Research Article

Horticultural Science and Technology. 28 February 2020. 9-20
https://doi.org/10.7235/HORT.20200002

ABSTRACT


MAIN

  • Introduction

  • Materials and Methods

  •   Materials

  •   Salicylic Acid and Drought Treatments

  •   Relative Water Content (RWC)

  •   Malondialdehyde (MDA) Content

  •   Total Chlorophyll Content Analysis

  •   Photosynthetic Rate Measurement

  •   Chlorophyll Fluorescence Measurement

  •   Enzyme Extraction for Antioxidant Enzyme Activity Measurement

  •   Catalase (CAT) Activity Assay

  •   Ascorbate Peroxidase (APX) Activity Assay

  •   Glutathione Reductase (GR) Activity Assay

  •   Statistical Analysis

  • Results and Discussion

  •   The Phenotype and Relative Humidity Depend on the Number of SA Treatments

  •   MDA Content Depends on the Number of SA Treatments

  •   Photosynthetic Integrity Depends on SA Treatment

  •   Changes in Antioxidant Enzyme Activities Depend on SA Treatment

  • Conclusion

Introduction

Drought stress influences various environmental factors and has been recognized as an critical factor in agricultural productivity (Yang et al., 2010; Sun et al., 2015; Vurukonda et al., 2016; Lee and Park, 2017). In plants exposed to drought stress, transpiration rates are decreased to maintain intracellular humidity levels, resulting in stomata closure. Absorption of CO2, the backbone of photosynthesis, is inhibited by stomata closure, which in turn is activated by abscisic acid (ABA)- mediated regulation of ion flux (Zhu, 2002; He et al., 2012; Khan et al., 2013a). Proton flux is interrupted by inhibiting photosynthesis, resulting in the formation of reactive oxygen species (ROS) (Mignolet-Spruyt et al., 2016). Plants have evolved various methods to reduce the damage incurred by ROS (Ramel et al., 2012). The activation of antioxidant enzymes like catalase (CAT) in the ascorbate-glutathione (ASC-GSH) cycle is essential for the defense response (Kono and Fridovich, 1982; Hernandez et al., 2000). When oxidative stress exceeds antioxidant capacity, ROS accumulate and cause damage to plants (Møller and Sweetlove, 2010). As such, there is a need to better understand the mechanism by which plants utilize stress defense signaling molecules like ethylene, jasmonic acid (JA), salicylic acid (SA), and Ca+ (Swarbreck et al., 2013; Khan and Khan, 2013b).

Among the different signaling molecules in plants, SA is an important molecule that is known to play a role in stress response (Raskin, 1992; Arfan et al., 2007; Lee et al., 2018). SA signaling regulates stress by influencing photosynthesis (Khan et al., 2012). In response to abiotic stress and the accumulation of ROS, SA inhibits the activity of CAT, leading to induction of H2O2 (Kono and Fridovich, 1982). The induced H2O2 is used as a signaling molecule to activate antioxidant mechanisms that reduce damage caused by ROS (Gechev et al., 2002; Møller and Sweetlove, 2010). Researchers have studied the effect of SA on plant growth for several decades (Hayat et al., 2010; Kazemi et al., 2010). However, some reports have demonstrated the negative effects of using high concentrations of exogenous SA (Pancheva et al., 1996; War et al., 2011). Therefore, it is important to determine optimal concentrations of exogenous SA that should be applied and to monitor the duration during which antioxidants are induced.

Chinese cabbage (Brassica rapa L. spp. pekinensis) is an economically important vegetable in Asia (China, Korea, and Japan) (Eom et al., 2018). Chinese cabbage is well known to be a rich source of functional compounds such as calcium, vitamin, carotenoids, free amino acids, proline, glucosinolates, and antioxidants (Wang et al., 2011). Since Chinese cabbage is an important food in Korea, it is especially important to control the drought stress of the seedlings during cultivation (Bray, 1997; Lee and Park, 2017). The control of drought stress in Chinese cabbage seedlings influences the yield and quality of mature leaves (Shawon et al., 2018). The present study reports that exogenous pretreatment with SA can induce antioxidant capacity in Chinese cabbage seedlings.

