ABSTRACT
ABSTRACT
In plants, cell wall bound phenolics change in response to stress. The aim of the study was to investigate the effect of NaCl induced stress on wall bound phenolics in four rice varieties, of which two (Bhutnath, Nonabokra) were salt tolerant and two (MTU 7029, Sujala) were salt sensitive. After germination, seedlings were grown in hydroponic solution and subjected to salinity stress (25 mM, 50 mM, 100 mM and 150 mM NaCl) on day 12. Wall bound phenolic compounds were determined by GC-MS based metabolite analysis. Total seven wall bound phenols were identified from the leaf tissues and eight from the root tissues. Ferulic acid and 4-hydroxycinnamic acid were found in all the four varieties. After NaCl treatment, these two wall bound phenols increased in the leaves of tolerant varieties only. Significant inverse correlation between leaf length and leaf fresh weight with wall bound ferulic acid and 4-hydroxycinnamic acid in Nonabokra suggests the positive role of these wall bound phenolics in salt tolerance.
Introduction
Salinity, the abiotic stress, limits crop production by increasing salinization of arable land and would result in up to 50% land loss by the year 2050.1 Plants respond to salinity by altering morphological, physiological, and biochemical processes. Rice, the most important cereal crop in the world, is the staple food for over half of the world's population.2 More than 90% of world's rice is produced and consumed in Asia.3 But increasing salinity in the deltas of Asian rivers due to rise in sea level4 is a matter of concern as rice is relatively salt sensitive amongst cereals.5 The yield of this crop can be significantly affected in presence of even 50 mM NaCl.6 So it is important to understand the responses of different rice varieties to salinity to develop enhanced salt tolerant rice through breeding.
Responses to salinity induced stress in rice has recently been reviewed.7 Different mechanisms to cope with salinity stress include biosynthesis and accumulation of organic osmolytes (e.g., sugars, polyols, amino acids, methylamines, urea etc.); ion homoeostasis and compartmentation; detoxification of Reactive Oxygen (ROS) Species through production of antioxidants.7 Salt tolerant Pokkali rice seedlings showed higher activity of ROS scavenging enzymes and the nonenzymatic antioxidants e.g., ascorbate, glutathione than the variety Pusa Basmati.8 Tolerance to salinity in Pokkali has been suggested to be derived largely from the constitutively maintained antioxidant enzymatic activities as well as induced antioxidant enzymes.9 In our previous study, elevation of signalling molecules gentisic acid and serotonin in the salt tolerant rice varieties Nonabokra and Bhutnath has been reported.10 In spite of different studies involving morphology, physiology and metabolism to understand responses to salt stress, little attention has been paid to the changes of wall bound phenolic compounds in rice.
Phenolic compounds are present in plants either in free form or in bound form. The bound phenolic compounds are ester linked to cell wall polymers. In cereals, phenolic compounds are found to be bound to cell wall, in which ferulic acid and its derivatives are the major ones.11 Cell walls of Graminae contain significant amounts of ferulic acid and p-coumaric acid, esterified to matrix polysaccharides.12-13 Ferulic acid bound to the cell walls can form diferulic bridges and through such bridges they are cross-linked among cell wall polysaccharides that would lead to a decrease in cell wall extensibility.14
Cell wall bound phenolics change in response to stress. Date palm root cell walls contain four wall bound phenolics such as p-hydroxybenzoic acid, p-coumaric acid, ferulic acid and sinapic acid which confer resistance to the action of cell wall-degrading enzymes of Fusarium oxysporum f. Sp. albedinis and the phenolics are reported to be present two times higher in resistant cultivars than in susceptible cultivars of date palm.15 Poaceae plants have previously been reported to increase wall bound phenolics. Wall bound ferulic acid, p-coumaric acid, and sinapic acid increased by salt stress and along with wall bound increased peroxidase enzyme activity contributed to the stiffening of cell wall during different leaf developmental stages in Aeluropus littoralis.16 In two genotypes of winter triticale (X Triticosecale Wittmack) also it was reported that ability to accumulate increased cell wall bound ferulic acid in the leaves under drought condition might be a reliable biochemical parameter indicating the plants draught resistance.17
In the present study, we investigated the effect of salinity stress on cell wall bound phenols in four rice varieties among which two were salt tolerant varieties and two were salt sensitive varieties.
Results
Totally eight wall bound phenolics were identified from the leaves and roots of the seedlings of four indica rice varieties with or without NaCl treatment. The results showed great variability in the presence of such phenolic compounds. However, ferulic acid and 4-hydroxycinnamic acid (Synonym p-coumaric acid) were detected in all the samples of leaf (Fig. 1) and root (Fig. 2) in all the varieties. Occasional detection of other phenolic metabolites in the leaves is presented in Table 1.
