Abstract
Seedlings of the salt-tolerant plant grewia [Grewia tenax (Forssk.) Fiori] and the moderately salt-tolerant tamarind (Tamarindus indica L.) were grown under controlled conditions and treated daily with NaCl solutions to investigate mechanisms of tolerance to salinity. Leaf micromorphology, cuticular wax load, chlorophyll fluorescence and light remission, as well as antioxidative potential were evaluated. As confirmed by energy-dispersive X-ray microanalysis in both species, absorption of sodium and chlorine increased with rising NaCl concentration in the treatment solution. In parallel, accumulation of calcium in grewia leaves was strongly reduced, leading to less crystals of calcium oxalate in leaf tissue. In grewia the cuticular wax load, chlorophyll content, and electron transport rate (ETR) were significantly reduced by comparatively low NaCl concentrations. In tamarind, in contrast, wax load and ETR were not significantly affected, while the decrease of chlorophyll content was less pronounced. Measurements of the antioxidative capacity and the imbalance between values of lipophilic and hydrophilic extracts at different NaCl concentrations confirmed that grewia is more salt tolerant than tamarind. This higher tolerance degree seemed to be associated with grewias’ more efficient scavenging of free radicals and the regulation of the antioxidative potential in lipophilic and hydrophilic extracts.
Similar content being viewed by others
Abbreviations
- DMSO:
-
Dimethyl sulfoxide
- EC:
-
Electrical conductivity
- EDX:
-
Energy-dispersive X-ray microanalysis
- ETR:
-
Electron transport rate
- Fm:
-
Maximum fluorescence
- Fo:
-
Ground fluorescence
- Fv/Fo:
-
Maximum quantum yield of PS2 photochemistry
- NDVI:
-
Normalized difference vegetation index
- NaCl:
-
Sodium chloride
- NIR:
-
Near infrared
- PAM:
-
Pulse amplitude modulated chlorophyll fluorescence
- PAR:
-
Photosynthetically active radiation
- ROS:
-
Reactive oxygen species
- SEM:
-
Scanning electron microscope
References
Arbona V, Flors V, Jacas J, Garcia-Augustin P, Gomez-Cadenas A (2003) Enzymatic and non enzymatic antioxidant responses of Carrizo citrange, a salt sensitive citrus rootstock to different levels of salinity. Plant Cell Physiol 44(4):388–394
Aziz AA, Junit SM, Razali N (2009) Tamarindus indica plant as a source of potent antioxidants with potential hypolipidaemic properties. In: 34. Congress of the Federation of European Biochemical Societies, FEBS J, vol 276, pp 297
Baker NR, Rosenqvist E (2004) Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities. J Exp Bot 55(403):1607–1621
Belkhodja R, Morales F, Abadia A, Gomez-Aparisi J, Abadia J (1994) Chlorophyll fluorescence as a possible tool for salinity tolerance screening in barley (Hordeum vulgare L.). J Plant Physiol 138:92–96
Blanke MM (1993) Determination of chlorophyll using DMSO. Vitic Enol Sci 47:32–35
Bondada BR, Oosterhuis DM, Murphy JB, Kim KS (1996) Effect of water stress on the epicuticular wax composition and ultrastructure of cotton (Gossypium hirsutum L.) leaf, bract and boll. Environ Exp Bot 36:61–69
Bringe K, Hunsche M, Schmitz-Eiberger M, Noga G (2007) Retention and rainfastness of mancozeb as affected by physicochemical characteristics of adaxial apple leaf surface after enhanced UV-B radiation. J Environ Sci Health B 42(2):133–141
Chaves MM, Flexas J, Pinheiro C (2008) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot Lond 103:551–560
Chevolleau S, Debal A, Ucciani E (1992) Determination of the antioxidant activity of plant extracts. Rev Fr Corps Gras 39(1–2):120–126
Cuartero J, Bolarin MC, Asins MJ, Moreno V (2006) Increasing salt tolerance in the tomato. J Exp Bot 57(5):1045–1058
