Journal of Experimental Botany, Vol. 54, No. 381, pp. 355-363,
January 2, 2003
© 2003 Oxford University Press
Spermidine and related-metabolic inhibitors modulate sugar and amino acid levels in Vitis vinifera L.: possible relationships with initial fruitlet abscission
Received 4 April 2002; Accepted 13 September 2002
Unité de Recherche Vignes et Vins de Champagne (URVVC), UPRES EA 2069, UFR Sciences, Université de Reims Champagne-Ardenne, BP 1039, F-51687 REIMS cedex 2, France
1 Fax: +33 326 913 342. E-mail: aziz.aziz{at}univ-reims.fr
Abbreviations: CHA, cyclohexylamine; DAO, diamine oxidase; Dap, 1,3-diaminopropane; GABA, 
-aminobutyric acid; HEH, ß-hydroxyethylhydrazine. MRT, Merlot; PN, Pinot noir; PA(s), polyamine(s); PAO, polyamine oxidase; Put, putrescine; Spd, spermidine; Spm, spermine.
 |
Abstract |
|---|
 Top Abstract IntroductionMaterials and methodsResultsDiscussionReferences |
|---|
The relationships between free polyamines (PAs), sugar and amino acid status were investigated in cuttings from two cultivars of Vitis vinifera L., Pinot noir (PN), a low abscising cultivar and Merlot (MRT), a high abscising one. In both cultivars free PAs decreased in inflorescences, but more drastically in MRT plants. Upon anthesis, this was associated with a decreased sugar content, especially sucrose, and an increase in total free amino acids. Thereafter, sucrose and amino acids showed opposite trends. In addition, darkening the PN plants at full flowering resulted in a dramatic decrease of PAs and sugars in inflorescences, but an increase in amino acid content, followed by high abscission. The concept that initial fruitlet abscission might be regulated by free PAs through changes in primary metabolites was hypothesized. Hence, the application of exogenous spermidine (Spd), but not putrescine (Put), prior to flowering markedly inhibits abscission. The Spd treatment also increased soluble sugar content but reduced amino acids in both leaves and inflorescences, while Put had no significant effect. By contrast, cyclohexylamine and ß-hydroxyethylhydrazine, as potent inhibitors of Spd synthase and PA-oxidases, respectively, exerted inverse effects on sugar, amino acid and abscission levels. Sucrose and free proline seemed to be highly sensitive to these treatments. This study suggests that Spd could regulate fruitlet abscission in grapevine by modulating, in a reverse way, the levels of sugars and amino acids in inflorescences.
Key words: Abscission, amino acids, grapevine, polyamines, proline, spermidine, sucrose, sugars.
|
Introduction |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Flower or fruitlet abscission is a common phenomenon that occurrs in many crop plants in response to developmental or environmental cues, leading to significant crop losses. This event is highly variable according to species and cultivar and appears to be a function of endogenous growth regulator status in ovaries and with metabolic regulation during floral development (Osborne, 1989; Gillaspy et al., 1993; Gonzalez-Carranza et al., 1998; Taylor and Whitelaw, 2001). Hormonal signals and competition for photoassimilates remain factors of prime importance among those influencing fruitlet abscission (Moss et al., 1972; Goldschmidt and Koch, 1996; Gomez-Cadenas et al., 2000). A regulatory role of polyamines (PAs) has also been suggested in flowering and initial fruitlet abscission (Evans and Malmberg, 1989; Aziz et al., 2001), but interactions of PAs with assimilated compounds as related to abscission remain still unknown.
Considerable research has suggested a close connection between PAs, such as putrescine (Put), spermidine (Spd) and spermine (Spm), and a large range of growth and developmental processes including flower induction, reproductive development, fruit set and growth, and fruit ripening (Applewhite et al., 2000; Aziz et al., 2001; Kakkar and Rai, 1993; Galston et al., 1997; Walden et al., 1997). This has been substantiated by the study of tobacco mutants and transformants with aberrant flowering habits that have an unusual metabolism and PA content (Malmberg and McIndoo, 1983). These mutants, which are deficient in PAs, showed alteration in floral morphology such as anthers partially turned into petals and ovules transformed into stamens. Conversely, Petunia mutants with irregular floral development display abnormal PA levels (Gerats et al., 1988) and male sterile mutants of maize lack PA accumulation in the anthers (Flores et al., 1989). It has also been demonstrated that exogenous application of PAs during fruit set increased the number and size of the fruit that set (Egea-Cortines and Mizrahi, 1991; Evans and Malmberg, 1989). On the other hand, it has been shown that PAs interact in some way with all plant hormones. PAs like cytokinins have antisenescence activity (Altman, 1989) and PA biosynthesis may compete with the biosynthesis of ethylene (Kushad and Dumbroff, 1991; Turano et al., 1997), which has been described as a stimulator of abscission (Ruperti et al., 1998). PAs could also play a role in the modulation of reduced nitrogen inside the cells and in the structure and functioning of the photosynthetic apparatus (Kotzabasis et al., 1993; Larher et al., 1998) because of their richness in amine groups and their biosynthesis through amino acid decarboxylases (Evans and Malmberg, 1989; Walden et al., 1997).
