Journal of Experimental Botany, Vol. 53, No. 369, pp. 747-756,
April 1, 2002
© 2002 Oxford University Press
Original Papers |
Methyl jasmonate alters polyamine metabolism and induces systemic protection against powdery mildew infection in barley seedlings
Department of Plant Biology, Plant and Crop Science Division, Scottish Agricultural College, Ayr Campus, Auchincruive Estate, Ayr KA6 5HW, UK
Received 6 August 2001; Accepted 12 November 2001
 |
Abstract |
|---|
 Top Abstract IntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Treatment of the first leaves of barley (Hordeum vulgare L. cv. Golden Promise) seedlings with methyl jasmonate (MJ) led to small, but significant increases in levels of free putrescine and spermine 1 d later and to significant increases in levels of free putrescine, spermidine and spermine by 4 d following treatment. MJ-treated first leaves also exhibited significant increases in the amounts of soluble conjugates of putrescine and spermidine 1, 2 and 4 d after treatment. In second leaves of plants where the first leaves had been treated with MJ, no significant changes in levels of free polyamines were observed, but significant increases in levels of soluble conjugates of putrescine and spermidine were detected. These changes were accompanied by increased activities of soluble ornithine decarboxylase (ODC), soluble and particulate arginine decarboxylase (ADC), and S-adenosylmethionine decarboxylase (AdoMetDC), in first and second leaves following treatment of the first leaves with MJ. Activities of soluble and particulate diamine oxidase (DAO) were also higher in first and second leaves following treatment of the first leaves with MJ. Treatment of the first leaves with MJ led to a significant reduction in powdery mildew (Blumeria graminis f. sp. hordei) infection on the second leaves and also resulted in significant increases in activities of the plant defence-related enzymes, phenylalanine ammonia lyase (PAL) and peroxidase.
Key words: Barley, methyl jasmonate, plant defence, polyamine metabolism, powdery mildew.
|
Introduction |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Jasmonic acid (3-oxo-2-[2'-cis-pentyl]-cyclopentane-l-acetate; JA) and its methyl ester, methyl jasmonate (MJ) are widespread natural regulators involved in many processes during plant development (Creelman and Mullet, 1995
; Sembdner and Parthier, 1993). They produce numerous biological effects including promotion of leaf senescence and abscission, stomatal closure, inhibition of root growth, and germination of non-dormant seeds (Creelman and Mullet, 1997). Recent work has implicated jasmonates in the signalling pathway mediating induced defence responses in pathogen—or insect—attacked plants (Creelman and Mullet, 1995; Farmer and Ryan, 1992). Jasmonates have been shown to induce various responses in plants, including the accumulation of a ribosome-inactivating protein (Chaudry et al., 1994), serine proteinase inhibitors (Farmer and Ryan, 1990), phenylalanine ammonia lyase, and thionin (Andresen et al., 1992), and chalcone synthase (Creelman and Mullet, 1995).
Jasmonates have also been shown to stimulate the production of secondary metabolites (Gundlach et al., 1992), including hydroxycinnamic acid amides (HCAs) (Lee et al., 1997; Mader, 1999; Biondi et al., 2000). HCAs are formed from the covalent binding of polyamines (putrescine, spermidine and spermine) to hydroxycinnamic acids like caffeic acid and coumaric acid. HCAs are widespread in plants and constitute the bulk of the acid-soluble polyamine pool (Flores and Martin-Tanguy, 1991). They are known to accumulate in response to pathogen infection and indeed, levels of free polyamines and acid-soluble conjugated polyamines have been shown to undergo profound changes in leaves infected with fungal pathogens (Walters, 2000). In recent work, Biondi et al. found that MJ up-regulated the expression of polyamine biosynthetic genes, and the oxidation and conjugation of polyamines in tobacco thin layers (Biondi et al., 2001).