Published online:
17 October 2017Figure 1. Changes in length, fresh weight, ferulic acid, and 4-hydroxycinnamic acid in leaf in response to different concentrations of NaCl. Y axis represents cmX1000 (mean ± se) for leaf length, mg X 100 (mean ± se) for leaf fresh weight, relative response ratio of phenolic metabolites per g leaf fresh weight (mean ± se); R2 values indicate significant increase or decrease with increase in salinity.
![]({"type":"image","src":"/na101/home/literatum/publisher/tandf/journals/content/kpsb20/2017/kpsb20.v012.i10/15592324.2017.1379643/20171017/images/medium/kpsb_a_1379643_f0001_oc.gif"})
Figure 1. Changes in length, fresh weight, ferulic acid, and 4-hydroxycinnamic acid in leaf in response to different concentrations of NaCl. Y axis represents cmX1000 (mean ± se) for leaf length, mg X 100 (mean ± se) for leaf fresh weight, relative response ratio of phenolic metabolites per g leaf fresh weight (mean ± se); R2 values indicate significant increase or decrease with increase in salinity.
Published online:
17 October 2017Figure 2. Changes in length, fresh weight, ferulic acid, and 4-hydroxycinnamic acid in root in response to different concentrations of NaCl. Y axis represents cmX1000 (mean ± se) for root length, mg X 100 (mean ± se) for root fresh weight, relative response ratio of phenolic metabolites per g root fresh weight (mean ± se); R2 values indicate significant increase or decrease with increase in salinity.
![]({"type":"image","src":"/na101/home/literatum/publisher/tandf/journals/content/kpsb20/2017/kpsb20.v012.i10/15592324.2017.1379643/20171017/images/medium/kpsb_a_1379643_f0002_oc.gif"})
Figure 2. Changes in length, fresh weight, ferulic acid, and 4-hydroxycinnamic acid in root in response to different concentrations of NaCl. Y axis represents cmX1000 (mean ± se) for root length, mg X 100 (mean ± se) for root fresh weight, relative response ratio of phenolic metabolites per g root fresh weight (mean ± se); R2 values indicate significant increase or decrease with increase in salinity.
Table 1. Wall bound phenolics occasionally detected.
Ferulic acid content increased significantly (240 ± 21 fold at 25 mM, 303 ± 54 fold at 50 mM, 630 ± 216 fold at 100 mm, and 759 ± 133 fold at 150 mM) in the cell wall with the increasing concentration of NaCl (R2 = 0.962), in the leaves of the tolerant variety Nonabokra. In Bhutnath leaf, there was also increase in the level of wall bound ferulic acid with increase of NaCl content (1.3 ± 0.4 fold at 25 mM, 2.9 ± 0.8 fold at 50 mM, 1.3 ± 0.2 fold at 100 mM and 1.4 ± 0.1 fold at 150 mM) (not statistically significant at all concentrations). There was significant increase in 4-hydroxycinnamic acid level (43 ± 4 fold at 25 mM, 43 ± 7 fold at 50 mM, 74 ± 28 fold at 100 mM, and 135 ± 19 fold at 150 mM) with increase in concentration of NaCl (R2 = 0.947) in Nonabokra leaves. The other salt tolerant variety Bhutnath showed increase (not statistically significant) in the level of this metabolite (1.1 ± 0.1 fold at 25 mM, 1.7 ± 0.3 fold at 50 mM and 100 mM, 1.2 ± 0.1 fold at 150 mM NaCl concentrations). In the leaves of the sensitive variety Sujala, ferulic acid and 4-hydroxycinnamic acid content showed a general trend of decrease except significant increase at 150 mM salt concentration (5.7 ± 0.6 and 3.5 ± 0.3 fold respectively) only. In the leaves of the sensitive variety MTU 7029, these hydroxycinnamic acids either decreased or did not exhibit significant changes (Figs. 1 & 2).
There were significant dose dependent decreases (R2 > 0.6) in leaf length and leaf fresh weight with increase in NaCl content in all the varieties (Fig. 1). Interestingly, Nonabokra revealed significant inverse correlation in wall bound ferulic acid content and leaf length (r = −0.96917) and leaf fresh weight (r = −0.93445). Sujala, although a salt sensitive variety, also showed significant inverse correlation of ferulic acid with leaf length (r = −0.852855) due to high increase of this metabolite at 50 mM NaCl. The other two varieties did not show such significant correlation between ferulic acid content and leaf length and fresh weight. Wall bound 4-hydroxycinnamic acid also showed significant inverse correlation with leaf length (r = −0.97703) and leaf fresh weight (r = −0.806455) in Nonabokra. In Sujala also, there was significant inverse correlation between leaf length and 4-hydroxycinnamic acid content. But in other varieties, such correlations were not significant (Table 2).
