Salt modulates gravity signaling pathway to regulate growth direction of primary roots in Arabidopsis

Plant root architecture is highly plastic during development and can adapt to many environmental stresses. The proper distribution of roots within the soil under various conditions such as salinity, water deficit, and nutrient deficiency greatly affects plant survival. Salinity profoundly affects the root system architecture of Arabidopsis (Arabidopsis thaliana). However, despite the inhibitory effects of salinity on root length and the number of roots, very little is known concerning influence of salinity on root growth direction and the underlying mechanisms. Here we show that salt modulates root growth direction by reducing the gravity response. Exposure to salt stress causes rapid degradation of amyloplasts in root columella cells of Arabidopsis. The altered root growth direction in response to salt was found to be correlated with PIN-FORMED2 (PIN2) messenger RNA abundance and expression and localization of the protein. Furthermore, responsiveness to gravity of salt overly sensitive (sos) mutants is substantially reduced, indicating that salt-induced altered gravitropism of root growth is mediated by ion disequilibrium. Mutation of SOS genes also leads to reduced amyloplast degradation in root tip columella cells and the defects in PIN2 gene expression in response to salt stress. These results indicate that the SOS pathway may mediate the decrease of PIN2 messenger RNA in salinity-induced modification of gravitropic response in Arabidopsis roots. Our findings provide new insights into the development of a root system necessary for plant adaptation to high salinity and implicate an important role of the SOS signaling pathway in this process.     

A mixed-model QTL analysis for salt tolerance in seedlings of crop-wild hybrids of lettuce

Cultivated lettuce is more sensitive to salinity stress than its wild progenitor species potentially due to differences in root architecture and/or differential uptake and accumulation of sodium. We have identified quantitative trait locis (QTLs) associated with salt-induced changes in root system architecture (RSA) and ion accumulation using a recombinant inbred line population derived from a cross between cultivated lettuce (Lactuca sativa ‘Salinas’) and wild lettuce (L. serriola). Components of RSA were quantified by replicated measurements of seedling growth on vertical agar plates containing different concentrations of NaCl in a controlled growth chamber environment. Accumulation of sodium and potassium ions was measured in replicates of greenhouse-grown plants watered with 100 mM NaCl water. A total of 14 QTLs were identified using multi-trait linkage analysis, including three major QTLs associated with general root development, root growth in salt stress condition, and ion accumulation. The three major QTLs, qRC9.1, qRS2.1, and qLS7.2, were linked with markers E35/M59-F-425, LE9050, and LE1053, respectively. This study provides regions of lettuce genome contributing to salt-induced changes in RSA and ion accumulation. Future fine-mapping of major QTLs will identify candidate genes underlying salt stress tolerance in cultivated lettuce.     

Root halotropism: Salinity effects on Bassia indica root

Abstract

Plant roots are responsible for the acquisition of nutrients and water from the soil and have an important role in plant response to soil stress conditions. The direction of root growth is gravitropic in general. Gravitropic responses have been widely studied; however, studies about other root tropisms are scarce. Soil salinity is a major environmental response factor for plants, sensed by the roots and affecting the whole plant. Our observations on root architecture of Kochia (Bassia indica) indicated that salinity may cue tropism of part of the roots toward increasing salt concentrations. We termed this phenomenon “positive halotropism”. It was observed that Kochia individuals in the field developed horizontal roots, originating from the main tap root, which was growing toward saline regions in the soil. Under controlled conditions in greenhouse experiments, Kochia plants were grown in pots with artificial soil salinity gradients, achieved by irrigation with saline and fresh water. It was shown that plants grown in low‐salt areas developed a major horizontal root toward the higher salt concentration region in the gradient. In regions of high salinity and in the absence of a salinity gradient, roots grew vertically without a major horizontal root. The novel finding of “positive halotropism” is discussed.     

The role of long-distance signalling in plant responses to nitrate and other nutrients.

The phenotypic plasticity that plants display in response to changes in their nutrient supply requires the operation of both short- and long-range signalling pathways. Long-distance signals arising in the root can provide the shoot with an early warning of fluctuations in external nutrient concentrations, while signals in the reverse direction are needed to ensure that root physiology and development are integrated with the nutritional demands of the shoot. In this review, the focus is on recent advances in the understanding of these long-distance signalling pathways with an emphasis on nitrate nutrition, and a personal view of the key issues for future research is put forward.     

