trends Ecol Evol 11: 290-295 [CrossRef][ISI]
Carpita NC (1996) The structure and biogenesis of the cell walls of grasses. Annu Rev Plant Physiol Plant Mol Biol 47: 445-476 [CrossRef][ISI]
Catling D (1992) Rice in Deep Water. MacMillan Press, London
Cho H-T,
Kende H
(1997a)
Expansins in deepwater rice internodes.
Plant Physiol
113:
1137-1143
Cho H-T,
Kende H
(1997b)
Expansins and internodal growth of deepwater rice.
Plant Physiol
113:
1145-1151
Cho H-T,
Kende H
(1997c)
Expression of expansin genes is correlated with growth in deepwater rice.
Plant Cell
9:
1661-1671
Cosgrove DJ
(1998)
Cell wall loosening by expansins.
Plant Physiol
118:
333-339
Hoffmann-Benning S, Kende H (1992) On the role of abscisic acid and gibberellin in the regulation of growth in rice. Plant Physiol 99: 1156-1161 [ISI]
Jackson MB (1985) Ethylene and responses of plants to soil waterlogging and submergence. Annu Rev Plant Physiol 36: 145-174 [CrossRef][ISI]
Ku HS, Suge H, Rappaport L, Pratt HK (1970) Stimulation of rice coleoptile growth by ethylene. Planta 90: 333-339
Kutschera U, Kende H (1988) The biophysical basis of elongation growth in internodes of deepwater rice. Plant Physiol 88: 361-366 [ISI]
Lorbiecke R, Sauter M (1998) Induction of cell growth and cell division in the intercalary meristem of submerged deepwater rice (Oryza sativa L.). Planta 204: 140-145 [CrossRef][ISI]
Métraux J-P, Kende H (1983) The role of ethylene in the growth response of submerged deep water rice. Plant Physiol 72: 441-446 [ISI]
Métraux J-P, Kende H (1984) The cellular basis of the elongation response in submerged deep-water rice. Planta 160: 73-77 [ISI]
Musgrave A, Jackson MB, Ling E (1972) Callitriche stem elongation is controlled by ethylene and gibberellin. Nature New Biol 238: 93-96 [ISI]
Raskin I, Kende H (1984a) Regulation of growth in stem sections of deep-water rice. Planta 160: 66-72 [ISI]
Raskin I, Kende H (1984b) Role of gibberellin in the growth response of submerged deep water rice. Plant Physiol 76: 947-950 [ISI]
Sauter M, Kende H (1992a) Gibberellin-induced growth and regulation of the cell division cycle in deepwater rice. Planta 188: 362-368 [ISI]
Sauter M,
Kende H
(1992b)
Levels of -glucan and lignin in elongating internodes of deepwater rice.
Plant Cell Physiol
33:
1089-1097
[ISI]
Sauter M, Mekhedov SL, Kende H (1995) Gibberellin promotes histone H1 kinase activity and the expression of cdc2 and cyclin genes during the induction of rapid growth in deepwater rice internodes. Plant J 7: 623-632 [CrossRef][ISI][Medline]
Sauter M, Seagull RW, Kende H (1993) Internodal elongation and orientation of cellulose microfibrils and microtubules in deepwater rice. Planta 190: 354-362 [ISI]
Shcherban TY,
Shi J,
Durachko DM,
Guiltinan MJ,
McQueen-Mason SJ,
Shieh M,
Cosgrove DJ
(1995)
Molecular cloning and sequence analysis of expansinsa highly conserved, multigene family of proteins that mediate cell wall extension in plants.
Proc Natl Acad Sci USA
92:
9245-9249
[Abstract]
Suge H (1985) Ethylene and gibberellin: regulation of internodal elongation and nodal root development in floating rice. Plant Cell Physiol 26: 607-614 [ISI]
Suge H (1987) Physiological genetics of internodal elongation under submergence in floating rice. Jpn J Genet 62: 69-80
Van der Knaap E (1998) Identification of gibberellin-induced genes in deepwater rice and the role of these genes in plant growth. PhD thesis. Michigan State University, East Lansing
Van der Knaap E,
Jagoueix S,
Kende H
(1997)
Expression of an ortholog of replication protein A1 (RPA1) is induced by gibberellin in deepwater rice.
