Nodule carbohydrate metabolism and polyols involvement in the response of Medicago sativa to salt stress
Highlights
► NaCl altered the content of compatible osmolytes and enzyme activities in M. sativa. ► Salt stress decreased Fo and increased the quantum efficiency of PSII (Fv/Fm ratio). ► The content of polyols was related with the response of the symbiosis to salt stress. ► Nodules increased the synthesis of pinitol in response to salt stress.
Introduction
Salinity is one of the major abiotic factors limiting global agricultural productivity, and it is estimated that one-third of the world's irrigated land are unsuitable for crops (Frommer et al., 1999). Salt stress drastically affects the photosynthesis (Soussi et al., 1998), the nitrogen metabolism (Cordovilla et al., 1994), the carbon metabolism (Delgado et al., 1993, Balibrea et al., 2003) and the plant nutrition (Mengel and Kirkby, 2001). Legumes are classified as salt-sensitive crop species (Läuchli, 1984) and their production is particularly affected by salt stress because these plants depend on symbiotic N2 fixation for their nitrogen requirement (Elsheikh and Wood, 1995). The limitation of productivity is associated with a lower growth of the host plant, poor development of the root nodules (Georgiev and Atkins, 1993) and consequently with a reduction of the nitrogen-fixation capacity (Ben Salah et al., 2011).
Under the variation of saline environments, plants develop different adaptive mechanisms (Rhodes et al., 2002, Sairam et al., 2006), some of which include the synthesis and accumulation of low-molecular weight organic compounds in the cytosol and organelles (Ashraf and Harris, 2004, Sairam et al., 2006). These compounds, collectively called compatible osmolytes, are simple sugars, disaccharides, sugar alcohols or polyols, amino acids and sulfonium compounds (Ashraf and Harris, 2004, Bartels and Sunkar, 2005, Ashraf and Foolad, 2007). A major function of the accumulation of the compatible osmolytes is the osmotic adjustment to counteract the high concentrations of inorganic salts in the vacuole and in the root medium (Zhu, 2001, Rhodes et al., 2002). Another function of the compatible osmolytes is the osmoprotection which may occur at lower salt concentrations. This role involves the protection of thylakoids and the plasma membrane, as well as the stabilization of proteins. Under salinity stress these compounds also act as a sink of energy or reducing power, as a source of carbon and nitrogen, or scavenging reactive oxygen species (Bartels and Sunkar, 2005, Sairam et al., 2006).
Soluble carbohydrates and their polyol derivatives are the most common osmolytes accumulating in plants in response to low water potentials. Cyclic polyols involve myoinositol, ononitol and pinitol. Myoinositol is derived from glucose-6-phosphate and can be further methylated to sequoyitol or ononitol, which are epimerized to d-pinitol (Loewus and Loewus, 1980). An increase in pinitol content has been shown to occur in plants subjected to a water deficit (Streeter et al., 2001, Matos et al., 2010) as well as to a high salinity (Sengupta et al., 2008). Salinity induces the expression of genes, one of which has been shown to be involved in pinitol synthesis (Vernon and Bohnert, 1992). Thus, the introduction of genes involved in the synthesis of proline (P5CF127A), betaines (betA) and polyols (mt1D, imt1) into plants contributes to abiotic stress tolerance (Rathinasabapathi, 2000, Chen and Murata, 2002). It has been also suggested that exogenous application of compatible solutes is an alternative approach to improve crop productivity under saline conditions (Makela et al., 1999, Chen and Murata, 2002).
The objective of the present work was to investigate changes induced by salinity on the content of some compatible osmolytes and enzyme activities of carbon metabolism in Medicago sativa grown under symbiotic conditions. In addition, the content of the polyols myoinositol and pinitol, as well as their relation with the adaptation of the symbiosis to salt stress, was also evaluated.
Section snippets
Biological material and growth conditions
Seeds of M. sativa (var. Aragon) were surface sterilized by immersion in 5% NaClO for 3 min and germinated in 0.8% water-agar plates at 28 °C in darkness. Two days after, seedlings were transferred to individual pots of about 200 ml containing a vermiculite–perlite mixture (3:1) and watered with N-free nutrient solution (Rigaud and Puppo, 1975). Each seedling, inoculated with 1 ml of a stationary culture of Sinorhizobium meliloti GR4 strain (ca. 109 cell ml−1), was grown in a controlled environmental
Results
Plant biomass and nitrogen fixation rate were markedly affected by salt stress conditions (Fig. 1). In control (0 mM NaCl) and treated plants (150 mM NaCl), the plant dry weight (PDW) increased with plant age, although plants grown without salt showed values of PDW higher than salinized plants in all harvests. At fructification stage (84 days after sowing, DAS) PDW decreased about 50% with the saline treatment. The NFR was maximal at the beginning of flowering stage (56 days after sowing, DAS) in
Discussion
Several papers have been written regarding the effect of salt stress on nitrogen fixation and on the enzymes of the carbon metabolism in nodules (Lopez et al., 2008, Lopez and Lluch, 2008) as well as on the accumulation of sugars and other compatible solutes (Bartels and Sunkar, 2005, Khadri et al., 2007), but the mechanisms implicated in these processes remain unclear. In the present work, we examined the changes in the content of polyols (myoinositol and pinitol), the presence of soluble
Acknowledgments
Financial support was obtained through the Andalusian Research Program (AGR-139) and the Spanish Ministry of Education and Science AGL2006-01279. The authors are grateful to anonymous reviewers for making valuable suggestions to earlier drafts of this study.
