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Contribution of inorganic cations and organic compounds to osmotic adjustment in root cultures of two Centaurium species differing in tolerance to salt stress

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Abstract

The effect of reduced availability of sugars on growth and essential metabolic processes in roots, resulting from decreased photosynthesis under salinity, was excluded by establishing a non-photosynthetic model-system in this study: root cultures of Centaurium maritimum (L.) Fritch and Centaurium spicatum (L.) Fritch. The contribution of inorganic cations and organic compounds (e.g. carbohydrates and amino acids) to the osmotic adjustment (OA) in roots during short-term exposure to various salt concentrations (0, 50, 100 or 200 mM NaCl) was emphasized. Observed morphological and histological changes in roots were species specific, and were dependent on salinity level. Although C. spicatum appears to be more tolerant to salt stress, both species employed similar strategies in response to elevated salinity to different extents, and displayed effective OA mechanisms. Under low and moderate salinity, inorganic cations were the major contributors to OA in roots of both species, followed by soluble sugars, while the relative contribution of proline (Pro) and free amino acids was insignificant. Osmotic adjustment under severe stress appears to be mediated by increased accumulation of organic compounds. The analysis of the intraspecies variability in salt response of C. spicatum and C. maritimum roots enabled the identification of some organic compounds which could be used as potential biochemical markers in screening for salt tolerance, including Pro in C. spicatum, and trehalose and polyols in C. maritimum.

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References

  • Alves AAC, Setter TL (2004) Abscisic acid accumulation and osmotic adjustment in cassava under water deficit. Environ Exp Bot 51:259–271

    Article  CAS  Google Scholar 

  • Ashraf M, Harris PJC (2004) Potential biochemical indicators of salinity tolerance in plants. Plant Sci 166:3–16

    Article  CAS  Google Scholar 

  • Bajji M, Lutts S, Kinet JM (2001) Water deficit effects on solute contribution to osmotic adjustment as a function of leaf ageing in three durum wheat (Triticum durum Desf.) cultivars performing differently in arid conditions. Plant Sci 160:669–681

    Article  PubMed  CAS  Google Scholar 

  • Bates IS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Benaroudj N, Lee DH, Goldberg AL (2001) Trehalose accumulation during cellular stress protects cells and cellular proteins from damage by oxygen radicals. J Biol Chem 276:24261–24267

    Article  PubMed  CAS  Google Scholar 

  • Berkan T, Üstünes L, Lermioglu F, Özer A (1991) Antiinflamatory, analgesic, and antipyretic effects of an aqueous extract of Erythraea centaurium. Planta Med 57:34–37

    Article  PubMed  CAS  Google Scholar 

  • Deak KI, Malamy J (2005) Osmotic regulation of root system architecture. Plant J 43:17–28

    Article  PubMed  CAS  Google Scholar 

  • Demir Y, Kocakalikan I (2002) Effect of NaCl and proline on bean seedlings cultured in vitro. Biol Plant 45:597–599

    Article  CAS  Google Scholar 

  • Gandonou CB, Errabii T, Arbini J, Idaomar M, Senhaji NS (2006) Selection of callus cultures of sugarcane (Saccharum sp.) tolerant to NaCl and their response to salt stress. Plant Cell Tiss Org Cult 87:9–16

    Article  CAS  Google Scholar 

  • Garcia AB, de Almeida Engler J, Iyer S, Gerats T, Van Montagu M, Caplan AB (1997) Effects of osmoprotectants upon NaCl stress in rice. Plant Physiol 115:159–169

    PubMed  CAS  Google Scholar 

  • Glauert AM, Glauert RH (1958) Araldite as an embedding medium for electron microscopy. J Biophys Biochem Cytol 4:191–194

    Article  PubMed  CAS  Google Scholar 

  • Greenway H, Munns R (1980) Mechanisms of salt tolerance in nonhalophytes. Annu Rev Plant Phys 31:149–190

    Article  CAS  Google Scholar 

  • Hare PD, Cress WA (1998) Metabolic implications of stress-induced proline accumulation in plants. Plant Growth Regul 21:79–102