The fungus Blumeria graminis f. sp. hordei is the cause of powdery mildew, one of the most important diseases of barley. Approximately 10–12 h after a powdery mildew conidium has germinated on a barley leaf surface, a specialized infection structure, the appressorium, is produced. Thereafter (approximately 12–20 h after inoculation), a penetration peg is produced from the appressorium with the objective of penetrating the epidermal cell directly. In a compatible interaction, penetration succeeds, an haustorium is produced within the epidermal cell, and growth of the powdery mildew occurs on the leaf surface. In some incompatible interactions, penetration fails and fungal development is halted, while in others, for example, those where the plant possesses specific genes for resistance to incompatible fungal isolates, a hypersensitive response can occur, resulting in death of the host cell (Carver et al., 1994; Hippe-Sanwald et al., 1992).
Jasmonates have been reported to induce local and systemic protection against Phytophthora infestans in tomato and potato (Cohen et al., 1993) and against Pythium ultimum in Norway Spruce (Kozlowski et al., 1999). In addition, although jasmonates had no effect on local resistance of barley to powdery mildew (Schweizer et al., 1993), MJ was shown to induce systemic protection to powdery mildew in barley seedlings and to provide control of powdery mildew in field-grown barley (Mitchell and Walters, 1995). In this report it is confirmed that MJ induces systemic protection in barley seedlings and, further, that MJ alters polyamine metabolism in treated leaves. This paper also reports, for the first time, an increase in polyamine conjugates in systemically protected leaves.
|
Materials and methods |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Plant material
Seedlings of the barley (Hordeum vulgare L.) cultivar Golden Promise (susceptible to powdery mildew) were grown under a 16 h photoperiod with irradiance at 360 µmol m-2 s-1 to provide a day temperature of 20 °C, with a night temperature of 10 °C. The powdery mildew fungus Blumeria graminis f. sp. hordei (isolate CC220) was maintained on Golden Promise and 1 d prior to the start of an experiment, infected plants were shaken to dislodge older conidia, thus ensuring a supply of young conidia for experimentation. In some experiments, second leaves of experimental plants were inoculated with conidia of powdery mildew using the method described earlier (Nair and Ellingboe, 1962
) to give an inoculation density of approximately 15 spores mm-2. Inoculated plants were incubated under the conditions described above.
Treatment with MJ
MJ (Serva, Feinbiochemica GmbH & Co., Heidelberg, Germany) was dissolved in ethanol and then diluted with distilled water to give a final concentration of 20 mM MJ. Since MJ vapour can induce plant defence responses (Farmer and Ryan, 1990) it was decided that in examining systemic protection in barley, the treated leaves should be isolated from the upper, second leaves. This was achieved by inserting first leaves into a plastic chamber (1.0 l volume) into which had been placed a cotton tipped applicator soaked in 20 mM MJ. The chambers were sealed and leaves exposed to MJ vapour for 2 h. First leaves of control plants were sealed in plastic chambers containing a cotton tipped applicator soaked in a 2% ethanol solution (reflecting the ethanol concentration in the 20 mM MJ solution). First and second leaves were then harvested 1, 2 and 4 d later for analysis. In some experiments, second leaves were inoculated with powdery mildew 2 d after treatment with MJ. Some of these plants were harvested 2 d later (4 d following MJ treatment) for analysis and others were left until 10 d following mildew inoculation, when the percentage leaf area of the second leaves covered with powdery mildew was recorded.
Determination of polyamines and polyamine conjugates
Polyamines and polyamine conjugates were extracted and hydrolysed using the method described previously (Slocum and Galston, 1985). This yielded a non-hydrolysed perchloric acid (used at 10%) supernatant, containing the unconjugated (‘free’) polyamines, and the hydrolysed supernatant and pellet fractions, containing polyamines liberated from various types of conjugates. The perchloric acid-soluble hydrolysate consists of polyamines conjugated to small molecules (PCA-soluble polyamine conjugates) and the perchloric acid-insoluble hydrolysate consists of polyamines conjugated to macromolecules (PCA-insoluble polyamine conjugates). These different polyamine fractions were then dansylated using a modified version of the procedure used by Friedman et al. (Friedman et al., 1982) and the dansylated polyamine separated by TLC and quantified by fluorescence spectrophotometry as described in detail previously (Coghlan and Walters, 1990).
