Involvement of polyamines in the drought resistance of rice
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1 Journal of Experimental Botany, Vol. 5, No., pp. 55, doi:1/jxb/erm2 Advance Access publication 1 March, RESEARCH PAPER Involvement of polyamines in the drought resistance of rice Jianchang Yang 1, Jianhua Zhang 2, *, Kai Liu 1, Zhiqin Wang 1 and Lijun Liu 1 1 Key Laboratory of Crop Genetics and Physiology of Jiangsu Province, Yangzhou University, Yangzhou, Jiangsu, China 2 Department of Biology, Hong Kong Baptist University, Hong Kong, China Received 1 December 2; Accepted 1 January Abstract This study investigated whether and how polyamines (PAs) in rice (Oryza sativa L.) plants are involved in drought resistance. Six rice cultivars differing in drought resistance were used and subjected to wellwatered and water-stressed treatments during their reproductive period. The activities of arginine decarboxylase, S-adenosyl-L-methionine decarboxylase, and spermidine (Spd) synthase in the leaves were significantly enhanced by water stress, in good agreement with the increase in putrescine (Put), Spd, and spermine (Spm) contents there. The increased contents of free Spd, free Spm, and insoluble-conjugated Put under water stress were significantly correlated with the yield maintenance ratio (the ratio of grain yield under waterstressed conditions to grain yield under well-watered conditions) of the cultivars. Free Put at an early stage of water stress positively, whereas at a later stage negatively, correlated with the yield maintenance ratio. No significant differences were observed in solubleconjugated PAs and insoluble-conjugated Spd and Spm among the cultivars. Free PAs showed significant accumulation when leaf water potentials reached 21 MPa to 2.2 MPa for the drought-resistant cultivars and 2.7 MPa to 2. MPa for the droughtsusceptible ones. The results suggest that rice has a large capacity to enhance PA biosynthesis in leaves in response to water stress. The role of PAs in plant defence to water stress varies with PA forms and stress stages. In adapting to drought it would be good for rice to have the physiological traits of higher levels of free Spd/free Spm and insoluble-conjugated Put, as well as early accumulation of free PAs, under water stress. Key words: Arginine decarboxylase (ADC), drought resistance, ornithine decarboxylase (ODC), polyamines, rice, S-adenosyl-L-methionine decarboxylase (SAMDC), spermidine synthase, water stress. Introduction Polyamines (PAs), spermidine (Spd), spermine (Spm), and their diamine obligate precursor putrescine (Put), have been frequently described as endogenous plant growth regulators or intracellular messengers mediating physiological responses (Galston, 1; Davies, 2). In higher plants, Put can be directly synthesized from ornithine via ornithine decarboxylase (ODC; EC 7) or indirectly from arginine via arginine decarboxylase (ADC; EC ) (Gemperlová et al., 2). Spd and Spm are synthesized via Spd synthase (EC 2.) and Spm synthase (EC 22), respectively, by sequential addition of aminopropyl groups to Put. This aminopropyl group is provided by decarboxylated S-adenosyl-L-methionine, which is a product of S-adenosyl-L-methionine decarboxylase (SAMDC; EC ) (Maiale et al., 2). Because of their polycationic nature at physiologically relevant ionic and ph conditions, PAs occur in cells not only in the free form but also in the soluble-conjugated and insoluble-conjugated forms (Martin-Tanguy, 21; Gemperlová et al., 2). Soluble-conjugated PAs are mostly linked to hydroxycinnamic acid monomers, and insoluble-conjugated PAs to hydroxycinnamic acid dimers and trimers, and to macromolecules such as proteins (Kasukabe et al., 2). PAs are implicated in many physiological processes such as cell division, morphogenesis, secondary Downloaded from at Pennsylvania State University on February, 21 * To whom correspondence should be addressed. jzhang@hkbu.edu.hk Abbreviations: ADC, arginine decarboxylase; DAWW, days after withholding water; ODC, ornithine decarboxylase; w leaf, leaf water potential; w soil, soil water potential; PA, polyamine; Put, putrescine; SAMDC, S-adenosyl-L-methionine decarboxylase; Spd, spermidine; Spm, spermine; WS, water-stressed; WW, well-watered; YMR, yield maintenance ratio. ª The Author []. Published by Oxford University Press [on behalf of the Society for Experimental Biology]. All rights reserved. For Permissions, please journals.permissions@oxfordjournals.org
