Abstract
Legumes can host rhizobia and mycorrhizal fungi, and this triple symbiosis might be exploited to improve saline soil fertility. Therefore, a greater understanding of the interaction of rhizobia and arbuscular mycorrhizal fungus during legume growth in saline soil is required. We investigated the efficiency of salt tolerance conferred by rhizobia in mycorrhizal Sesbania cannabina. Greenhouse experiments were conducted in which S. cannabina plants inoculated with Glomus mosseae BGC NM03D (GM), and two rhizobia strains Agrobacterium pusense YIC4105 (4105) and Neorhizobium huautlense YIC4083 (4083), were exposed to 100 and 200 mM NaCl. Under 200 mM NaCl stress, plants inoculated with 4105, rather than 4083, showed significant increases in shoot and root dry mass compared with non-inoculated plants. Simultaneously, a significant increase over GM-inoculated plants in mycorrhizal colonization and dependency was recorded for 4105 + GM-inoculated plants compared with 4083 + GM-inoculated plants. In addition, under NaCl stress, significant increases in the number and mass of nodules, nitrogenase activity, and leghemoglobin content of nodules occurred in 4105 + GM-inoculated plants compared with 4083 + GM-inoculated plants. Furthermore, the activities of antioxidant enzymes in rhizobia-inoculated plants were significantly higher in the GM + 4105 group than the 4083 + GM group. The malondialdehyde content of plants from the 4105 + GM group was significantly lower than in the 4083 + GM group. Thus, the results revealed a synergistic relationship among the 4105 and GM in alleviating salt stress in S. cannabina. Salt-tolerant rhizobia might improve the salinity tolerance of S. cannabina by enhancing the antioxidant system.
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References
Aebi H (1984) Catalase in vitro. In: Packer L (ed) Methods in enzymology. Academic Press, Orlando, pp 121–126
Alguacil MM, Hernandez JA, Caravaca F, Portillo B, Roldan A (2003) Antioxidant enzyme activities in shoots from three mycorrhizal shrub species afforested in a degraded semi-arid soil. Physiol Plant 118:562–570. doi:10.1034/j.1399-3054.2003.00149.x
Al-Karaki GN, Hammad R, Rusan M (2001) Response of two tomato cultivars differing in salt tolerance to inoculation with mycorrhizal fungi under salt stress. Mycorrhiza 11:41–47. doi:10.1007/s005720100098
Anthraper A, Dubois JD (2003) The effect of NaCl on growth, N2 fixation (acetylene reduction), and percentage total nitrogen in Leucaena leucocephala (Leguminosae) Var. K-8. Am J Bot 90:683–692. doi:10.3732/ajb.90.5.683
Aryal UK, Xu HL, Fujita M (2003) Rhizobia and AM fungal inoculation improve growth and nutrient uptake of bean plants under organic fertilization. J Sustain Agric 21:29–41. doi:10.1300/J064v21n03_04
Azcón R, Rubio R, Barea JM (1991) Selective interactions between different species of mycorrhizal fungi and Rhizobium meliloti strains, and their effects on growth, N2 fixation (N15) in Medicago sativa at four salinity levels. New Phytol 117:399–404. doi:10.1111/j.1469-8137.1991.tb00003.x
Camprubi A, Calvet C (1996) Isolation and screening of mycorrhizal fungi from Citrus nurseries and orchards and inoculation studies. HortScience 31:366–369
Carmen B, Roberto D (2009) Medicago truncatula improves salt tolerance when nodulated by an indole-3-acetic acid-overproducing Sinorhizobium meliloti strain. J Exp Bot 60:3097–3107. doi:10.1093/jxb/erp140
Castillo FI, Penel I, Greppin H (1984) Peroxidase release induced by ozone in Sedum album leaves. Plant Physiol 74:846–851
Copeman RH, Martin CA, Stutz JC (1996) Tomato growth in response to salinity and mycorrhizal fungi from saline or nonsaline soil. HortScience 31:341–344