Salinity tolerance of citrus rootstocks: Effects of salt on root and leaf mineral concentrations

The effects of three concentrations of sodium chloride (NaCl) on seven citrus rootstocks were studied under greenhouse conditions. Leaf and root mineral concentrations and seedling growth were measured. Sodium chloride was added to the nutrient solution to achieve final osmotic potentials of –0.10, –0.20, and –0.35 MPa. Increasing the concentration of NaCl in the nutrition solution reduced growth proportionally and altered leaf and root mineral concentrations of all rootstocks. Significant differences in leaf and root mineral concentration among rootstocks were also found under stressed and non-stressed conditions. Salinity caused the greatest growth reduction in Milam lemon and trifoliate orange and the least reduction in sour orange and Cleopatra mandarin. No specific nutrient deficiency was the sole factor reducing growth and causing injury to citrus rootstocks. Sodium chloride sensitivity of citrus rootstocks in terms of leaf burn symptoms and growth reduction could be attributed more to Cl than to Na. Sodium and Cl concentrations were greater in the leaves than in the roots, particularly at the medium and high salinity levels. Root Cl was not useful for assessing injury because no differences were found in root Cl concentrations among rootstocks. Increasing salinity level did not affect the level of N and Ca in the roots but did reduce N and Ca levels in the leaves. No relationship in mineral concentration or accumulation seemed to exist between citrus leaves and roots. At the –0.10 MPa salinity level, sour orange, rough lemon, and Milam were not able to exclude either Na or Cl from their leaves. Trifoliate orange and its two hybrids (Swingle citrumelo and Carrizo citrange) excluded Na at the lowest salt level used, but were unable to exclude Na at the higher salinity levels. Similarly, Cleopatra mandarin excluded Cl at the lowest salt level, but was not able to exclude Cl at higher salt concentrations. Hence, the ability of citrus rootstocks to exclude Na or Cl breaks down at higher salt concentrations.Florida Agricultural Experiment Station Journal Series No. R-02276.     

Arbuscular mycorrhizal symbiosis influences strigolactone production under salinity and alleviates salt stress in lettuce plants

Arbuscular mycorrhizal (AM) symbiosis can alleviate salt stress in plants. However the intimate mechanisms involved, as well as the effect of salinity on the production of signalling molecules associated to the host plant-AM fungus interaction remains largely unknown. In the present work, we have investigated the effects of salinity on lettuce plant performance and production of strigolactones, and assessed its influence on mycorrhizal root colonization. Three different salt concentrations were applied to mycorrhizal and non-mycorrhizal plants, and their effects, over time, analyzed. Plant biomass, stomatal conductance, efficiency of photosystem II, as well as ABA content and strigolactone production were assessed. The expression of ABA biosynthesis genes was also analyzed.     

Root plasticity under abiotic stress

Abiotic stresses increasingly threaten existing ecological and agricultural systems across the globe. Plant roots perceive these stresses in the soil and adapt their architecture accordingly. This review provides insights into recent discoveries showing the importance of root system architecture (RSA) and plasticity for the survival and development of plants under heat, cold, drought, salt, and flooding stress. In addition, we review the molecular regulation and hormonal pathways involved in controlling RSA plasticity, main root growth, branching and lateral root growth, root hair development, and formation of adventitious roots. Several stresses affect root anatomy by causing aerenchyma formation, lignin and suberin deposition, and Casparian strip modulation. Roots can also actively grow toward favorable soil conditions and avoid environments detrimental to their development. Recent advances in understanding the cellular mechanisms behind these different root tropisms are discussed. Understanding root plasticity will be instrumental for the development of crops that are resilient in the face of abiotic stress.

Recent discoveries show the importance of root system architecture plasticity for the survival and growth of plants under several abiotic stresses.     

Critical role of divalent cations and Na+ efflux in Arabidopsis thaliana salt tolerance

Detrimental effects of salinity on plants are known to be partially alleviated by external Ca²⁺. Previous work demonstrated that the Arabidopsis SOS3 locus encodes a Ca²⁺‐binding protein with similarities to CnB, the regulatory subunit of protein phosphatase 2B (calcineurin). In this study, we further characterized the role of SOS3 in salt tolerance. We found that reduced root elongation of sos3 mutants in the presence of high concentrations of either NaCl or LiCl is specifically rescued by Ca²⁺ and not Mg²⁺, whereas root growth is rescued by both Ca²⁺ and Mg²⁺ in the presence of high concentrations of KCl. Phenocopies of sos3 mutants were obtained in wild‐type plants by the application of calmodulin and calcineurin inhibitors. These data provide further evidence that SOS3 is a calcineurin‐like protein and that calmodulin plays an important role in the signalling pathways involved in plant salt tolerance. The origin of the elevated Na : K ratio in sos3 mutants was investigated by comparing Na⁺ efflux and influx in both mutant and wild type. No difference in Na⁺ influx was recorded between wild type and sos3; however, sos3 plants showed a markedly lower Na⁺ efflux, a property that would contribute to the salt‐oversensitive phenotype of sos3 plants.     