2 Yang et al. metabolism, senescence, and apoptosis (Bouchereau et al., 1; Davies, 2; Kuehn and Phillips, 25). In recent years, attention has been focused on the role of PAs in plant defence against abiotic and biotic stresses (Galston, 21; Ma et al., 25; Liu et al., 2). A general phenomenon observed is that PAs can alter their titres in response to various types of environmental stresses such as low and high temperatures (Song et al., 22; Hummel et al., 2; Imai et al., 2), salinity (Maiale et al., 2; Roy et al., 25; Liu et al., 2), and water stress (Capell et al., 2; Kasukabe et al., 2; Ma et al., 25). As compared with stressintolerant plants, stress-tolerant plants generally have a large capacity to enhance PA biosynthesis in responses to stress, resulting in a 2- to -fold increase of endogenous PA levels over those in unstressed plants (Kasukabe et al., 2). Treatment with a PA biosynthetic enzyme inhibitor reduces stress tolerance but the concomitant treatment with exogenous PAs restores it (Lee et al., 17; He et al., 22; Liu et al., 2). However, there is a report that Put and Spd levels decrease, rather than increase, in salt-stressed rice (Oryza sativa L.) plants, and Spm accumulation induced by treatment with cyclohexylamine shows no reduction in leaf injury associated with the stress (Maiale et al., 2). Increases in Spd and Spm in wheat (Triticum aestivum) plants under water stress are observed to be associated with a reduction in drought tolerance (Zhang et al., ). So far, the physiological role of PAs in tolerance to environmental stress remains uncertain (Bais and Ravishankar, 22; Capell et al., 2; Ma et al., 25). Drought is the major abiotic stress factor limiting crop productivity worldwide (Saini and Westgate; 2; Sharp et al., 2). Rice as a paddy field crop is particularly susceptible to soil water deficit (Inthapan and Fukai, 1; Cabuslay et al., 22). Water stress during reproductive development can reduce grain yield by 5 % in different cultivars of rice, which display wide genotypic differences in susceptibility to water stress during this period (Garrity and O Toole, 1; Sheoran and Saini, ). Development and adoption of drought-resistant rice cultivars is believed to be important in coping with drought in the future (Fukai and Cooper, ; Cabuslay et al., 22; Condon et al., 2). In spite of numerous reports on phonological, morphological, physiological, biochemical, and molecular adaptive mechanisms, drought tolerance remains poorly understood, and the development of droughtresistant rice cultivars is relatively slow (Fukai and Cooper, ; Cabuslay et al., 22; Condon et al., 2). Recently, it was suggested that enhancement in crop drought resistance would be achieved through the manipulation of PA metabolism (Capell et al., 2). However, little is known about how PAs perform when rice is subjected to long-term drought stress during the reproductive period and whether such performances are correlated with drought resistance. The purpose of this study was to investigate the changes in contents of free PAs, soluble-conjugated PAs, and insoluble-conjugated PAs, and the activities of enzymes involved in PA biosynthesis in rice plants subjected to water stress during the reproductive period by using six cultivars differing in drought resistance, and to determine whether and how PAs are involved in drought resistance. Materials and methods Plant materials and growth conditions The experiment was conducted on a farm at Yangzhou University, Jiangsu Province, China (2 #N, 11 25#E) during the rice growing season (May October). Six rice (Oryza sativa L.) cultivars, Han-51,,, Han-A,, and were used. The first three are indica and last three are japonica. All the cultivars have a similar growth period ranging from 1 to 2 d from sowing to grain maturity but differ in drought resistance as shown in Table 1. The seeds were sown in a paddy field on 11 May. Seedlings ( d old) were then transplanted to porcelain pots. Each porcelain pot ( cm in height and 25 cm in diameter, 1.72 l in volume) was filled with 2 kg of sandy loam soil [Typic fluvaquents, Entisols (US taxonomy)] that contained organic matter at 2.