Abstract
We studied salt stress-induced biochemical changes in young, hydroponically grown plants of mangrove,Bruguiera parviflora (Rhizophoraceae). Our focus was on the effect of NaCI (applied at 100, 200, 400, or 500 mM) on leaf pigments, total soluble proteins, total free amino acids, carbohydrates, polyphenols, and proline. The total Chi content increased for 14 d after treatment with 100 mM NaCI, then gradually stabilized. At 400 mM, the total Chi content slowly decreased over the 45-d test period. However, the Chia:b ratio remained unchanged in isolated chloroplasts and in leaf tissue. Percent changes in the carotenoids content followed the same trend as for Chi, except for a 1.5-fold decrease during the 400-mM NaCI treatment, compared with the control. The total sugar content increased by 2.5-fold by Day 45 after treatment with 400 mM NaCI, whereas the starch content measured in the same treatment decreased by 40 to 45%. Leaf protein content decreased as salinity increased, which suggests either a possible disruption in the protein synthesis mechanism or, more likely, an increase in proteolytic activity. The total amino-acid pool increased steadily, by four-fold, in the 45-d, 400-mM treatment Both proline and polyphenols accumulated with increasing levels of salinity, which confirms the role of proline as a stress-induced protective metabolite in the adaptive process of this species. Our results showed that a true mangrove such as 8.parviflora can easily be sustained and propagated under low-salinity conditions. At high levels of salinity (~400 mM, beyond which they could not survive), the plants became adapted to salt stress after two to three weeks. During this adaptive period, changes in pigment and protein levels also occurred. The accumulation of proline and polyphenols played a key role in the plant’s stressinduced adjustment to NaCI under hydroponic culture conditions.
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Aarrouf J, Darbelley N, Demandre C, Razafindramboa N, Perbal G (1999) Effect of horizontal clinorotation on the root system and on lipid breakdown in rapeseed (Brassica napus) seedlings. Plant Cell Physiol40: 396–405
AbElBaki GK, Siefritz F, Man HM, Welner H, Kaldenhoff R, Kaiser WM (2000) Nitrate reductase inZea mays L. under salinity. Plant Cell Environ23: 515–521
Agastian P, Kingsley SJ, Vivekanandan M (2000) Effect of salinity on photosynthesis and biochemical characteristics in mulberry genotypes. Photosynthetica38: 287–290
Alia, Paradhasaradhi P, Mohanty P (1997) Involvement of proline in protecting thylakoids against free radical induced photodamage. J Photochem Photobiol38: 253–257
Alia, Saradhi PP (1993) Suppression of mitochondrial electron transport activity is the prime cause behind stress induced proline accumulation. Biochem Biophys Res Commun403: 54–58
Allakhverdiev SI, Sakamoto A, Nishiyama Y, Inaba M, Murata N (2000) Ionic and osmotic effects of NaCI-induced inactivation of photosystems I and II inSynechococcus sp. Plant Physiol123: 1047–1056
Arnon Dl (1949) Copper enzymes in isolated chloroplasts, polyphenol oxidase inBeta vulgaris. Plant Physiol24: 1–15
Ashihara H, Adachi K, Otawa M, Yasumoto E, Fukushima Y, Kato M, Sano H, Sasamoto H, Baba S (1997) Compatible solutes and inorganic ions in the mangrove plantAvicennia marina and their effects on the activities of enzymes. Z Naturforsh52c: 433–440
Aubert S, Hennion F, Bouchereau A, Gout E, Blingy R, Dome AJ (1999) Subcellular compartmentation of proline in the leaves of the sub-antarctic Kerguelen cabbagePringlea antiscorbutica R-Br.In vivo C-13 NMR study. Plant Cell Environ22: 255–259
Aziz A, Martin TJ, Larther F (1999) Salt stress-induced proline accumulation and changes in tyramine and polyamine levels are linked to ionic adjustment in tomato leaf discs. Plant Sci145: 83–91
Ball MC, Farquhar GD (1984) Photosynthetic and stomatal responses of two mangrove species,Avicennia marina andAegiceras corniculatum, to long term salinity and humidity conditions. Plant Physiol74: 1–6
Banijbatana D (1957) Mangrove forest in Thailand,In Proceedings of the 9th Pacific Science Congress, Bangkok, pp 22–34
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil39: 205–207
Chandler SF, Dodds JH (1983) The effect of phosphate, nitrogen and sucrose in the production of phenolics and solasidine in callus cultures ofSolanum laciniatum. Plant Cell Rep2: 105–108
Damerval C, Vienne P, Zivy M, Thiellement H (1986) Technical improvement in two-dimensional electrophoresis increase the level of genetic variation detected in wheat seedling proteins. Electrophoresis7: 52–54
Das P, Basak UC, Das AB (1997) Restoration of mangrove vegetation in mahanadi delta of Orissa, India. Mangroves and Saltmarshes1: 155–161
DionisioSese ML, Tobita S (2000) Effects of salinity on sodium content and photosynthetic responses of rice seedlings differing in salt tolerance. J Plant Physiol157: 54–58
Dubey RS, Singh AK (1999) Salinity induces accumulation of soluble sugars and alters the activity of sugar metabolizing enzymes in rice plants. Biol Plant42: 233–239
Dubinsky Z, Stambler N (1996) Eutrophication, marine pollution and coral reef. Glob Change Biol2: 511–526