Several reports indicate that the transition of ovary to fruitlets as well as fruitlet abscission are dependent on nutrient availability (Moss et al., 1972; Gillaspy et al., 1993; Gomez-Cadenas et al., 2000). A decrease in the photosynthetic production of sucrose related to pruning or shading the leaves caused a proportional increase in fruitlet abscission (Goldschmidt and Koch, 1996). Some experiments with citrus have shown that defoliation induced fruitlet abscission by reducing soluble sugars, but did not cause nitrogen deficiency (Mehouachi et al., 1995; Gomez-Cadenas et al., 2000). Authors suggested that the sucrose status of the fruitlets is a major factor in the mechanism that triggered fruitlet abscission. Nevertheless, changes in carbon metabolism in plants during development are known to be associated with alterations in nitrogen metabolism (Huppe and Turpin, 1994). Turano and Kramer (1993) determined the interaction of carbon and nitrogen availability on PA accumulation in soybean by using a detached leaf system. To date, no information is available about the regulatory effect of PAs on the status of carbon and nitrogen compounds in higher plants, experiencing abscission. On the one hand, it has been reported that Put, Spd and Spm are present in chloroplasts, thylakoid membranes, photosystem II membranes, and the light-harvesting complex (Kotzabasis et al., 1993). Thus, it has been suggested that PAs could be involved in the maintenance of photosynthetic activity during the senescence process. On the other hand, PAs have been proposed to participate in the plasticity of amino acid metabolism in both rape and tomato subjected to abiotic stresses (Aziz et al., 1998, 1999; Larher et al., 1998). Also pea shoots, oat leaves and soybean seedlings were shown to metabolize Put and Spd to GABA, glutamate, aspartate, sugars, and organic acids (Rastogi and Davies, 1991).
In the present study, the changes occurring in free PAs, soluble sugar and amino acid contents during floral development were investigated in inflorescences of cuttings from two grapevine cultivars exhibiting different abscission potentials: Merlot a ‘high abscising’ cultivar and Pinot noir a ‘low abscising’ one. The relationships between free PA, primary metabolites and abscission were examined in cuttings under photoperiod conditions and after their transfer to a transient continuous dark. Furthermore, to assess the mechanism of PA action on the regulation of fruitlet abscission, the effects of pre-anthesis-supplied Put, Spd and their related metabolic inhibitors on soluble sugar and amino acid contents were reported in different parts of the grapevine cuttings. Information regarding these interactions should be of value in understanding the physiological and biochemical processes involved in initial grapevine fruitlet abscission.
|
Materials and methods |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Plant material and growth conditions
Three-node-long cuttings of two cultivars of Vitis vinifera L., Pinot noir (clone 521) and Merlot (clone 181) were collected from 6-year-old plants. Cuttings were surface-sterilized with 0.05% cryptonol and rooted as described by Mullins and Rajasekaran (1981). Selected rooted cuttings were placed in plastic pots filled with vermiculite substrate and grown in a culture chamber (16 h photoperiod, temperature 25/20 °C day/night, irradiance of 200 µmol s–1 m–2 (fluorescent lights Philips TLD36W/83), relative humidity 75/90% day/night). Only a single flowering stem was allowed to develop on each plant during growth as described in Aziz et al. (2001). Abscission was estimated as a percentage of original flowers.
Polyamine and inhibitor treatments
Putrescine and spermidine were added to the nutritive solution at concentrations ranging from 0.1 to 1 mM, one week before anthesis. Cyclohexylamine (CHA) and ß-hydroxyethylhydrazine (HEH) were also supplied separately at various concentrations (from 0.5 to 2 mM) in the nutritive solution. Plants were grown under culture chamber conditions as described above. Plants were divided into roots, leaves and flowers or fruitlets and then weighed and frozen in liquid nitrogen before analysis. All experiments were replicated at least three times.
