Effect of exogenously applied amino acids on photosynthetic pigments, metabolites and enzymatic antioxidants in Zea mays L. subjected to salt stress

doi:10.21203/rs.3.rs-4864510/v1

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Effect of exogenously applied amino acids on photosynthetic pigments, metabolites and enzymatic antioxidants in Zea mays L. subjected to salt stress

https://doi.org/10.21203/rs.3.rs-4864510/v1

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The current study has been designed to investigate the effect of different concentrations (0, 25, 75, 100 ppm) amino acids including Methionine (Met), Tryptophan (Tryp), Glycine Betaine (GB) and Lysine (Lys) in alleviating the effect of salt stress. The experiment was performed on maize plants under two stress conditions (0, 120 mM NaCl). Effect of salinity reduced the morpho-physiological parameters along with antioxidant activities. Application of amino acids exhibit potential of tolerance for saline stress. All applications of amino acids increased the growth parameters, however, maximum shoot length, biomass of shoot was noted under the application of lysine while root length, number of leaves and biomass of root was improved by the application of glycine betaine, methionine and tryptophan respectively. Photosynthetic pigments were increased under the influence of glycine betaine. Amino acids also triggered the antioxidant activity and increase the production of metabolites. Phenolics, total soluble proteins (TSP) and superoxide dismutase (SOD) were improved by the application of glycine betaine, catalase (CAT), peroxidase (POD) and flavonoids were improved by the application of tryptophan, while total free amino acids (TFA) were more under the effect of methionine application. With increasing concentrations of amino acids the parameters were also in increasing pattern. Because of amino acids application, enhancement of studied parameters under saline environment is linked to increased photosynthetic pigments, improved metabolites and modulated antioxidants activites in Zea mays L.

Methionine

Lysine

Tryptophan

Glycine betaine

Biomass

Growth

Maize

In recent times, the demand of cereals has boosted significantly due to rapid increase in global population. Climate variations has disturbed production of crops via increasing the severity and frequencies of biotic and abiotic stresses. Among abiotic factors, salinity is the main issue which possess severe risks on crop production[1]. Plants are imposed by salt stress throughout their life cycle. Currently, 950 Mha of the total land area (10%) and 230 Mha of the total irrigated area (50%) are under salt stress around the globe [2].

Maize is the second largest widely cultivated crop and accounts for 1137 million tons estimated global production with significant contribution towards global food security [3]. It has been proven in Biphasic model of salinity induced growth reduction which was presented by Munns et al.[4] osmotic and ionic stresses are responsible for reduction in cereals growth during first and second phase, respectively. Salinity negatively effects on growth and yield of maize attributes throughout plant life cycle which mainly depends on length and severity of the stress [3, 5]. Similarly, in another study high salt concentration reduced the maize kernel weight and yield significantly at the reproductive stage compared to non-saline conditions [6]. Changes in climate leads to alterations in soil fertility attributes such as nutrients levels, organic matter, temperature, moisture contents and microbiota. To combat these challenges, need sustainable agrotechnology which can improve soil productivity [7].