% and available N, P, and K at 1,., and. mg kg 1, respectively. Each pot was planted with six seedlings. On the day of transplanting (1 11 June), 1 g of N as urea,. g of P as single superphosphate, and g of K as KCl were mixed into the soil in each pot. N as urea was also applied at mid-tillering ( g per pot) and panicle initiation (. g per pot) stages. All the cultivars headed on 2 25 August (5% of plants), flowered on 25 August, and were harvested on 1 October. The water level in the pot was kept at 1 2 cm until elongation of the flag leaf was complete when water stress treatments were initiated. The total precipitation during the growing season was 51. mm, 7% of which was in June and July. The mean solar radiation was 17. MJ m 2 d 1. Table 1. Grain yield and yield maintenance ratio of rice Plants were pot-grown, and well-watered (WW) and water-stressed (WS) treatments were conducted from complete elongation of the flag leaf to grain maturity (experiment 1). Values of grain yield were means of all plants harvested from 1 plots of each treatment at maturity. The yield maintenance ratio (YMR) was calculated as (grain yield under the WS treatment)/(grain yield under the WW treatment). Cultivars Grain yield (g pot 1 ) YMR WW WS Han * Han-A. *. 2 5.**.7 52.** ** 5.**. *, ** Significant differences from the WW at P¼ and P¼ levels, respectively, within the same cultivar. Downloaded from at Pennsylvania State University on February, 21
3 Water-stress treatments Experiment 1 The experiment was a 2 (six cultivars and two levels of soil moisture) factorial design with treatments. Each treatment had pots, of which 2 were used for destructive sampling during the experiment and 1 for the final harvest. From the complete elongation of the flag leaf (7 d before anthesis) till grain maturity, two levels of soil water potential (w soil ) were imposed by controlling water application. For the well-watered (WW) treatment the pot was flooded to a depth of 1 2 cm (w soil ¼ MPa) by manually applying tap water; for the water-stressed (WS) treatment w soil was maintained at MPa. The w soil in the WS treatment was monitored with tension meters (Soil Science Research Institute, Nanjing, China) buried at a depth of 2 cm in the soil. Tension meter readings were recorded every h from h to 1 h. When the readings dropped to the desired value, l of tap water per pot was added to the WS treatment. The pots were placed in a field and sheltered from rain by a removable polyethylene shelter during rain. Experiment 2 All plants of the six cultivars were pot-grown as described above. Each cultivar had pots. From the complete elongation of the flag leaf, half the plants were either well watered (w soil ¼ MPa) by manually applying tap water or water stressed by withholding water. The water-stressed plants were not watered until the flag leaf was seriously wilted [leaf water potential was 1. MPa to 1. MPa, d after withholding water (DAWW)]. Sampling and leaf water potential measurement In experiment 1, 2 flag leaves on main stems from each treatment were sampled at -d intervals from the beginning of withholding water to 2 DAWW. Half the sampled leaves was frozen in liquid nitrogen and subsequently stored at 7 C pending PA extraction and quantification. The other half of the sampled leaves was frozen in liquid nitrogen pending measurement of enzymatic activities. Plants in 1 pots of each treatment were harvested at maturity to determine grain yield. In experiment 2, 1 flag leaves on main stems from each treatment were sampled daily from 1 h to 11 h and from 1 h to h from the beginning of withholding water to when the flag leaf was seriously wilted. Half the sampled leaves were used for measuring PAs and the other half for measuring leaf water potential (w leaf ). A pressure chamber (model, Soil Moisture Equipment Corp., Santa Barbara, CA, USA) was used for w leaf measurement. Extraction and quantification of PAs Free PA fractions were estimated