Table 2. Correlation between metabolites and length/fresh weight with increase in NaCl concentration.
Root length in Nonabokra and Sujala decreased significantly with increase in NaCl concentration. Root fresh weight decreased significantly in Nonabokra and Bhutnath with increase in salinity (Fig. 2). In the roots, both ferulic acid and 4-hydroxycinnamic acid decreased in the tolerant variety Nonabokra, and the sensitive variety MTU 7029. Bhutnath root also showed a trend of decrease in ferulic acid content in response to NaCl induced stress. However, 4-hydroxycinnamic acid level showed a trend of increase in Bhutnath (2.6 ± 0.5 fold at 25 mM, 1.6 ± 0.1 fold at 50 mM, 0.7 ± 0.07 fold at 100 mM, and 1.6 ± 0.4 fold at 150 mM NaCl). In Sujala, however, both of these phenols also showed a trend of increase in response to NaCl induced stress being high at 50 mM (29 ± 17 fold for ferulic acid, 14 ± 6 fold for 4-hydroxycinnamic acid) and 150 mM (17.7 ± 4.9 fold for ferulic acid, 12.8 ± 1.7 fold for 4-hydroxycinnamic acid) NaCl concentrations. Inverse correlation existed between root fresh weight and 4-hydroxycinnamic acid content for both the metabolites in Sujala. Positive correlation between the decrease in root fresh weight and the decrease in these wall bound metabolites were significant in Nonabokra (r = 0.84729 for ferulic acid, r = 0.7215 for 4-hydroxycinnamic acid), and MTU 7029 (r = 0.9985 for ferulic acid, r = 0.9807 for 4-hydroxycinnamic acid) (Table 2). However, the ratios of leaf/root length and leaf / root fresh weight remained unchanged in all the varieties after treatment with different NaCl concentrations. But the ratios of ferulic acid in leaf and root and that of 4-hydroxycinnamic acid were high in Nonabokra and MTU 7029, decreased in Sujala (except ferulic acid at 100 mM NaCl treatment). Bhutnath showed mild increase in ferulic acid ratio in leaf and root (Table 3).
Table 3. Ratio of length, fresh weight, relative response ratio of phenolic metabolites in leaf and root.
It was also interesting to note that the mean relative response ratios (per g fresh weight) of ferulic acid in the leaves of the salt tolerant varieties (111 in Nonabokra and 12416 in Bhutnath) were significantly lower than that in the sensitive varieties (29418 in MTU 7029 and 27170 in Sujala) under control condition without NaCl induced stress. Similarly for 4-hydroxycinnamic acid also the mean relative response ratios were lower in the tolerant varieties (253 in Nonabokra and 9774 in Bhutnath) than that in the sensitive varieties (13295 in MTU 7029 and 26886 in Sujala) in the leaves under control condition. And the tolerant varieties, particularly Nonabokra containing very low level of ferulic acid and 4-hydroxycinnamic acid, showed significant high increase in the level of these wall bound phenolic compounds, after treatment with NaCl.
Discussion
During the present study maximum increase in wall bound ferulic acid and 4-hydroxycinnamic acid was observed in the variety Nonabokra, considered to be one of the most salt tolerant varieties and the salt tolerance donor in classical breeding.18-19 The other tolerant variety Bhutnath also showed a trend of increase in these wall bound phenolics, although there was no significant dose dependent correlation. Wall bound ferulic acid and 4-hydroxycinnamic acid from Nonabokra leaf also showed significant inverse correlation between increased wall bound phenolics and decreased leaf length and fresh weight. This suggests that the increased level of ferulic acid and 4-hydroxycinnamic acid may have contributed to the survival of Nonabokra in saline condition better than the other varieties.
Cell wall phenolic characteristics have previously been correlated to cell growth. The deposition of ferulic acid and diferulic acid in cell wall was suggested to be related to the cessation of internodal elongation of floating rice.20-21 Progressive accumulation of wall phenolics was also suggested to be related to inhibition of wall extensibility and root growth by water deficit in maize.22 Light induced increase in cell wall bound ferulic acid and diferulic acid was related to growth inhibition in Avena coleoptile.23 Increased wall bound ferulic acid and other phenolics were also related to stiffening of cell wall in leaf of A. littoralis under salt stress.16 The results of the present study also suggests superiority of Nonabokra variety to other varieties for salt tolerance in terms of increased level of cell wall bound ferulic acid and 4-hydroxycinnamic acid with increase of NaCl concentration and their significant inverse correlation with leaf length and leaf fresh weight. Future work on the biochemical changes involving key enzymes related to phenol metabolism is required.