Plant biostimulants are labelled as metabolic enhancers, plant probiotics, plant strengthers, biofertilizers and biostimulators [8]. In other words biostimulants can be defined as products which enhance the nutritional processes of plants independently of the nutrient content of the product. These products such as humic substances, plant growth promoting bacteria, amino acids and seaweed extracts that alter the plant physiological processes and support plant growth and development and stress responses upon application [9]. According to prediction, the biostimulants market will reach to 5.1 billion USD by 2027, compared to 3 billion USD reported in 2021 [10]. This incline in production and marketing trend reveals increased application of biostimulants industries in crop production [8]. Among amino acids, methionine is a vital amino acid which involves in various physiological processes in plants. It acts as an effective regulator in growth and development of plants under abiotic stress conditions [11]. Some reports have highlighted that foliar application of methionine showed positive interactions with plant pigments, osmolytes accumulation, increased uptake of potassium (K), calcium (Ca), phosphorous contents (P), efficient removal of reactive oxygen species which ultimately results in improved growth of cowpea and wheat under water deficient conditions [12, 13]. Further, Lysine also contributes in several responses against biotic and abiotic stresses via Sacharopine pathway (SACPATH) [14]. According to some recent reports, Iron and zinc chelated fertilizers complexed with lysine amino acid results in improvement of growth and yield in crops like in Brassica napus and rice under salt and cadmium stress via increase in plant biomass, gaseous exchange attributes, and antioxidant enzymes responses [15–17]. L-trytophan also known as ß-3-indolylalanine (IAA) is very unique amino acid with an indole ring. Some studies have shown its promising results after spray on soil, as seed priming agent. Plants taken up soil applied tryptophan directly via roots or soil microbes metabolized it in to many products such as serotonin, niacin and auxins and these products subsequently absorbed by plant roots [18]. The controlled use of tryptophan exert positive effects on plant growth and yield due to continuous release of auxins [19]. Both foliar and soil applied tryptophan showed positive effect on auxin biosynthesis and its crosstalk with other phytohormones not only under normal conditions but also under stressful environment [20]. Tryptophan is absorbed by leaf epidermis during foliar application and improves the growth and yield attributes in three bread wheat cultivars and lettuce plants as reported by [21, 22].

Osmo-protectants reserve the cellular apparatus of plants from stress induced injuries without altering the normal metabolic functions at cellular level. These include a wide range of compounds such as trehalose, phenolics, Glycine betaine (GB), proline, sugars etc. [23]. GB is a quarterly ammonium compound which is synthesized endogenously in chloroplast as a response to salt and drought environment [24]. Reports showed that foliar applied GB results in increased biomass, leaf pigments, leaf area, proline, primary secondary metabolites, as well as reduction in lipid peroxidation rates in maize under water deficient conditions [25]. In another study, foliar applied GB relieved the pepper plants from low temperature and low light stress via reduction in photoinhibition and oxidative stress [26]. While, Hamani et al. [27] linked exogenous applied GB with stomatal characteristics such as photosynthetic rate (Pn), transpiration rate (Tr), intracellular CO2 concentration (Ci) and stomatal conductance under salt stress. However, comparative studies on Methionine, Lysine, Tryptophan and Glycine betaine under salt stress in terms of morphological, physiological and biochemical attributes in maize are not reported in literature. This study was designed to evaluate the effects of four amino acids individually at different concentrations on maize growth, biomass, leaf pigments, metabolites, and antioxidant enzymes activities under salt stress.

Plant material and growth conditions

Seeds of maize cultivar (YH-5427) were obtained from Ayub Agriculture Research Institute, (AARI) Faisalabad. The pot experiment was conducted in an experimental area of University of Lahore. The laboratory work was performed in General Botany Research Lab, Institute of Molecular Biology and Biotechnology, The University of Lahore. Th experiment was set in January-February, 2022 with following conditions average temperature 12.1°C/53.7°F- 15°C/59°F, Relative humidity 46 − 41% and average sunlight hours/ Day 10–11 hours. Sterilized seeds were sown in plastic pots and arranged in Completely Randomized Design (CRD).

NaCl Stress Treatments

Two weeks old maize plants were subjected under 120 mM salt stress in form of NaCl while control plants were irrigated with normal water (0 mM NaCl). Stress treatments were applied twice with an interval of five days.

Amino acid treatments

After 2 weeks of stress treatments, upon visible symptoms of stress, plants were sprayed with 0 ppm, 25 ppm, 75 pp, 100 ppm of each amino acid (Methionine, Lysine, Tryptophan, Glycine betaine) individually by use of hand sprayer. 0.5% Tween-20 was used as surfactant in each amino acid solution preparation. Foliar application of amino acids were performed 3 times with an interval of 5 days. Approximately, 200–230 ml amino acids solution was applied to each plant in whole duration. Plants were grown for the period of 2 weeks after stress and amino acid applications. All these treatments were applied with 3 replicates. Plant fresh samples were collected for growth attributes and preserved at 20°C for further biochemical analysis.