Polyamine extraction and analysis
Frozen samples were powdered and mixed with 1 M HCl. The homogenates were kept for 1 h on ice and centrifuged for 20 min at 24 000 g to obtain free polyamines. HPLC equipped with a fluorescence spectrophotometer detector (Waters) was used to separate and quantify polyamines prepared as their dansyl derivatives according to the method of Flores and Galston (1982). The column was a reverse phase hypersil C18 (particle size 5 µm, 4.6x250 mm, Supelco). Dansylated polyamines were eluted with a programmed methanol:water solvent gradient as described in Aziz et al. (1997).
Carbohydrate and amino acid extraction and analysis
Samples (1 g FW) were placed into test tubes containing 3 ml ethanol and kept in a water bath at 90 °C until complete ethanol evaporation. 2 ml of distilled water were then added and the tubes vigorously shaken. The corresponding crude extracts were centrifuged at 12 000 g for 10 min to remove insoluble particles. Sugar concentrations were determined by enzymatic methods. Glucose was estimated using the Boehringer-Mannheim UV method at 340 nm in enzymatic reactions coupled to the production of NADPH. The fructose content was calculated from the difference between the glucose content before and after treatment of the samples with 30 units ml–1 phosphoglucose isomerase. Sucrose was determined by measuring glucose after hydrolysis with 30 units ml–1 ß-fructosidase and subtracting the free glucose values. Total soluble sugars were determined using the anthrone method of Roe (1955). Total amino acids were analysed using the ninhidrin reagent (Rosen, 1957). Proline was determined according the method described by Aziz et al. (1998).
|
Results |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Polyamine contents in inflorescences as related to abscission sensitivity
Previous experiments using grapevine cuttings (Aziz et al., 2001) have shown that abscission was higher in Merlot (MRT) than in Pinot noir (PN). This is also the case when both cultivars grafted on the same rootstock were compared (Paschalidis et al., 2001). As shown in Fig. 1, in inflorescences of PN, the free PA amounts decreased gradually after anthesis and remained important even after full bloom. However, in inflorescences of MRT the content of total free PAs decreased before anthesis and reached a lower level thereafter. The inset shows individual free PA contents in roots, leaves and inflorescences of PN and MRT at full flowering. Among them Spd, and Dap (a product of Spd and/or Spm oxidation) were the most abundant in leaves and inflorescences of PN, while Spm and Put were present almost in equal amounts. Spd and Dap were at least 2.5 times higher in PN than MRT. Spd was also represented at the highest percentage among PAs covalently bound in the soluble fraction (data not shown). Interestingly, the situation in inflorescences at full flowering, in respect to all other organs analysed, presented a high level of free Spd and Dap in PN (Fig. 1, inset).
|
Sugar contents in inflorescences as related to abscission sensitivity
Figure 2 illustrates the changes of glucose, fructose and sucrose contents in inflorescences from PN and MRT during floral development. The general patterns of sugars were similar in both cultivars, but their levels were relatively higher in inflorescences of PN (Fig. 2A). It was observed that sucrose was the predominant carbohydrate in both cultivars. Sucrose concentration decreased within 7 d after anthesis to approximately 20% and 35% of its initial value in PN and MRT, respectively, then sucrose increased markedly. After full bloom sucrose concentration was higher in inflorescences of PN than MRT. Glucose and fructose represented less than 30% of total sugar contents and showed similar changes during development of the two cultivars. Fructose concentration gradually decreased during development, it also dropped by 60% at day 7 after anthesis and remained relatively unchanged. Glucose content slightly increased in both cultivars.
|
Amino acid contents in inflorescences as related to abscission sensitivity
The concentrations of total free amino acids from inflorescences of two cultivars were compared during development (Fig. 3). At the initial sampling time (day 10 before anthesis), the amino acid pool was 1.5 time higher in inflorescences of MRT compared to those of PN. After an initial rise in both cutivars, with a maximum at anthesis, the amino acid level declined during the post-anthesis stages, which coincides with sucrose accumulation in inflorescences (Fig. 2). This decline was greater in inflorescences of PN than in MRT.