Salinity induces oxidative stress responsible for much of the crop damage. Increased radical production in salt tolerant varieties was protected by antioxidant enzymes.24 Previous studies reported changes in the level of the antioxidant enzymes in the salt tolerant rice varieties. Nonabokra showed better performance than the variety Pokkali, with lesser accumulation of sodium ion in the leaves, several fold increase in proline content, less loss of chlorophyll content. Nonabokra was a better performer by greater induction of phenolics, proline, low lipid peroxidation, moderate free radical accumulation and sustaining high guaiacol peroxidase activity. Their results confirmed that the variety Nonabokra was less prone to oxidative damage and free radicals than Pokkali.25
It has been reported that hydroxycinnamic acids from the cell wall act as reductants and are auto-oxidizable.26-27 Involvement of ROS scavenging through the wall bound phenolics may also be a mechanism of salt tolerance in Nonabokra.
Plants possess a rapid, systematic communication network mediated through signals transmitted between the distant sites within the organism.28 Such rapid long distance signals are responsible for initiating a multitude of physiological responses.29 Further research is required to unravel such complex mechanisms of salt tolerance in this important crop plant.
Materials and methods
Plant materials
Seeds of four varieties of rice (Oryza sativa L.) Nonabokra, Bhutnath, Sujala and MTU 7029 or Swarna were obtained from Rice Research Station, Chinsurah, Directorate of Agriculture, Government of West Bengal, India.
Chemicals
All the chemicals have been purchased from Merck Specialities Pvt. Ltd., India.
Plant growth and treatment conditions
Seeds, after surface sterilization with 5% sodium hypochlorite solution for 15 min, followed by washing with distilled water, were germinated on moist filter paper for 3 days in dark in petridishes. Emerged seedlings were transferred near the rim of culture tubes, inside covered with blotting paper. One fourth of the tube was filled with hydroponic nutrient solution composed of 2 mM Ca(NO3)2, 5 mM KNO3, 5 mM NH4NO3, 2 mM MgSO4, 0.1 mM KH2PO4, 0.5 mM Na2SiO3, 0.05 mMNaFe(III)EDTA, 5 µM MnCl2, 5 µM ZnSO4, 0.5 µM CuSO4, 0.1 µM NaMoO3, and 5 µM H3BO3.30 Two seedlings were grown in one culture tube for 12 days. Temperature was set at 32 ± 2 °C with photo periodic condition 12 h light and 12 h darkness (photon flux intensity 135 µmol/min/s). Seedlings were treated with NaCl (25 mM, 50 mM, 100 mM and 150 mM) on seventh day after germination. Root and shoot parts were harvested separately and immediately shock frozen by liquid nitrogen. The root and shoot of the control and NaCl treated plant materials were crushed separately in liquid nitrogen and homogenized into powder.
Extraction of wall bound phenols
Powdered material (120–150 mg) was extracted with methanol in microcentrifuge tube. The residual material, after centrifugation, was continuously stirred with 20% DMSO for 24 h to remove starch. Complete hydrolysis of all the materials was done by amylase for 3 h and the hydrolyzed materials were washed thoroughly by water, acetone, methanol:chloroform (1:1 v/v), methanol and water. Extraction with 20 mM ammonium oxalate (pH 4.0) at 70 °C for 2 h was carried out. The residue was suspended in 1M NaOH solution containing 0.05 mg/ml NaBH4 and stirred for 24 h. After complete hydrolysis, the mixture was centrifuged and the supernatant was acidified to pH 2.0 with HCl and then extracted with ethyl acetate.20 Ethyl acetate extract was evaporated to dryness.
Gas Chromatography-Mass Spectrometry (GC-MS) analysis
Determination of wall bound phenolics was carried out by GC-MS based metabolite analysis. The extracts were derivatized for 90 min at 28°C with methoxyamine hydrochloride in pyridine (5 µl of 20 mg/ml) followed by a 30 min shaking with 45 µl of N-methyl-N-(trimethylsilyl)trifluoroacetamide at 37 °C for trimethylsilylation of acidic protons to increase volatility of metabolites. FAME markers dissolved in chloroform was used as Retention Index (RI) markers. GC-MS analysis was carried out using Agilent 7890 A GC equipped with 5975C inert MSD with Triple Axis Detector. HP-5MS capillary column (Agilent J&W GC columns, USA) was used. The analysis was done with oven temperature programme set as 1 min hold at 60°C to 325°C (at 10°C/min ramp), hold for 10 min before cooling down (37.5 min total run time). MSD transfer line and ion source were set at 290°C and 230°C respectively. Helium was used as carrier gas with flow rate of 0.723 ml/min (carrier linear velocity 31.141 cm/sec).31 For identification of metabolites, using automated mass spectral deconvolution and identification system (AMDIS) to deconvolute resulting chromatogramme. Fragmentation pattern of mass spectra and retention time were compared with those present in Agilent Fiehn GC/MS Metabolomics RTL library (Agilent Technologies, USA, 2008) for identification of peaks.All the phenolic metabolites, except 3-hydroxyflavonewas further authenticated by comparing the Rt and mass spectral fragmentation pattern with that of pure metabolites. Peak area obtained from the wall bound phenols was normalized by dividing it with fresh weight of the sample to obtain relative response ratios.