Proc Natl Acad Sci USA
94:
9979-9983
Van der Knaap E, Kende H (1995) Identification of a gibberellin-induced gene in deepwater rice using differential display of mRNA. Plant Mol Biol 28: 589-592 [ISI][Medline]
Vergara BS, Jackson B, De Datta SK (1976) Deep water rice and its response to deepwater stress. In Climate and Rice. International Rice Research Institute, Los Baños, Philippines, pp 301-319
This article has been cited by other articles:
|
|
 |
|
  G. M. Pastori, G. Kiddle, J. Antoniw, S. Bernard, S. Veljovic-Jovanovic, P. J. Verrier, G. Noctor, and C. H. Foyer Leaf Vitamin C Contents Modulate Plant Defense Transcripts and Regulate Genes That Control Development through Hormone Signaling PLANT CELL, April 1, 2003; 15(4): 939 - 951. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. B. JACKSON and P. C. RAM Physiological and Molecular Basis of Susceptibility and Tolerance of Rice Plants to Complete Submergence Ann. Bot., January 1, 2003; 91(2): 227 - 241. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. I. BOAMFA, P. C. RAM, M. B. JACKSON, J. REUSS, and F. J. M. HARREN Dynamic Aspects of Alcoholic Fermentation of Rice Seedlings in Response to Anaerobiosis and to Complete Submergence: Relationship to Submergence Tolerance Ann. Bot., January 1, 2003; 91(2): 279 - 290. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
W. H. VRIEZEN, Z. ZHOU, and D. VAN DER STRAETEN Regulation of Submergence-induced Enhanced Shoot Elongation in Oryza sativa L. Ann. Bot., January 1, 2003; 91(2): 263 - 270. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. A. C. J. VOESENEK, J. J. BENSCHOP, J. BOU, M. C. H. COX, H. W. GROENEVELD, F. F. MILLENAAR, R. A. M. VREEBURG, and A. J. M. PEETERS Interactions Between Plant Hormones Regulate Submergence-induced Shoot Elongation in the Flooding-tolerant Dicot Rumex palustris Ann. Bot., January 1, 2003; 91(2): 205 - 211. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 D. P. O'Neill and J. J. Ross Auxin Regulation of the Gibberellin Pathway in Pea Plant Physiology, December 1, 2002; 130(4): 1974 - 1982. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. Sauter, G. Rzewuski, T. Marwedel, and R. Lorbiecke The novel ethylene-regulated gene OsUsp1 from rice encodes a member of a plant protein family related to prokaryotic universal stress proteins J. Exp. Bot., December 1, 2002; 53(379): 2325 - 2331. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Y. Lee and H. Kende Expression of alpha -Expansin and Expansin-Like Genes in Deepwater Rice Plant Physiology, November 1, 2002; 130(3): 1396 - 1405. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G. Rzewuski and M. Sauter The novel rice (Oryza sativa L.) gene OsSbf1 encodes a putative member of the Na+/bile acid symporter family J. Exp. Bot., September 1, 2002; 53(376): 1991 - 1993. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
F. Fiorani, G. M. Bogemann, E. J.W. Visser, H. Lambers, and L. A.C.J. Voesenek Ethylene Emission and Responsiveness to Applied Ethylene Vary among Poa Species That Inherently Differ in Leaf Elongation Rates Plant Physiology, July 1, 2002; 129(3): 1382 - 1390. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Z. Zhou, J. de Almeida Engler, D. Rouan, F. Michiels, M. Van Montagu, and D. Van Der Straeten Tissue Localization of a Submergence-Induced 1-Aminocyclopropane-1-Carboxylic Acid Synthase in Rice Plant Physiology, May 1, 2002; 129(1): 72 - 84. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. J.M. Peeters, M. C.H. Cox, J. J. Benschop, R. A.M. Vreeburg, J. Bou, and L. A.C.J. Voesenek Submergence research using Rumex palustris as a model; looking back and going forward J. Exp. Bot., March 1, 2002; 53(368): 391 - 398. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Y. Lee and H. Kende Expression of beta -Expansins Is Correlated with Internodal Elongation in Deepwater Rice Plant Physiology, October 1, 2001; 127(2): 645 - 654. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. S. Barry, E. A. Fox, H.-c. Yen, S. Lee, T.-j. Ying, D. Grierson, and J. J. Giovannoni Analysis of the Ethylene Response in the epinastic Mutant of Tomato Plant Physiology, September 1, 2001; 127(1): 58 - 66. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. Van Der Straeten, Z. Zhou, E. Prinsen, H. A. Van Onckelen, and M. C. Van Montagu A Comparative Molecular-Physiological Study of Submergence Response in Lowland and Deepwater Rice Plant Physiology, February 1, 2001; 125(2): 955 - 968. [Abstract] [Full Text]
|
|
|
|
|
|
H. Mergemann and M. Sauter Ethylene Induces Epidermal Cell Death at the Site of Adventitious Root Emergence in Rice Plant Physiology, October 1, 2000; 124(2): 609 - 614. [Abstract] [Full Text]
|
|
|
|
|
|
M. Ghassemian, E. Nambara, S. Cutler, H. Kawaide, Y. Kamiya, and P. McCourt Regulation of Abscisic Acid Signaling by the Ethylene Response Pathway in Arabidopsis PLANT CELL, July 1, 2000; 12(7): 1117 - 1126. [Abstract] [Full Text]
|
|
|
|
|
|
E. van der Knaap, J. H. Kim, and H. Kende A Novel Gibberellin-Induced Gene from Rice and Its Potential Regulatory Role in Stem Growth Plant Physiology, March 1, 2000; 122(3): 695 - 704. [Abstract] [Full Text]
|
|
|
|
|
|
E. van der Knaap, W.-Y. Song, D.-L. Ruan, M. Sauter, P. C. Ronald, and H. Kende Expression of a Gibberellin-Induced Leucine-Rich Repeat Receptor-Like Protein Kinase in Deepwater Rice and Its Interaction with Kinase-Associated Protein Phosphatase Plant Physiology, June 1, 1999; 120(2): 559 - 570. [Abstract] [Full Text]
|
|
|
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| ASPB JOURNALS | PLANT PHYSIOLOGY | THE PLANT CELL | |
|---|---|---|---|