Determination of maize growth attributes

Total number of leaves were counted and noted for each plant. Shoot and root lengths of plants were measured using scale meter. Fresh and dry biomass of shoot and roots was weighed on an electric balance.

Determination of photosynthetic pigments

Plant pigments such as chl a, chl b, total chlorophyll and carotenoids were determined according to protocol of Arnon et al. [28]. For this purpose, maize leaves (0.05 g) were taken from each treatment in falcon tubes and extracted in 5 ml 80% acetone. The tubes were kept overnight at 4⁰C in freezer. Absorbance was measured on spectrophotometer at different wavelengths 663 nm, 645 nm and 480 nm for chl a, chl b, and carotenoids, respectively

Determination of primary and secondary metabolites

Leaf samples were extracted in phosphate buffer solution (0.2 M) for biochemical examination after 3 weeks of amino acids treatments. Total free amino acids were estimated by Hamilton and Van Slyke (1943) and OD measured at 570 nm. Bradford method[29] was used to determine total soluble proteins in plant leaves. The absorbance of BSA solution was measured at 595 nm on spectrophotometer (UV/V spectrophotometer HALO SB-10). The method described by Pekal and Pyrzynska, (2014) was used to calculate the total flavonoid contents at 465 nm OD. Further the total phenolic content of leaves was assessed using the Folin-Denis reagent as reported by Julkunen-Titto (1985) and OD was measured at 765 nm.

Determination of antioxidant enzymes activities

Fresh maize leaves (500 mg) were homogenized in 5 mL of phosphate buffer (50 mM, pH 7.8) at 4°C. For 15 minutes, this extract was centrifuged at 12,000 rpm. Supernatant was collected in autoclaved eppendrof tubes and used for the determination of peroxidase (POD) and catalase (CAT). CAT and POD activity was determined by using the protocol of Chance & Maehly [30]. SOD activity was measured using the Beauchamp et al. [31] approach. The SOD activity was determined as enzyme unit (EU) on per g fresh basis and per mg protein. For DPPH scavenging assay, 0.1 M DPPH solution SOD was prepared in methanol. One ml sample of each cultivar was taken and mixed with 2 ml of DPPH solution separately. Immediately after mixing the extract with DPPH solution, change in color was observed, which indicated the scavenging activity of plant. After 30 minutes the samples were placed in the spectrophotometer and absorbance was recorded at517 nm [32]. DPPH solution alone was used as a negative control. The whole procedure was performed in triplicate and following formula was used for the calculation of inhibition percentage. Effect of scavenging (%age Inhibition = [1-Xsample (517nm) /X control (517nm)] ×100

Statistical analysis

The experiment data was analyzed by computer based software (STATISTIX 8.1) by analysis of Variance (ANOVA). Pairwise comparison between the groups were taken by Tukey HSD test.

Influence of foliar application of amino acids on growth indices of Maize under saline stress

Irrespective of application of amino acids, shoot and root lengths (cm), fresh and dry biomass (g) and number of leaves in maize were greater in the soil without stress. Under salt stressed condition, an average reduction in shoot length was 23%, root length was 32%, fresh and dry weight of shoot by 51% and 40%, respectively, while, fresh and dry weight of root by 50% and 30% respectively, was recorded in maize plants. Moreover, number of leaves in maize plants were reduced by an average of 20% under salt stressed condition as compared to normal soil. The foliar application of different concentrations (0, 25, 75 and 100 ppm) of amino acids exhibited an improvement in these growth indices as compared to their respective salt stressed plants, although 100ppm concentration of almost all the amino acids exhibited maximum increase in all studied growth indices. In case of shoot length, 100ppm concentrations of methionine(met), tryptophan(tryp) and lysine(lys) exhibited and increase of 32, 33 and 37% more longer roots as compared to their respective controls grown under salt stress. While 75ppm of glycine betaine exhibited maximum 33% increase in shoot length under saline stress condition. In comparison to salt stressed control maize plants, root length showed an increase of 34, 42, 43 and 32% when foliarly treated with 100ppm methionine, tryptophan, glycine betaine and lysine, respectively under salt stress. Fresh biomass of shoots was maximum (69%) when plants were treated with 100ppm tryptophan and lysine, separately, under salt stress followed by the plants (62%) treated with 100ppm glycine betaine. Fresh biomass of root from foliarly applied 100ppm amino acids under stressed condition were in the order glycine betaine > tryptophan > lysine > methionine with respective increase of 80%, 72%, 67% and 59%. Dry biomass of roots from amino acids (100ppm) treated maize plants were in the order of tryp > met > lys > GB with respective increase 62%, 61%, 59% and 26% relative to the stressed plants. Number of leaves per plant exhibited an order of met > tryp > lys > GB with respective increase of 52%, 37%, 33% and 28% as compared to non-treated maize plants under stress. Overall 100 ppm of all the amino acids applied separately performed better in all the studied growth attributes (Table 1)