Cordovilla MP, Ligero F, Lluch C (1999) Effects of NaCl on growth and nitrogen fixation and assimilation of inoculated and KNO3 fertilized Vicia faba L. and Pisum sativum L. plants. Plant Sci 140:127–136. doi:10.1016/S0168-9452(98)00201-5
Del VC, Barea JM, Azcon-Agular C (1999) Diversity of arbuscular mycorrhizal fungus populations in heavy-metal-contaminated soils. Appl Environ Microbiol 65:718–723
Delgado MJ, 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. doi:10.1016/0038-0717(94)90286-0
Dhindsa RS, Plumb-Dhindsa P, Throne TA (1981) Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation and decreased levels of superoxide dismutase and catalase. J Exp Bot 32:93–101
Freeman S (2003) Chapter 37: plant defense systems. Prentice Hall, Englewood Cliffs
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. doi:10.1590/S1677-04202004000300003
Ghazi N, Al-Karaki GN (2006) Nursery inoculation of tomato with arbuscular mycorrhizal fungi and subsequent performance under irrigation with saline water. Sci Hortic 109:1–7. doi:10.1016/j.scienta.2006.02.019
Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84:489–500. doi:10.1111/j.1469-8137.1980.tb04556.x
Gomez JM, Hernandez JA, Jimenez A, del Rio LA, Sevilla F (1999) Differential response of antioxidative enzymes of chloroplast and mitochondria to long term NaCl stress of pea plants. Free Radical Res 31:S11–S18
Hartree EF (1957) Haematin compounds. In: Paech K, Tracey MV (eds) Modern methods of plant analysis. Springer, New York, pp 197–245
Heikham E, Rupam K, Bhoopander G (2009) Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann Bot 104:1263–1280. doi:10.1093/aob/mcp251
Hernandez JA, Almansa MS (2002) Short-term effects of salt stress on antioxidant systems and leaf water relations of pea leaves. Physiol Plant 115:251–257. doi:10.1034/j.1399-3054.2002.1150211.x
Hoagland A (1950) The water-culture method for growing plants without soil. University of California, College of Agriculture, Agricultural Experiment Station, Berkeley, California
Kazunori S, Natsuko O, Tomomitsu K (2013) Involvement of autoregulation in the interaction between rhizobial nodulation and AM fungal colonization in soybean roots. Biol Fertil Soils 49:1141–1152. doi:10.1007/s00374-013-0804-8
Martha O, Clarence AR (1999) Hydrogen peroxide is generated systemically in plant leaves by wounding and systemin via the octadecanoid pathway. Proc Natl Acad Sci USA 25:6553–6557
Mohamed HA, Abdel-Wahab EE, Nivien AN, David MK, Fatthy MM (2014) Synergistic interaction of Rhizobium leguminosarum bv. Viciae and arbuscular mycorrhizal fungi as a plant growth promoting biofertilizers for faba bean (Vicia faba L.) in alkaline soil. Microbiol Res 169:49–58. doi:10.1016/j.micres.2013.07.007
Moran JF, James EK, Rubio MC, Sarath G, Klucas RV, Becana M (2003) Functional characterization and expression of a cytosolic iron-superoxide dismutase from Cowpea root nodules. Plant Physiol 133:773–782. doi:10.1104/pp.103.023010
Mortimer PE, Pérez-Fernández MA, Valentine AJ (2008) The role of arbuscular mycorrhizal colonization in the carbon and nitrogen economy of the tripartite symbiosis with nodulated Phaseolus vulgaris. Soil Biol Biochem 40:1019–1027. doi:10.1016/j.soilbio.2007.11.014
Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250. doi:10.1046/j.0016-8025.2001.00808.x
Nair S, Jha PK, Babu CR (1993) Induced salt tolerant rhizobia, from extremely salt tolerant Rhizobium gene pools, from reduced but effective symbiosis under non-saline growth. Microbios 74:39–51
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880
Phillips JM, Hayman DS (1970) Improved procedures for clearing and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–160
Plenchette C, Fortin JA, Furlan V (1983) Growth response of several plant species to mycorrhiza in soil of moderate P fertility. I: mycorrhizal dependency under field conditions. Plant Soil 70:191–209. doi:10.1007/BF02374780