following the method of Flores and Galston (12), while the soluble-conjugated and insolubleconjugated fractions were analysed following the method described by Liu et al. (2) with modifications. Briefly, the sampled leaves (1 g) were homogenized with a pre-chilled mortar and pestle in ml of 5% (v/v) perchloric acid. The homogenates were incubated at 5 C for 1 h and then centrifuged at 25 g for 2 min. After centrifugation, the supernatant and pellet were collected separately. To extract soluble-conjugated PAs, aliquots (2 ml) of the supernatant were mixed with 2 ml of N HCl and heated at 11 C for 1 h in flame-sealed glass ampoules. After acid hydrolysis, HCl was evaporated from the tubes by further heating at C and the residues were resuspended in ml of 5% (v/v) perchloric acid. To extract insoluble-conjugated PAs, the pellet was rinsed four times with 5% perchloric acid to remove any trace of soluble PA and then dissolved by vigorous vortexing in 2 ml of 1 N NaOH. The mixture was centrifuged at 25 g for 2 min and the supernatant was hydrolysed under the same conditions mentioned above. PAs in the non-hydrolysed supernatant, hydrolysed supernatant, and hydrolysed pellet were derived with benzoyl chloride and were quantified by HPLC (Waters 25 Sparations Module; Waters, USA) as described by DiTomaso et al. (1). Ten microlitres of samples redissolved in methanol (%, v/v) were injected in to a fixed 2 ll loop for loading onto a. mm25 mm, 5 lm particle size reverse-phase (C 1 ) column (Waters). Samples were eluted from the column by a Perkin-Elmer Series 1 pump at 25 C with a flow rate of. ml min 1. PA peaks were detected by a Perkin-Elmer LC-5 with absorbance at 25 nm. Solubleconjugated PA contents were calculated by subtracting the free PAs in the non-hydrolysed supernatant from the PAs in the hydrolysed supernatant. 1,-Hexanediamine was used as an internal standard. The PA levels were the average of four replicates and expressed as nmol g 1 fresh weight. Determination of polyamine biosynthetic enzyme activity Sampled leaves (about. g fresh weight) were ground to a fine powder and homogenized with ml of extraction buffer (ph.) containing 25 mm potassium phosphate, 5 lm ethylenediaminetetraacetic acid, 1 lm phenylmethylsulfonyfluoride, 1 mm 2- mercaptoethanol, and 25 mm ascorbic acid. After centrifugation at 25 g at C for 2 min, the supernatant was dialysed overnight against the extraction buffer. The activities of ADC, ODC, and SAMDC were determined by measuring CO 2 evolution as described by Lee et al. (17). Spd synthase activity was assayed according to Kasukabe et al. (2). An aliquot of the supernatant was incubated at 7 C for min in a reaction mixture consisting of M TRIS-HCl (ph.), lm Put, 25 lm decarboxylated S- adenosyl-l-methionine, and 2 lm adenine. The reaction product (5#-deoxy-5#-methyl-thioadenosine) was quantified via HPLC (Waters 25 Sparations Module) equipped with a fluorescence detector (Waters 5 Multi k, USA) and a reverse phase (C 1 ) column (Waters). 1,7-Heptanediamine was used as the internal standard. Proteins in the extract were quantified as described by Bradford (17). Statistical analysis The results were analysed for variance using the SAS/STAT statistical analysis package (version., SAS Institute, Cary, NC, USA). Data from each sampling date were analysed separately. Means were tested by least significant difference at the P¼ level (LSD ). Linear regression was used to evaluate the relationship between PA contents in the flag leaf and drought resistance of the rice cultivars. Results Polyamines and drought resistance in rice 7 Grain yield and drought resistance The grain yield of all the cultivars was significantly reduced when the plants were subjected to long-term water stress (Table 1). The reduction was mainly attributed to the decrease in grain set and filling-grain percentage (data not shown). However, the effect of water stress on grain yield varied greatly with cultivars when they were compared with their respective controls (WW plants). Among the six cultivars, the two drought-resistant cultivars, Han- 51 and Han-A, were the least affected and therefore showed the highest YMR [(WS grain yield)/(ww grain yield) higher than.], whereas both drought-susceptible cultivars, and, were the most affected and exhibited the lowest YMR (lower than ), Downloaded from at Pennsylvania State University on February, 21