Silicon improves salinity tolerance and affects ammonia assimilation in maize roots

The present study was conducted to evaluate the effect of different salt concentrations (50 and 200 mM NaCl) on growth, permeability properties (electrolyte leakage, cell viability) and activity of glutamine synthetase (GS) and glutamate dehydrogenase (GDH) in roots of maize seedlings. Both salt concentrations significantly affected growth and permeability properties of maize seedling roots and this negative effect increased with concentration of salt and duration of experiments. On the other hand salinity induced only small changes in the activities of GS and GDH, usually small increase in the activity was observed. To characterise the possible protective effect of silicon (Si) on maize roots exposed to saline stress, different concentrations of Si were simultaneously applied to both, low (50 mM) and high (200 mM) salt concentrations. Possible protective effects of Si on studied parameters were analysed in time range of 3 days treatment with the most positive effect on salt-induced root growth inhibition at high salt concentration and electrolyte leakage. The results show significant increase in GDH activity under all the tested conditions, although the mechanisms underlying this increase have not been elucidated. The results indicate that silicon may ameliorate the salt-induced root growth inhibition and increase the plant vigour at stressful conditions.     

Involvement of the ethylene-signalling pathway in sugar-induced tolerance to the herbicide atrazine in Arabidopsis thaliana seedlings

Soluble sugars can induce tolerance to otherwise lethal concentrations of the herbicide atrazine in Arabidopsis thaliana seedlings. This sugar-induced tolerance involves modifications of gene expression which are likely to be related to sugar and xenobiotic signal transduction. Since it has been suggested that ethylene- and sugar-signalling pathways may interact, the effects of glucose (Glc) and sucrose (Suc) on seedling growth and tolerance to atrazine were analysed in etr1-1, ein2-1, ein4, and sis1/ctr1-12 ethylene-signalling mutant backgrounds, where key steps of ethylene signal transduction are affected. Both ethylene-insensitive and ethylene-constitutive types of mutants were found to be affected in sugar-induced chlorophyll accumulation and root growth and in sugar-induced tolerance to atrazine. Interactions between ethylene and sugars were thus shown to take place during enhancement of seedling growth by low-to-moderate (up to 80 mM) sugar concentrations. The strong impairment of sugar-induced atrazine tolerance in etr1-1, ein2-1, and ein4 mutants demonstrated that this tolerance required active signalling pathways and could not be ascribed to mere metabolic effects nor to mere growth enhancement. Sugar-induced atrazine tolerance thus seemed to involve activation by sugar and atrazine of hexokinase-independent sugar signalling pathways and of ethylene signalling pathways, resulting in derepression of hexokinase-mediated Glc repression and in induction of protection mechanisms against atrazine injury.     

Brassinolide alleviates salt stress and increases antioxidant activity of cowpea plants (Vigna sinensis)

Soil salinity is one of the most severe factors limiting growth and physiological response in Vigna sinensis plants. Plant salt stress tolerance requires the activation of complex metabolic activities including antioxidative pathways, especially reactive oxygen species and scavenging systems within the cells which can contribute to continued growth under water stress. The present investigation was carried out to study the role of brassinolide in enhancing tolerance of cowpea plants to salt stress (NaCl). Treatment with 0.05?ppm brassinolide as foliar spray mitigated salt stress by inducing enzyme activities responsible for antioxidation, e.g., superoxide dismutase, peroxidase, polyphenol oxidase, and detoxification as well as by elevating contents of ascorbic acid, tocopherol, and glutathione. On the other hand, total soluble proteins decreased with increasing NaCl concentrations in comparison with control plants. However, lipid peroxidation increased with increasing concentrations of NaCl. In addition to, the high concentrations of NaCl (100 and 150?mM) decreased total phenol of cowpea plants as being compared with control plants. SDS-PAGE of protein revealed that NaCl treatments alone or in combination with 0.05?ppm brassinolide were associated with the disappearance of some bands or appearance of unique ones in cowpea plants. Electrophoretic studies of ??-esterase, ??-esterase, polyphenol oxidase, peroxidase, acid phosphatase, and superoxide dismutase isoenzymes showed wide variations in their intensities and densities among all treatments.     

