JXB Advance Access originally published online on May 21, 2004
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Journal of Experimental Botany, Vol. 55, No. 401, pp. 1383-1390, June 1, 2004
© 2004 Oxford University Press
RESEARCH PAPER |
Decreased reactive oxygen species concentration in the elongation zone contributes to the reduction in maize leaf growth under salinity
Received 27 November 2003; Accepted 5 March 2004
IFFIVE-INTA, Camino a 60 Cuadras Km 5 1/2, 5119 Córdoba, Argentina
* To whom correspondence should be addressed. Fax: +54 351 4974330. E-mail: gertale{at}uolsinectis.com.ar
Abbreviations: ROS, reactive oxygen species; SEZ, segments from the leaf elongation zone; SEZc or SEZs, SEZ from non-salinized or salinized plants, respectively; DPI, diphenylene iodonium; FC, fusicoccin; REGR, relative elongation growth rate; NBT, nitro blue tetrazolium; XTT, Na, 3'-[1-[(phenylamino)-carbonyl]-3, 4-tetrazolium](4-methoxy-6-nitro) benzene sulphonic acid hydrate; SOD, superoxide dismutase.
 |
Abstract |
|---|
 Top Abstract IntroductionMaterials and methodsResults and discussionReferences |
|---|
Reactive oxygen species (ROS) in the apoplast of cells in the growing zone of grass leaves are required for elongation growth. This work evaluates whether salinity-induced reductions in leaf elongation are related to altered ROS production. Studies were performed in actively growing segments (SEZ) obtained from leaf three of 14-d-old maize (Zea mays L.) seedlings gradually salinized to 150 mM NaCl. Salinity reduced elongation rates and the length of the leaf growth zone. When SEZ obtained from the elongation zone of salinized plants (SEZs) were incubated in 100 mM NaCl, the concentration where growth inhibition was approximately 50%, O2•– production, measured as NBT formazan staining, was lower in these than in similar segments obtained from control plants. The NaCl effect was salt-specific, and not osmotic, as incubation in 200 mM sorbitol did not reduce formazan staining intensity. SEZs elongation rates were higher in 200 mM sorbitol than in 100 mM NaCl, but the difference could be cancelled by scavenging or inhibiting O2•– production with 10 mM MgCl2 or 200 µM diphenylene iodonium, respectively. The actual ROS believed to stimulate growth is •OH, a product of O2•– metabolism in the apoplast. SEZs elongation in 100 mM NaCl was stimulated by a •OH-generating medium. Fusicoccin, an ATPase stimulant, and acetate buffer pH 4, could also enhance elongation in these segments, although both failed to increase ROS activity. These results show that decreased ROS production contributes to the salinity-associated reduction in grass leaf elongation, acting through a mechanism not associated with pH changes.
Key words: Leaf elongation, maize, monocot growth, reactive oxygen species, salt stress.
|
Introduction |
|---|
|
TopAbstractIntroductionMaterials and methodsResults and discussionReferences |
|---|
Reactive oxygen species (ROS) participate in development, hormone action, and responses to biotic and abiotic stresses (Alvarez et al., 1998; Mittler, 2002). While oxidative damage, a ‘negative’ consequence of ROS presence, is a common response to many environmental stresses and has led to extensive studies of the antioxidant system (Mittler, 2002), more recently, growing evidence supports a ‘positive’ role for ROS in signalling events that regulate ion channel activity (Foreman et al., 2003) and gene expression (Neill et al., 2002).
In plant cells, ROS, mainly H2O2, superoxide anion (O2•–), and hydroxyl radical (•OH) are generated in the cytosol, chloroplasts, mitochondria, and the apoplastic space (Bowler and Fluhr, 2000; Mittler, 2002). ROS produced in the apoplast of cells in the growing zone of maize leaf blades are required for elongation growth (Rodríguez et al., 2002). Apoplastic ROS can participate in the regulation of cell expansion through a modulation of Ca2+ channel activity (Demidchik et al., 2003; Foreman et al., 2003). Apoplastic ROS can also regulate growth by affecting the rheological properties of cell walls (Cosgrove, 1999), contributing both to wall loosening (Miller, 1986; Fry, 1998; Schweikert et al., 2000; Schopfer, 2001) and stiffening (Ogawa et al., 1997; Schopfer, 1996).