Enzyme assays
Ornithine decarboxylase (ODC; EC 4.1.1.17) and arginine decarboxylase (ADC; EC 4.1.1.19) were assayed using a modified version of the method described earlier (Tiburcio et al., 1985) and described in detail later (Coghlan and Walters, 1990).
S-adenosylmethionine decarboxylase (AdoMetDC: EC 4.1.1.50) was assayed as follows: plant tissue was ground at 0 °C in 10 mM potassium phosphate buffer: (1 g fresh weight per 2.5 ml) containing 2 mM dithiothreitol, 1 mM MgCl2, 0.1 mM EDTA, and 0.1 mM pyridoxal phosphate, pH 7.6. Extracts were spun at 0 °C at 25000 g for 15 min. To each 1 ml of supernatant, 430 mg of (NH4)2SO4 was added and the precipitates were then redissolved in 1 ml of buffer. AdoMetDC activity was assayed by measurement of 14CO2 released after incubation with S-adenosyl [1-14C]methionine. The incubation mixture comprised of 100 mM sodium phosphate pH 7.4, 0.2 mM S-adenosyl-L-methionine, 1.0 mM putrescine, 0.925 kBq S-adenosyl-L-[1-14C]methionine (1.85 GBq mol-1 m-3, Amersham) and 0.1 mM of enzyme extract, in a total volume of 0.4 ml. The remainder of the assay was carried out as described for ODC.
Determination of DAO activity
Diamine oxidase (DAO; EC 1.4.3.6) activity was assayed by following the production of [14C] 
' pyrroline from labelled putrescine as described in detail previously (Scaramagli et al., 1999). Briefly, leaf samples were homogenized in 100 mM potassium phosphate buffer, pH 8, containing 2 mM dithiothreitol, and centrifuged at 20000 g for 30 min at 4 °C. Aliquots (0.2 ml) of the supernatant on the resuspended pellet were then incubated with 7.4 kBq [1,4-14C]putrescine (3.7 GBq mol-1 m-3; Amersham International, UK) for 30 min, in the presence or absence of 100 µM unlabelled putrescines. The reaction was stopped by adding 2% (w/v) sodium carbonate and the product ([14C]pyrroline) extracted immediately in 1 ml toluene, and 500 µl of the lipophilic phase withdrawn and added to 2 ml scintillation fluid (Emulsifier Safe; Packard) and the radioactivity counted.
Phenylalanine ammonia lyase (PAL; EC 4.3.1.5) was assayed as described earlier (Southerton and Deverall, 1990). Briefly, a 250 mg sample of leaf tissue was ground in a cold mortar and pestle containing 2.5 ml sodium borate buffer (0.1 M, pH 8.8). A 1.5 ml aliquot of the homogenate was transferred to a centrifuge tube and 0.75 ml supplemented borate buffer containing 3 mM ß-mercaptoethanol and 3 mM EDTA was added to the homogenate and mixed thoroughly. The tube was then centrifuged at 20000 g for 15 min at 4 °C. The supernatant was used as the enzyme extract and samples were kept on ice at all times.
A 300 µl sample of leaf extract was incubated at 40 °C with 0.6 ml of borate buffer containing 0.6 µM L-phenylalanine. A blank with no L-phenylalanine was also prepared. After 2 h the reaction was stopped by adding 100 µl 6 M HCI. The product (cinnamic acid) was extracted by adding 1.0 ml of chloroform and mixing thoroughly on a vortex mixer. This was then centrifuged at 1300 g for 5 min at 4 °C. A 0.5 ml aliquot was then taken from the lower, chloroform phase, the chloroform evaporated by blowing nitrogen over the sample and the residue was then redissolved in 0.1 ml borate buffer (0.1 M, pH 8.8). Absorbance was measured at 270 nm and a standard curve produced using 0.1–10 µg ml-1 cinnamic acid. Enzyme activity is expressed as µg cinnamic acid mg-1 protein h-1.