Delarosaibarra M, Maiti RK (1995) Biochemical mechanism in glossy sorghum lines for resistance to salinity stress. J Plant Physiol 146(4):515–519
El-Siddig K, Gebauer J, Ebert G, Ali AM, Inanaga S (2004) Influence of salinity on emergence and early seedling growth of Tamarindus indica L. Eur J Hortic Sci 69(2):79–81
El-Siddig K, Gunasena HPM, Prasad BA, Pushpakumara DKNG, Ramana KVR, Vijayanand P, Williams JT (2006) Tamarind, Tamarindus indica. Southampton Centre for Underutilised Crops, Southampton
Ferrer JP, Montero AR, Hurtado YV, Ferrada CR, Carballo C (2008) Tamarindus indica L.: evaluation of the mutagenic and antioxidant potential. Latin Am J Pharm 27(3):375–379
Foyer CH (1993) Ascorbic acid. In: Alscher RG, Hess JL (eds) Antioxidants in higher plants. CRC Press, Boca Raton, pp 31–58
Franceschi VR, Nakata PA (2005) Calcium oxalate in plants: formation and function. Ann Rev Plant Biol 56:41–71
Fricke W, Akhiyarova G, Wei WX, Alexandersson E, Miller A, Kjellbom PO, Richardson A, Wojciechowski T, Schreiber L, Veselov D, Kudoyarova G, Volkov V (2006) The short-term growth response to salt of the developing barley leaf. J Exp Bot 57(5):1079–1095
Fryer MJ (1992) The antioxidant effects of thylakoid vitamin E. Plant Cell Environ 15:381–392
Gebauer J, El-Siddig K, Ebert G (2001) Response of Tamarindus indica seedlings to salt stress. J Appl Bot Angew Bot 75:97–100
Gebauer J, El-Siddig K, Salih AA, Ebert G (2004) Tamarindus indica L. seedlings are moderately salt tolerant when exposed to NaCl-induced salinity. Sci Hortic Amsterdam 103:1–8
Gebauer J, El-Siddig K, El Tahir BA, Salih AA, Ebert G, Hammer K (2007) Exploiting the potential of indigenous fruit trees: Grewia tenax (Forssk.) Fiori in Sudan. Genet Resour Crop Evol 54:1701–1708
Hartl WP, Klapper H, Barbier B, Ensikat H-J, Dronskowski R, Müller P, Ostendorp G, Tye A, Bauer R, Barthlott W (2007) Diversity of calcium oxalate crystals in Cactaceae. Can J Bot 85:501–517
Hunsche M, Noga G (2008) Applicability of the energy dispersive X-ray microanalysis for quantification of irregular calcium deposits on fruit and leaf cuticles. J Microsc Oxford 232:453–462
Hunsche M, Blanke M, Noga G (2010) Does the microclimate under hail nets influence micromorphological characteristics of apple leaves and cuticles? J Plant Physiol. doi:10.1016/j.jplph.2010.02.007
Jenks AJ, Hasegawa PM, Jain SM, Foolad MR (2007) Advances in molecular breeding toward drought and salt tolerant crops. Springer, New York 817 p
Khemiss F, Ghoul-Mazgar S, Moshtaghie AA, Saidane D (2006) Study of the effect of aqueous extract of Grewia tenax fruit on iron absorption by everted gut sac. J Ethnopharmacol 103:90–98
Lamien-Meda A, Lamien CE, Compaore MMY, Meda RNT, Kiendrebeogo M, Zeba B, Millogo FF, Nacoulma OG (2008) Polyphenol content and antioxidant capacity of fourteen wild edible fruits from Burkina Faso. Molecules 13(3):581–594
Lichtenthaler HK, Buschmann C, Knapp M (2005) How to correctly determine the different chlorophyll fluorescence parameters and the chlorophyll fluorescence decrease ratio RFd of leaves with the PAM fluorometer. Photosynthetica 43:379–393
Lutts S, Kinet JM, Bouharmont J (1996) NaCl-induced senescence in leaves of rice (Oryza sativa L.) cultivars differing in salinity resistance. Ann Bot Lond 78:389–398
Mishra SK, Subrahmanyam D, Singhal GS (1991) Interrelationship between salt and light stress on primary processes of photosynthesis. J Plant Physiol 138:92–96
Misra AN, Srivastava A, Strasser RJ (2001) Utilization of fast chlorophyll a fluorescence technique in assessing the salt/ion sensitivity of mung bean and Brassica seedlings. J Plant Physiol 158:1173–1181
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Ann Rev Plant Biol 59:651–681