Salinity is a common constraint to agricultural productivity (Rains, 1991), and the reduction of leaf expansion is one of the primary effects of salt stress (Munns and Termaat, 1986). In grasses, stress conditions that decrease leaf elongation rates affect the blade elongation zone, located at the base of the growing leaf blade (Langer, 1979), reducing the length of the zone and elemental growth rates within it (Bernstein et al., 1993; Neves-Piestun and Bernstein, 2001; Ortega and Taleisnik, 2003; Thomas et al., 1999). Increased ROS formation was observed after exposure of Arabidopsis roots to high salt (Demidchik et al., 2003), and apoplastic increases in O2•– were reported in pea plants under salt stress (Hernández et al., 2001). Cations, both divalent and monovalent, induced O2•– production in tobacco cell suspension cultures through the activity of NADPH oxidase (Kawano et al., 2001), and a major portion of the O2•– was released extracellularly. If changes in ROS concentration also occur in the leaf expansion zone in response to saline treatments, it is expected they would contribute to regulating leaf elongation under these conditions. Such a possibility has not yet been experimentally tested. In this work it was examined whether salinity affects ROS production in the leaf elongation zone and if this action contributes to regulating leaf elongation under this condition.
|
Materials and methods |
|---|
|
TopAbstractIntroductionMaterials and methodsResults and discussionReferences |
|---|
Plant material
Seeds of maize (Zea mays cv. Prozea 30, Produsem, Pergamino, Argentina) were sown on moist vermiculite contained in plastic net frames placed over 4.5 l black plastic trays containing aerated water. Trays were kept at 25 °C under a light panel of fluorescent and incandescent lights providing 95 µmol photons m–2 s–1 illumination, with a 12 h photoperiod. When the second leaf emerged, 6 d after sowing, the water was changed to one of half-strength Hoagland solution (Hoagland and Arnon, 1950), which included 25 mM NaCl in the saline treatment. This solution was changed daily, increasing the NaCl concentration from 25 mM to 50 mM, then to 100 mM, and then to 150 mM NaCl. Solutions were then replaced every 2 d, until day 14 when plants were processed.
Growth measurements and Na+ content
The third leaf, used as the experimental system, began to appear above the sheath whorl when plants were at 100 mM NaCl, and was at least 10 cm long on day 14. At this stage the sheath was about 2 mm long, thus its contribution to whole-leaf growth was negligible. Relative elongation growth rates (REGRs) within the blade expansion zone were calculated from the displacement of pinpricks in a 24 h interval according to Schnyder et al. (1987), as previously described for this system (Rodríguez et al., 2002). Briefly, the basal zone of the seedling was pricked through the sheath whorl with needles placed 5 mm apart, and, after 24 h, the sheath whorl was opened and the third leaf exposed and examined under a stereoscopic microscope to determine the distance between marks. Segmental growth was quantified as a relative growth rate (Hunt, 1978), termed relative elemental growth rate, REGR=(ln Lf–ln Li) (
t)–1 where Li and Lf denote the initial and final segment length, respectively, and t stands for the duration of the experiment.
REGR was plotted versus average segment midpoint position (Peters and Bernstein, 1997) to yield profiles of relative elemental elongation rates. Pricking reduced the velocity of leaf elongation by 50% in control plants, but not in salt-treated plants. The data shown are for pricked plants.
Elongation in isolated segments from leaf three was measured as described in detail previously (Rodríguez et al., 2002). Segments (SEZ), comprising the region from 10–20 mm from the leaf base (ligule), were gently vacuum infiltrated for 1.5 min and incubated for 3 h in various treatment solutions. Digital images of each segment were obtained before and after the incubation period, by means of a scanner (AGFA Snapscan Touch, Agfa-Gevaert Group, Morstel, Belgium), and length measurements were obtained with an image processing software (Optimas 6.1, Optimas Corporation, Bothell, WA). Growth was expressed as percentage length increase in that period. In some cases, images were also obtained at regular intervals (10 min) within that period to calculate growth kinetics.
To determine Na+ concentration, plant samples were weighed (fresh and dry weight), boiled in distilled water and solution aliquots used for ion content determination by flame photometry (digital flame analyser 2655-00, Cole-Parmer Instrument Co., Chicago, Illinois).