References (48)
- et al.
Increased salt and drought tolerance by d-ononitol production in transgenic Arabidopsis thaliana
Biochemical and Biophysical Research Communications
(2011) - et al.
Roles of glycine betaine and proline in improving plant abiotic stress resistance
Environmental and Experimental Botany
(2007) - et al.
Potential biochemical indicators of salinity tolerance in plants
Plant Science
(2004) - et al.
Response of nitrogen fixation in relation to nodule carbohydrate metabolism in Medicago ciliaris lines subjected to salt stress
Journal of Plant Physiology
(2009) - et al.
Enhancement of tolerance of abiotic stress by metabolic engineering of betaines and other compatible solutes
Current Opinion in Plant Biology
(2002) - et al.
Nodulation and N2 fixation by soybean inoculated with salt-tolerant rhizobia or salt-sensitive bradyrhizobia in saline soil
Soil Biology and Biochemistry
(1995) - et al.
Sodium chloride–ABA interaction in two common bean (Phaseolus vulgaris) cultivars differing in salinity tolerance
Environmental and Experimental Botany
(2007) - et al.
Myoinosytol: biosynthesis and metabolism
- et al.
Growth and nitrogen fixation in Lotus japonicus and Medicago truncatula under NaCl stress: nodule carbon metabolism
Journal of Plant Physiology
(2008) - et al.
Protein measurement with the Folin phenol reagent
Journal of Biological Chemistry
(1951)
Pinitol accumulation in mature leaves of white clover in response to a water deficit
Environmental and Experimental Botany
Metabolic engineering for stress tolerance: installing osmoprotectant synthesis pathways
Annals of botany
Plant salt tolerance
Trends in Plant Science
Sucrolytic activities during fruit development of Lycopersicon genotypes differing in tolerance to salinity
Physiologia Plantarum
Drought and salt tolerance in plants
Critical Reviews in Plant Sciences
Variability in the response of six genotypes of N2-fixing Medicago ciliaris to NaCl
Symbiosis
Determination of sugar compounds in olive plant extracts by anion-exchange chromatography with pulsed amperometric detection
Analytical Chemistry
The effect of salinity on N fixation and assimilation in Vicia faba
Journal of Experimental Botany
Nitrogen fixation and carbon metabolism by nodules and bacteroids of pea plants under sodium chloride stress
Physiologia Plantarum
Aluminum tolerance in wheat (Triticum aestivum L.). II. Aluminum stimulated excretion of malic acid from root apices
Plant Physiology
Taking transgenic plants with a pinch of salt
Science
Oxygen regulation of a nodule located carbonic anhydrase in alfalfa
Plant Physiology
Effects of salinity on N2 fixation, nitrogen metabolism and export and diffusive conductance of cowpea root nodules
Symbiosis
Overexpression of the Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation
Plant Physiology
Cited by (27)
Polyols-related gene expression is affected by cyclic desiccation in lichen microalgae
2021, Environmental and Experimental BotanyCitation Excerpt :We provide evidences of the regulation of transcript levels of main sugar alcohols-related genes and the possible role of NO as a modulator of gene expression, which lead both microalgae species to the osmoprotectants accumulation. Studies demonstrated the role of polyols as a defensive strategy against abiotic stress, promoting osmotic adjustment, protecting membranes, or controlling cellular ROS levels (Nishizawa-Yokoi et al., 2008; Keunen et al., 2013; Palma et al., 2013). In our previous work, analyzing one cycle of D/R, the metabolic profile revealed that sugar alcohol played a key role in DT of both, Csol and TR9 microalgae.
Role of metabolites in abiotic stress tolerance in legumes
2021, Abiotic Stress and Legumes: Tolerance and ManagementCircadian regulation of abiotic stress tolerance in legumes
2021, Abiotic Stress and Legumes: Tolerance and ManagementMetabolism regulation during salt exposure in the halophyte Cakile maritima
2020, Environmental and Experimental BotanyCitation Excerpt :Myo-inositol, glycerol, and xylitol were enriched in salt stress conditions and over time. Myo-inositol is involved, among other roles, in osmoprotection of Mesembryanthemum crystallinum and Medicago in response to salt stress (Palma et al., 2013; Vernon’ and Bohnert’, 1992). More broadly, myo-inositol and glycerol were used as osmoprotectants in response to drought and salt stress (Kumari and Parida, 2018) even if in some plant species, the abundance of sugar alcohols, particularly glycerol, was reduced in response to salt stress (Paidi et al., 2017; Wu et al., 2013).
Effects of dopamine on growth, carbon metabolism, and nitrogen metabolism in cucumber under nitrate stress
2020, Scientia HorticulturaeThe expression of alfalfa MsPP2CA1 gene confers ABA sensitivity and abiotic stress tolerance on Arabidopsis thaliana
2019, Plant Physiology and BiochemistryCitation Excerpt :A number of genes likely associated with its albeit limited capacity to tolerate salinity have been isolated and characterized. These have encoded various transcription factors (Winicov and Bastola, 1999; Chen et al., 2012), microRNAs (Long et al., 2015), and the synthesis of certain metabolites (Palma et al., 2013). However, there is still little information about the role of PP2Cs in the abiotic stress response of alfalfa.