    Article  Google Scholar 

  • Hare PD, Cress WA, van Staden J (1998) Dissecting the roles of ocmolyte accumulation during stress. Plant Cell Environ 21:535–553

    Article  CAS  Google Scholar 

  • Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responces to high salinity. Annu Rev Plant Phys 51:463–499

    Article  CAS  Google Scholar 

  • He C, Yang A, Zhang W, Gao Q, Zhang J (2010) Improved salt tolerance of transgenic wheat by introducing betA gene for glycine betaine synthesis. Plant Cell Tiss Organ Cult 101:65–78

    Article  CAS  Google Scholar 

  • Kondo Y, Takano F, Hojo H (1994) Suppression of chemically and immunologically induced hepatic injuries by gentiopicroside in mice. Planta Med 60:414–416

    Article  PubMed  CAS  Google Scholar 

  • Kumarasamy Y, Nahar L, Cox PJ, Jaspars M, Sarker SD (2003) Bioactivity of secoiridoid glucosides from Centaurium erythraea. Phytomedicine 10:344–347

    Article  PubMed  CAS  Google Scholar 

  • Lee G, Carrow RN, Duncan RR, Eiteman MA, Rieger MW (2008) Synthesis of organic osmolytes and salt tolerance mechanisms in Paspalum vaginatum. Environ Exp Bot 63:19–27

    Article  CAS  Google Scholar 

  • Lokhande VH, Nikam TD, Penna S (2010) Biochemical, physiological and growth changes in responce to salinity in callus cultures of Sesuvium portulacastrum L. Plant Cell Tiss Org Cult 102:17–25

    Article  Google Scholar 

  • Maksimović V, Mojović M, Vučinić Ž (2006) Monosaccharide-H2O2 reactions as a source of glzcolate and their stimulation by hzdroxyl radicals. Carbohyd Res 341:2360–2369

    Article  Google Scholar 

  • Mišić D, Šiler B, Filipović B, Popović Z, Živković S, Cvetić T, Mijović A (2009) Rapid in vitro selection of salt-tolerant genotypes of the potentially medicinal plant Centaurium maritimum (L.) Fritsch. Arch Biol Sci Belgrade 61:57–69

    Google Scholar 

  • Munns R (2005) Genes and salt tolerance: bringing them together. New Phytol 167:645–663

    Article  PubMed  CAS  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681

    Article  PubMed  CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol Plantarum 15:473–497

    Article  CAS  Google Scholar 

  • Neocleous D, Vasilakakis M (2007) Effects of NaCl stress on red raspberry (Rubus idaeus L. ‘Autumn Bliss’). Sci Hortic-Amsterdam 112:282–289

    Article  CAS  Google Scholar 

  • Niiho Y, Yamazaki T, Nakajima Y, Yamamoto T, Ando H, Hirai Y, Toriizuka K, Ida Y (2006) Gastroprotective effects of bitter principles isolated from Gentian root and Swertia herb on experimentally-induced gastric lesions in rats. J Nat Med 60:82–88

    Article  CAS  Google Scholar 

  • Nikolić N, Kostić Lj, Djordjević A, Nikolić M (2011) Phosphorus deficiency is the major limiting factor for wheat on alluvium polluted by the copper mine pyrite tailings: a black box approach. Plant Soil 339:485–498

    Article  Google Scholar 

  • Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Safe 60:324–349

    Article  CAS  Google Scholar 

  • Parvaiz A, Satyawati S (2008) Salt stress and phyto-biochemical responses of plants—a review. Plant Soil Environ 54:89–99

    CAS  Google Scholar 

  • Rhodes D, Samaras Y (1994) Genetic control of osmoregulation in plants. In: Strange K (ed) Cellular and molecular physiology of cell volume regulation. CRC Press, Boca Raton, FL, pp 339–353

    Google Scholar 

  • Richardson SG, McCree KJ (1985) Carbon balance and water relations of Sorghum exposed to salt and water stress. Plant Physiol 79:1015–1020

    Article  PubMed  CAS  Google Scholar 

  • Roitch T (2004) Plant response to stress: source-sink regulation by stress. In: Goodman RM (ed) Encyclopedia of plant and crop science. Marcel Dekker, New York, pp 1010–1013