Detection of localized accumulation of O2•– in leaf segments
O2•– accumulation in tissues was determined with nitro blue tetrazolium (NBT), which reacts with O2•–, producing a blue formazan precipitate. Control reactions included 10 mM MnCl2, a highly effective O2•– dismutating catalyst agent (Hernández et al., 2001). Segments were gently infiltrated (1.5 min) with a 0.01% NBT solution in water or other solutions (100 mM NaCl or 200 mM sorbitol), depending on the experiment, and incubated in the dark in the same solution, for 2 h at 30 °C, with very slow shaking. Stained segments were mounted on a glass slide, and scanned. Colour images were first inverted to obtain a negative, transformed to black and white 8-bit images, and formazan colour intensity (in the negative corresponding to the lighter tones of grey), determined by an image processing software (Image J 1.29 Wayne Rasband, National Institutes of Health, USA).
Determination of O2•– release
O2•– release to the medium was determined spectrophotometrically, using Na, 3'-[1-[(phenylamino)-carbonyl]-3, 4-tetrazolium](4-methoxy-6-nitro) benzene sulphonic acid hydrate [XTT (Frahry and Schopfer, 2001)]. Groups of 10 SEZ were gently infiltrated and incubated 2 h in 1.5 ml of aqueous solution containing 500 mM XTT, with/without 100 mM NaCl, with/without 3.5 units ml–1 superoxide dismutase (SOD). Aliquots were read at 470 nm in a spectrophotometer (Beckman DU Series 600, Beckman Instruments, Fullerton, CA). Specific absorbance due to the presence of O2•– was calculated as the difference in A470 between samples without and with SOD.
Verification of the effect of NaCl on the formazan formation reaction
The effect of NaCl on the formazan reaction was determined in vitro. O2•– was generated by wounding SEZ in an aqueous medium. The medium was immediately divided into two fractions, one of which was salinized with 100 mM NaCl, and 0.01% NBT was added to both fractions. A560 was measured after 30 min incubation at 30 °C in the dark. Alternatively, O2•– was generated by illuminating a riboflavin solution in the presence or absence of 100 mM NaCl.
Statistical analysis
Data were analysed by one-way or two-way ANOVA and DGC tests (Di Rienzo et al., 2002), using InfoStat (InfoStat 2002. Grupo InfoStat. Facultad de Ciencias Agropecuarias. Universidad Nacional de Córdoba. Ver. 1.1. Córdoba, Argentina)
|
Results and discussion |
|---|
|
TopAbstractIntroductionMaterials and methodsResults and discussionReferences |
|---|
Experimental system
In monocots, leaf growth reflects events taking place at the elongation zone located at the base of the leaf, and the analysis of the spatial distribution of growth can provide initial information on the effects of stress. In this zone, the distribution of REGRs exhibits a typical tailed bell shape (Bernstein et al., 1993; Volenec and Nelson, 1981), which can be altered by stress in various ways: growth rates may be generally decreased, maximum growth rates may be reduced or shifted proximally, and the elongation zone may be shortened (Fricke, 2002).
In maize leaf three from control plants, highest REGRs were registered between 10 and 25 mm from the ligule (Fig. 1). Salinity (150 mM NaCl) reduced the highest REGR values, similar to the effects reported on leaf three of salt-stressed barley (Fricke and Peters, 2002). Significant differences in REGR between control and salinized plants were observed at and beyond 10 mm from the ligule, and the growth zone was shorter in salt-treated plants.
|
Segments spanning from 10–20 mm from the ligule were chosen for the following experiments, aimed at evaluating the relationship between salinity, ROS production, and elongation growth. Such segments were termed SEZ, and it had been previously shown that SEZ obtained from non-salinized plants and incubated in aqueous solutions reproduced the ROS production pattern of intact leaves (Rodríguez et al., 2002).
NaCl effects on ROS production by segments from the leaf elongation zone (SEZ)
To evaluate ROS production in segments obtained from salt-treated plants (SEZs), the incubation medium contained 100 mM NaCl, a salt concentration where growth was approximately 50% of that achieved by segments from control plants (SEZc) incubated in water (Fig. 2), and similar to the average REGR reduction in homologous segments from intact leaves, caused by providing 150 mM NaCl to the growth medium (Fig. 1). When SEZs were incubated in media with higher water potential, elongation was either greatly stimulated (in water) or less inhibited, as in 50 mM NaCl.
|
In non-salinized maize plants, the presence of apoplastic O2•– was detected in cells from the blade elongation zone (Rodríguez et al., 2002). In the current experiments, O2•– presence was determined by nitro blue tetrazolium (NBT) formazan staining.
