Nitric oxide reverses glucose-mediated photosynthetic repression in wheat (Triticum aestivum L.) under salt stress☆
Introduction
Plants are frequently exposed to environmental stresses that adversely affect their growth, development, and productivity (Khan et al., 2015). The continual increase in the abiotic stress factors is because of increased pressure on restricted agricultural land for higher productivity to match the pace of increase of human population, which is expected to become above 9 billion by 2050. This situation will lead to approximately 2.3 billion individuals facing food scarcity problems (FAO 2009).
Salt stress is one of the major environmental factors that plants encounter. It has been estimated that more than 45 million hectares comprising about 20% of irrigated agricultural land worldwide is salt affected (Munns and Tester, 2008; Shrivastava and Kumar, 2015). The excess accumulation of ions in plants found growing in salt stress leads to disturbed Na+/K+ homeostasis, enhanced production of reactive oxygen species (ROS), thereby causing oxidation of membrane lipids, protein and nucleic acids (Gill and Tuteja, 2010), growth inhibition and loss of productivity (Zhang et al., 2006; Khan et al., 2009; Fatma and Khan, 2014; Fatma et al., 2016a, Fatma et al., 2016b; Ahmad et al., 2016; Asgher et al., 2017). The potential antioxidant system, enzymatic or non-enzymatic in plants helps to counteract the effects of ROS. The increased accumulation of osmoprotectants and compatible solutes are also helpful in combating salt stress-impacts in plants (Khan et al., 2012; Khan and Khan, 2014; Ahmad et al., 2016; Abdel Latef and Chaoxing, 2014). Notably, these major mechanisms are integrated and triggered through the action of signaling molecules (Filippou et al., 2013; Ahmad et al., 2016). Nitric oxide (NO) has been reported to act as signaling molecule and improves salt stress tolerance in plants through activating antioxidant system (Fatma et al., 2016a, Fatma et al., 2016b; Per et al., 2017a, Per et al., 2017b). It has recently been recognized as a potential plant hormone related to plant defense reactions (Fatma et al., 2016a, Fatma et al., 2016b; Per et al., 2017a, Per et al., 2017b). It is a small free radical gaseous signaling molecule (Per et al., 2017a, Per et al., 2017b; Asgher et al., 2017) that readily diffuses across the cell membrane and interacts with various cellular compounds (Correa-Aragunde et al., 2015; Hasanuzzaman et al., 2018). NO interacts with a broad range of molecules leading to alteration in protein activity, reduced glutathione (GSH) biosynthesis, peroxynitrite formation and proline accumulation. These molecules individually or interactively mitigate salt stress effects (Per et al., 2017a, Per et al., 2017b; Hasanuzzaman et al., 2018). Additionally, NO mediates plant salt stress responses through maintenance of ionic homeostasis and reversal of oxidative damage and its effect on quantum yield of PSII (Wu et al., 2014; Fatma et al., 2016a, Fatma et al., 2016b), photosynthetic potential and growth promotion (Fatma and Khan, 2014; Fatma et al., 2016a, Fatma et al., 2016b; Ahmad et al., 2016; Hasanuzzaman et al., 2018).
Apart from NO acting as signaling molecule, sugars (including glucose) also acts as an important nutrient and signaling molecule in plants (Seckin et al., 2009). The use of glucose (Glu) as a stress-minimizing agent has been reported in plants (Hu et al., 2012; Huang and Cavalieri, 1979). Exogenously applied Glu under salt stress has been reported to act as osmoprotectant and ROS-scavenger (Almodares et al., 2008; Pattanagul and Thitisaksakul, 2008; Rosa et al., 2009). Glucose has been shown to maintain ionic homeostasis (Nemati et al., 2011; Hu et al., 2012), and promote seed germination, prevent water loss, restrict chlorophyll destruction and activate antioxidants enzyme activity (Hu et al., 2012). In fact, the cellular level of Glu, as a result of either endogenous production or exogenous application augments the positive and negative functions in plants. For example, accumulation of sugars to high levels inhibits photosynthesis and leads to stunted growth and necrotic leaves. In contrast, lower level of sugar enhances photosynthesis (Rolland et al., 2002). Studies have shown growth and photosynthetic responses of plants to individual effects of NO and Glu under salt stress, but how plants respond to the interactive effects of NO and Glu in mitigating salt stress effects are not clear. The present study was undertaken to with the aim to find out the possible mechanisms induced by nitric oxide that mediate in counteracting the adverse effects of accumulated Glu under salt stress. It was postulated that application of nitric oxide will induce the major mechanisms to counteract the effects of accumulated Glu in salt stressed wheat (Triticum aestivum L.). The hypothesis was tested by studying photosynthetic and biochemical parameters, such as ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) activity, gas exchange parameters, activity of nitrate reductase (NR) and nitrogen (N) content, oxidative stress parameters (H2O2 and lipid peroxidation), defense system components (non-enzymes/metabolites: cysteine, proline, and GSH; enzymes: superoxide dismutase, SOD, ascorbate peroxidase, APX, catalase, CAT and glutathione reductase, GR). Additionally, leaf analysis for Na+, Cl− and K+ and scanning electron microscopy of stomata were also performed to strengthen the mechanism involved.