4 Yang et al. and the two cultivars with medium resistance to drought, and, were intermediate and their YMR was higher than. (Table 1). Changes in enzymatic activities Figure 1 illustrates the changes in activities of ADC, ODC, SAMDC, and Spd synthase in the flag leaf during the water-stress treatment. When plants were well watered, activities of all the enzymes decreased gradually with the ageing of the leaves, and showed no significant differences among the six cultivars (Fig. 1). Water stress significantly enhanced the activities of SAMDC and Spd synthase. The enhancement was greatest for drought-resistant cultivars, lowest for drought-susceptible ones, and intermediate for cultivars with medium resistance to drought (Fig. 1m x). ADC activity was also enhanced by water stress (Fig. 1a f). It was enhanced much more in drought-resistant cultivars than in drought-susceptible ones during the first DAWW, whereas the latter showed higher ADC activity than the former at 2 DAWW and 2 DAWW. ODC activity in the flag leaves was much lower when compared with any of the other three enzymes. There were no significant differences in the enzyme activity between WW and WS plants (Fig. 1g l). Activity of arginine decarboxylase (nmol mg -1 protein h -1 ) Well-watered a b c d e Han-51 Han-A Water-stressed Activity of ornithine decarboxylase (nmol mg -1 protein h -1 ) Han-51 Han-51 Han-51 2 Han-A Han-A Han-A... Activity of S-adenosyl-L-methionine decarboxylase (nmol mg -1 protein h -1 )... g h i j k m n o p q Spermidine synthase activity (nmol mg -1 protein h -1 ) s t u v w Downloaded from at Pennsylvania State University on February, 21 f l 2 r x Fig. 1. Changes in activities of arginine decarboxylase (a f), ornithine decarboxylase (g l), S-adenosyl-L-methionine decarboxylase (m r), and spermidine synthase (s x) in the flag leaves of rice under well-watered (filled circles) and water-stressed (open circles) treatments. The water-stressed treatment was conducted from complete elongation of the flag leaf till grain maturity (experiment 1). Vertical bars represent standard error of the mean (n¼) where these exceed the size of the symbol.
5 Polyamines and drought resistance in rice Changes in polyamine contents Very similar to the changes in activities of the enzymes, contents of free PAs (free Put, free Spd, and free Spm) slowly decreased with the ageing of the flag leaves and showed no significant differences among the cultivars when plants were well watered (Fig. 2). The content of free PAs in WS leaves increased and exhibited one peak for each cultivar. The peak values and time of appearance varied greatly with cultivar. At an early water stress stage ( DAWW), drought-resistant cultivars showed the highest peak of free Put accumulation, drought-susceptible ones had the smallest peak, and the cultivars with medium resistance to drought were intermediate. However, droughtsusceptible cultivars exhibited the highest peak of free Put at a later water stress stage (2 2 DAWW) (Fig. 2a f). During the whole period of withholding water, droughtresistant cultivars had more free Spd and free Spm in the leaves than drought-susceptible ones (Fig. 2g r). Changes in free PAs were consistent with those in activities of ADC, SAMDC, and Spd synthase under water stress (Fig. 1). Free-putrescine content (nmol g -1 FW) a b c d e f Han-51 Han-A Well-watered Water-stressed 2 2 Free-spermidine content (nmol g -1 FW) g h i j k l Han-51 Han-A 2 2 Free-spermine content (nmol g -1 FW) m n o p q r Han-51 Han-A 2 2 Downloaded from at Pennsylvania State University on February, 21 Fig. 2. Changes in contents of free putrescine (a f), free spermidine (g l), and free spermine (m r) in the flag leaves of rice under well-watered (filled circles) and water-stressed (open circles) treatments. The water-stressed treatment was conducted from complete elongation of the flag leaf till grain maturity (experiment 1). Vertical bars represent standard error of the mean (n¼) where these exceed the size of the symbol.