SEZc, incubated for 2 h in water containing 0.01% NBT showed intense formazan staining (Fig. 3A), which was inhibited by adding MnCl2, a O2•– dismutating catalyst agent (Hernández et al., 2001). When either SEZc or SEZs were incubated in 100 mM NaCl, much lower formazan deposition was observed. Various salts of Na+ or Cl– (NaNO2, Na2(SO4), and KCl), in 100 mM concentration of the ions in question, exerted similar inhibitory effects on formazan deposition (Fig. 4), thus, both ions seemed to be capable of affecting O2•– production. Incubation in phosphate salts at the same osmotic potential also exerted a similar effect.
|
|
To rule out possible effects of NaCl on formazan formation, the reaction was checked in vitro. Leaf segments were wounded in water to induce O2•– production (Orozco-Cárdenas et al., 2001), and aliquots were immediately assayed for NBT formazan formation in the presence or absence of 100 mM NaCl. A560 values were 0.0459 and 0.0406 respectively, and not significantly different (t-test, P=0.39, n=5), in accordance with the common practice of including NaCl in reaction mixtures leading to formazan formation (see, for example, Lopukhina et al., 2001). Similar effects were obtained when O2•– was generated in vitro by illuminating a riboflavin solution in the presence or absence of NaCl (data not shown). Further evidence that O2•– production could be visualized under saline conditions was provided by wounding: when SEZs were firmly pressed with forceps, and incubated in a salinized NBT solution, formazan deposition could be distinctively seen in the wounded areas (Fig. 5). Therefore, the inhibitory effect of NaCl on formazan staining in the elongation zone of intact leaves, was due to salinity-associated changes in O2•– concentration and not to an artefact associated with formazan generation.
|
The inhibitory effect of NaCl on formazan staining described above could have resulted from osmotic or salt-specific effects. To distinguish between these alternatives, formazan staining was compared in SEZs incubated in 100 mM NaCl and in 200 mM sorbitol, a solution iso-osmotic with the former. SEZs incubated in 200 mM sorbitol and 0.01% NBT had intense staining (Fig. 3B), indicating that osmotic effects failed to reduce formazan deposition, and suggesting that the ionic, and not the osmotic component of NaCl was inhibiting O2•– formation. Intense staining was also observed when SEZs were incubated in water. Since whole tissue SEZs Na+ concentration (183 mM on a water basis) decreased after segments were incubated for 2 h in water or sorbitol (to 54 and 140 mM, respectively), a decrease expected to result mainly from the washout of the apoplastic free space (Lüttge and Higinbotham, 1979), those results may indicate that infiltration and incubation with either water or sorbitol decreased apoplastic NaCl concentration, and, thus, reverted the inhibition on O2•– production exerted by the salt.
The addition of DPI was effective for reducing formazan staining in SEZs incubated in sorbitol or water (Fig. 3B), indicating that the source of O2•– was affected. O2•– released by the segments to the incubation medium was measured by Na, 3'-[1-[(phenylamino)-carbonyl]-3, 4-tetrazolium](4-methoxy-6-nitro) benzene sulphonic acid hydrate (XTT). A470 values were much lower in the presence of NaCl after 2 h incubation (Table 1). Since O2•– is not readily transported across membranes, XTT formazan in the incubation medium could have been formed only from apoplastic O2•–. The results from those measurements support the idea that salinity exerted a negative effect on apoplastic O2•– concentration.
|
Together, these results indicate incubation in NaCl decreased apoplastic O2•– concentration, and treatments that reduced Na+ concentration, restored it, possibly by exerting effects from the apoplastic side.
The salt-specific reduction of apoplastic O2•– concentration by NaCl contrasts with other recent reports of increased O2•– production in response to saline stress, where O2•– production was measured shortly (minutes) after subjecting plants (Demidchik et al., 2003) or suspension cultures (Kawano et al., 2001) to ion shocks. The O2•– production peak lasted less than 1 min in suspension cultures (Kawano et al., 2001), possibly suggesting that it is transient, while the observations from this study reflect steady-state conditions. Hernández et al. (2001), reported increased apoplastic O2•– concentration under a steady-state salinity condition, but in expanded leaf blades, and in relation to the appearance of necrotic lesions, while changes are reported here in tissues that are actively expanding and not senescent.
