Salanity

Environmental and Experimental Botany 58 (2006) 17–24

Physiological and nutritional indicators of tolerance to salinity in chickpea plants growing under symbiotic conditions
N.A. Tejera a,∗ , M. Soussi b , C. Lluch a a Departamento de Fisiolog´a Vegetal, Facultad de Ciencias, Universidad de Granada, Campus de Fuentenueva s/n, 18071 Granada, Spain ı b Departamento de Fisiolog´a y Bioqu´mica Vegetal, Centro de Ciencias Medioambientales, CSIC. 28006 Madrid, Spain ı ı Received 13 April 2005; accepted 15 June 2005

Abstract Alterations of plant growth, nitrogenase activity and nutrient concentration as a consequence of salt treatments were studied in five chickpea (Cicer arietinum L.) cultivars from Spain and Syria. Plants, in symbiosis with Mesorhizobium ciceri ch-191 strain, were grown under controlled conditions for 32 days and subjected to salinity stress. Parameters of growth and nitrogen fixation were affected under salt stress in all cultivars tested; plant dry weight decreased by about 15% in ILC1919; and in Sirio and Lechoso about 50% with the highest salt dosage (100 mM NaCl). ILC1919 showed a less growth accompanied by a lower dry matter formation under low salt conditions compared with most of the salt sensitive cultivar. Nitrogenase activity decreased by about 60% in the salt-resistant cultivar (cv. ILC1919) and more than 90% in salt-sensitive cultivars (cv. Sirio and Lechoso) with the highest salt dosage during the reproductive growth. We show that the higher NaCl tolerance of the ILC1919 cultivar is supported by the less N2 fixation inhibition, a higher root-to-shoot ratio, normalized nodule weight and shoot K/Na ratio; and a reduced foliar accumulation of Na+ . Moreover, our results reveal the effectiveness of these nutritional and physiological indicators in the selection of salinity-tolerant chickpea plants growing under symbiotic conditions. © 2005 Elsevier B.V. All rights reserved.
Keywords: Cicer arietinum; Legumes; NaCl; Nutrient

References: Asch, F., Dingkuhn, M., Wittstock, C., Doerffling, K., 1999. Sodium and potassium uptake of rice panicles as affected by salinity and season in relation to yield components. Plant Soil 207, 133–145. Ashraf, M., McNeilly, T., 2004. Salinity tolerance in Brassica oilseeds. Crit. Rev. Plant Sci. 23, 157–174. Baalbaki, R.Z., Zurayak, R.A., Adlan, M.A.M., Saxena, C.M., 2000. Effect of nitrogen source and salinity levels on salt accumulation of two chickpea genotypes. J. Plant Nutr. 23, 805–814. Balibrea, M.E., Cuartero, J., Bolar´n, M.C., P´ rez-Alfocea, F., 2003. Activı e ities during fruit development of Lycopersicon genotypes differing in tolerance salinity. Physiol. Plant 118, 38–46. Benlloch, M., Ojeda, M.A., Ramos, J., Rodr´guez-Navarro, A., 1994. Salt ı sensitivity and low discrimination between potassium and sodium in bean plants. Plant Soil 166, 117–123. Bouat, A., Crouzet, C., 1965. Notes techniques sur un appareil semiautomatiques de clorage de l’azote et de certains compos´ s volatiles. e Ann. Agric. 