Peroxidase (EC 1.11.1.7) activity was assayed as described earlier (Southerton and Deverall, 1990). A 250 mg sample of leaf tissue was ground in a cold mortar and pestle with 2.5 ml sodium borate buffer (0.1 M, pH 8.8). A further 0.75 ml sodium borate buffer was added and thoroughly mixed with the leaf preparation. A 1.5 ml sample was then transferred to a centrifuge tube and centrifuged at 20000 g for 15 min at 4 °C. The supernatant was used as the enzyme extract and samples were kept on ice until required in the assay. 10 µl of the enzyme sample was added to 2.95 ml supplemented phosphate buffer (0.1 M, pH 7.0) containing 0.9 µM guiacol and 0.36 µM hydrogen peroxide. Absorbance at 470 nm was then recorded for 2 min at 25 °C and enzyme activity expressed as the in absorbance mg-1 protein.
|
Results |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Free and conjugated polyamines in plants treated with MJ
Treatment of first leaves of barley seedlings with MJ produced no significant effect on levels of free polyamines in the second leaves (Fig. 1a
). However, treated first leaves exhibited significant increases in levels of free putrescine and spermine 1 d following treatment, and in levels of all three polyamines 4 d after treatment (Fig. 1b). No significant changes in levels of free polyamines were observed 2 d following treatment. By contrast, levels of soluble conjugates of putrescine and spermidine were significantly increased in first and second leaves 1, 2 and 4 d after exposure of the first leaves to MJ (Fig. 2a, b). Levels of spermine conjugates were much smaller than the levels of the other polyamine conjugates and in some cases could not be detected; levels of spermine conjugates were not altered following treatment with MJ (Fig. 2a, b).
|
) Control; (
) treated with MJ: put, putrescine; spd, spermidine; spm, spermine. (a) Second leaves, (b) first leaves. Values represent means of five replicates ±SE. Significant differences from controls shown at *P<0.05 and **P<0.01.
|
Activities of polyamine biosynthetic and catabolic enzymes
Soluble ODC activity was significantly increased in both first and second leaves of barley following exposure of the first leaves to MJ, while no changes were observed for activity of particulate ODC (Fig. 3). Very large and significant increases in activities of both soluble and particulate ADC were found in first and second leaves after the first leaves had been treated with MJ (Fig. 4). Thus, 1 d following treatment of the first leaves with MJ, activities of soluble and particulate ADC had increased 6.5-fold and 12-fold, respectively (Fig. 4). Activity of the cytosolic enzyme AdoMetDC was increased significantly in first and second leaves of barley following exposure of the first leaves to MJ, with a 4-fold increase in enzyme activity detected in first leaves 1 d after treatment with MJ (Fig. 5).
|
|
|
Large and significant increases in soluble and particulate DAO activity were found in both first and second leaves of barley following treatment of the first leaves with MJ (Fig. 6
). For example, soluble DAO activity was increased 4.2-fold in second leaves 2 d following exposure of the first leaves to MJ, while 4 d after treatment of the first leaves, activity of particulate DAO had increased 2-fold in these leaves (Fig. 6).
|
Induced systemic protection in MJ-treated plants
Exposure of the first leaves of barley seedlings to MJ resulted in a significant reduction in powdery mildew infection on the second leaves (Fig. 7a). Activities of the plant defence-related enzymes PAL and peroxidase were increased significantly in second leaves following treatment of the first leaves with MJ, with a 5-fold increase in PAL activity and an approximately 3-fold increase in peroxidase activity observed in second leaves 1 and 2 d after treatment of the first leaves (Fig. 7b, c). Inoculation of the second leaves 2 d after first leaves had been exposed to MJ led to a further increase in PAL activity but not in peroxidase activity (Fig. 7b, c).