Materials and Methods

Materials

The Chinese cabbage (Brassica campestris L.) cultivar named ‘Chooseol’ was used in this study. The seedlings of Chinese cabbage were cultivated in a growth chamber (25°C, relative humidity 60%, 12/12h (light/dark), 200 µmol m-2·s-1) for 39 days. Samples (0.1 g) were collected from the upper side of the sixth leaf of seedlings and stored at ‑70°C.

Salicylic Acid and Drought Treatments

Seedlings were treated with salicylic acid at a 0.1 mM final concentration from an aqueous solution. 500 mL of salicylic acid solution was applied to leaves of 23-day-old Chinese cabbage seedlings. For SA treating group 40 pots each. And analysis were conducted in triplicate. Control plants (without salicylic acid) and those treated for three and six times before stopping irrigation were used for the study. Control seedlings were treated with distilled water instead of the salicylic acid solution.

Drought stress was induced after salicylic acid treatment of 28-day-old seedlings by stopping irrigation for 12 days.

Relative Water Content (RWC)

Relative water content was calculated using the following equation (Misra and Dwivedi, 2004).

$$\mathrm{Relative}\;\mathrm{water}\;\mathrm{content}(\%)=(\mathrm{fresh}\;\mathrm{weight}–\mathrm{dry}\;\mathrm{weight})/\mathrm{fresh}\;\mathrm{weight}\times100$$ (1)

Malondialdehyde (MDA) Content

0.1 g leaf sample was used to measure MDA content. The degree of lipid peroxidation in plant tissues was measured by applying Metwally’s method (Metwally et al., 2003). The MDA content of plants was quantified following reaction with thiobarbituric acid. Using a mortar and pestle, 5 mL of 0.1% (w/v) trichloroacetic acid was added to the homogenized samples. 2 mL of the homogenized sample was scooped up and centrifuged for 5 minutes at 10,000 g. After centrifugation, 0.4 mL of the supernatant was taken and 1.6 mL of 25% (v/v) trichloroacetic acid was added. The mixture was then heated up to 95°C for 15 minutes, after which the reaction was stopped immediately. After centrifuging the mixture at 10,000 g for 5 minutes, the absorbance of the supernatant was measured at 532 nm and 600 nm using a UV-Visible Spectrophotometer (UV-2450, Shimadzu, Kyoto, Japan). The MDA content was determined using a molar extinction coefficient of 155 mmol-1·L-1·cm-1.

Total Chlorophyll Content Analysis

The content of total chlorophyll in plant tissue was measured using 0.1 g of leaf sample by modifying Arnon’s method (Arnon, 1949). The sample was ground using a mortar and pestle and 10 mL of 80% acetone solution was added. The sample was then wrapped in a foil and stored for 7 days at 4°C in the dark. Next, the absorption coefficient of the chlorophyll extracted acetone solution was measured at 645 nm and 663 nm using a UV-Visible Spectrophotometer (UV-2450, Shimadzu, Kyoto, Japan). The chlorophyll content was determined by using the following equation.

$$\mathrm{Total}\;\mathrm{Chlorophyll}\;(µ\mathrm g/\mathrm{mL})\;=\;20.2\;\times\;\mathrm A645\;+\;8.02\;\times\;\mathrm A663$$ (2)

Photosynthetic Rate Measurement

Photosynthetic rates of plant leaves were measured using a Portable Photosynthesis System (LI-6400, Biosciences, USA). Relative humidity was measured as 50 ‑ 60%, CO2 flow rate as 400 mmol/s, chamber temperature at 20°C and light quantity as 200 µmol·m-2·s-1. The upper side of the sixth leaf from a seedling was used to measure photosynthetic rate.

Chlorophyll Fluorescence Measurement

Chlorophyll fluorescence in the leaves of plants was measured using a Chlorophyll Fluorimeter (Pocket Pea; Hansatech, UK). After maintaining the leaves in the dark for 30 minutes, the fluorescence of the leaves, excluding the veins, was measured at 627 nm for 300 µs.