Changes caused by salinity in apoplastic O2•– concentration in the growing zone of leaf blades could have resulted from either an inhibition of ROS-generating mechanisms, or from the activation of antioxidant defence elements (Hernández et al., 2001) or both, and such alternatives must be tested with further experiments. Preliminary results from SOD activity measurements in apoplastic fluid do not indicate increased activation of this enzyme in salinized plants.
Relation of ROS to elongation growth under salinity
Whether the change in ROS concentration under salinity was relevant for modulating elongation under that condition was assessed next. Incubation in 200 mM sorbitol, iso-osmotic with 100 mM NaCl, was less inhibitory to SEZs elongation than the salt (Fig. 6). Since O2•– content in SEZs was higher in 200 mM sorbitol than in 100 mM NaCl (Fig. 3B), it was asked whether that relative elongation stimulation was ROS-dependent. The addition of either 200 µM DPI or 10 mM MnCl2 to the sorbitol incubation medium (effective for reducing O2•– content, Fig. 3B), inhibited elongation by approximately 50% (Fig. 6). Therefore, in sorbitol-incubated SEZs, where both growth and O2•– content were higher than in 100 mM NaCl, reducing O2•– content reduced elongation rates. As expected, 200 µM DPI had no effect on growth of SEZs incubated in 100 mM NaCl (results not shown).
|
Conversely, growth in SEZs could be stimulated by supplying apoplastic ROS. The actual ROS exerting the growth-stimulating action is believed to be •OH (Foreman et al., 2003; Schopfer, 2001). •OH can be generated in the apoplast in the presence of H2O2, ascorbate, and Cu2+ or Fe2+ (Fry et al., 2001; Halliwell and Gutteridge, 1990), in a reaction requiring, first, the generation of O2•–, which is then dismutated to H2O2 by apoplastic superoxide dismutase (Ogawa et al., 1997). When SEZs were incubated in a solution of 100 mM NaCl containing 0.2 mM ascorbate, 0.2 mM CuCl2 and 0.2 mM H2O2, elongation was higher than in NaCl alone, and similar to the level attained in 200 mM sorbitol (Fig. 6). The kinetics of SEZs elongation in that medium was very similar to that of SEZc in water. Thus, adding •OH to the SEZs saline incubation medium, reverted the inhibition in elongation, providing support to the idea that salinity-decreased ROS production negatively affected elongation, and that the growth-stimulating action of ROS is •OH-dependent.
It has been demonstrated that ROS can regulate cell expansion through the activation of Ca2+ channels (Foreman et al., 2003). Exposure of Arabidopsis roots to NaCl caused a rapid reduction of cytosolic Ca2+ concentration (Cramer and Jones, 1996), and a strong positive correlation was found between Ca2+ concentration and root elongation rates. Thus, it was asked whether the observed ROS effects on SEZs elongation were also mediated by Ca2+. The Ca2+ chelating agent, ethylene glycol bis (ß-aminoethylether)-N,N,N',N'-tetraacetic acid (EGTA), added to the salinized .OH-generating medium, in a concentration of 1 mM, completely reversed the growth stimulation (Fig. 6), and depressed elongation to values even lower than those attained with 100 mM NaCl. This result, while acknowledging that EGTA may affect membrane permeability by removing Ca2+, suggests that the stimulating action of ROS on SEZs elongation requires an external source of Ca2+. This ion is part of signal transduction chains and it is also involved in the modulation of actin dynamics and exocytosis, but the relationship between cytosolic Ca2+ and altered growth rates is not completely understood (Bush, 1995).
SEZs elongation could also be stimulated by fusicoccin (FC) (Neves-Piestun and Bernstein, 2001), an enhancer of plasmalemma H+-ATPase activity (Marré, 1979). The effect of FC on SEZs elongation is accompanied by the lowering of apoplastic pH (Neves-Piestun and Bernstein, 2001). Both low pH and FC stimulated elongation in SEZs incubated in 100 mM NaCl (Fig. 7A), although both treatments failed to increase ROS activity (Fig. 7B). It has been shown that pH-dependent elongation cannot be reduced by adding ROS scavengers to the incubation medium (Schopfer, 2001), which is consistent with the idea that ROS and pH activate elongation through different mechanisms. Elongation stimulated by FC could only be partially inhibited by including EGTA in the incubation medium (Fig. 7A). The partial reversion by EGTA of FC-stimulated elongation indicates that (a) FC is also stimulating elongation through a Ca2+-related mechanism, but (b) that the effect of FC is not entirely dependent on external Ca2+, in accordance with the report that FC does not stimulate Ca2+ uptake in plasmalemma vesicles (Zocchi and Rabotti, 1993).
|
Taken together, these results indicate that ROS play a role in the regulation of leaf elongation under salinity, possibly by a Ca2+-requiring mechanism, however, they also show that ROS are not necessarily a common feature in all mechanisms that participate in the regulation of elongation under such conditions, since low pH stimulation of elongation was not accompanied by higher ROS production.