6 5 Yang et al. Changes in soluble-conjugated PA contents in the flag leaf were similar to those in free PAs (Fig. ). The WS treatment significantly increased soluble-conjugated PA levels. However, there were no significant differences among the cultivars in either Put, Spd, or Spm in the soluble-conjugated form when w soil was the same (Fig. ), indicating that soluble-conjugated PAs in rice plants may play a minor role defending against drought. The WS treatment significantly enhanced insolubleconjugated PA levels in the flag leaf (Fig. ). Droughtresistant cultivars accumulated more insoluble-conjugated Put than drought-susceptible cultivars (Fig. a f), but the differences in either insoluble-conjugated Spd or insoluble-conjugated Spm were insignificant among the cultivars when w soil was the same (Fig. g r). Regression analysis demonstrated that the relative content [(PAs under WS)/(PAs under WW)] of free Put 5 a 25 2 g m Soluble-conjugated putrescine content (nmol g -1 FW) b c d e f Han-51 Han-A Well-watered Water-stressed Soluble-conjugated spermidine content (nmol g -1 FW) h i j k l Han-51 Han-A Soluble-conjugated spermine content (nmol g -1 FW) n o p q r Han-51 Han-A Downloaded from at Pennsylvania State University on February, Fig.. Changes in contents of soluble-conjugated putrescine (a f), soluble-conjugated spermidine (g l), and soluble-conjugated spermine (m r) in the flag leaves of rice under well-watered (filled circles) and water-stressed (open circles) treatments. The water-stressed treatment was conducted from complete elongation of the flag leaf till grain maturity (experiment 1). Vertical bars represent standard error of the mean (n¼) where these exceed the size of the symbol.
7 Polyamines and drought resistance in rice 51 a 2 g m 2 2 Han-51 Han-51 Han-51 b 2 2 h n Insoluble-conjugated putrescine content (nmol g -1 FW) c d e f Han-A Well-watered Water-stressed 2 2 Insoluble-conjugated spermidine content (nmol g -1 FW) i j k l Han-A 2 2 Insoluble-conjugated spermine content (nmol g -1 FW) o p q r Han-A 2 2 Downloaded from at Pennsylvania State University on February, 21 Fig.. Changes in contents of insoluble-conjugated putrescine (a f), insoluble-conjugated spermidine (g l), and insoluble-conjugated spermine (m r) in the flag leaves of rice under well-watered (filled circles) and water-stressed (open circles) treatments. The water-stressed treatment was conducted from complete elongation of the flag leaf till grain maturity (experiment 1). Vertical bars represent standard error of the mean (n¼) where these exceed the size of the symbol. at DAWW and free Spd, free Spm, and insolubleconjugated Put during the whole period of withholding water were significantly or very significantly correlated with the YMR of cultivars (r¼.* to.**, P < and, respectively). A negative correlation was observed between the YMR and the relative content of free Put at 2 DAWW and 2 DAWW (r¼ * to.**, P < and, respectively). The correlation coefficients of the YMR with soluble-conjugated PAs (Put, Spd, and Spm) and higher insoluble-conjugated PAs (Spd and Spm) were insignificant (Table 2). As shown in Figs 2, the leaf contained 1- to 2-fold more free PAs than insoluble-conjugated PAs or solubleconjugated PAs when the comparison was made within
8 52 Yang et al. Table 2. Correlations of the relative contents of polyamines in the flag leaf with the yield maintenance ratio of rice Plants were pot-grown, and well-watered (WW) and water-stressed (WS) treatments were conducted from complete elongation of the flag leaf to grain maturity (experiment 1). Data are from Figs 2 and Table 1. The relative contents of polyamines were calculated as (contents under the WS treatment)/(the content under the WW treatment). Polyamines 2 2 Free polyamines Putrescine.7** *.** Spermidine.**.*.7**.** Spermine.**.** **.** Soluble-conjugated polyamines Putrescine. 1. Spermidine..7 Spermine.7. Insoluble-conjugated polyamines Putrescine **.*.**.** Spermidine..2 Spermine *, ** Correlation significance at P¼ and P¼ levels, respectively (n¼). the same cultivar and within the same soil moisture treatment, indicating that most PAs in rice leaves are in the free form. Leaf water potentials for free PA accumulation In experiment 2, the w leaf thresholds for significant accumulation of free PAs were measured to determine further the relationship between PAs in response to water stress and drought resistance. As shown in Fig. 5, the w leaf thresholds were very different among the cultivars. The thresholds for the accumulation of free Put, free Spd, and free Spm were 1 to, to, and. to.2 MPa, respectively, for the drought-resistant cultivars, and.7 to.72,.7 to, and to. MPa, respectively, for drought-susceptible cultivars. The cultivars with medium resistance to drought had thresholds between the above two types of cultivars (Fig. 5), indicating that drought-resistant cultivars accumulate free PAs earlier than drought-susceptible ones under water stress. Figure 5 also shows that drought-resistant cultivars had a greater ratio of free Put to free Spd or to free Spm (Put/ Spd and Put/Spm) than drought-susceptible ones when w leaf was greater than 1. MPa, whereas the result was reversed when the w leaf was less than that value (Fig. 5). These results were very similar to those obtained from experiment 1 although the treatment conditions were different between the experiments. Discussion The results of the present study showed that rice has a large capacity to enhance PA biosynthesis in leaves in response to water stress during the reproductive period. The increase in Put or Spd/Spm titres, especially in the free form, was in agreement with the enhancement in activities of ADC or SAMDC and Spd synthase in the stressed leaves, whereas the ODC activity remained essentially unchanged (Fig. 1). These results suggest that Put synthesis is primarily the result of increased ADC activity, rather than ODC activity, in the water-stressed rice plant. The rise of ADC activity in concert with the enhanced activity of SAMDC and Spd synthase may have contributed to the significant increase in the free and conjugated Spd and Spm contents under water stress. It was observed that the increase in PA biosynthesis was closely associated with drought resistance in rice (Table 1; Figs 1, 2,, and 5). Drought-resistant cultivars had higher SAMDC and Spd synthase activities and accumulated more free Spd and free Spm in the leaves than droughtsusceptible ones under water stress (Figs 1, 2, and 5). The relative contents of free Spd and free Spm [(contents under the WS)/(contents under the WW)] were significantly correlated with the YMR of the cultivars (Table 2), implying that both free Spd and free Spm are involved in rice tolerance to drought. The mechanism by which free Spd and free Spm enhance plant drought tolerance is not clear. It is generally believed that higher PAs (Spd and Spm) can bind strongly to the negative charges in cellular components such as nucleic acids, proteins, and phospholipids, and thereby stabilize the membranes under stress conditions (Smith, ; Szegletes et al., 2; Kasukabe et al., 2; Ma et al., 25). PAs have been observed to be correlated with activities of antioxidant enzymes such as superoxide dismutase, catalase, and peroxidase, and to act as freeradical scavengers and control many aspects of RNA and protein turnover (Tiburcio et al., 1; Bouchereau et al., 1; Liu et al., 2). Recently it was observed that overexpression of Spd synthase enhances tolerance to multiple environmental stresses and up-regulates the expression of various stress-regulated genes in transgenic Arabidopsis thaliana (Kasukabe et al., 2). Modulation of the polyamine biosynthetic pathway in transgenic rice confers tolerance of drought stress (Capell et al., 2). Thus it is conceivable that the reactive oxygen speciesscavenging, membrane-protecting, and gene expressionpromoting properties of Spd and Spm account, at least in part, for water stress tolerance in rice. Although the phenomenon that Put accumulates in plants under abiotic stress has been observed for more than 5 years, the physiological role of Put in abiotic stress responses remains a matter of controversy (Bouchereau et al., 1; Chen and Zhang, 2; Capell et al., 2; Kuehn and Phillips, 25). The results presented here demonstrate that the changes in ADC activity and Put levels under drought stress and their relationship with drought resistance of rice cultivars varied greatly with the Downloaded from at Pennsylvania State University on February, 21
9 Polyamines and drought resistance in rice 5 Relative content of free-polyamines (%) duration or severity of the stress (Figs 1, 2, and 5). At an early stage in water stress or under a situation of moderate stress (w leaf >1. MPa), the drought-resistant cultivars accumulated more free Put in leaves than the droughtsusceptible ones, whereas the latter showed a higher peak value than the former when plants were subjected to longterm drought stress or to serious stress (w leaf <1. MPa). The YMR of the cultivars was significantly correlated with free Put content at an early stage of water stress ( DAWW) but negatively correlated with free Put contents at a later stage (2 DAWW and 2 DAWW) (Table 2). The results suggest that, under drought conditions, drought-resistant rice cultivars are able to accumulate free Put earlier in the leaves, with faster declines and smaller peak values. Little is known about how the temporal profile of early accumulation, a fast decline, and a smaller peak of free Put in rice leaves performs the compatibility activity during drought stress. Capell et al. (2) observed, by using transgenic rice