Statistical analysis
The differences in values between the control and treated samples were tested for significance by t-test (p < 0.05 considered as statistically significant). Fold changes (mean ± standard error), ratios (mean ± standard error), correlation coefficient (r), and linear regression (R-squared value) were calculated using Microsoft Excel.
| Sujala | MTU 7029 | Bhutnath | Nonabokra | |||||
|---|---|---|---|---|---|---|---|---|
| Metabolites | Leaf | Root | Leaf | Root | Leaf | Root | Leaf | Root |
| 4-Hydroxybenzoic acid | ||||||||
| 0 mM | − | − | − | − | − | − | − | − |
| 25 mM | − | − | − | − | − | − | − | − |
| 50 mM | − | − | − | − | − | − | − | − |
| 100 mM | − | − | − | − | − | − | − | − |
| 150 mM | + | − | − | − | − | − | − | − |
| 4-Hydroxy-3-methoxybenzoic acid | ||||||||
| 0 mM | − | − | − | − | − | − | − | − |
| 25 mM | − | − | − | − | − | − | − | − |
| 50 mM | + | + | + | − | − | + | − | − |
| 100 mM | + | − | − | − | − | − | − | − |
| 150 mM | + | − | − | − | − | − | − | − |
| Quinic acid | ||||||||
| 0 mM | − | − | − | − | − | |||
| 25 mM | − | + | − | − | + | − | − | − |
| 50 mM | − | + | − | + | − | − | − | − |
| 100 mM | − | + | − | − | − | − | − | − |
| 150 mM | − | + | − | − | − | − | − | − |
| Gallic acid | ||||||||
| 0 mM | − | − | − | − | − | − | − | − |
| 25 mM | − | + | − | − | + | − | − | − |
| 50 mM | − | − | − | + | − | − | + | − |
| 100 mM | − | + | − | − | − | + | + | − |
| 150 mM | − | − | − | − | − | − | + | − |
| Hydroquinone | ||||||||
| 0 mM | − | − | − | − | − | − | − | − |
| 25 mM | − | − | − | − | − | − | − | − |
| 50 mM | − | − | − | − | − | − | + | − |
| 100 mM | − | − | − | − | − | − | − | − |
| 150 mM | − | − | − | − | − | − | − | − |
| Shikimic acid | ||||||||
| 0 mM | − | − | − | − | − | − | − | − |
| 25 mM | − | + | − | − | − | − | − | − |
| 50 mM | − | − | − | − | − | − | − | − |
| 100 mM | − | − | − | − | − | − | − | − |
| 150 mM | − | − | − | − | − | − | − | − |
| 3-Hydroxyflavone | ||||||||
| 0 mM | − | − | − | − | − | − | − | − |
| 25 mM | − | − | − | − | − | − | − | − |
| 50 mM | − | − | − | + | − | − | − | − |
| 100 mM | − | − | − | − | − | − | − | − |
| 150 mM | − | − | − | − | − | − | − | − |
| Alizarin | ||||||||
| 0 mM | − | − | − | − | − | − | − | − |
| 25 mM | − | − | − | + | − | − | − | − |
| 50 mM | − | − | − | − | − | − | − | − |
| 100 mM | − | − | − | − | − | − | − | − |
| 150 mM | − | − | − | − | − | − | − | − |
| Correlation (r) | |||
|---|---|---|---|
| Variety | Length or fresh wt | Ferulic Acid | 4-Hydroxycinnamic acid |
| Nonabokra | Leaf length | −0.969174665 | −0.977030575 |
