Contribution of Rhizobium–Legume Symbiosis in Salt Stress Tolerance in Medicago truncatula Evaluated through Photosynthesis, Antioxidant Enzymes, and Compatible Solutes Accumulation

Abstract

The effects of salt stress on the growth, nodulation, and nitrogen (N) fixation of legumes are well known, but the relationship between symbiotic nitrogen fixation (SNF) driven by rhizobium–legume symbiosis and salt tolerance in Medicago truncatula is not well studied. The effects of the active nodulation process on salt stress tolerance of Medicago truncatula were evaluated by quantifying the compatible solutes, soluble sugars, and antioxidants enzymes, as well as growth and survival rate of plants. Eight weeks old plants, divided in three groups: (i) no nodules (NN), (ii) inactive nodules (IN), and (iii) active nodules (AN), were exposed to 150 mM of NaCl salt stress for 0, 8, 16, 24, 32, 40, and 48 h in hydroponic system. AN plants showed a higher survival rate (30.83% and 38.35%), chlorophyll contents (37.18% and 44.51%), and photosynthesis compared to IN and NN plants, respectively. Improved salt tolerance in AN plants was linked with higher activities of enzymatic and nonenzymatic antioxidants and higher K+ (20.45% and 39.21%) and lower Na+ accumulations (17.54% and 24.51%) when compared with IN and NN plants, respectively. Additionally, higher generation of reactive oxygen species (ROS) was indicative of salt stress, causing membrane damage as revealed by higher electrolyte leakage and lipid peroxidation. All such effects were significantly ameliorated in AN plants, showing higher compatible solutes (proline, free amino acids, glycine betaine, soluble sugars, and proteins) and maintaining higher relative water contents (61.34%). This study advocates positive role of Rhizobium meliloti inoculation against salt stress through upregulation of antioxidant system and a higher concentration of compatible solutes.

Effect of Salinity on Growth, Ion Accumulation and Mineral Nutrition of Different Accessions of a Crop Wild Relative Legume Species, Trifolium fragiferum

“…Thus, active rhizobial symbiosis improved salinity tolerance of Medicago sativa plants through increased osmotic adjustment and enzymatic antioxidative capacity [ 54 ]. Similar findings have been described also for Medicago truncatula [ 55 ]. It has been also established that presence of rhizobial symbiosis modulates interaction between T. fragiferum and T. repens on the background of increased substrate salinity [ 44 ].…”

Impact of Two Strains of Rhizobium leguminosarum on the Adaptation to Terminal Water Deficit of Two Cultivars Vicia faba

“…Another striking feature was the fact that Rhizobium in nodules can influence the proline concentration in roots and in leaves a mechanism that remains to be elucidated but that has already been observed [52]. Indeed, Irshad et al [52] observed higher compatible solutes (proline, free amino acids, glycine betaine, soluble sugars, and proteins) on Medicago truncatula plant organs with active nodules compare to non-nodulated ones in the salt stress tolerance process. The conclusion of the authors was that Rhizobium meliloti inoculation play a key role against salt stress through induction of antioxidant system and accumulation of compatible solutes was advise by the authors [52].…”

“…Moreover, a correlative study demonstrated that the nodules of drought-tolerant soybean cultivar accumulated higher levels of proline compared to the sensitive cultivar [1]. Another striking feature was the fact that Rhizobium in nodules can influence the proline concentration in roots and in leaves a mechanism that remains to be elucidated but that has already been observed [52]. Indeed, Irshad et al [52] observed higher compatible solutes (proline, free amino acids, glycine betaine, soluble sugars, and proteins) on Medicago truncatula plant organs with active nodules compare to non-nodulated ones in the salt stress tolerance process.…”

“…Indeed, Irshad et al [52] observed higher compatible solutes (proline, free amino acids, glycine betaine, soluble sugars, and proteins) on Medicago truncatula plant organs with active nodules compare to non-nodulated ones in the salt stress tolerance process. The conclusion of the authors was that Rhizobium meliloti inoculation play a key role against salt stress through induction of antioxidant system and accumulation of compatible solutes was advise by the authors [52]. High proline level was also positively correlated with the high level of H 2 O 2 recorded for MLT genotype.…”

An integrative, multidisciplinary approach to the study of the impact of climate change on legume agro-physiology and metabolism

“…Lipid peroxidation is the oxidative damage of membrane lipid and has been widely described in photosynthetic tissues, however in non-photosynthetic subterranean tissues, such as root and nodules, the extent of lipid peroxidation or the presence of the main antioxidant inhibiting lipid peroxidation propagation, vitamin E, has been much less studied. For example, lipid peroxidation has been previously described in both, determinate Matamoros et al, 2018) and indeterminate nodules Naya et al, 2007;Palma et al, 2014;Wang et al, 2016;Tysiganov et al, 2020;Irshad et al, 2021); however, the presence of vitamin E has been only showed in nodules of soybean .…”