Section snippets
Plant material, growth conditions, and treatments
Healthy seeds of wheat (Triticum aestivum L.) cultivar WH 711 were surface sterilized with 0.01% HgCl2 followed by repeated washings with double distilled water. The sterilized seeds were sown in 23-cm diameter earthen pots filled with sufficient quantity of sand. The pots were kept in net house of the Department of Botany, Aligarh Muslim University, Aligarh (India) under natural day/night conditions with photosynthetically active radiations (PAR, 680 μ mol m−2 s-1; average day/night
Selection of SNP concentration (Experiment 1)
Among the SNP concentrations tested, 10 and 25 μM SNP increased net photosynthesis by 5.6% and 20.8%, and plant dry mass by 9.1% and 24.2% compared to the control plants. The maximum and about equal increase of 34.0% in net photosynthesis and plant dry mass compared to the control plants was noted with 50 μM SNP (Table 1a).
Application of SNP resulted in increased Glu content and ethylene evolution. SNP at 10, 25 and 50 μM SNP increased Glu content by 6.9%, 18.9% and 29.4% and ethylene evolution
Discussion
Salinity in agricultural soils has become a major constraint to crop production (Shahbaz and Ashraf, 2013; Fatma and Khan, 2014; Fatma et al., 2016a, Fatma et al., 2016b; Asgher et al., 2017), as it substantially decreases nutritional homeostasis, oxidative stress, photosynthesis, growth and metabolism (Munns and Tester, 2008; Fatma and Khan, 2014; Fatma et al., 2016a, Fatma et al., 2016b). As a sustainable approach, this study revealed mechanisms underlying SNP-mediated improvements in
Conclusion
It may be concluded that SNP increases photosynthesis and growth of plants both under normal as well as salt stress conditions, whereas glucose results in a decline in the photosynthetic performance under these conditions. Under salt stress, the higher glucose accumulation as a part of protective mechanism inhibited photosynthesis in a feedback mechanism due to increased biosynthesis of carbohydrates. The application of SNP in the presence of glucose under salt stress maximally alleviated salt
References (85)
Catalase in vitro
Methods Enzymol.
(1984)- et al.
Roles of glycine betaine and proline in improving plant abiotic stress resistance
Environ. Exp. Bot.
(2007) - et al.
Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions
Anal. Biochem.
(1987) - et al.
Cadmium-induced functional and ultra structural alterations in roots of two transgenic cotton cultivars
J. Hazard. Mater.
(2009) - et al.
Interplay between nitric oxide and sulfur assimilation in salt tolerance in plants
Crop J.
(2016) - et al.
The nitric oxide donor sodium nitroprusside regulates polyamine and proline metabolism in leaves of Medicago truncatula plants
Free Radic. Biol. Med.
(2013) Control of plant development and gene expression by sugar signaling
Curr. Opin. Plant Biol.
(2005)- et al.
Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants
Plant Physiol. Biochem.
(2010) - et al.
Variation in photosynthesis and growth of mustard cultivars: role of ethylene sensitivity
Sci. Hort.
(2012) - et al.
Growth, photosynthesis and Antioxidant metabolism in mustard (Brassica juncea L.) cultivars differing in ATP-sulfurylase activity under salinity stress
Sci. Hort.
(2009)
Salicylic acid-induced abiotic stress tolerance and underlying mechanisms in plants
Front. Plant Sci.
Sugar distribution in sweet stalk sorghum
Food Chem.