Enzyme Extraction for Antioxidant Enzyme Activity Measurement

2 mL of 25 mM potassium phosphate buffer (pH 7.8) containing 0.4 mM EDTA-4H, 1 mM ascorbic acid, and 2% (w/v) polyvinylpolypyrrolidone were added to a powdered sample and homogenized. The homogenized sample solution was placed in a 2 mL microcentrifuge tube using a micropipette and centrifuged at 15,000 g for 20 minutes. The supernatant obtained was used as a coenzyme extract to measure the antioxidant activities of the enzymes catalase (CAT; EC 1.11.1.6), ascorbate peroxidase (APX; EC 1.11.1.11), and glutathione reductase (GR; EC 1.6.4.2). Total protein was quantified by the Bradford colorimetric method using the coenzyme extract (Bradford, 1976).

Catalase (CAT) Activity Assay

CAT enzyme activity analysis was performed using the method of Aebi (1974). 0.95 mL of the reaction buffer [50 mM potassium phosphate buffer (pH 7.0), 10 mM H2O2] was added to a cubic cell and absorbance at 240 nm was stabilized at 25°C for 30 seconds using a UV-Visible Spectrophotometer (UV-2450, Shimadzu, Kyoto, Japan). 0.05 mL of the crude enzyme extract was then placed in the cubic cell and the change in absorbance was measured for 1 minute.

CAT activity was quantified by the reduction of H2O2 observed upon addition of CAT, and 1 unit was defined as the amount of reduction obtained by 1 µmol enzyme per minute.

Ascorbate Peroxidase (APX) Activity Assay

The analysis of APX enzyme activity was performed as described by Nakano and Asada (1981). 0.94 mL of the reaction buffer [25 mM potassium phosphate buffer (pH 7.0), 0.25 mM AsA (ascorbic acid), 0.1 mM EDTA-4H] was added to a cubic cell, 0.05 mL of the crude enzyme extract was added, and then UV-Visible Spectrophotometer (UV-2450, Shimadzu, Kyoto, Japan) absorbance was stabilized at 290 nm for 30 seconds at 25°C. 10 µL of 10 mM H2O2 was then added to the cubic cell and the change in absorbance was measured for 1 minute.

The activity of APX was calculated as the change in the oxidation rate of AsA used during the reaction of APX, and 1 unit was defined as the amount of reduction obtained by 1 µmol enzyme per minute.

Glutathione Reductase (GR) Activity Assay

GR enzyme activity was analyzed by modifying the method of Foyer and Halliwell (1976). 0.85 ml of the reaction buffer [25 mM potassium phosphate buffer (pH 7.8), 0.06 mM NADPH] was added to a cubic cell and 0.1 mL of the crude enzyme extract was added. It was stabilized at 340 nm for 1 minute 25°C. 10 mM GSSG 0.05 mL was then added in the cubic cell and the change in absorbance was measured for 1 minute.

The activity of GR was calculated as the change in oxidation rate of NADPH used by GR during reaction, and 1 unit was defined as the amount of decrease caused by 1 µmol of reactant per minute.

Statistical Analysis

All experiments and analyses were conducted in a completely randomized design with 3 replicates with individual seedlings for each treatment. Statistical analysis was performed by SAS (version 9.4; SAS Institute, Inc., Cary, NC, USA). Duncan’s multiple range test was used to determine the differences between means (p < 0.05).

Results and Discussion

The Phenotype and Relative Humidity Depend on the Number of SA Treatments

Following 12 days of drought stress, the phenotypes of seedlings were different in response to all treatments. The SA concentration used was established by previous studies, since high concentrations can cause toxicity and low concentrations may not have effects on oxidative stress tolerance (Fariduddin et al., 2003; War et al., 2011; Khan et al., 2015). In the control seedlings, all the leaves were dry, while those treated six times with SA exhibited a phenotype that was less affected by drought stress (Fig. 1). The phenotype depended on the number of treatments and showed an improvement as the number of treatments increased from three to six.

http://static.apub.kr/journalsite/sites/kshs/2020-038-01/N0130380102/images/HST_38_01_02_F1.jpg
Fig. 1.

The effect of exogenous salicylic acid (SA) application on Chinese cabbage seedlings during drought conditions. Photo was taken 12 days after drought treatment. (A) control, (B) three times SA treated, (C) six times SA treated.