|
) treated with MJ plus inoculation of second leaves. Values represent means of 20 replicates (A) and five replicates (B, C) ±SE. Significant differences from controls are shown at **P<0.01. |
Discussion |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
The present study has demonstrated a striking increase in the levels of soluble conjugates of putrescine and spermidine in first leaves of barley treated with MJ vapour and in untreated second leaves on those plants. So 1 d after the first leaves were treated with MJ, 4-fold and 5-fold increases in soluble putrescine and spermidine conjugates, respectively, were observed in second leaves. By contrast, levels of free polyamines in second leaves were not affected by treatment of first leaves with MJ, although increases in free putrescine and spermine were observed in MJ-treated first leaves 1 d following treatment and in all polyamines 4 d after treatment. The increase in soluble polyamine conjugates found here in treated first leaves agrees with other reports which have shown MJ-induced accumulation of coumaroyl conjugates of putrescine in barley leaf segments (Lee et al., 1997
) and as much as 10-fold increases in soluble polyamine conjugates in micropropagated potato plants treated with JA (Mader, 1999). It also agrees with recent work (Biondi et al., 2001) which reported very large increases in acid-soluble polyamine conjugates in tobacco thin layers treated with MJ. However, this is the first report of increased levels of polyamine conjugates in untreated leaves on plants where the lower leaves have been treated with MJ. Why MJ should increase levels of polyamine conjugates in uninfected second leaves on otherwise infected plants is not known, but the mechanism responsible for this effect is worthy of further investigation.
As indicated earlier, acid-soluble polyamine conjugates are mainly HCAs (Flores and Martin-Tanguy, 1991), which are formed by the conjugation of polyamines to phenolic acids like caffeic, coumaric and ferulic acids. Interestingly, jasmonates are known to increase the formation of phenolic compounds by stimulating the phenylpropanoid pathway. For example, it was shown that exposure of various plant cell cultures to MJ increased PAL activity (Gundlach et al., 1992), while it was demonstrated that the JA-induced accumulation of acid-soluble polyamine conjugates could be reduced by prior treatment with a PAL inhibitor (Mader, 1999). Since, in the present work, MJ treatment of first leaves led to increased activities of the polyamine biosynthetic enzymes ODC, ADC and AdoMetDC, as well as an increase in PAL activity, it would appear that both substrates for the formation of soluble polyamine conjugates were likely to have been increased in amount in these tissues. The increase in activities of the three polyamine biosynthetic enzymes noted here agrees with other work (Biondi et al., 2001) which also found increased activities of ODC, ADC and AdoMetDC in MJ-treated tobacco thin layers. However, whereas Biondi et al. observed increases in both soluble and particulate activities of ODC and ADC (Biondi et al., 2001), in the current study, particulate ODC activity was not affected by MJ treatment, while both soluble and particulate ADC activities were increased. Indeed, the increases in ADC activities were very substantial, with for example, a 12-fold increase in particulate ADC activity detected in second leaves of barley seedlings when the first leaf had been exposed to MJ. Whether this increase in the activities of the three biosynthetic enzymes is related to HCA formation and/or to other processes in the leaves is not known. It has been suggested that ODC is preferentially implicated in cell division while ADC is involved in cell elongation and stress responses (Flores and Martin-Tanguy, 1991; Cohen, 1998). Further, the relative contributions of ODC and ADC to HCA formation is still uncertain (Burtin et al., 1989; Robins et al., 1991).