Gadallah MAA (1999) Effects of proline and glycinebetaine onVicia faba response to salt stress. Biol Plant42: 249–257
Gilbert GA, Gadush MV, Wilson C, Madore MA (1998) Amino acid accumulation in sink and source tissues ofColeus blumei Benth. during salinity stress. J Exp Bot49: 107–114
Hassanein AM (1999) Alterations in protein and esterase patterns of peanut in response to salinity stress. Biol Plant42: 241–248
Hernandez S, Deleu C, Larher F (2000) Proline accumulation by leaf tissues of tomato plants in response to salinity. Comptes Rendus de L Academie Des Sciences Seric III, Sciences de La Vie, Life Sci323: 551–557
Hoagland DR, Arnon Dl (1940) Crop production in artificial solutions and in soil with special reference to factors influencing yields and absorption of inorganic nutrients. Soil Sci50: 463
Hotta M, Nemoto S, Mimura T (2000) Re-evaluation of role of vacuole during salt adaptation in higher plant cells. Plant Cell Physiol41: 79
lyengar ERR, Reddy MP (1996) Photosynthesis in high salttolerant plants,In M Pesserkali, ed, Hand book of Photosynthesis, Marshal Dekker, Baton Rouge, LA, USA, pp 56–65
Kennedy BF, De Fillippis LF (1999) Physiological and oxidative response to NaCI of the salt tolerantGrevillea ilicifolia and the salt sensitiveGrevillea arenaria. J Plant Physiol155: 746–754
Kerepesi I, Galiba G (2000) Osmotic and salt stressinduced alteration in soluble carbohydrate content in wheat seedlings. Crop Sci40: 482–487
Kumar N, Sharma PN (1995) Effect of phosphorous deficiency stress on photosynthesis in mulberryMorus alba L. Ind J Exp Biol33: 616–619
Lee TM, Liu CH (1999) Correlation of decreases in calcium contents with proline accumulation in the marine green macroalgaUlva fasciata exposed to elevated NaCI contents in seawater. J Exp Bot50: 1855–1862
Liu CH, Shih MC, Lee TM (2000) Free proline levels inUlva (Chlorophyta) in response to hypersalinity: Elevated NaCI in seawater versus concentrated seawater. J Phycol36: 118–119
Lovelock C, Clough BF, Woodrow E (1992) Distribution and accumulation of ultraviolet-radiation-absorbing compounds in leaves of tropical mangroves. Planta188: 143–154
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin Phenol reagent. J Biol Chem193: 265–275
McCready RM, Guggolz J, Silviera V, Owens HS (1950) Determination of starch and amylose in vegetables. Anal Chem22: 1156–1158
Moore S, Stein WH (1948) Photometric ninhydrin method for use in chromatography of amino acids. J Biol Chem176: 367–388
Moorthy P, Kathiresan K (1999) Photosynthetic efficiency in Rhizophoracean mangroves with reference to compartmentalization of photosynthetic pigments. Revista Biol Trop47: 21–25
Muthukumarasamy M, Gupta SD, Pannerselvam R (2000) Enhancement of peroxidase, polyphenol oxidase and Superoxide dismutage activities by triadimefon in NaCI stressedRaphanus satrvus L. Biol Plant43: 317–320
Nelson N (1944) A photometric adaptation of the Somogyi method for the determination of glucose. J Biol Chem153: 375–380
Papageorgiou GC, Murata N (1995) The unusually strong stabilizing effect of glycinebetaine on the structure and function of oxygen evolving photosystem II complex. Photosyn Res44: 243–252
Popp M, Larther F, Weigel P (1985) Osmotic adaptation in Australian mangroves. Vegetatio61: 247–254
Porra RJ, Thompson, WA, Kriendemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophyll a and b extracted with four different solvents: Verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochem Biophys Acta975: 384–394
Prado FE, Boero C, Gallardo M, Gonzalez JA (2000) Effect of NaCI on germination, growth and soluble sugar content inChenopodium quinoa Willd. Seeds Bot Bull Acad Sinica41: 27–34
Santiago LS, Lau TS, Melcher PJ, Steele OC, Goldstein G (2000) Morphological and physiological responses of HawaiianHibiscus tiliaceus population to light and salinity. Intl J Plant Sci161: 99–106
Singleton VL, Rossi JA (1965) Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid. Am J Enal Vitric163: 144–158
Somogyi M (1945) A new reagent for determination of sugars. J Biol Chem160: 61–68
Sugihara K, Hanagata, N, Dubinsky Z, Baba S, Karube J (2000) Molecular characterization of cDNA encoding oxygen evolving enhancer protein 1 increased by salt treatment in the mangroveBruguiera gymnorrhiza. Plant Cell Physiol41: 1279–1285
Takemura T, Hanagata N, Sugihara K, Baba S, Karube I, Dubinsky Z (2000) Physiological and biochemical responses to salt stress in the mangrove,Bruguiera gymnorrhiza. Aquat Bot68: 15–28
Tanaka Y, Fukuda A, Nakamura A, Yamada A, Saito T (2000) Molecular cloning and characterization of mangrove Na+/H+ antiporter cDNA. Plant Cell Physiol41: 27
Theuri MM, Kinyamario, JI, van Speybroeck D (1999) Photosynthesis and related physiological process in two mangrove species,Rhizophora mucronata andCeriops tagal, at Gazi Bay, Kenya. Afr J Ecol37: 180–193
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Parida, A., Das, A.B. & Das, P. NaCl stress causes changes in photosynthetic pigments, proteins, and other metabolic components in the leaves of a true mangrove,Bruguiera parviflora, in hydroponic cultures. J. Plant Biol. 45, 28–36 (2002). https://doi.org/10.1007/BF03030429
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DOI: https://doi.org/10.1007/BF03030429