Salinity and ROS modulation of leaf elongation
This paper shows that leaf elongation can be stimulated by ROS under saline conditions. Apoplastic ROS have been implied in the control of growth through effects on cell wall properties (Fry et al., 2001; Fry, 1998) and ion balance (Demidchik et al., 2002). Salinity was shown to inhibit root hair elongation via alterations in the tip-focused Ca2+ gradient that regulates root hair growth (Halperin et al., 2003), and by a reduction in cytosolic Ca2+ in Arabidopsis roots (Cramer and Jones, 1996). Similar mechanisms are likely to operate in the leaf expansion zone mediated by ROS. ROS in the apoplast may be generated by the activity of several sources such as plasmalemma NAD(P)H oxidases, apoplastic peroxidases, amine and oxalate oxidases (Bolwell and Wojtaszek, 1997). The experiments of this study indicate that O2•– levels in the apoplast change in response to salinity, thus, the participation of NAD(P)H oxidase, an enzyme complex generating superoxide in the apoplast, may be expected. However, since the DPI concentration used in this case was high enough to inhibit both NAD(P)H oxidase and peroxidases (Bolwell et al., 1998), the elucidation of this point must await results from experiments with isolated membranes, which are currently underway.
Salinity may restrict leaf elongation growth by affecting rates of water or osmolytes uptake, turgor generation, and wall properties. Many of these effects are common consequences to both osmotic and ionic stress. Toxic salinity effects may also result from the build-up of excessive ion concentration and from ion imbalance, which, in turn may affect signalling chains. These are salt-specific effects, and the effects of salinity on apoplastic ROS concentration are of this kind. In an evaluation of the expression levels for 127 proteins in different tissues of rice plants subject to phytohormone, biotic and abiotic stress treatments, Cooper et al. (2003) showed that, although for many genes expression changed similarly in response to the treatments, in a few cases, salt and osmotic stress resulted in significantly different levels of expression.
|
Acknowledgements |
|---|
The authors thank Dr Samuel Taleisnik for critically reading the manuscript and the technical assistance of Paola Suarez is gratefully acknowledged. This work was supported by the Agencia de Promoción Científica y Tecnológica of Argentina (FONCYT grant 6869) and Fundación Antorchas, and it is part of AAR’s doctorate.
|
References |
|---|
|
TopAbstractIntroductionMaterials and methodsResults and discussionReferences |
|---|
Alvarez ME, Pennell RI, Meijer PJ, Ishikawa A, Dixon RA, Lamb C. 1998. Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell 92, 773–784.[CrossRef][Web of Science][Medline]
Bernstein N, Lauchli A, Silk WK. 1993. Kinematics and dynamics of sorghum (Sorghum bicolor L.) leaf development at various Na/Ca salinities. I. Elongation growth. Plant Physiology 103, 1107–1114.[Abstract]
Bolwell G, Davies D, Gerrish C, Auh C, Murphy TM. 1998. Comparative biochemistry of the oxidative burst produced by rose and French bean cells reveals two distinct mechanisms. Plant Physiology 116, 1379–1385.
Bolwell GP, Wojtaszek P. 1997. Mechanisms for the generation of reactive oxygen species in plant defence—a broad persepective. Physiological and Molecular Plant Physiology 51, 347–366.
Bowler C, Fluhr R. 2000. The role of calcium and activated oxygens as signals for controlling cross-tolerance. Trends in Plant Science 5, 241–246.[CrossRef][Web of Science][Medline]
Bush D. 1995. Calcium regulation in plant cells and its role in signalling. Annual Review of Plant Physiology and Plant Molecular Biology 46, 95–112.[CrossRef][Web of Science]
Cooper B, Clarke JD, Budworth P, et al. 2003. A network of rice genes associated with stress response and seed development. Proceedings of the National Academy of Sciences, USA 100, 4945–4950.