16, 107–118. Burias, N., Planchon, C., Paul, M.H., 1990. Phenotypic and genotypic distribution of nodules on soybean root system inoculated with Bradyrhizobium japonicum strain G49. Agronomie 10, 57–62. CIETA, 1969. Comit´ Inter-Institutos para el estudio de t´ cnicas anal´ticas de e e ı diagn´ stico foliar. M´ todos de referencia para la determinaci´ n de eleo e o mentos minerales en vegetales. Anal. Edaf. Agrobiol. XXVIII, 409–431. Cordovilla, M.P., Oca˜ a, A., Ligero, F., Lluch, C., 1995a. Salinity effects n on growth analysis and nutrient composition in four grain legumesRhizobium symbiosis. J. Plant Nutr. 18, 1595–1609. Cordovilla, M.P., Ligero, F., Lluch, C., 1995b. Influence of host genotypes on growth, symbiotic performance and nitrogen assimilation in faba bean (Vicia faba L.) under salt stress. Plant Soil 172, 289– 297. Cordovilla, M.P., Oca˜ a, A., Ligero, F., 1994. Lluch C.: The effect of salinity n on N2 fixation and assimilation in Vicia faba. J. Exp. Bot. 45, 1483–1488. Delgado, M.J., Garrido, J.M., Lluch, C., 1993. Nitrogen fixation and carbon metabolism by nodules and bacteroids of pea plants under sodium chloride stress. Physiol. Plant 89, 824–829. Delgado, M.J., Ligero, F., Lluch, C., 1994. Effects of salt stress on growth and nitrogen fixation by pea, faba-bean, common bean and soybean plants. Soil Biol. Biochem. 26, 371–376. Elsheikh, E.A.E., Wood, M., 1990. Effect of salinity on growth, nodulation and nitrogen yield of chickpea (Cicer arietinum L.). J. Exp. Bot. 41, 1263–1269. Garg, N., Singla, R., 2004. Growth, photosynthesis, nodule nitrogen and carbon fixation in the chickpea cultivars under salt stress. Braz. J. Plant Physiol. 16, 137–146. Gong, Z., Koiwa, H., Cushman, M.A., Ray, A., Bufford, D., Kore-eda, S., Matsumoto, T.K., Zhu, J., Cushman, J.C., Bressan, R.A., Hasegawa, P.M., 2001. Genes that are uniquely stress regulated in salt overly sensitive (sos) mutants. Plant Physiol. 126, 363–375. Grattan, S.R., Grieve, C.M., 1999. Salinity mineral nutrient relations in horticultural crops. Sci. Hortic. 78, 127–157. Greenway, H., Munns, R., 1980. Mechanism of salt tolerance in nonhalophytes. Annu. Rev. Plant Physiol. 31, 149–190. Herdina, J.A., Silsbury, J.H., 1990. Estimating nitrogenase activity of faba bean (Vicia faba L.) by acetylene reduction (AR) assay. Aust. J. Plant Physiol. 17, 489–502. Hulse, J.H., 1991. Nature, composition and utilization of grain legumes. In: Patencheru, A.P. (Ed.), Uses of Tropical Legumes. Proceedings of a Consultants Meeting, 27–30 March 1989. ICRISAT Center, ICRISAT, India, pp. 502–524. Lachica, M., Aguilar, A., Ya˜ ez, J., 1973. An´ lisis foliar.M´ todos utilizados n a e en la Estaci´ n Experimental del Zaidin, CSIC (II). Anal. Edaf. Agrobiol. o XXXII, 1033–1047. Lauchli, A., 1984. Salt exclusion: an adaptation of legume for crops and pastures under saline conditions. In: Staples, R.C., Toenniessen, G.H. (Eds.), Salinity Tolerance in Plants. Strategies for Crop Improvement. John Wiley and Sons, New York, pp. 171–187. Leonard, L.T., 1943. A simple assembly for use in testing of culture of rhizobia. J. Bacteriol. 45, 523–527. Ligero, F., Lluch, C., Olivares, J., 1986. Evolution of ethylene from root of Medicago sativa plants inoculated with Rhizobium meliloti. J. Plant Physiol. 125, 361–365. Mansour, M.M., 2000. Nitrogen containing compounds and adaptation of plants to salinity stress. Biol. Plant 43, 491–500. Mengel, K., Kirkby, E.A., 2001. Principles of Plant Nutrition. Kluwer Academic Publishers, Dordrecht/Boston/London. Minchin, F.R., Witty, J.F., Sheehy, J.E., Muller, M., 1983. A mayor error in the acetylene reduction assay: decreases in nodular nitrogenase activity under assay conditions. J. Exp. Bot. 34, 641–649. 