|
Effect of light on metabolite levels and abscission
When PN plants grown with a 16 h photoperiod were kept in the continuous dark, the free PA and soluble sugar contents decreased drastically in inflorescences (Table 1). Within 48 h of darkness the free PA and soluble sugar contents decreased by about 58% and 30% of the initial values obtained at full flowering, respectively. Spd and sucrose contents were the most sensitive to continuous dark. They decreased by 65% and 30%, respectively. However, under these conditions the free amino acid content increased by about 40% within 48 h of darkness. Free proline was 2-fold higher in inflorescences of darkened plants. Consequently, the amino acid/sugar ratio in inflorescences increased more than 2-fold during the dark period. Darkening plants resulted also in a substantial increase in the abscission rate.
|
Effects of exogenous polyamines and related-inhibitors on sugar contents
The effects of PAs and related metabolic inhibitors on sugar concentration were investigated in roots, leaves and inflorescences of the two grapevine cultivars. As shown in Fig. 4, Spd treatment increased the total soluble sugar levels in all organs examined from both cultivars, while Put had no effect. The Spd effects were more pronounced in MRT than in PN. In the presence of 0.5 mM Spd the amount of soluble sugars increased 2-fold and 1.8-fold in inflorescences and leaves of MRT. Soluble sugars also increased in roots of MRT plants treated with Spd.
|
By contrast, when cuttings from both cultivars were treated either with different concentrations of CHA or HEH, the soluble sugar content was decreased in all organs examined (Fig. 5). With 2 mM HEH, the level of sugars was reduced by about 40% and 20% in inflorescences of PN and MRT, respectively. At high concentration CHA exerted also a depressive effect on sugar content particularly apparent in PN.
|
Effects of exogenous polyamines and related inhibitors on amino acid contents
Figure 6 represents the change in amino acid contents in different parts of cuttings from PN and MRT treated with various concentrations of Put and Spd. At full flowering, in non-treated plants, the total amino acid level was about 1.5-fold higher in inflorescences of MRT than PN, while in the other organs their levels were similar in both cultivars. Application of Spd caused a marked decrease of amino acid content in roots, leaves and inflorescences, while Put had no significant effect. In inflorescences, total amino acid content decreased by about 35% in both cultivars.
|
By contrast, amino acid contents increased in inflorescences of both cultivars when they treated with CHA or HEH. Their level was 1.5-fold higher in HEH-treated plants than in the control. Amino acid contents were also higher in roots of MRT treated with HEH, but they were not changed in those of PN (Fig. 7).
|
Like total amino acids, the level of proline was higher in inflorescences than other organs (Fig. 8). It was also very sensitive to the preceding treatments. Thus, the application of Spd in the external medium caused a decrease in proline content in inflorescences. The proline level remained relatively unchanged in the other organs. However, Put addition at the same concentration did not cause any significant change in the proline level in all organs examined. The proline content also increased in roots, leaves and inflorescences of both cultivars treated with CHA or HEH (Fig. 9). Proline content increased with increasing concentration of each inhibitor. Compared to the control (0 mM), in the presence of 2 mM HEH the proline level was 3-fold and 2-fold higher in inflorescences of PN and MRT, respectively.
|
|
|
Discussion |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Like many fruit trees species, some grapevine cultivars exhibited massive fruitlet abscission even under favorable growing conditions. In the present study, some aspects of the regulatory functions exerted by polyamines (PAs) and their related inhibitors have been investigated on sugar and amino acid levels experienced by two grapevine cultivars which exhibited different abscission sensitivities. It appeared that the low level of free PAs in the inflorescences is correlated with abscission sensitivity. At the fruit set stage, about 65% of flowers and young fruits on MRT had abscised against about 35% on those of PN, which conserved a high level of free PAs (with Spd as the major one) in their inflorescences. Thus, the high level of free PA observed in inflorescences of the low abscising cultivar suggests that these compounds may have an important function in reproductive organ development and/or fertility as reported for other plants (Bagni and Torrigiani, 1992; Galston et al., 1997). In this context PAs could be suited to serve either as a nitrogenous source or as signal molecules regulating the abscission processes in grapevine. This hypothesis is consistent with all the known facts on PAs relating to reproductive activity (for a review see Galston et al., 1997).