Netondo GW, Onyango JO, Beck E (2004) Sorghum and salinity: II. Gas exchange and chlorophyll fluorescence of sorghum under salt stress. Crop Sci 44:806–811
Paula FS, Kabeya LM, Kanashiro A, de Figueiredo ASG, Azzolini AECS, Uyemura SA, Lucisano-Valim YM (2009) Modulation of human neutrophil oxidative metabolism and degranulation by extract of Tamarindus indica L. fruit pulp. Food Chem Toxicol 47(1):163–170
Peńuelas J, Isla R, Filella I, Araus JL (1997) Visible and near-infrared reflectance assessment of salinity effects on barley. Crop Sci 37:198–202
Percival GC, Fraser GA, Oxenham G (2003) Foliar salt tolerance of Acer genotypes using chlorophyll fluorescence. J Arboric 29(2):61–65
Rong-Hual L, Pei-Pol G, Baumz M, Grando S, Ceccarelli S (2006) Evaluation of chlorophyll content and fluorescence parameters as indicators of drought tolerance in barley. Agric Sci China 5(10):751–757
Saied AS, Sohail M, Gebauer J, Buerkert A (2010) Response of Grewia tenax (Forssk.) Fiori to NaCl-induced salinity. Eur J Hortic Sci 75(1):42–50
Sairam RK, Tyagi A (2004) Physiology and molecular biology of salinity stress tolerance in plants. Curr Sci India 86(3):407–421
Schmitz M, Noga G (2000) Selected plant components and their antioxidative capacity in hydrophilic and lipophilic extracts of Phaeseolus vulgaris, Malus domestica and Vitis vinifera leaves. Eur J Hortic Sci 65:65–73
Serrano R, Gaxiola R (1994) Microbial models and salt stress tolerance in plants. CRC Crit Rev Plant Sci 13(2):121–138
Shabala SN, Shabala SI, Martynenko AI, Babourina O, Newman IA (1998) Salinity effect on bioelectric activity, growth, Na+ accumulation and chlorophyll fluorescence of maize leaves: a comparative survey and prospects for screening. Aust J Plant Physiol 25(5):609–616
Smilie RM, Nott R (1982) Salt tolerance in crop plants monitored by chlorophyll fluorescence in vivo. Plant Physiol 70:1049–1054
Sudjaroen Y, Haubner R, Wurtele R, Hull EE, Erben G, Spiegelhalder B, Changbumrung S, Bartsch H, Owen RW (2005) Isolation and structure elucidation of phenolic antioxidants from Tamarind (Tamarindus indica L.) seeds and pericarp. Food Chem Toxicol 43(11):1673–1682
Vijayan K, Chakraborti SP, Ercisli S, Ghosh PD (2008) NaCl induced morpho-biochemical and anatomical changes in mulberry (Morus spp.). Plant Growth Regul 56(1):61–69
Winter K, Gademann R (1991) Daily changes in CO2 and water vapor exchange, chlorophyll fluorescence, and leaf water relations in the halophyte Mesembryanthemum crystallinum during the induction of crassulacean acid metabolism in response to high NaCl salinity. Plant Physiol 95:768–776
Xu HL, Gauthier L, Gosselin A (1995) Stomatal and cuticular transpiration of greenhouse tomato plants in response to high solutions electrical-conductivity and low soil-water content. J Am Soc Hortic Sci 120(3):417–422
Yang Z, Rao MN, Elliott NC, Kindler SD, Popham TW (2005) Using ground-based multispectral radiometry to detect stress in wheat caused by greenbug (Homoptera: Aphididae) infestation. Comput Electron Agric 47:121–135
Zhu J-K (2001) Plant salt tolerance. Trends Plant Sci 6(2):66–71
Acknowledgments
The authors thank Libeth Schwager, Gertrudis Heimes, and Knut Wichterich for their support in the laboratory activities and scanning electron microscope work.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Hunsche, M., Bürling, K., Saied, A.S. et al. Effects of NaCl on surface properties, chlorophyll fluorescence and light remission, and cellular compounds of Grewia tenax (Forssk.) Fiori and Tamarindus indica L. leaves. Plant Growth Regul 61, 253–263 (2010). https://doi.org/10.1007/s10725-010-9473-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10725-010-9473-x