DAO typically catalyses the oxidation of putrescine to yield pyrroline, ammonia and hydrogen peroxide. There are many reports of DAO from legumes, but fewer reports of DAO activity in cereals. Nevertheless, DAO has been purified to homogeneity from barley (Cogoni et al., 1990) and its activity in response to external stimuli has been studied (Tamai et al., 2000; Lin and Kao, 2001). The present study demonstrated very substantial increases in both soluble and particulate DAO activities in MJ-treated first, and in second leaves, of barley. Soluble and particulate DAO activities have also been shown to increase in MJ-treated tobacco thin layers (Biondi et al., 2001). DAO activity produces hydrogen peroxide (H2O2), which is a substrate for peroxidase. Since peroxidases are responsible for the cross-linking of cell wall components, it has been proposed that the role of DAO is to generate the H2O2 required for lignification during both normal growth and in response to pathogen infection (Angelini et al., 1993). Since peroxidase activity was also found to have increased in second leaves of barley seedling where the first leaf had been treated with MJ, it is possible that the combined increase in activities of DAO and peroxidase is related to plant defence. Indeed, such leaves also exhibited a 5-fold increase in PAL activity, which catalyses the first committed step in phenylpropanoid synthesis and provides phenolics for, among other activities, plant defence. PAL activity has been shown to increase in interactions between barley and powdery mildew, and the phenolic compounds that are synthesized as a result, accumulate in papillae and cell wall haloes, and throughout the cytoplasm and walls of dead or dying cells (Carver et al., 1995). In fact, Carver et al. suggest that synthesis of phenols is important in many forms of resistance to B. graminis (Carver et al., 1995). In the present work, PAL activity was not only increased in second leaves following treatment of the lower leaf with MJ, but inoculation with powdery mildew increased PAL activity in those leaves further. As indicated earlier, PAL also provides the phenolic substrates required for the formation of acid-soluble polyamine conjugates or HCAs. Interestingly, HCAs have been implicated in plant resistance to pathogens (Walters, 2000) and in recent work, three spermidine conjugates were shown to reduce mycelial growth of Pyrenophora avenae and powdery mildew infection of barley seedlings (Walters et al., 2001). It seems therefore that exposure of the first leaves of barley to MJ vapour leads to an increase in activity associated with plant defence against pathogens in the second leaves. Not surprisingly therefore, such leaves also exhibit greatly reduced infection by powdery mildew compared to controls, in agreement with previous work (Mitchell and Walters, 1995).
In the present study, first leaves to be treated with MJ were sealed in a plastic chamber during treatment. This was required in order to minimize the loss of MJ vapour and its subsequent effect on the second leaves of experimental plants. This is all the more important since it is known that jasmonates exert direct antifungal effects, including direct effects on the development of germlings of B. graminis f. sp. hordei (Schweizer et al., 1993; Mitchell, 1998). What is not known is whether, following treatment of the first leaves of barley with MJ, it is transported to the second leaves or whether another compound(s) acts as the long distance signal.
|
Acknowledgments |
|---|
AM is grateful to SAC and the University of Glasgow for the award of a William Stewart Postgraduate Scholarship. SAC receives grant-in-aid from the Scottish Executive, Environment and Rural Affairs Department.
|
Notes |
|---|
1 To whom correspondence should be addressed. Fax: +44(0)1292525314. E-mail: d.walters{at}au.sac.ac.uk
|
References |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Andresen I, Becker W, Schluter K, Burges J, Parthier B, Apek K. 1992. The identification of leaf thionin as one of the main jasmonate-induced proteins of barley (Hordeum vulgare). Plant Molecular Biology 19, 193–204.[Web of Science][Medline]
Angelini R, Bragaloni M, Federico R, Infantino A, Porta-Puglia A. 1993. Involvement of polyamines, diamine oxidase and peroxidase in resistance of chick-pea to Ascochyta rabiei. Journal of Plant Physiology 142, 704–709.
Biondi S, Fornalé S, Oksman-Caldentey K-M, Eeva M, Agostani S, Bagni N. 2000. Jasmonates induce over-accumulation of methyl putrescine and conjugated polyamines in Hyoscyamus muticus L. root cultures. Plant Cell Reports 19, 691–697.
Biondi S, Scaramagli S, Capitani F, Altamura MM, Torrigiani P. 2001. Methyl jasmonate up-regulates biosynthetic gene expression, oxidation and conjugation of polyamines, and inhibitors shoot formation in tobacco thin layers. Journal of Experimental Botany 52, 231–242.
Burtin D, Martin-Tanguy J, Paynot M, Rossin N. 1989. Effects of the suicide inhibitors of arginine and ornithine decarboxylase activities on organogenesis, growth free polyamine and hydroxycinnamoyl putrescine levels in leaf explants of Nicotiana Xanthi n.c. cultivated in vitro on a medium producing callus formation. Plant Physiology 89, 104–110.
Carver TLW, Zeyen RJ, Bushnell WR, Robins MP. 1994. Inhibition of phenylalanine ammonia lyase and cinnamyl-alcohol dehydrogenase increases quantitative susceptibility of barley to powdery mildew (Erysiphe graminis DC). Physiological and Molecular Plant Pathology 44, 261–272.