The findings support the hypothesis that soluble sugar availability could also be a determinant in the control of abscission of reproductive organs (Mehouachi et al., 1995; Gomez-Cadenas et al., 2000), since the low level of sucrose in the inflorescence after anthesis was associated with high abscission. Indeed, sucrose content increased markedly after anthesis in the inflorescences of low abscising plants. Mehouachi et al. (1995) have shown that defoliation-induced sucrose shortage provoked fruitlet abscission in citrus. It was noted that the post-anthesis sucrose accumulation was accompanied by a slight increase of hexoses in inflorescences. This would indicate that the increase of sucrose content may occur through its synthesis or its transport from source organs as reported for tomato (D’Aoust et al., 1999).
It was also shown that the amino acid level declined during the post-anthesis stages, which coincides with sucrose accumulation in inflorescences. This decline was greater in inflorescences of the low abscising cultivar, which could be due either to increased protein synthesis or to decreased proteolysis. Slocum and Galston (1985) have reported that protein synthesis was active in tobacco ovary tissues between anthesis and fertilization. The breakdown of proteins in different parts of the grapevine and translocation of free amino acids to the inflorescences may also contribute to the increased amino acid level.
The changes occurring in the high abscising grapevines appeared similar to those brought about when low abscising plants were darkened. Indeed, darkening resulted in a decrease of PA and sugar contents, and an increase of amino acid levels in inflorescences. Dark had also a detrimental effect on growth, flowering and abscission (more than 85% of floral organs had abscised). This suggests that the allocation of assimilates into the inflorescence could be photoregulated and implies communication, which could be mediated either directly via light (e.g. photoreceptors) (Galston, 1983; Yoshida and Hirasawa, 1998) or indirectly via photosynthesis and source–sink effects (Goldschmidt and Koch, 1996).
It was also shown that abscission can be inhibited by application of Spd (but not Put) prior anthesis by about 40% and 50% in PN and MRT. Direct or indirect Spd effects might be mediated by the enhanced level of Spd itself through its preferential accumulation in the inflorescences (Aziz et al., 2001) or by a suspected control at the level of nutrient adjustment in sink organs. Similarly, it was shown that the abscission percentage increased in response to CHA added in the external medium. CHA also lowered Spd, Spm and Dap in leaves and flowers of grapevine (Aziz et al., 2001). These effects revealed the contribution of the Spd synthase pathway in modulating Spd concentration in inflorescences. Spd synthase activity was detected in pea ovaries and a gene encoding this enzyme was highly expressed in flowers at anthesis (Alabadi and Carbonell, 1999). Recent reports (Applewhite et al., 2000; Tassoni et al., 2000) indicate a close connection between a high level of Spd and reproductive development in several lines of Arabidopsis. This is in accordance with the finding that inhibition of Spd synthesis in tobacco caused the malformation of anthers, including lack of pollen, replacement of anthers by petals and infertility (Burtin et al., 1991).
The metabolites resulting from the catabolism of Spd may also be involved in the regulation of grapevine abscission, because ß-hydroxyethylhydrazine (HEH), a potent inhibitor of polyamine oxidases (PAO), strongly increased the abscission of floral organs in both cultivars. Total abscission was observed at the end of flowering in the presence of HEH. Martin-Tanguy (1997) reported that, in male-sterile flowers of tobacco, PAO are involved in the adjustment of PA concentration during sexual differentiation. It has been reported that PA oxidation ensures recycling of the reduced carbon and nitrogen to Krebs cycle through the formation of 
1-pyrroline and GABA (Aziz et al., 1998).
Taking into account that the changes occurring in PA content precede those of sugars and amino acids, an attempt was made to characterize a relationship between PAs and these compounds at full flowering. For instance, it appeared that exogenous Spd induces an increase in soluble sugar content in both leaves and inflorescences, while CHA and HEH had a depressive effect especially at the level of inflorescences. The main sugar concerned is sucrose, which represents about 50% of the total soluble sugars. This result suggests that Spd metabolism may influence either sucrose synthesis or its accumulation in favour of the sink organs. Recent studies showed that the reduced level of sucrose in the inflorescences was associated with an inhibition of sucrose synthase activity, which seems to be a determinant for tomato fruit set (D’Aoust et al. 1999).