Porcel R, Barea JM, Ruiz-Lozano JM (2003) Antioxidant activities in mycorrhizal soybean plants under drought stress and their possible relationship to the process of nodule senescence. New Phytol 157:135–143. doi:10.1046/j.1469-8137.2003.00658.x
Puppo A, Groten K, Bastian F, Carzaniga R, Soussi M, Lucas MM, de Felipe MR, Harrison J, Vanacker H, Foyer CH (2005) Legume nodule senescence: roles for redox and hormone signalling in the orchestration of the natural aging process. New Phytol 165:683–701. doi:10.1111/j.1469-8137.2004.01285.x
Rao DLN (1998) Biological amelioration of salt-affected soils. Microbial interactions in agriculture and forestry, vol 1. Science Publishers, Enfield, pp 21–238
Rosa P, Ricardo A, Juan MR (2012) Salinity stress alleviation using arbuscular mycorrhizal fungi: a review. Agron Sustain Dev 32:181–200. doi:10.1007/s13593-011-0029-x
Salwa J, Moez J, Férid L, Mohamed EA (2005) Changes in ascorbate peroxidase, catalase, guaiacol peroxidase and superoxide dismutase activities in common bean (Phaseolus vulgaris) nodules under salt stress. J Plant Physiol 162:929–936. doi:10.1016/j.jplph.2004.10.005
Singh RP, Choudhary A, Gulati A, Dahiya HC, Jaiwal PK, Sengar RS (1997) Response of plants to salinity in interaction with other abiotic and factors. In: Jaiwal PK, Singh RP, Gulati A (eds) Strategies for improving salt tolerance in higher plants. Science Publishers, Enfield, pp 25–39
Singh JS, Pandey VC, Singh DP (2011) Efficient soil microorganisms: a new dimension for sustainable agriculture and environmental development. Agric Ecosyst Environ 140:339–353
Smith IK, Vierheller TL, Thorne CA (1988) Assay of glutathione reductase in crude tissue homogenates using 5,5′-dithiobis(2-nitrobenzoic acid). Anal Biochem 175:408–413. doi:10.1016/0003-2697(88)90564-7
Sudhakar C, Lakshmi A, Giridarakumar S (2001) Changes in the antioxidant enzymes efficacy in two high yielding genotypes of mulberry (Morus alba L.) under NaCl salinity. Plant Sci 161:613–6199. doi:10.1016/S0168-9452(01)00450-2
Tian CY, Feng G, Li XL, Zhang FS (2004) Different effects of arbuscular mycorrhizal fungal isolates from saline or non-saline soil on salinity tolerance of plants. Appl Soil Ecology 26:143–148. doi:10.1016/j.apsoil.2003.10.010
Vincent JM (1970) A manual for the practical study of root nodule bacteria. Black-well Scientific, Oxford
Walsh KB (1995) Physiology of the legume nodule and its response to stress. Soil Biol Biochem 27:637–655. doi:10.1016/0038-0717(95)98644-4
Weissenhorn I, Leyval C, Berthelin J (1993) Cd-tolerant arbuscular mycorrhizal (AM) fungi from heavy-metal polluted soils. Plant Soil 158:250–256. doi:10.1007/BF00011053
Zahran HH (1991) Conditions for successful Rhizobium-legume symbiosis in saline environments. Biol Fertil Soils 12:73–80. doi:10.1007/BF00369391
Zahran HH (1999) Rhizobium–legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev 63:968–989
Acknowledgments
This work was financed by the Strategic Priority Research Program of the Chinese Academy of Sciences (Grant No. XDA11020403), the Key Research Program of the Chinese Academy of Sciences (Grant No. KZZD-EW-14), the National Natural Science Foundation of China (31370108 and 31570063), One Hundred-Talent Plan of Chinese Academy of Sciences (CAS), Yantai Science and Technology Project (2013JH021).
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Ren, CG., Bai, YJ., Kong, CC. et al. Synergistic Interactions Between Salt-tolerant Rhizobia and Arbuscular Mycorrhizal Fungi on Salinity Tolerance of Sesbania cannabina Plants. J Plant Growth Regul 35, 1098–1107 (2016). https://doi.org/10.1007/s00344-016-9607-0
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DOI: https://doi.org/10.1007/s00344-016-9607-0