Carver TLW, Zeyen RJ, Lyngkjaer MF. 1995. Plant cell defences to powdery mildew of Gramineae. Aspects of Applied Biology 42, 257–266.
Chaudhry B, Müller-Uri F, Cameron-Mills V, Gough S, Simpson D, Skriver K, Mundy J. 1994. The barley 60 kDa jasmonate-induced protein (JIP60) is a novel ribosome-inactivating protein. The Plant Journal 6, 815–824.[Web of Science][Medline]
Coghlan SE, Walters DR. 1990. Polyamine metabolism in ‘green-islands’ on powdery mildew infected barley leaves: possible interactions with senescence. New Phytologist 116, 417–424.
Cohen SS. 1998. A guide to the polyamines. New York: Oxford University Press.
Cohen Y, Gysi U, Niderman T. 1993. Local and systemic protection against Phytopthora infestans induced in potato and tomato plants by jasmonic acid and jasmonic methyl ester. Phytopathology 83, 1054–1062.
Creelman RA, Mullet JE. 1995. Jasmonic acid distribution and action in plants: regulation during development and response to biotic and abiotic stress. Proceedings of the National Acaademy of Sciences, USA 92, 4114–4119.
Creelman RA, Mullet JE. 1997. Biosynthesis and action of jasmonates in plants. Annual Review of Plant Physiology and Plant Molecular Biology 48, 355–381.[Web of Science][Medline]
Farmer EE, Ryan CA. 1990. Interplant communication: airborne methyl jasmonate induces synthesis of proteinase inhibitors in plant leaves. Proceedings of the National Academy of Sciences, USA 87, 7713.
Farmer EE, Ryan CA. 1992. Octadecanoid precursors of jasmonic acid activate the synthesis of wound-inducible proteinase inhibitors. The Plant Cell 4, 129–134.
Flores HE, Martin-Tanguy J. 1991. Polyamines and plant secondary metabolites. In: Slocum RD, Flores HE, eds. Biochemistry and physiology of polyamines in plants. Boca Raton, Florida: CRC Press, 57–76.
Friedman R, Altman A, Bachrach U. 1982. Polyamines and root formation in mung bean hypocotyl cuttings. Plant Physiology 70, 844–848.
Gogoni A, Piras C, Farci R, Melis A, Floris G. 1990. Hordeum vulgare seedlings amino oxidase. Purification and properties. Plant Physiology 93, 818–821.
Gundlach H, Müller MJ, Kutchan TM, Zenk MH. 1992. Jasmonic acid is a signal transducer in elicitor-induced plant cell cultures. Proceedings of the National Academy of Sciences, USA 90, 2389–2393.
Hippe-Sanwald S, Hermanns M, Sommerville SC. 1992. Ultrastructural comparison of incompatible and compatible interactions in the barley powdery mildew disease. Protoplasma 168, 27–40.
Kozlowski G, Buchala A, Métraux J-P. 1999. Methyl jasmonate protects Norway spruce [Picea abies (L.) Karst.] seedlings against Pythium ultimum Trow. Physiological and Molecular Plant Pathology 55, 53–58.
Lee J, Vogt T, Schmidt J, Parthier B, Löbler M. 1997. Methyl jasmonate-induced accumulation of coumaroyl conjugates in barley leaf segments. Phytochemistry 44, 589–592.
Lin CC, Kao CH. 2001. Cell wall peroxidase activity, hydrogen peroxide level and NaCl-inhibited root growth of rice seedlings. Plant and Soil 230, 135–143.[Web of Science]
Mader JC. 1999. Effects of jasmonic acid, silver nitrate and L-AOPP on the distribution of free and conjugated polyamines in roots and shoots of S. tuberosum in vitro. Journal of Plant Physiology 154, 79–88.
Mitchell AF. 1998. Expression of systemic resistance in Hordeum vulgare against Erysiphe graminis by treatment with abiotic elicitors. PhD thesis, University of Glasgow.
Mitchell AF, Walters DR. 1995. Systemic protection in barley against powdery mildew infection using methyl jasmonate. Aspects of Applied Biology 42, 323–326.