The relative water content (RWC) also showed a significant difference. The highest RWC was observed in the six times treated group, while the lowest was in the control. The RWC started to decrease for all the three groups after six days, and the control rapidly decreased by day 12. SA treatment maintained RWC the most in the six times treated group as compared to the untreated (control) group, while the three times treated group maintained RWC better than the control but less than the six times treated group (Fig. 2). During drought stress conditions, reduced plant RWC is a frequently observed phenotype (Siddique et al., 2000).

http://static.apub.kr/journalsite/sites/kshs/2020-038-01/N0130380102/images/HST_38_01_02_F2.jpg
Fig. 2.

The effect of exogenous salicylic acid on relative water content (%) of seedlings under drought stress for 12 days. Error bars indicate ± SD of three replicates. Control: SA untreated; SA three times: SA treated three times; SA six times: SA treated six times.

In the control, the seedlings started to die under drought stress after 9 days at a death rate of 66.7%. Interestingly, death was delayed and the death rate was decreased by treating with SA. This might be the result of a physiological response to SA that increases alternative pathway under stress conditions in plants (Moynihan et al., 1995). Notably, death did not occur until 12 days in the six times treated seedling group (Table 1). The change in RWC in the plants caused by the drought condition occurred internally, showing a form in which the leaves of the plants sagged. In more severe cases, the leaves withered.

Table 1. Death rate (%) of Chinese cabbage seedlings during drought stress conditions. Seedlings were treated with 0.1 mM SA either three or six times before stopping irrigation. Water was sprayed as a control

DAT (days after drought treatment) Control SA treat
Three times Six times
9 22.22 ez 0 g 0 g
10 33.33 d 0 g 0 g
11 41.67 c 20 f 0 g
12 66.67 a 50 b 0 g

zDifferences in the data indicated by the same letters are not statistically significant (p < 0.05)

MDA Content Depends on the Number of SA Treatments

Under drought stress conditions, ROS accumulation results in the oxidation of lipids (Laughton et al., 1989). MDA content is an indicator of plant cell damage caused by lipid peroxidation (Heath and Packer, 1968).

In our study, the untreated control seedlings showed higher MDA content than the other treatments. The MDA content in untreated seedlings increased during all of the drought stress conditions. It slowly increased up to 6 days, and rapidly increased after 6 days. Furthermore, when the Chinese cabbage seedlings were treated with SA, it was found that MDA contents were remarkably low, indicating these plants had less damage than the untreated controls. However, the six times SA treated seedlings had slightly higher MDA contents than the three times SA treated seedlings. This was perhaps due to the fact that SA initially induced H2O2, which quickly decreased (Fig. 3). Overall, six times SA treated seedlings showed the lowest MDA contents after 12 days. These results suggest that pretreatment with SA equips the cabbage seedlings to counter oxidative stress (Belkhadi et al., 2010; Saruhan et al., 2012).

http://static.apub.kr/journalsite/sites/kshs/2020-038-01/N0130380102/images/HST_38_01_02_F3.jpg
Fig. 3.

The effect of exogenous SA on malondialdehyde (MDA) content (nmol·ml-1) under drought stress conditions. Error bars indicate ± S.D. of three replicates. Control: SA untreated; SA three times: SA treated three times; SA six times: SA treated six times.

Photosynthetic Integrity Depends on SA Treatment

Plant growth begins with photosynthesis and progresses through a series of primary metabolism processes (Schwachtje and Baldwin, 2008; Detmann et al., 2012). Additionally, photosynthesis has a significant effect on plant growth and leaf yield (Detmann et al., 2012). If photosynthesis in plants is hindered, plant growth can be inhibited because of insufficient CO2 fixation in the stroma of chloroplasts (Schurr et al., 2006; Schwachtje and Baldwin, 2008). Therefore, photosynthesis is important for the growth of plants and plant growth directly depends on the efficiency of the photosynthetic apparatus.

In our present research, we analyzed the photosynthesis rate, chlorophyll fluorescence, and chlorophyll contents. The PI(ABS) value obtained through the measurement of chlorophyll fluorescence indicates the efficiency of the photosystems, the reaction center where photosynthesis occurs (Mathur et al., 2011). We have shown that in untreated seedlings, photosynthetic efficiency was significantly reduced. On the contrary, the groups treated with SA showed about 1.5 times more efficient photosynthesis than the non-treated group, with the six times SA treated seedlings showing the most efficient photosynthesis (Fig. 4A)

http://static.apub.kr/journalsite/sites/kshs/2020-038-01/N0130380102/images/HST_38_01_02_F4.jpg
Fig. 4.