Exogenous Spd and its metabolic inhibitors also influenced the amino acid content in grapevine. In contrast to CHA and HEH, Spd strongly reduced the level of total amino acids both in leaves and inflorescences, while Put had no effect. The free proline level in the inflorescences was highly sensitive to these treatments. These effects are sustained by additional results showing that exogenous Spd enhanced the protein content in the inflorescences (data not shown). This suggests that the reduction of amino acid and free proline amounts relies to some extent on the inhibition of protein degradation by Spd (Balestrieri et al., 1987). In contrast, CHA and HEH might increase the release of amino acids and free proline from proteolysis. The effect of Spd on proline level could be related, at least in part, to the control of substrate availability, since PAs and proline synthesis require common precursors, glutamate, arginine and ornithine. Alternatively, the target(s) of Spd could be located at the level of enzymes involved in glutamate metabolism (Larher et al., 1998; Brugière et al., 1999). In response to Spd inhibitors, proline accumulation could reflect the extent of damage caused to protein synthesis, while the effects of Spd could be attributed to their antisenescence properties as reported in tomato (Aziz et al., 1998) and rape leaf tissues (Larher et al., 1998) subjected to osmotic stress.
This study has shown that a low level of PA and sugar are correlated with a high amino acid content in the inflorescence and subsequent fruitlet abscission. These adjustments seem to be dependent on the light, which could be of importance in fertility and fruit setting, probably by maintaining the fluxes of nitrogenous and carbon substrates in favour of the reproductive organs. One new factor is that Spd and its metabolic pathways seem to be involved in the regulation of grapevine fruitlet abscission directly or indirectly through interaction with soluble sugar and amino acid accumulation in sink organs. This recent proposal suggests that Spd could act as a component of the self regulatory mechanism that adjusts fruitlet load to carbon and nitrogen compounds and, possibly, offers a physiological basis for the photoassimilate competition-induced abscission occurring under natural conditions.
|
Acknowledgements |
|---|
I am grateful to Professor G Vernet for his encouragement and helpful advice and to Professor C Clément for his valuable discussion and reading of the manuscript. This work was supported in part by the Mumm–Perrier-Jouët Society (Epernay, France).
|
References |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Alabadi D, Carbonell J. 1999. Differential expression of two spermidine synthase genes during early fruit development and in vegetative tissues of pea. Plant Molecular Biology 39, 933–943.[CrossRef][Web of Science][Medline]
Altman A. 1989. Polyamines and plant hormones. In: Bachrach U, Heimer YM, eds. The physiology of polyamines, Vol. 31. Boca Raton, FL: CRC Press Inc., 121–145.
Applewhite PB, Kaur-Sawhney R, Galston AW. 2000. A role for spermidine in the bolting and flowering of Arabidopsis. Physiologia Plantarum 108, 314–320.[CrossRef]
Aziz A, Brun O, Audran JC. 2001. Involvement of polyamines in the control of fruitlet physiological abscission in grapevine (Vitis vinifera). Physiologia Plantarum 113, 50–58.[CrossRef]
Aziz A, Martin-Tanguy J, Larher F. 1997. Plasticity of polyamine metabolism associated with high osmotic stress in rape leaf discs and with ethylene treatment. Plant Growth Regulation 21, 153–163.[CrossRef]
Aziz A, Martin-Tanguy J, Larher F. 1998. Stress-induced changes in polyamine and tyramine levels can regulate proline accumulation in tomato leaf discs treated with sodium chloride. Physiologia Plantarum 104, 195–202.[CrossRef]
Aziz A, Martin-Tanguy J, Larher F. 1999. Salt stress-induced proline accumulation and changes in tyramine and polyamine levels are linked to ionic adjustment in tomato leaf discs. Plant Science 145, 83–91.[CrossRef]
Bagni N, Torrigiani P. 1992. Polyamines: a new class of growth substances. In: Karssen CM, Van Loon LC, Vreugdenhil D, eds. Progress in plant growth regulation. Dordrecht, The Netherlands: Kluwer Academic Publishers, 264–275.
Balestrieri W, Cioni P, Romagnoli A, Bernini S, Fissi A, Felicioli R. 1987. Mechanism of polyamine inhibition of leaf protease. Archives of Biochemistry and Biophysics 255, 460–463.[CrossRef][Web of Science][Medline]
Brugière N, Dubois F, Limami AM, Lelandais M, Roux Y, Sangwan RS, Hirel B. 1999. Glutamine synthetase in the phloem plays a major role in controlling proline production. The Plant Cell 11, 1995–2011.
Burtin D, Martin-Tanguy J, Tepfer D. 1991. 