Cosgrove DJ. 1999. Enzymes and other agents that enhance cell wall extensibility. Annual Review of Plant Physiology and Plant Molecular Biology 50, 391–417.[CrossRef][Web of Science][Medline]
Cramer GR, Jones RL. 1996. Osmotic stress and abscisic acid reduce cytosolic calcium activities in roots of Arabidopsis thaliana. Plant, Cell and Environment 19, 1291–1298.[CrossRef]
Demidchik V, Bowen HC, Maathuis FJM, Shabala SN, Tester MA, White PJ, Davies JM. 2002. Arabidopsis thaliana root non-selective cation channels mediate calcium uptake and are involved in growth. The Plant Journal 32, 799–808.[CrossRef][Web of Science][Medline]
Demidchik V, Shabala SN, Coutts KB, Tester MA, Davies JM. 2003. Free oxygen radicals regulate plasma membrane Ca2+ and K+- permeable channels in plant root cells. Journal of Cell Science 116, 81–88.
Di Rienzo JA, Guzmán AW, Casanoves F. 2002. A multiple comparisons method based on the distribution of the root node distance of a binary tree. Journal of Agricultural, Biological, and Environment Statistics 7, 1–14.
Foreman J, Demidchik V, Bothwell JH, et al. 2003. Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422, 442–446.[CrossRef][Medline]
Frahry G, Schopfer P. 2001. NADH-stimulated, cyanide-resistant, superoxide production in maize coleoptiles analyzed with a tetrazolium-based assay. Planta 212, 175–183.[CrossRef][Web of Science][Medline]
Fricke W. 2002. Biophysical limitation of cell elongation in cereal leaves. Annals of Botany 90, 157–167.
Fricke W, Peters WS. 2002. The biophysics of leaf growth in salt-stressed barley. A study at the cell level. Plant Physiology 129, 374–388.
Fry S, Dumville J, Miller J. 2001. Fingerprinting of polysaccharides attacked by hydroxyl radicals in vitro and in the cell walls of ripening pear fruit. Biochemical Journal 357, 729–737.[CrossRef][Web of Science][Medline]
Fry SC. 1998. Oxidative scission of plant cell wall polysaccharides by ascorbate induced hydroxyl radicals. Biochemical Journal 332, 505–515.
Halliwell B, Gutteridge JMC. 1990. Role of free radicals and catalytic metal ions in human disease: an overview. In: Packer L, Glazer AN, eds. Methods in enzymology. New York: Academic Press, 1–85.
Halperin SJ, Gilroy S, Lynch JP. 2003. Sodium chloride reduces growth and cytosolic calcium, but does not affect cytosolic pH, in root hairs of Arabidopsis thaliana L. Journal of Experimental Botany 54, 1269–1280.
Hernández JA, Ferrer MA, Jiménez A, Ros Barceló A, Sevilla F. 2001. Antioxidant systems and O2•–/H2O2 production in the apoplast of pea leaves: its relation with salt-induced necrotic lesions in minor veins. Plant Physiology 127, 817–831.
Hoagland DR, Arnon DI. 1950. The water-culture method for growing plants without soil. California Agricultural Experiment Station Circular 1–32.
Hunt R. 1978. Plant growth analysis. London: Edward Arnold.
Kawano T, Kawano N, Muto S, Lapeyrie F. 2001. Cation-induced superoxide generation in tobacco cell suspension culture is dependent on ion valence. Plant, Cell and Environment 24, 1235–1241.[CrossRef]
Langer RHM. 1979. How grasses grow. London: Edward Arnold.
Lopukhina A, Dettenberg M, Weiler EW, Hollander-Czytko H. 2001. Cloning and characterization of a coronatine-regulated tyrosine aminotransferase from Arabidopsis. Plant Physiology 126, 1678–1687.
Lüttge U, Higinbotham N. 1979. Transport in plants. New York: Springer-Verlag.
Marré E. 1979. Fusicoccin: a tool in plant physiology. Annual Review of Plant Physiology 30, 273–288.[Web of Science]
Miller AR. 1986. Oxidation of cell wall polysaccharides by hydrogen peroxide: a potential mechanism for cell wall breakdown in plants. Biochemical and Biophysical Research Communications 141, 238–244.[CrossRef][Web of Science][Medline]
Mittler R. 2002. Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science 9, 405–410.