plants expressing the Datura stramonium adc gene, that transgenic plants produced a c e Han-51 Leaf water potential (-MPa) Putrescine Spermidine Spermine Han-A b d f Leaf water potential (-MPa) Fig. 5. Relative contents of free putrescine (filled circles), free spermidine (filled squares), and free spermine (filled triangles) in the flag leaves of rice at different leaf water potentials. The relative content of polyamines was calculated as the content in water-stressed leaves as a percentage of that in well-watered leaves. The water-stressed plants were not watered from complete elongation of the flag leaf until the flag leaf was seriously wilted (experiment 2). Vertical bars represent standard error of the mean (n¼) where these exceed the size of the symbol. much higher levels of Put (free form) under stress, promoting Spd and Spm synthesis and, ultimately, protecting the plants from drought. In contrast, an increase in Put in wild-type plants in response to the onset of drought was insufficient to trigger the conversion of Put to Spd and Spm. Their results suggest that a high level of Put at an early stage of drought is necessary for plants to adapt to stress by triggering the conversion of Put to the higher PAs. On the other hand, mass accumulation of Put, which extends beyond its involvement as a single precursor for the higher PAs along the pathway, can be toxic to plants by catalysing the formation of oxidation products (DiTomaso et al., 1; Watson and Malmberg, ; Richard and Alexandra, 17). It was observed that the drought resistance of rice cultivars was not only associated with PA (Put, Spd, and Spm) levels, but was also associated with the response time at which PAs are significantly elevated under water stress (Fig. 5). The drought-resistant cultivars had a higher w leaf threshold for obvious free PA accumulation than the drought-susceptible ones, suggesting that Downloaded from at Pennsylvania State University on February, 21
10 5 Yang et al. drought-resistant cultivars have the ability to respond early to water stress through increases in PA levels. It is proposed that an early response to stress signals would help plants to adapt to stress and prevent them from being seriously damaged (Nilsen and Orcutt, ; Chen and Zhang, 2). It can therefore be speculated that early accumulation of PAs or a higher w leaf threshold of PA elevation may be useful physiological traits of rice in adaptation to water stress. The results presented in Fig. also showed that water stress obviously induced the increases of three insolubleconjugated PAs in the flag leaf. However, only the insolubleconjugated Put levels in WS leaves exhibited significant differences among the cultivars and significantly correlated with the YMR (Table 2), suggesting that insolubleconjugated Put, but neither insoluble-conjugated Spd nor insoluble-conjugated Spm, would be involved in drought tolerance. An explanation for the mechanism by which insoluble-conjugated Put plays a role in drought resistance may be that the conversion of free Put to insolubleconjugated Put could alleviate the wounding effect of free Put on membranes of plant cells (DiTomaso et al., 1) and stabilize the configuration and function of proteins by preventing the proteins from denaturing under stress (Serafini-Fracassini, ). In conclusion, the present results demonstrate that increased PA levels are closely associated with the enhanced activities of ADC, SAMDC, and Spd synthase in water-stressed rice leaves. Contents of free Spd and free Spm in the leaves are correlated with the drought resistance of the cultivars. A high level of free Put at an early stress stage and insoluble-conjugated Put during the whole stress period helps the plant to adapt to stress. Both soluble-conjugated PAs (Put, Spd, and Spm) and higher insoluble-conjugated PAs (Spd and Spm) play a minor role in the defence against drought. Higher levels of free Spd/free Spm and insoluble-conjugated Put and early accumulation of PAs under water stress are useful physiological traits of rice in adaptation to drought. Acknowledgements We are grateful for grants from the National Natural Science Foundation of China (Project No. 725), the Research Grant Council of Hong Kong (HKBU 21/M, HKBU 25/5M), and the University Grants Committee of Hong Kong (AOE/B-7/). References Bais HP, Ravishankar GA. 22. Role of polyamines in the ontogeny of plants and their biotechnological applications. Plant Cell Tissue and Organ Culture, 1. Bouchereau A, Aziz A, Larther F, Martin-Tanguy J. 1. Polyamines and environmental challenges: recent development. Plant Science 1, 1 5. Bradford MM. 17. A rapid and sensitive method for quantification of microquantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, Cabuslay GS, Ito O, Alejar AA. 22. 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