In vitro stability of nitrate reductase from barley leaves
Phytochemistry.
Sugar and hormone connections
Trends Plant Sci.
Nitric oxide improves S-assimilation and GSH production to prevent inhibitory effects of cadmium stress on photosynthesis in mustard (Brassica juncea L.)
Nitric Oxide
Approaches in modulating proline metabolism in plants for salt and drought stress tolerance: phytohormones, mineral nutrients and transgenics
Plant Physiol. Biochem.
Exogenous nitric oxide protects cucumber roots against oxidative stress induced by salt stress
Plant Physiol. Biochem.
Soil salinity: a serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation
Saudi J. Biol. Sci.
Does inoculation with Glomus mosseae improve salt tolerance in pepper plants?
J. Plant Growth Regul.
Nitric oxide mitigates salt stress by regulating levels of osmolytes and antioxidant enzymes in chickpea
Front. Plant Sci.
Exogenous application of nitric oxide modulates osmolyte metabolism, antioxidants, enzymes of ascorbate-glutathione cycle and promotes growth under cadmium stress in tomato
Protoplasma.
Nitrogen availability impacts oilseed rape (Brassica napus L.) plant water status and proline production efficiency under water-limited conditions
Planta
The effects of salt stress on parameters and carbohydrates contents in sweet sorghum
Res. J. Environ. Sci.
Determination of glutathione and glutathione disulfide in biological samples
Methods Enzymol.
Nitric oxide signaling and its crosstalk with other plant growth regulators in plant responses to abiotic stress
Environ. Sci. Pollut. Res.
Rapid determination of free proline for water stress studies
Plant Soil
Expression levels of some starch metabolism related genes in flag leaf of two contrasting rice genotypes exposed to salt stress
Aus. J. Crop Sci.
Nitric oxide is a ubiquitous signal for maintaining redox balance in plant cells: regulation of ascorbate peroxidase as a case study
J. Exp. Bot.
Leaf senescence correlated within creased level of membrane permeability, lipid peroxidation and decreased level of SOD and CAT
J. Exp. Bot.
Nitric oxide protects photosynthetic capacity inhibition by salinity in Indian mustard
J. Funct. Environ. Bot.
Nitric oxide alleviates salt stress inhibited photosynthetic performance by interacting with sulfur assimilation in mustard
Front. Plant Sci.
The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism
Planta.
A spectrophotometric method for the direct determination of cysteine in the presence of other naturally occurring amino acids
Biochem. J.
Nitric oxide induces stomatal closure and enhances the adaptive plant responses against drought stress
Plant Physiol.
Superoxide dismutases: I. Occurrence in higher plants
Plant Physiol.
Effects of nitric oxide on salt stress tolerance in Kosteletzkya virginica
Life Sci. J.
Mitochondrial adaptations to NaCl. Complex I is protected by anti-oxidants and small heat shock proteins, whereas complex II is protected by proline and betaine
Plant Physiol.
Nitric oxide pre treatment enhances antioxidant defense and glyoxalase systems to confer PEG-induced oxidative stress in rape seed
J. Plant Interact.
Nitric oxide-induced salt stress tolerance in plants: ROS metabolism, signaling, and molecular interactions
Plant Biotechnol. Rep.
Effects of exogenous glucose on seed germination and antioxidant capacity in wheat seedlings under salt stress
Plant Growth Regul.
Proline oxidase and water stress-induced proline accumulation in spinach leaves
Plant Physiol.
Ethephon increases photosynthetic-nitrogen use efficiency, proline and antioxidant metabolism to alleviate decrease in photosynthesis under salinity in mustard
Plant Signal. Behav.
Cited by (100)
Adaptive responses of nitric oxide (NO) and its intricate dialogue with phytohormones during salinity stress
2024, Plant Physiology and BiochemistryActive oxygen generation induced by the glucose sensor TaHXK7-1A decreased the drought resistance of transgenic Arabidopsis and wheat (Triticum aestivum L.)
2024, Plant Physiology and BiochemistryMitigation of arsenic stress in Brassica juncea L. using zinc oxide-nanoparticles produced by novel hydrothermal synthesis
2023, South African Journal of Botany
- ☆
This article is part of a special issue entitled is “Revisiting the role of ROS and RNS in plants under a changing environment” published at the journal Environmental and Experimental Botany 161.