24 N.A. Tejera et al. / Environmental and Experimental Botany 58 (2006) 17–24 Santos, C.V., Falc˜ o, I.P., Pinto, G.C., Oliveira, H., Loureiro, J., 2002. Nutria ent responses and glutamate and proline metabolism in sunflower plants and calli under Na2 SO4 stress. J. Plant Nutr. Soil Sci. 165, 366–372. Saxena, N.P., Saxena, M.C., Ruckenbauer, P., Rana, R.S., El-Fouly, M.M., Shabana, R., 1994. Screening techniques and sources of tolerance to salinity and mineral nutrient imbalances in cool season food legumes. Euphytica 73, 85–93. Seeman, J.R., Sharkey, T.D., 1986. Salinity and nitrogen effects on photosynthesis, ribulose 1,5 biphosphate carboxylase and metabolite pool sizes in Phaseolus vulgaris L. Plant Physiol. 82, 555–560. Soussi, M., Lluch, C., Oca˜ a, A., 1999. Comparative study of nitrogen n fixation and carbon metabolism in two chickpea (Cicer arietinum L.) cultivars under salt stress. J. Exp. Bot. 50, 1701–1708. Soussi, M., Oca˜ a, A., Lluch, C., 1998. Effects of salt stress on growth, n photosynthesis and nitrogen fixation in chickpea (Cicer arietinum L.). J. Exp. Bot. 49, 1329–1337. Tejera, N.A., Campos, R., Sanju´ n, J., Lluch, C., 2004. Nitrogenase and a antioxidant enzyme activities in Phaseolus vulgaris nodules formed by Rhizobium tropici isogenic strains with varying tolerance to salt stress. J. Plant Physiol. 161, 329–338. Vessey, J.K., 1994. Measurement of nitrogenase activity in legume root nodules: in defense of the acetylene reduction assay. Plant Soil 158, 151–162. Wyn Jones, R.G., Brady, C.J., Speirs, J., 1979. Ionic and osmotic-regulation in plants. In: Laidman, D.L., Wyn Jones, R.G. (Eds.), Recent Advances in Biochemistry of Cereals. Academic Press, London, pp. 63–103. Pessarakli, M., Zhou, M., 1990. Effect of salt stress on nitrogen fixation by different cultivars of green beans. J. Plant Nutr. 13, 611–629. Rao, D.L.N., Giller, K.E., Yeo, A.R., Flowers, T.J., 2002. The effect of salinity and sodicity upon nodulation and nitrogen fixation in chickpea (Cicer arietinum). Ann. Bot. 89, 563–570. Rao, D.L.N., Sharma, P.C., 1995. Alleviation of salinity stress in chickpea by Rhizobium inoculation or nitrate supply. Biol. Plant 37, 405– 410. Raven, J.A., 1985. Regulation of pH and generation of osmolarity in vascular plants: a cost-benefit analysis in relation to efficiency of use of energy, nitrogen and water. New Phytol. 101, 25–77. Rigaud, J., Puppo, A., 1975. Indole-3-acetic acid catabolism by soybean bacteroids. J. Gen. Microbiol. 88, 223–228. Rogers, M.E., Grieve, C.M., Shannon, M.C., 1998. The response of Lucerne (Medicago sativa L.) to sodium sulphate and chloride salinity. Plant Soil 202, 271–280. Rogers, M.E., Noble, C.L., Nicolas, M.E., Halloran, G.M., 1993. Variation in yield potential and salt tolerance of selected cultivars and natural populations of Trifolium repens L. Aust. J. Agric. Res. 44, 785– 798. Samaras, Y., Bressan, R.A., Csonka, L.N., Garc´a-Rios, M.G.D., Urzo, P., ı Rodes, D., 1994. Proline accumulation during drought and salinity. In: Smirnoff, N., Davies, W.J. (Eds.), Environment and Plant Metabolism. Flexibility and Acclimation. BIOS Scientific Publications, Lancaster, United Kingdom, pp. 161–187.