Influence of foliar application of amino acids on photosynthetic pigments of maize under saline stress

Stress caused negative effect on the pigments (Chl a, b, Total and carotenoids) of the maize plants as compared to the control condition. Under stressed condition chl a, b, total and carotenoids decreased by an average of 36.5%, 37.2%, 37.1% and 23.8%, respectively as compared to their respective controls (Fig. 1). These parameters increased with increasing concentration of each amino acid. At 100ppm concentration of tryptophan an increase of 60% in chlorophyll a was observed followed by methionine (56%) and lysine (55%), while glycine betaine exhibited 42% raise in maize plants grown under saline stress (Fig. 1a). Chlorophyll b showed an order of amino acids, GB > tryp > met > lys with increase of 75%, 65%, 60% and 59%, respectively (Fig. 1b). For total chlorophyll content the order of amino acids with 100ppm concentration was GB > tryp > lys > met showed respective increase of 66%, 64%, 62% and 61% (Fig. 1c). For carotenoid content 100ppm of aminoacids showed descending order as GB > lys > met > tryp with their respective increase of 71%, 70%, 62% and 51% under saline condition (Fig. 1d).

Influence of foliar application of amino acids on metabolites of maize under saline stress

Under saline medium a significant (p ≤ 0.05) increase in the synthesis total free amino acids (TFA) (37%), Total soluble proteins (TSP) (11%), phenolics and flavonoids (68%) as compared to control conditions has been recorded (Fig. 2). Total free amino acids from foliarly applied treatments of amino acids were in the order met > tryp > lys > GB at 100ppm with respective increases of 55%, 46%, 32% and 24% relative to the saline treatment (Fig. 2a). At 100ppm concentration of GB, an increase of 43% in Total Soluble Protein was observed followed by tryptophan (41%) and methionine (32%), while lysine exhibited 8% raise in maize plants grown under saline stress (Fig. 2b). Phenolics from foliarly treated plants were in the order GB > met > tryp > lys with respective increases of 43%, 31%, 30% and 20%, relative to the saline control plants (Fig. 2c). Flavoniods from aminoacids treatments at the concentrations of 100ppm were in the order tryp > met > GB > lys with respective increases of 64%, 55%, 54% and 52% relative to the non treated plants under salt stress (Fig. 2d).

Influence of foliar application of amino acids on antioxidants of maize under saline stress

Results showed that antioxidants were significantly (p ≤ 0.05) influenced by the application of different concentrations (0, 25, 75 and 100 ppm) amino acids as they increased in the saline soil as compared to the non saline soil (Fig. 3). Salt stress significantly (p ≤ 0.05) effects the enzymatic antioxidants including catalase (CAT) by an average of 45%, peroxidase (POD) by 39%, DPPH by 31% and superoxide dismutase (SOD) by 42% as compared to the control plants. CAT from aminoacids treated plants at 100ppm concentration were in the order tryp > lys > met > GB with respective increases of 47%, 46%, 44% and 35%, relative to the control plants under saline condition (Fig. 3a). POD from foliarly treated plants at 100ppm concentration were in the order tryp > lys > met > GB with respective increases of 47%, 46%, 44% and 35%, relative to the control plants under saline condition (Fig. 3b). Irrespective of aminoacids applied in his study, DPPH was increased as compared to its respective control under saline condition. The order of 100ppm aminoacids was lys > GB > tryp > met with respective increase of 54%, 49%, 34% and 33% (Fig. 3c). SOD from foliarly treated plants in reference to aminoacids were in the order tryp > GB > lys > met with increasing perspective of 48%, 46%, 40% and 38% relative to the control saline plants. (Fig. 3d).