-DL-Difluoromethylornithine, a specific, irreversible inhibitor of putrescine biosynthesis, induces a phenotype in tobacco similar to that ascribed to the root-inducing, left-hand transferred DNA of Agrobacterium rhizogenes. Plant Physiology 95, 461–468.
D’Aoust MA, Yelle S, Nguyen-Quoc B. 1999. Antisense inhibition of tomato fruit sucrose synthase decreases fruit setting and the sucrose unloading capacity of young fruit. The Plant Cell 11, 2407–2418.
Egea-Cortines M, Mizrahi Y. 1991. Polyamines in cell division, fruit set and development and seed germination. In: Slocum RD, Flores HE, eds. Biochemistry and physiology of polyamines in plants. Boca Raton, FL:. CRC Press, 143–154.
Evans PT, Malmberg RL. 1989. Do polyamines have roles in plant development? Annual Review of Plant Physiology and Plant Molecular Biology 40, 235–269.[Web of Science]
Flores HE, Galston AW. 1982. Analysis of polyamines in higher plants by high performance liquid chromatography. Plant Physiology 69, 701–706.
Flores HE, Protacio CM, Signs MW. 1989. Primary and secondary metabolism of polyamines in plants. In: Poulton JE, Romeo JT, Cohen EE, eds. Plant nitrogen metabolism, Vol. 23. New-York: Plenum Press, 329–393.
Galston AW. 1983. Polyamines as modulators of plant development. BioScience 33, 382–388.[CrossRef][Web of Science]
Galston AW, Kaur-Sawhney R, Altabella T, Tiburcio F. 1997. Plant polyamines in reproductive activity and response to abiotic stress. Botanica Acta 110, 197–207.
Gerats AGM, Kaye C, Collins C, Malmberg RL. 1988. Polyamine levels in Petunia genotypes with normal and abnormal floral morphologies. Plant Physiology 86, 390–393.
Gillaspy G, Ben-David H, Gruissem W. 1993. Fruits: a developmental perspective. The Plant Cell 5, 1439–1451.
Goldschmidt EE, Koch KE. 1996. Citrus. In: Zamski E, Schaffer A, eds. Photoassimilate distribution in plant and crops. New York, Basel, Hong Kong: Dekker, 797–823.
Gomez-Cadenas A, Mehouachi J, Tadeo FR, Primo-Millo E, Talon M. 2000. Hormonal regulation of fruitlet abscission induced by carbohydrate shortage in citrus. Planta 210, 636–643.[CrossRef][Web of Science][Medline]
Gonzalez-Carranza ZH, Lozoya-Gloria E, Roberts JA. 1998. Recent developments in abscission: shedding light on the shedding process. Trends in Plant Science 3, 10–14.
Huppe HC, Turpin DH. 1994. Integration of carbon and nitrogen metabolism in plant and algal cells. Annual Review of Plant Physiology and Plant Molecular Biology 45, 577–607.[Web of Science]
Kakkar RK, Rai VK. 1993. Plant polyamines in flowering and fruit ripening, Phytochemistry 33, 1281–1288.[CrossRef]
Kotzabasis K, Fotinou C, Roubelakis-Angelakis KA, Ghanotakis D. 1993. Polyamines in the photosynthetic apparatus. Photosystem II highly resolved subcomplexes are enriched in spermine. Photosynthesis Research 38, 83–88.[CrossRef]
Kushad MM, Dumbroff EB. 1991. Metabolic and physiological relationships between the polyamine and ethylene biosynthetic pathways. In: Slocum RD, Flores HE, eds. The biochemistry and physiology of polyamines in plants. Boca Raton, FL: CRC Press, 78–89.
Larher F, Aziz A, Deleu C, Lemesle P, Ghaffar A, Bouchard F, Plasman M. 1998. Suppression of the osmoinduced proline response of rapeseed leaf discs by polyamines. Physiologia Plantarum 102, 139–147.[CrossRef]
Malmberg RL, McIndoo J. 1983. Abnormal floral development of a tobacco mutant with elevated polyamine levels. Nature 305, 623–625.[CrossRef][Web of Science]
Martin-Tanguy J. 1997. Conjugated polyamines and reproductive development: biochemical, molecular and physiological approaches. Physiologia Plantarum 100, 675–688.[CrossRef]
Mehouachi J, Serna D, Zaragoza S, Agusti M, Talon M, Primo-Millo E. 1995. Defoliation increases fruit abscission and reduces carbohydrate levels in developing fruits and woody tissues of Citrus unshiu. Plant Science 107, 189–197.[CrossRef]
Moss GI, Steer BT, Kriedemann PE. 1972. The regulatory role of inflorescence leaves in fruit-setting by sweet orange (Citrus sinensis). Physiologia Plantarum 27, 432–438.[CrossRef]
Mullins MG, Rajasekaran K. 1981. Fruiting cuttings: revised method for producing test plants of grapevine cultivars. American Journal of Enology and Viticulture 32, 35–40.