| Leaf fresh weight | −0.934452305 | −0.806455426 | |
| Root length | 0.437201307 | 0.23386357 | |
| Root fresh weight | 0.847291223 | 0.721523028 | |
| Bhutnath | Leaf length | 0.316615796 | −0.414585213 |
| Leaf fresh weight | −0.045968442 | −0.389720892 | |
| Root length | 0.312606163 | 0.52877445 | |
| Root fresh weight | 0.545237535 | −0.043330208 | |
| MTU 7029 | Leaf length | 0.129072852 | 0.112923187 |
| Leaf fresh weight | 0.324576582 | −0.128161325 | |
| Root length | 0.785222211 | 0.776605499 | |
| Root fresh weight | 0.99858058 | 0.980728224 | |
| Sujala | Leaf length | −0.852855484 | −0.765852372 |
| Leaf fresh weight | −0.628089629 | −0.546341117 | |
| Root length | −0.412769409 | −0.561114033 | |
| Root fresh weight | −0.633039635 | −0.753108621 | |
| Concentration of NaCl (mM) | |||||
|---|---|---|---|---|---|
| 0 | 25 | 50 | 100 | 150 | |
| Leaf/Root length | |||||
| Nonabokra | 1.46 ± 0.02 | 1.43 ± 0.03 | 1.53 ± 0.03 | 1.83 ± 0.04 | 2.03 ± 0.06 |
| Bhutnath | 1.47 ± 0.02 | 1.34 ± 0.04 | 1.36 ± 0.05 | 1.25 ± 0.03 | 1.10 ± 0.03 |
| MTU 7029 | 2.91 ± 0.08 | 3.12 ± 0.28 | 2.86 ± 0.10 | 2.45 ± 0.12 | 2.56 ± 0.19 |
| Sujala | 1.27 ± 0.02 | 1.28 ± 0.02 | 1.33 ± 0.02 | 1.31 ± 0.03 | 1.18 ± 0.04 |
| Leaf/Root fresh weight | |||||
| Nonabokra | 1.00 ± 0.03 | 1.01 ± 0.01 | 0.96 ± 0.02 | 0.99 ± 0.03 | 0.98 ± 0.02 |
| Bhutnath | 1.00 ± .01 | 1.01 ± 0.01 | 1.01 ± 0.01 | 1.00 ± 0.01 | 1.01 ± 0.01 |
| MTU 7029 | 1.01 ± 0.02 | 1.00 ± 0.02 | 1.00 ± 0.01 | 1.00 ± 01 | 1.00 ± 0.01 |
| Sujala | 0.99 ± 0.02 | 0.98 ± 0.02 | 0.98 ± 0.02 | 0.97 ± 0.02 | 0.97 ± 0.01 |
| Leaf/Root 4-hydroxycinnamic acid | |||||
| Nonabokra | 0.01 ± 0.00 | 14 ± 2.13 | 9.4 ± 5 | 272075 ± 102922 | 5.2 ± 1.65 |
| Bhutnath | 0.18 ± 0.06 | 0.13 ± 0.01 | 0.30 ± 0.06 | 0.82 ± 0.20 | 0.26 ± 0.05 |
| MTU 7029 | 0.21 ± 0.06 | 2.4 ± 1.3 | 4.7 ± 2.7 | 3.72 ± 1.85 | 4.67 ± 3.06 |
| Sujala | 8.52 ± 5.03 | 1.21 ± 0.47 | 0.50 ± 0.22 | 0.90 ± 0.27 | 0.88 ± 0.15 |
| Leaf/Root ferulic acid | |||||
| Nonabokra | 0.10 ± 0.09 | 216635 ± 18995 | 245818 ± 108990 | 1005433 ± 344934 | 642253 ± 324421 |
| Bhutnath | 1.005 ± 0.4 | 0.79 ± 0.21 | 1.83 ± 0.49 | 3.67 ± 0.77 | 1.66 ± 0.35 |
| MTU 7029 | 3.47 ± 1.82 | 15 ± 6.53 | 44546 ± 18420 | 240731 ± 80714 | 234416 ± 112259 |
| Sujala | 193469 ± 99793 | 18674 ± 4949 | 1.82 ± 0.54 | 81459 ± 26507 | 12.62 ± 4.05 |
Acknowledgments
This work was supported by West Bengal State Council of Science and Technology under grant 104/WBSCST/F/0520/14. We also acknowledge Government of India (FIST programme) for instrumental facility, and Dr. Santanu Aich, Rice Research Station Chinsurah, for his help in plant material collection.
