Investigations of some intertidal green macroalgae to hyposaline stress: Detrimental role of putrescine under extreme hyposaline conditions
Introduction
Polyamines have been implicated in the regulation of plant growth and development [1]. In plants, putrescine is synthesized from arginine or ornithine through arginine decarboxylase (ADC; EC 4.1.1.19) or ornithine decarboxylase (ODC; EC 4.1.1.17), and is then converted to spermidine/spermine by the addition of propylamine groups from decarboxylated S-adenosylmethionine that is derived from S-adenosylmethionine (SAM) by the action of S-adenosylmethionine decarboxylase (SAMDC; EC 4.1.1.50) [2]. Under stresses, polyamines accumulate as a consequence of plant responses 1, 2.
Although effects of salinity on polyamine metabolism have been studied in several plant systems 3, 4, 5, 6, 7, 8, the change of polyamine pattern seems to depend on the system and duration of exposure to salinity stress. In Vicia faba [6]or barley [7], no accumulation of putrescine or spermidine could be found under hypersalinity. In contrast, the short-term exposure of Brassica campestris to hypersaline conditions leads to an increase of levels of polyamines and activities of both ADC and ODC, while long-term exposure had less effects [8]. Krishnamurthy and Bhagwat [4]showed that hypersaline stress elicited an accumulation of putrescine in salt-sensitive rice cultivars, but spermidine and spermine accumulated in salt-tolerant ones. A contrasting result from Lin and Kao (1995) [5]showed that increasing NaCl leads to a decrease in free putrescine levels but an increase in spermidine levels in a salt-sensitive rice cultivar, cv. Taichung Native 1.
Polyamines are present in prokaryotic and eukaryotic algae 9, 10, 11, 12, 13, 14. Uncommon polyamines (norspermidine and norspermine) are also widespread in eukaryotic algae [12]. They play a vital role in cell growth and development. In Chlorella vulgaris Beijernck var vulgaris fa vulgaris [13]or Euglena gracilis Z [14], a rise of polyamines, especially putrescine and spermidine, before cell division is suggested to be associated with DNA replication and this putrescine increase is derived from ODC. Changes in environmental factors also influence the biosynthesis of polyamines in algae. High light intensity enhances polyamine biosynthesis in Chlorella [13]. When exposed to mercury, both putrescine and 1,3-diaminopropane increased but spermidine, spermine and norspermidine decreased in a green alga, Chlorogonium elongatum (Dang) France [15]. A rise of culture temperature causes an increase of spermine and/or norspermine in Cyanidium caldarium, a unicellular thermoacidophilic red alga [11].
Since salinity fluctuates in intertidal regions, marine macroalgae from intertidal habitats have a well-developed ability to resist salinity change 16, 17, and their physiological and biochemical responses to altered salinity have been extensively studied 17, 18. As we know, the responses of polyamine biosynthesis to salinity stress have been not well studied in macroalgae. Recently, we found that free putrescine and spermidine in Ulva fasciata Delile, an intertidal green macroalga, accumulated under 5‰ and accumulated putrescine might be correlated with hyposaline injury [19]. This study was conducted to investigate the changes of polyamine (free, soluble conjugated and insoluble conjugated forms) levels to extreme hyposaline conditions (5‰) in some green macroalgae inhabiting intertidal regions of southern Taiwan, which are Ulva fasciata Delile, Ulva reticulata Foreek., Ulva lactuca L., Valoniopsis pachynema (Mart.) Boergs., Chaetomorpha crassa, Chlorodesmis formosana Yam. and Boodlea composita (Harv.) Brand. Both specific growth rate and chlorophyll levels were used to evaluate the tolerance of algae to 5‰. To investigate whether putrescine is correlated with hyposaline injury, α-difluoromethylarginine (DFMA, 0.2 mM) or α-difluoromethylornithine (DFMO, 0.2 mM), the specific inhibitors of ADC and ODC, respectively, were applied together with or without 0.5 mM putrescine in axenically cultured U. fasciata to inhibit the 5‰-induced putrescine accumulation, and both specific growth rate and chlorophyll levels were determined. Changes of both specific growth rate and chlorophyll levels in response to exogenously applied polyamines were examined in axenically cultured U. fasciata grown at 30‰.
Section snippets
Plant materials and treatments
Green macroalgae, Ulva fasciata Delile, Ulva reticulata Foreek., Ulva lactuca L., Valoniopsis pachynema (Mart.) Boergs., Chaetomorpha crassa, Chlorodesmis caespitosa L. Agardh and Boodlea composita (Harv.) Brand (Chlorophyta) were collected on 5th March 1997 from the intertidal regions at Wanliton, Kenting, Pinton, Taiwan, ROC. After extensive washing with autoclaved artificial seawater (500 mM NaCl, 10 mM KCl, 30 mM MgSO4, 10 mM CaCl2 and 10 mM Tris–HCl, pH 7.8), thallus with fresh weight
Specific growth rate and chlorophyll levels
Specific growth rate was compared among algae to evaluate the tolerance to 5‰. As shown in Fig. 1A, 5‰ inhibited the growth of all algae but the specific growth rate was less inhibited in C. caespitosa and in C. crassa, the specific growth rate was close to zero.
Compared with complete bleaching in other algae, C. caespitosa appeared green even 4 days of exposure to 5‰ and C. crassa was only slightly bleached. Changes of total chlorophyll levels in response to 5‰ agreed with appearance changes.
Discussion
Polyamines including putrescine, spermidine and spermine are present in intertidal green macroalgae used in this study, which are rich in putrescine and spermidine. This coincides with the results of Hamana and Matsuzaki [12]that putrescine and spermidine are abundant in eukaryotic algae while spermine is only found in several algae at trace levels. Badini et al. [9]also found that putrescine, spermidine and spermine exist in Ulva rigida with putrescine being the most abundant.
Polyamine
Acknowledgements
The author thanks Dr P.P. McCann (Merrill-Dow Research Center, Cincinnati, OH) for providing DFMA and DFMO. This paper is based upon work supported by the National Science Council, Executive Yuan, Taiwan, ROC, under Grant No. NSC 86-2611-B-110-009, and the Research Affair Department, National Sun Yat-sen University, Kaohsiung, Taiwan, ROC.
References (21)
- et al.
Effect of NaCl on the levels of putrescine and related polyamines in plants differing in salt tolerance
Plant Sci. Lett.
(1978) Amine levels in mineral deficient Hordeum vulgaris leaves
Phytochemistry
(1973)- et al.
Effects of salt stress on polyamine metabolism in Brassica campestris
Phytochemistry
(1995) - et al.
Occurrence of sym-homospermidine as the major polyamine in nitrogen-fixing cyanobacteria
Biochem. Biophys. Res. Commun.
(1983) - et al.
Polyamines of unicellular thermoacidophilic red alga Cyanidium caldarium
Phytochemistry
(1990) - et al.
Biosynthesis of polyamines in Euglena gracilis
Phytochemistry
(1980) - et al.
Changes in polyamine and glutathione contents of a green alga, Chlorogonium elongatum (Dang) France exposed to mercury
Environ. Exp. Bot.
(1992) - et al.
Spectrophotometric characteristics of chlorophylls a and b and their phaeophytins in ethanol
Biochim. Biophys. Acta
(1965) - A.W. Galston, R. Kaur-Sawhney, Polyamines as endogenous growth regulator, in: P.J. Davies (Ed.), Plant Hormones and...
- et al.
Do polyamines have roles in plant development?
Annu. Rev. Plant Physiol. Plant Mol. Biol.
(1989)
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