Increased trehalose biosynthesis improves Mesorhizobium ciceri growth and symbiosis establishment in saline conditions

Abstract

Cicer arietinum (chickpea) is a legume very sensitive to salinity, and so are most of its rhizobial symbionts belonging to the species Mesorhizobium ciceri. We observed that exogenous trehalose (i.e., added to the growth medium) can significantly improve growth of M. ciceri strain Rch125 under moderate salinity. In order to test if endogenous trehalose (i.e., synthesized by the cell) could also enhance salt tolerance, strain Rch125 was genetically modified with various trehalose biosynthesis genes from Sinorhizobium meliloti 1021 (otsA, treS, treY) and Mesorhizobium loti MAFF 303099 (otsAB). We found that overexpression of otsA or otsAB, but not treS or treY, significantly improved M. ciceri Rch125 growth in saline media. This growth improvement correlated with enhanced trehalose accumulation in otsA-and otsABmodified cells, suggesting that increased trehalose synthesis via trehalose-6-phosphate can enhance bacterial salt tolerance. Chickpea plants inoculated with M. ciceri Rch125 derivatives carrying extra otsAB or otsA genes formed more nodules and accumulated more shoot biomass than wild type inoculated plants when grown in the presence of NaCl. These results support the notion that improved salt tolerance of the bacterial symbiont can alleviate the negative effects of salinity on chickpeas, and that such improvement in M. ciceri can be achieved by manipulating trehalose metabolism.

High Salt Tolerance of a Bradyrhizobium Strain and Its Promotion of the Growth of Stylosanthes guianensis

“…Salinity is one of the most serious environmental stresses limiting the growth of rhizobia, which fix atmospheric N 2 and supply host plants with N [ 6 , 9 ]. Cumulative results suggest that rhizobia show different levels of tolerance to salt stresses [ 2 , 5 , 26 ].…”

“…The accumulation of osmoprotective compounds by de novo biosynthesis in rhizobia is considered an effective strategy of adaptation by rhizobia to salt stress by protecting cells from desiccation and osmotic stress [ 6 , 11 , 12 ]. Furthermore, application of exogenous osmoprotective compounds increases the salt tolerance of rhizobial strains, such as Mesorhizobium sp.…”

“…To date, more than 800 million hectares of land globally, representing 40% of the world’s land surface, are affected by salinity, which is an important factor limiting the growth of rhizosphere rhizobia [ 3 , 4 ]. Salinity has detrimental effects on the activity of rhizobia, such as decreasing the rhizobial cell number and restricting root infection, accompanied by inhibiting nodule development and impairing nodule activity [ 2 , 5 , 6 ].…”

“…Rhizobial growth is affected by NaCl treatment, and different rhizobial strains exhibit significant differences in salt tolerance capability [ 2 , 6 ]. For example, the Rhizobium japonicum strain USDA191 is more tolerant to 0.4 M NaCl treatment than is the strain USDA110 [ 7 ].…”

Physiological Characterization and Genetic Diversity Assessment of the Rhizobial Populations Inhabiting <em>Gliricidia sepium</em> in selected Locations of Ampara District, Sri Lanka

“…High salt concentrations have shown to have negative effects on growth and distribution of Rhizobium sp. in soil (Jenkins et al, 1989) through limiting root infection via reducing the number of Rhizobial cells followed by inhibition of nodule growth and damaging the activity of nodules (Laranjo and Oliveira, 2011;Brígido et al, 2012;Moussaid et al, 2015). However, several studies have identified salt tolerant Rhizobia.…”