References
- Wang W, Vinocur B, Altman AA. Plant responses to drought, salinity and extreme temperatures: Towards genetic engineering for stress tolerance. Planta. 2003;218:1–14. doi:10.1007/s00425-003-1105-5. [Crossref], [PubMed], [Web of Science ®], [Google Scholar]
- Zhai CK, Lu CM, Zang Q, Sun GJ, Lorenz KJ. Comparative study on nutritional value of Chinease and North American wild rice. J Food Compost Anal. 2001;14:371–382. doi:10.1006/jfca.2000.0979. [Crossref], [Web of Science ®], [Google Scholar]
- Khush G. What it will take to feed 5.0 billion rice consumers in 2030. Plant Mol Biol. 2005;59:1–6. doi:10.1007/s11103-005-2159-5. [Crossref], [PubMed], [Web of Science ®], [Google Scholar]
- Dayton L. Agribiotechnology: Blue-sky rice. Nature. 2014;514:S52–S54. doi:10.1038/514S52a. [Crossref], [PubMed], [Web of Science ®], [Google Scholar]
- Kavita PG, Miller AJ, Mathew MK, Maathuis FJ. Rice cultivars with differing salt tolerance contain similar cation channels in their root cells. J Exp Bot. 2012;63:3289–3296. doi:10.1093/jxb/ers052. [Crossref], [PubMed], [Web of Science ®], [Google Scholar]
- Yeo A, Flowers T. Salinity resistance in rice (Oryza sativa L.) and a pyramiding approach to breeding varieties for saline soils. Australian J Plant Physiol. 1986;13:161–173. doi:10.1071/PP9860161. [Crossref], [Google Scholar]
- Hoang TML, Tran TN, Nguyen TKT, Williams B, Wurm P, Bellairs S, Mundree S. Improvement of salinity stress tolerance in rice: challenges and opportunities. Agronomy. 2016;6:54. doi:10.3390/agronomy6040054. [Crossref], [Web of Science ®], [Google Scholar]
- Vaidyanathan H, Sivakumar P, Chakrabarty R, Thomas G. Scavenging of reactive oxygen species in NaCl-stressed rice (Oryza sativa L.)-differential response in salt tolerant and sensitive varieties. Plant Sci. 2003;165:1411–1418. doi:10.1016/j.plantsci.2003.08.005. [Crossref], [Web of Science ®], [Google Scholar]
- HeeLee M, Cho E, Wi S, Bae H, Kim JE, Cho JY, Lee S, Kim JH, Chung B. Divergences in morphological changes and antioxidant responses in salt-tolerant and salt-sensitive rice seedlings after salt stress. Plant Physiol Biochem. 2013;70:325–335. doi:10.1016/j.plaphy.2013.05.047. [Crossref], [PubMed], [Web of Science ®], [Google Scholar]
- Gupta P, De B. Metabolomics analysis of rice responses to salinity stress revealed elevation of serotonin, and gentisic acid levels in leaves of tolerant varieties. Plant Signal Behav. 2017;12:e1335845. doi:10.1080/15592324.2017.1335845. [Taylor & Francis Online], [Google Scholar]
- Bonoli M, Marconi E, Caboni MF. Free and bound phenolic compounds in barley (Hordeum vulgare L.) flours: Evaluation of the extraction capability of different solvent mixtures and pressurized liquid methods by micellar electrokinetic chromatography and spectrophotometry. J Chromatogr A. 2004;1057:1–12. doi:10.1016/j.chroma.2004.09.024. [Crossref], [PubMed], [Web of Science ®], [Google Scholar]
- Harris PJ, Hartley RD. Detection of bound ferulic acid in the cell walls of the graminae by ultraviolet fluorescence microscopy. Nature. 1976;259:508–510. doi:10.1038/259508a0. [Crossref], [Web of Science ®], [Google Scholar]
- Shibuya N. Phenolic acids and their carbohydrate esters in rice endosperm cell walls. Phytochemistry. 1984;23:2233–2237. doi:10.1016/S0031-9422(00)80526-9. [Crossref], [Web of Science ®], [Google Scholar]
- Fry SC. Cross-linking of matrix polymers in the growing cell walls of angiosperms. Annual Rev Plant Physiol. 1986;37:165–186. doi:10.1146/annurev.pp.37.060186.001121. [Crossref], [Google Scholar]
- Modafar CE, Boustani EE. Cell wall bound phenolic acid and lignin contents in date palm as related to its resistance to Fusarium oxysporum. Biologia Plantarum. 2001;44:125–130. doi:10.1023/A:1017942927058. [Crossref], [Web of Science ®], [Google Scholar]
- Haghighi L, Majd A, Nematzadeh G, Shokri M, Kelij S, Irian S. Salt-induced changes in cell wall peroxidise (CWPRX) and phenolic content of Aeluropus littoralis (Willd) Parl. Australian J Crop Sci. 2014;8(2):296–300. [Google Scholar]
- Hura T, Hura K, Grzesiak S. Possible contribution of cell-wall-bound ferulic acid in drought resistance and recovery in triticale seedlings. J Plant Physiol. 2009;166(16):1720–1733. doi:10.1016/j.jplph.2009.04.012. [Crossref], [PubMed], [Web of Science ®], [Google Scholar]