Osborne DJ. 1989. Abscission. Critical Review in Plant Science 8, 103–129.
Paschalidis KA, Aziz A, Geny L, Primikirios NI, Roubelakis-Angelakis KA. 2001. Polyamines in grapevine. In: Roubelakis-Angelakis KA, ed. Molecular biology and biotechnology of the grapevine. Dordrecht, The Netherlands: Kluwer Academic Publishers, 109–151.
Rastogi R, Davies PJ. 1991. Effects of light and plant growth regulators on polyamine metabolism in higher plants. In: Slocum RD, Flores HE, eds. Biochemistry and physiology of polyamines in plants. Boca Raton, FL: CRC Press, 187–199.
Roe JH. 1955. The determination of sugar in blood and spinal fluid with anthrone reagent. Journal of Biological Chemistry 212, 335–343.
Rosen H. 1957. A modified ninhydrin colorimetric analysis for amino acids. Archives of Biochemistry and Biophysics 67, 10–15.[CrossRef][Web of Science][Medline]
Ruperti B, Bonghi C, Tonutti P, Ramina A. 1998. Ethylene biosynthesis in peach fruitlet abscission. Plant, and Cell Environment 21, 731–737.[CrossRef]
Slocum RD, Galston AW. 1985. Changes in polyamine biosynthesis associated with post fertilization growth and development in tobacco ovary tissues. Plant Physiology 79, 336–343.
Tassoni A, Van Buuren M, Franceschetti M, Fornalès S, Bagni N. 2000. Polyamine content and metabolism in Arabidopsis thaliana and effect of spermidine on plant development. Plant Physiology and Biochemistry 38, 383–393.[CrossRef]
Taylor JE, Whitelaw CA. 2001. Signal abscission. New Phytologist 151, 323–339.[CrossRef][Web of Science]
Turano FJ, Kramer GF. 1993. Effect of metabolic intermediates on the accumulation of polyamines in detached soybean leaves. Phytochemistry 34, 959–968.[CrossRef]
Turano FJ, Kramer GF, Wang CY. 1997. The effect of methionine, ethylene and polyamine catabolic intermediates on polyamine accumulation in detached soybean leaves. Physiologia Plantarum 101, 510–518.[CrossRef]
Walden R, Cordeiro A, Tiburcio AF. 1997. Polyamines: small molecules triggering pathways in plant growth and development. Plant Physiology 113, 1009–1013.[CrossRef][Web of Science][Medline]
Yoshida I, Hirasawa E. 1998. Photoinduction of arginine decarboxylase activity in leaves of Pharbitis nil. Phytochemistry 49, 2255–2259.[CrossRef][Web of Science][Medline]
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  G. Lebon, G. Wojnarowiez, B. Holzapfel, F. Fontaine, N. Vaillant-Gaveau, and C. Clement Sugars and flowering in the grapevine (Vitis vinifera L.) J. Exp. Bot., July 1, 2008; 59(10): 2565 - 2578. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
I. El-Sharkawy, W. S. Kim, S. Jayasankar, A. M. Svircev, and D. C. W. Brown Differential regulation of four members of the ACC synthase gene family in plum J. Exp. Bot., May 1, 2008; 59(8): 2009 - 2027. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. Della Mea, F. De Filippis, V. Genovesi, D. Serafini Fracassini, and S. Del Duca The Acropetal Wave of Developmental Cell Death of Tobacco Corolla Is Preceded by Activation of Transglutaminase in Different Cell Compartments Plant Physiology, June 1, 2007; 144(2): 1211 - 1222. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. A. Paschalidis and K. A. Roubelakis-Angelakis Spatial and Temporal Distribution of Polyamine Levels and Polyamine Anabolism in Different Organs/Tissues of the Tobacco Plant. Correlations with Age, Cell Division/Expansion, and Differentiation Plant Physiology, May 1, 2005; 138(1): 142 - 152. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||