The effect of exogenous SA on chlorophyll fluorescence. (A) total chlorophyll content (µg/ml), (B) and photosynthetic rate (µmol CO2 m-2 s-1), (C) in drought condition for 12 days. Error bars indicate ± S.D. of three replicates. Differences in the data indicated by the same letters are not statistically significant (p < 0.05). Control: SA untreated; SA three times: SA treated three times; SA six times: SA treated six times.

The total chlorophyll content was analyzed to determine the capacity to perform photosynthesis (Dai et al., 2009). The chlorophyll content tended to decrease during the 12 days after drought stress condition. When compared to the control, the SA treated group showed a similar tendency to the untreated group up to 9 days, but unlike the untreated group, which had a sharp decrease, the SA treated group contained a steady amount of chlorophyll even on day 12 (Fig. 4B).

Measuring photosynthetic performance and its capacity, we found that the photosynthetic rate decreased by about 10% up to 3 days after irrigation was stopped, after which the rate increased until day 6. After that, the photosynthetic rate drastically decreased. The photosynthesis rate decreased from 6 day after the irrigation was interrupted, and the rate of the untreated SA seedlings converged close to zero. However, the SA treated group showed a higher photosynthetic rate than the untreated group (Fig. 4C).

The photosynthetic performance of the photosystems, as determined by chlorophyll fluorescence, decreased in the untreated SA group (Fig. 4A). A similar trend was also observed in the analysis of the total amount of chlorophyll (Fig. 4B).

The photosynthesis rate, which is highly related to plant growth and is a result of internal physiological activity of plants, started to decrease slightly after irrigation was stopped (Fig. 4C) (Schurr et al., 2006). This is presumed to be the result of ABA-mediated closing of the stoma to prevent water loss under drought stress conditions, due to interrupted irrigation (Miyashita et al., 2005). Later, the photosynthesis rate increased up to 6 days after irrigation was stopped (Fig. 4C). This is presumed to be the mechanism by which plants gain energy through reprogramming, equilibrating, and maximizing the photosynthesis rate after survival under drought stress conditions (Chaves et al., 2009).

Our investigation of the photosynthetic apparatus revealed that SA treatment was effective in maintaining and improving the efficiency of photosynthesis. Furthermore, we showed that when plants were placed under drought stress conditions, they underwent reprogramming to maintain their physiological growth.

Changes in Antioxidant Enzyme Activities Depend on SA Treatment

Plants experience abiotic stress under extreme conditions of water and temperature (Sharma and Dubey, 2005; Hu et al., 2008). Under abiotic stress, ROS accumulate in plants and can damage biomolecules including lipids, proteins, and nucleic acids (Smirnoff, 1993; Munne-Bosch and Penuelas, 2003). Antioxidants counter ROS and thus play a vital role in maintaining homeostasis in plant cells under stress conditions (Kadioglu et al., 2011).

The present study analyzed the antioxidant enzymes catalase (CAT), ascorbate peroxidase (APX), and glutathione deductase (GR), all of which are known to protect plant cells from ROS-induced damage (Møller, 2001). In the absence of SA treatment, CAT activity decreased up to 6 days after stopping irrigation and then increased afterwards. This trend was similar in the two SA treated groups. However, in the treated groups, the extent of decrease in activity was lower and the day of lowest activity was delayed (Fig. 5A).

http://static.apub.kr/journalsite/sites/kshs/2020-038-01/N0130380102/images/HST_38_01_02_F5.jpg
Fig. 5.

The effect of exogenous SA on antioxidant activity related to drought tolerance. (A) catalase activity (µmol H2O2 degradation·min-1·mg protein-1), (B) ascorbate peroxidase activity (µmol H2O2 degradation·min-1·mg protein-1), (C) glutathione reductase activity (µmol NADPH degradation·min-1·mg protein-1) under drought stress conditions for 12 days. Error bars indicate ± S.D. of three replicates. Control: SA untreated; SA three times: SA treated three times; SA six times: SA treated six times.