Munns R, Termaat A. 1986. Whole-plant responses to salinity. Australian Journal of Plant Physiology 13, 143–160.[Web of Science]
Neill S, Desikan R, Hancock J. 2002. Hydrogen peroxide signalling. Current Opinion in Plant Biology 5, 388–395.[CrossRef][Web of Science][Medline]
Neves-Piestun BG, Bernstein N. 2001. Salinity-induced inhibition of leaf elongation in maize is not mediated by changes in cell wall acidification capacity. Plant Physiology 125, 1419–1428.
Ogawa K, Kanematsu S, Asada K. 1997. Generation of superoxide anion and localization of Cu Zn-superoxide dismutase in the vascular tissue of spinach hypocotyls: Their association with lignification. Plant and Cell Physiology 38, 1118–1126.
Orozco-Cárdenas ML, Narváez-Vásquez J, Ryan CA. 2001. Hydrogen peroxide acts as a second nessenger for the induction of defence genes in tomato plants in response to wounding, systemin, and methyl jasmonate. The Plant Cell 13, 179–191.
Ortega L, Taleisnik E. 2003. Elongation growth in leaf blades of Chloris gayana under saline conditions. Journal of Plant Physiology 160, 517–522.[CrossRef][Web of Science][Medline]
Peters WS, Bernstein N. 1997. The determination of relative elemental growth rate profiles from segmental growth rates: a methodological evaluation. Plant Physiology 113, 1395–1404.[Abstract]
Rains DW. 1991. Salinity and alkalinity as an issue in world agriculture. In: R. Choukr-Allah, ed. Plant salinity research. New challenges. Agadir: Institut Agronomique et Veterinaire Hassan II.
Rodríguez A, Grunberg K, Taleisnik E. 2002. Reactive oxygen species in the elongation zone of maize leaves are necessary for leaf extension. Plant Physiology 129, 1627–1632.
Schnyder H, Nelson CJ, Coutis JH. 1987. Assessment of spatial distribution of growth in the elongation zone of grass leaf blades. Plant Physiology 85, 290–293.
Schopfer P. 1996. Hydrogen peroxide-mediated cell-wall stiffening in vitro in maize coleoptiles. Planta 199, 43–49.[Web of Science]
Schopfer P. 2001. Hydroxyl radical-induced cell-wall loosening in vitro and in vivo: implications for the control of elongation growth. The Plant Journal 28, 679–688.[CrossRef][Web of Science][Medline]
Schweikert C, Liszkay A, Schopfer P. 2000. Scission of polysaccharides by peroxidase-generated hydroxyl radicals. Phytochemistry 53, 565–570.[CrossRef][Web of Science][Medline]
Thomas H, James AR, Humphreys MW. 1999. Effects of water stress on leaf growth in tall fescue, Italian ryegrass and their hybrid: rheological propeties of expansion zones of leaves, measured on growing and killed tissue. Journal of Experimental Botany 50, 221–231.
Volenec JJ, Nelson CJ. 1981. Cell dynamics in leaf meristems of contrasting tall fescue genotypes. Crop Science 21, 381–385.
46 Zocchi C, Rabotti G. 1993. Calcium transport in membrane vesicles isolated from maize coleoptiles. Effect of indoleacetic acid and fusicoccin. Plant Physiology 101, 135–139.[Abstract]
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  A. A. Rodriguez, S. J. Maiale, A. B. Menendez, and O. A. Ruiz Polyamine oxidase activity contributes to sustain maize leaf elongation under saline stress J. Exp. Bot., November 1, 2009; 60(15): 4249 - 4262. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. Zhu, S. Alvarez, E. L. Marsh, M. E. LeNoble, I.-J. Cho, M. Sivaguru, S. Chen, H. T. Nguyen, Y. Wu, D. P. Schachtman, et al. Cell Wall Proteome in the Maize Primary Root Elongation Zone. II. Region-Specific Changes in Water Soluble and Lightly Ionically Bound Proteins under Water Deficit Plant Physiology, December 1, 2007; 145(4): 1533 - 1548. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Karkonen and S. C Fry Effect of ascorbate and its oxidation products on H2O2 production in cell-suspension cultures of Picea abies and in the absence of cells J. Exp. Bot., May 1, 2006; 57(8): 1633 - 1644. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||