Improved growth of salinity-stressed soybean after inoculation with salt pre-treated mycorrhizal fungi

Two sets of experiments to determine the effect of mycorrhiza on soybean (Glycine max) growth under saline conditions and to investigate the salt acclimation of mycorrhizal fungi were conducted. In the first experiment, the effect of an arbuscular mycorrhizal (AM) fungus Glomus etunicatum on mineral nutrient, proline and carbohydrate concentrations and growth of soybean. Under different NaCl concentrations (0, 50, 100, 150 and 200mM) was evaluated. Salinity decreased AM colonization. In both the M and nonAM plants shoot and root proline and shoot Na and Zn concentrations were increased under salinity. Soybean plants inoculated with the AM fungus had significantly higher fresh and dry weight, root proline, P, K and Zn but lower shoot proline and Na concentrations compared to the non inoculated plants. In the second experiment, the AM fungus was pre-treated with NaCl (salt acclimation) then was used as inoculum for soybean plants subjected to 100mM NaCl. Root colonization, fresh and dry weight, root proline, P, K and Zn concentrations were greater in soybean plants inoculated with the salt pre-treated fungus, compared to those inoculated with the nonsalt pre-treated fungus. However, for Na, the situation was the opposite. Based on these results, the AM inoculation helps the growth of soybean plants grown in saline conditions. When the AM fungus was pre-treated with NaCl with a gradual increase of concentration, and then exposed to a sudden salt stress, their efficiency was increased. This may be due to the acclimation of the AM fungus to salinity.     

A novel in vitro tissue culture approach to study salt stress responses in citrus

In citrus, a major crop throughout the world, growth and yield are seriously affected by salinity. Different approaches, including agronomical, physiological and molecular methods, have been used to address this problem. In this work, an in vitro experimental system has been developed to study the toxic effect of NaCl on three citrus genotypes, avoiding the ion filter that represents the root system. To carry out the experiments, shoots were obtained from nodal segments of Cleopatra mandarin, Carrizo citrange and citrumelo CPB4475 plants growing in a greenhouse. Shoots were cultured in control or NaCl-supplemented media. After testing several salt concentrations, 60 mM NaCl was selected as saline treatment. Shoots accumulated similar levels of chloride when cultured without roots and exhibited similar leaf damage. No increases in malondialdehyde levels were observed in any genotype (as a measure of oxidative stress). Similar patterns of hormonal signalling (in terms of abscisic acid and salicylic acid contents) were exhibited in the three genotypes, despite their different tolerance under field conditions. All data together indicate that, without root system, all genotypes had the same behaviour under salt stress. The in vitro culture system has been proved as a useful tool to study biochemical processes involved in the response of citrus to salt stress.     

Intrinsic water use efficiency controls the adaptation to high salinity in a semi-arid adapted plant,henna (Lawsonia inermis L.)

Adaptation to salinity of a semi-arid inhabitant plant, henna, is studied. The salt tolerance mechanisms are evaluated in the belief that gas exchange (water vapor and CO₂) should play a key role on its adaptation to salt stress because of the strong evaporation conditions and soil water deficit in its natural area of distribution. We grow henna plants hydroponically under controlled climate conditions and expose them to control (0 mM NaCl), and two levels of salinity; medium (75 mM NaCl) and high (150 mM NaCl). Relative growth rate (RGR), biomass production, whole plant and leaf structure and ultrastructure adaptation, gas exchange, chlorophyll fluorescence, nutrients location in leaf tissue and its balance in the plant are studied. RGR and total biomass decreased as NaCl concentration increased in the nutrient solution. At 75 mM NaCl root biomass was not affected by salinity and RGR reached similar values to control plants at the end of the experiment. At this salinity level henna plant responded to salinity decreasing shoot to root ratio, increasing leaf specific mass (LSM) and intrinsic water use efficiency (iWUE), and accumulating high concentrations of Na⁺ and Cl⁻ in leaves and root. At 150 mM NaCl growth was severely reduced but plants reached the reproductive phase. At this salinity level, no further decrease in shoot to root ratio or increase in LSM was observed, but plants increased iWUE, maintaining water status and leaf and root Na⁺ and Cl⁻ concentrations were lower than expected. Moreover, plants at 150 mM NaCl reallocated carbon to the root at the expense of the shoot. The effective PSII quantum yield [Y(II)] and the quantum yield of non-regulated energy dissipation [Y(NO)] were recovered over time of exposure to salinity. Overall, iWUE seems to be determinant in the adaptation of henna plant to high salinity level, when morphological adaptation fails.