    Google Scholar 

  • Rosen H (1957) A modified ninhydrin colorimetric analysis for amino acids. Arch Biochem Biophys 67:10–15

    Article  PubMed  CAS  Google Scholar 

  • Shabala L, Cuin TA, Newman IA, Shabala S (2005) Salinity-induced ion flux patterns from the excised roots of Arabidopsis sos mutants. Planta 222:1041–1050

    Article  PubMed  CAS  Google Scholar 

  • Shimazaki Y, Ookawa T, Hirasawa T (2005) The root tip and accelerating region suppress elongation of the decelerating region without any effects on cell turgor in primary roots of maize under water stress. Plant Physiol 139:458–465

    Article  PubMed  CAS  Google Scholar 

  • Šiler B, Mišić D, Nestorović J, Banjanac T, Glamočlija J, Soković M, Ćirić A (2010) Antibacterial and antifungal screening of Centaurium pulchellum crude extracts and main secoiridoid compounds. Nat Prod Commun 5:1525–1530

    PubMed  Google Scholar 

  • Simonović AD, Anderson MD (2007) Analysis of methionine oxides and nitrogen-transporting amino acids in chilled and acclimated maize seedlings. Amino Acids 33:607–613

    Article  PubMed  Google Scholar 

  • Somboonwatthanaku I, Dorling S, Leung S, McManus MT (2010) Proline biosynthetic gene expression in tissue cultures of rice (Oryza sativa L.) in responce to saline treatment. Plant Cell Tiss Org Cult 103:369–376

    Article  CAS  Google Scholar 

  • Sun J, Li L, Liu M, Wang M, Ding M, Deng S, Lu C, Zhou X, Shen X, Zheng X, Chen S (2010) Hydrogen peroxide and nitric oxide mediate K*/Na+ homeostasis and antioxidant defense in NaCl-stressed callus cells of two contrasting poplars. Plant Cell Tiss Organ Cult 103:205–215

    Article  CAS  Google Scholar 

  • Tester M, Davenport RJ (2003) Na+ transport and Na+ tolerance in higher plants. Ann Bot 52:503–527

    Article  Google Scholar 

  • Türkan I, Demiral T (2009) Recent developments in understanding salinity tolerance. Environ Exp Bot 67:2–9

    Article  Google Scholar 

  • van der Sluis WG (1985) Chemotaxonomical investigations of the genera Blackstonia and Centaurium (Gentianaceae). Plant Syst Evol 149:253–286

    Article  Google Scholar 

  • Woodward AJ, Bennett IJ (2005) The effect of salt stress and abscisic acid on proline production, chlorophyll content and growth of in vitro propagated shoots of Eucalyptus camaldulensis. Plant Cell Tiss Org Cult 82:189–200

    Article  CAS  Google Scholar 

  • Zhao X, Tan HJ, Liu YB, Li XR, Chen GX (2009) Effect of salt stress on growth and osmotic regulation in Thellungiella and Arabidopsis callus. Plant Cell Tiss Org Cult 98:97–103

    Article  CAS  Google Scholar 

  • Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71

    Article  PubMed  CAS  Google Scholar 

  • Zhu JK (2002) Salt and drought signal transduction in plants. Annu Rev Plant Biol 53:247–273

    Article  PubMed  CAS  Google Scholar 

  • Zhu JK (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6:441–445

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work is financially supported by the Serbian Ministry of Education and Science (grants 173024, 173040, and 173028). We dedicate this work to our dear colleague, Professor Dr. Dragoljub Grubišić, whom we wish to remember with affection.

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Correspondence to Danijela Mišić.

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Mišić, D., Šiler, B., Nestorović Živković, J. et al. Contribution of inorganic cations and organic compounds to osmotic adjustment in root cultures of two Centaurium species differing in tolerance to salt stress. Plant Cell Tiss Organ Cult 108, 389–400 (2012). https://doi.org/10.1007/s11240-011-0050-4

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  • DOI: https://doi.org/10.1007/s11240-011-0050-4

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