Principal Component Analysis

Principal component analysis shows the two most dominant components, PC1 (48.2%) and PC2 (17.1%), accounting for 65.3% variability. The PCA biplot; the length of arrows from the origin point depicted the contribution of each parameter studied in this work. The alignment of arrows with PC1 and PC2 showed positive and negative correlations among parameters. Numericals 1–32 represented various treatments employed in this study. Where numbers 1–16 represented treatments of Methionine, Tryptophane, Glycine, and Lysine at 0, 25, 75, and 100 (unit) in control whereas 17–32 represented these treatments in stressed plants. Measured variables depict two major clusters based on associations among variables. The first group of variables plots in the positive PC1 and PC2 quadrant consisting of parameters including SOD, phenolics, flavonoids, etc. The second group is formed in the positive PC1 and negative PC2 quadrant of the biplot comprising of the parameters including RFW, chlorophyll, and root and shoot lengths. Such divide and trend are a reflection of responses and internal metabolic mechanisms against prevailing environmental stresses (Fig. 4).

Correlation

Data revealed that all the growth, biomass, enzymatic oxidants, metabolites and photosynthetic pigment attributes of maize plants were connected with one another in order to support the veracity of the conclusions above (Fig. 5). All the enzymatic attributes (SOD, CAT, DPPH and POD) and metabolites (primary and secondary) were negatively correlated with chlorophyll contents, biomass as well as growth parameters, however, a significant positive correlation was noticed for chlorophyll and carotenoids contents with the seedling dry weight. Similarly, the phenolics contents were negatively correlated with the Total Soluble Proteins (Fig. 5).

Plants have built up many mechanisms to withstand salts existence inside the cells or for the exclusion of salts out of their cells. The response of crops towards salt stress and their possible strategies may vary from crop to crop [27]. In this regard, the exogenous application of amino acids is a well known agriculture practice worldwide as it links with sustainable agriculture due to amazing role of amino acids in various physiological, biochemical and metabolic processes of plants such as photosynthesis, water relations, nutrient absorption, antioxidant capacity and stress signaling pathways which leads to good quality crops [33]. Therefore, we assessed the effectiveness of four exogenously applied amino acids on maize plant in upregulation of growth and biochemical processes exposed to salt stress. In the current study it is recorded that application of amino acids not only improve the growth indices in the control but also under salt stress which is detrimental for plant health same in the case of maize plants. Among the studied growth factors the application of lysine exhibited maximum increase in shoot length, fresh weight of shoot and dry weight of shoot while glycine betaine positively influenced root length and fresh weigh of root. Among the other two parameters studied, dry weight of root was maximum influenced by the application of tryptophan and number of leaves were maximum under the effect of methionine as compared to the other amino acids applied under salt stress. In line with our findings, the positive role of lysine in form of lysine-chelated zinc and iron-lysine complex exogenous application has been noted to improve the early growth and biomass accumulation in maize under waste water treatment [15, 17, 34]. Further, the foliar application of GB and Tryptophan is found helpful on plant root growth and in reducing biomass loss brought on by salt stress [22, 35].

In comparison to other physiological functions in plants, photosynthetic machinery is very sensitive to stress as pigments reduced under stress. In the present study, cholorophyll content and carotenoids were positively influenced by the application of different concentrations of amino acids, but maximum increase in Chlorophyll a, total chlorophyll and caretonid were recorded under the effect of GB while Chlorophyll b was highest under the effect of tryptophan foliar application under salt stress. In this regard, Hamani et al. [27] also positively linked GB with stomatal characteristics such as an increase of transpiration rate (Tr), stomatal conductance (gs), intracellular CO2 concentration (Ci) and evolution of photosynthetic rate (Pn) in cotton seedlings. Therefore, it is suggested that GB positively influence on photosynthetic machinery and related processes. Similarly, Yasmin et al. [20] also reported that soil applied tryptophan application increased the chlorophyll biosynthesis in maize.