We observed similar trends for APX and GR activities. In the case of APX, without SA treatment, the enzyme activity decreased until day 3, and then increased afterwards. Following SA treatment, the lowest point of enzyme activity was delayed or not observed. In the case of the three times treated seedlings, the enzyme activity was delayed by 3 days, whereas in the six times treated seedlings, the enzyme activity continued to increase until day 12 (Fig. 5B). In the case of GR, without SA treatment, the enzyme activity decreased up to day 3 and then increased. For the SA treated groups, there were no significant changes in the enzyme activity (Fig. 5C).

Based on previous findings, we believe that the accumulation of ROS due to drought stress results in decreased enzyme activity in the untreated group (Janda et al., 2003). Later on, cellular reprogramming, which increases the antioxidant activity in plants to regain energy in extreme environments (e.g., drought stress), also increases enzyme activity in the untreated group (Chaves et al., 2009; Kocsy et al., 2013).

Additionally, treatment with SA decreased the activity of CAT on day 0. This is presumably because SA initially inhibits the activity of CAT by enhancing the accumulatio of H2O2, which may be used as a signal transduction agent to activate antioxidant mechanisms (Landberg and Greger, 2002; Janda et al., 2003).

Conclusion

The present research reports the benefits of treating Chinese cabbage seedlings, which are affected by drought stress, with SA. Chinese cabbage seedlings are usually transplanted when they are grown for about 3 ‑ 6 weeks. Oftentimes, plants have poor rooting when transplanting, so they can easily be affected by drought stress caused by insufficient water absorption (Sasaki, 2004). Thus, it is very important to manage ROS homeostasis in seedlings during transplantation. In the case of Chinese cabbage seedlings damaged by drought stress, the seedlings displayed decreased relative water content, lower rates of photosynthesis, and enhanced lipid peroxidation. We show that pretreatment of the Chinese cabbage seedlings with SA rescues the negative physiological responses while positively impacting the phenotype of the seedlings. This might be caused by altered signal transduction following exogenous SA treatment (Raskin, 1992). SA plays an important role as a signaling molecule in seedlings, which induces antioxidant activities, alleviates lipid peroxidation, protect the photosynthetic apparatus, and ultimately results in overcoming drought stress. Thus, we propose that SA pretreatment of Chinese cabbage seedlings may be useful as an effective control measure to combat drought stress. In support of this, we demonstrated that the best results were obtained after treating seedlings six times with 0.1 mM SA.

Acknowledgements

This work was supported by the 2017 sabbatical year research grant of the University of Seoul.

Author Contributions Statement

This study was designed and managed by Ie-Sung Shim. Seongmin Kim, JicHyun Lee and YeRyung Cha prepared and performed the experiment and analysis. YeRyung Cha wrote this manuscript.

Compliance with Ethical Standards

The authors declare that they have no conflict of interest.