- Kurotani KI, Kazumasa Y, Yosuke T, Daisuke O, Maiko T, Hirotsugu K, Hidemitsu N, Makoto H, Hiroaki I, Tsukaho H, Shin T. Stress tolerance profiling of a collection of extant salt tolerant rice varieties and transgenic plants over expressing abiotic stress tolerance genes. Plant Cell Physiol. 2015;56:1867–1876. doi:10.1093/pcp/pcv106. [Crossref], [PubMed], [Web of Science ®], [Google Scholar]
- Moons A, Bauw G, Prinsen E, Montagu MV, Straeten DVD. Molecular and physiological responses to abscisic acid and salts in roots of salt-sensitive and salt-tolerant indica rice varieties. Plant Physiol. 1995;107:177–186. doi:10.1104/pp.107.1.177. [Crossref], [PubMed], [Web of Science ®], [Google Scholar]
- Azuma T, Okita N, Nanmori T, Yasuda T. Changes in cell wall bound phenolic acids in the internodes of submerged floating rice. Plant Prod Sci. 2005;8:441–446. doi:10.1626/pps.8.441. [Taylor & Francis Online], [Web of Science ®], [Google Scholar]
- Azuma T, Okita N, Nanmori T, Yasuda T. Relationship between the deposition of phenolic acids in the cell walls and the cessation of rapid growth in internodes of floating rice. Plant Prod Sci. 2005;8:447–453. doi:10.1626/pps.8.447. [Taylor & Francis Online], [Web of Science ®], [Google Scholar]
- Fan L, Linker R, Gepstein S, Tanimoto E, Yamamoto R, Neumann PM. Progressive inhibition by water deficit of cell wall extensibility and growth along the elongation zone of maize roots is related to increased lignin metabolism and progressive stelar accumulation of wall phenolics. Plant Physiol. 2006;140:603–612. doi:10.1104/pp.105.073130. [Crossref], [PubMed], [Web of Science ®], [Google Scholar]
- Miyamoto K, Veda J, Takeda S, Ida K, Hoson T, Masuda Y, Kamisaka S. Light induced increase in the contents of ferulic and diferulic acids in cell walls of Avena coleoptiles: its relationship to growth inhibition by light. Physiologia Plantarum. 1994;92:350–355. doi:10.1111/j.1399-3054.1994.tb05347.x. [Crossref], [Web of Science ®], [Google Scholar]
- Dionisio-Sese ML, Tobita S. Antioxidant responses of rice seedlings to salinity stress. Plant Sci. 1998;135:1–9. doi:10.1016/S0168-9452(98)00025-9. [Crossref], [Web of Science ®], [Google Scholar]
- Ghosh N, Adak MK, Ghosh PD, Gupta S, Sen Gupta DN, Mandal C. Differential responses of two rice varieties to salt stress. Plant Biotechnol Rep. 2011;5:89–103. doi:10.1007/s11816-010-0163-y. [Crossref], [Web of Science ®], [Google Scholar]
- Takahama U. Oxidation of vacuolar and apoplastic phenolic substrates by peroxidise: physiological significance of the oxidation reactions. Phytochem Rev. 2004;3:207–219. doi:10.1023/B:PHYT.0000047805.08470.e3. [Crossref], [Google Scholar]
- Kukavica B, Mojovic M, Vuccinic Z, Maksimovic V, Takahama U, Jovanovic SV. Generation of hydroxyl radical in isolated pea root cell wall bound peroxidise, Mn-SOD and phenolics in their production. Plant Cell Physiol. 2009;50:304–317. doi:10.1093/pcp/pcn199. [Crossref], [PubMed], [Web of Science ®], [Google Scholar]
- Choi WG, Toyota M, Kim SH, Hilleary R, Gilroy S. Salt stress-induced Ca2+ waves are associated with rapid, long-distance root-to-shoot signaling in plants. Proc Natl Acad Sci U S A. 2014;111:6497–6502. doi:10.1073/pnas.1319955111. [Crossref], [PubMed], [Web of Science ®], [Google Scholar]
- Stephan AB, Schroeder JI. Plant salt stress status is transmitted systemically via propagating calcium waves. Proc Natl Acad Sci U S A. 2014;111:6126–6127. doi:10.1073/pnas.1404895111. [Crossref], [PubMed], [Web of Science ®], [Google Scholar]
- Widodo , Patterson JH, Newbigin E, Tester M, Bacic A, Roessner U. Metabolic responses to salt stress of barley (Hordeum vulgare L.) cultivars, Sahara and Clipper, which differ in salinity tolerance. J Exp Bot. 2009;60:4089–4103. doi:10.1093/jxb/erp243. [Crossref], [PubMed], [Web of Science ®], [Google Scholar]
- Das S, Dutta M, Chaudhury K, De B. Metabolomic and chemometric study of Achras sapota L. fruit extracts for identification of metabolites contributing to the inhibition of α-amylase and α-glucosidase. European Food Res Technol. 2016;242:733–743. doi:10.1007/s00217-015-2581-0. [Crossref], [Web of Science ®], [Google Scholar]