Excessive synthesis of metabolites is always proved to be a shielding effort of the plant under stress environment and the foliar spray of amino acids further increase their content which has been observed in the current study. Where, phenolics and total soluble proteins were increased with the application of glycine betaine while flavonoids and total free amino acids were increased in the effect of tryptophan and methionine, respectively, under salt stress. Our results are quite comparable with reports of Rahman et al. [36] who investigated the regulation of metabolites under foliar application of amino acids.

Under stress condition, the over production of reactive oxygen species (ROS) is always evident as the sign of oxidative stress which causes the improvement of enzymatic antioxidants which has in turn influenced by the tropical application of amino acids. In the present study, catalase and superoxide were increased under the application of tryptophan while superoxide dismutase and DPPH scavenging assay was enhanced under the effect of GB and lysine, respectively, under salt stress. In line with our findings, it has been reported previously, the involvement of GB in efficient scavenging of excess free radicals by upregulating the CAT, POD and SOD enzyme activities via activating the ROS scavenging genes i.e CaSOD, CaCAT, and CaPOD in Capsicum annum [26]. Other reports also highlighted role of other amino acids in activation of these enzymes [11, 12, 37, 38]. Overall, these findings suggests the beneficial role of all amino acids on maize growth, biomass, primary and secondary metabolites, as well as contributes in improving photosynthetic and antioxidant machinery of maize plant subjected under salt stress condition. This data could be useful for farmers and stockholders to formulate amino acids commercial preparations. Further, it is suggested to link or verify this data using latest omics approaches and to investigate the gene expression changes in maize plant after amino acid application by high through put techniques.

Statements & Declarations

Ethical approval and consent to participate

We declare that the manuscript reporting studies do not involve any human participants, human data or human tissues. So, it is not applicable.

Consent for publication

Not applicable

Competing Interests

One of the authors has conflict of interests with Pervaiz Ahmed, Editor BMC Plant Biology.

Funding

Researchers Supporting Project number (RSP2024R393), King Saud University, Riyadh, Saudi Arabia.

Author Contribution

MHA & ZZ; Experimentation, Methodology, HB & NA; Formal analysis and Data curation, ZuN; Supervision and Validation, SU; Statistical analysis, AAS; Resource acquisition and Investigation and SS & MKG; Conceptualization, writing-original draft preparation. All authors read and approved the final manuscript.

Acknowledgement

Authors are thankful to Researchers Supporting Project number (RSP2024R393), King Saud University, Riyadh, Saudi Arabia.

Data Availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Table 1 is available in the Supplementary Files section.

Competing interest reported. One of the authors has conflict of interests with Pervaiz Ahmed, Editor BMC Plant Biology.

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Effect of exogenously applied amino acids on photosynthetic pigments, metabolites and enzymatic antioxidants in Zea mays L. subjected to salt stress

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Version 1

Abstract

Figures

Introduction

Material and Methods

Plant material and growth conditions

NaCl Stress Treatments

Amino acid treatments

Determination of maize growth attributes

Determination of photosynthetic pigments

Determination of primary and secondary metabolites

Determination of antioxidant enzymes activities

Statistical analysis

Results

Influence of foliar application of amino acids on growth indices of Maize under saline stress

Influence of foliar application of amino acids on photosynthetic pigments of maize under saline stress

Influence of foliar application of amino acids on metabolites of maize under saline stress

Influence of foliar application of amino acids on antioxidants of maize under saline stress

Principal Component Analysis

Correlation

Discussion

Declarations

Statements & Declarations

Consent for publication

Funding

Author Contribution

Acknowledgement

Data Availability

References

Tables

Additional Declarations

Supplementary Files

Status:

Version 1