Nair SKR, Ellingboe AH. 1962. A method of controlled inoculation with conidiospores of Erysiphe graminis var tritici. Phytopathology 52, 714.
Robins RJ, Parr AJ, Walton NJ. 1991. Studies on the biosynthesis of tropane alkaloids in Datura stramonium L. transformed root cultures. 2. On the relative contributions of L-arginine and L-ornithine to the formation of the tropane ring. Planta 183, 196–201.
Scaramagli S, Biondi S, Torrigiani P. 1999. Methylglyoxal (bis-guanyphydrazone) inhibition of organogenesis is not due to S-adenosylmethionine decarboxylase inhibition/polyamine depletion in tobacco thin layers. Physiologia Plantarum 107, 353–360.
Schweizer P, Gees R, Mösinger E. 1993. Effect of jasmonic acid on the interaction of barley (Hordeum vulgare L.) with the powdery mildew Erysiphe graminis f. sp. hordei. Plant Physiology 102, 503–511.[Abstract]
Sembdner G, Parthier B. 1993. The biochemistry and the physiological and molecular actions of jasmonates. Annual Review of Plant Physiology and Molecular Biology 44, 569–589.[Web of Science]
Slocum RD, Galston AW. 1985. Change in polyamine biosynthesis associated with post-fertilization growth and development in tobacco ovary tissue. Plant Physiology 79, 336–343.
Southerton SG, Deverall BJ. 1990. Changes in phenylalanine ammonia-lyase and peroxidase activities in wheat cultivars expressing resistance to the leaf-rust fungus. Plant Pathology 39, 223–230.
Tamai T, Shimada Y, Sugimoto T, Shiraishi N, Oji Y. 2000. Potassium stimulates the efflux of putrescine in roots of barley seedlings. Journal of Plant Physiology 157, 619–626.
Tiburcio AF, Kaur-Sawhney R, Ingersoll R, Galston AW. 1985. Correlation between polyamines and pyrrolidine alkaloids in developing tobacco callus. Plant Physiology 78, 323–326.
Walters DR. 2000. Polyamines in plant-microbe interactions. Physiological and Molecular Plant Pathology 57, 137–146.
Walters D, Meurer-Grimes B, Rovira I. 2001. Antifungal activity of three spermidine conjugates. FEMS Microbiology Letters 10030, 1–4.
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  R. Angelini, A. Tisi, G. Rea, M. M. Chen, M. Botta, R. Federico, and A. Cona Involvement of Polyamine Oxidase in Wound Healing Plant Physiology, January 1, 2008; 146(1): 162 - 177. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 K. Niemi, S. Sutela, H. Haggman, C. Scagel, J. Vuosku, A. Jokela, and T. Sarjala Changes in polyamine content and localization of Pinus sylvestris ADC and Suillus variegatus ODC mRNA transcripts during the formation of mycorrhizal interaction in an in vitro cultivation system J. Exp. Bot., August 1, 2006; 57(11): 2795 - 2804. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 D. R. WALTERS, T. COWLEY, and H. WEBER Rapid Accumulation of Trihydroxy Oxylipins and Resistance to the Bean Rust Pathogen Uromyces fabae Following Wounding in Vicia faba Ann. Bot., May 1, 2006; 97(5): 779 - 784. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. D. Broeckling, D. V. Huhman, M. A. Farag, J. T. Smith, G. D. May, P. Mendes, R. A. Dixon, and L. W. Sumner Metabolic profiling of Medicago truncatula cell cultures reveals the effects of biotic and abiotic elicitors on metabolism J. Exp. Bot., January 1, 2005; 56(410): 323 - 336. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 H. Chen, B. C. McCaig, M. Melotto, S. Y. He, and G. A. Howe Regulation of Plant Arginase by Wounding, Jasmonate, and the Phytotoxin Coronatine J. Biol. Chem., October 29, 2004; 279(44): 45998 - 46007. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. Yoda, Y. Yamaguchi, and H. Sano Induction of Hypersensitive Cell Death by Hydrogen Peroxide Produced through Polyamine Degradation in Tobacco Plants Plant Physiology, August 1, 2003; 132(4): 1973 - 1981. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||