References

1
Aebi H (1974) Catalase. In Methods of enzymatic analysis. Academic press, Cambridge, Massachusetts, pp 673-684. doi:10.1016/B978-0-12-091302-2.50032-3
10.1016/B978-0-12-091302-2.50032-3
2
Arfan M, Athar HR, Ashraf M (2007) Does exogenous application of salicylic acid through the rooting medium modulate growth and photosynthetic capacity in two differently adapted spring wheat cultivars under salt stress? J Plant Physiol 164:685-694. doi:10.1016/j.jplph.2006.05.010
10.1016/j.jplph.2006.05.01016884826
3
Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1. doi:10.1104/pp.24.1.1
10.1104/pp.24.1.116654194PMC437905
4
Belkhadi A, Hediji H, Abbes Z, Nouairi I, Barhoumi Z, Zarrouk M, Djebali W (2010) Effects of exogenous salicylic acid pre-treatment on cadmium toxicity and leaf lipid content in Linum usitatissimum L. Ecotoxicol Environ Saf 73:1004-1011. doi:10.1016/j.ecoenv.2010.03.009
10.1016/j.ecoenv.2010.03.00920399499
5
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254. doi:10.1016/0003-2697(76)90527-3
10.1016/0003-2697(76)90527-3
6
Bray EA (1997) Plant responses to water deficit. Trends Plant Sci 2:48-54. doi:10.1016/S1360-1385(97)82562-9
10.1016/S1360-1385(97)82562-9
7
Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: Regulation mechanisms from whole plant to cell. Ann Bot 103:551-560. doi:10.1093/aob/mcn125
10.1093/aob/mcn12518662937PMC2707345
8
Dai Y, Shen Z, Liu Y, Wang L, Hannaway D, Lu H (2009) Effects of shade treatments on the photosynthetic capacity, chlorophyll fluorescence, and chlorophyll content of Tetrastigma hemsleyanum Diels et Gilg. Environ Exp Bot 65:177-182. doi:10.1016/j.envexpbot.2008.12.008
10.1016/j.envexpbot.2008.12.008
9
Detmann KC, Araújo WL, Martins SC, Sanglard LM, Reis JV, Detmann E, DaMatta FM (2012) Silicon nutrition increases grain yield, which, in turn, exerts a feed‐forward stimulation of photosynthetic rates via enhanced mesophyll conductance and alters primary metabolism in rice. New Phytol 196:752-762. doi:10.1111/j.1469-8137.2012.04299.x
10.1111/j.1469-8137.2012.04299.x22994889
10
Eom S, Baek S A, Kim J, Hyun T (2018) Transcriptome analysis in Chinese cabbage (Brassica rapa ssp. pekinensis) provides the role of glucosinolate metabolism in response to drought stress. Molecules 23:1186. doi:10.3390/molecules23051186
10.3390/molecules2305118629762546PMC6099646
11
Fariduddin Q, Hayat S, Ahmad A (2003) Salicylic acid influences net photosynthetic rate, carboxylation efficiency, nitrate reductase activity, and seed yield in Brassica juncea. Photosynthetica 41:281-284. doi:10.1023/B:PHOT.0000011962.05991.6c
10.1023/B:PHOT.0000011962.05991.6c
12
Foyer CH, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplasts: A proposed role in ascorbic acid metabolism. Planta 133:21-25. doi:10.1007/BF00386001
10.1007/BF0038600124425174
13
Gechev TS, Gadjev I, Van Breusegem F, Inzé D, Dukiandjiev S, Toneva V, Minkov I (2002) Hydrogen peroxide protects tobacco from oxidative stress by inducing a set of antioxidant enzymes. Cell Mol Life Sci 59:708-714. doi:10.1007/s00018-002-8459-x
10.1007/s00018-002-8459-x12022476
14
Hayat Q, Hayat S, Irfan M, Ahmad A (2010) Effect of exogenous salicylic acid under changing environment: A review. Environ Exp Bot 68:14-25. doi:10.1016/j.envexpbot.2009.08.005
10.1016/j.envexpbot.2009.08.005
15
He J, Duan Y, Hua D, Fan G, Wang L, Liu Y, Chen Z, Han L, Qu LJ, et al. (2012) DEXH box RNA helicase-mediated mitochondrial reactive oxygen species production in Arabidopsis mediates crosstalk between abscisic acid and auxin signaling. Plant Cell 24:1815-1833. doi:10.1105/tpc.112.098707
10.1105/tpc.112.09870722652060PMC3442571
16
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189-198. doi:10.1016/0003-9861(68)90654-1
10.1016/0003-9861(68)90654-1
17
Hernandez J, Jimenez A, Mullineaux P, Sevilla F (2000) Tolerance of pea plants (Pisum sativum) to long-term salt stress is associated with induction of antioxidant defences. Plant Cell Environ 23:853-862. doi:10.1046/j.1365-3040.2000.00602.x
10.1046/j.1365-3040.2000.00602.x
18
Hu WH, Song XS, Shi K, Xia XJ, Zhou YH, Yu JQ (2008) Changes in electron transport, superoxide dismutase and ascorbate peroxidase isoenzymes in chloroplasts and mitochondria of cucumber leaves as influenced by chilling. Photosynthetica 46:581. doi:10.1007/s11099-008-0098-5
10.1007/s11099-008-0098-5
19
Janda T, Szalai G, Rios-Gonzalez K, Veisz O, Páldi E (2003) Comparative study of frost tolerance and antioxidant activity in cereals. Plant Sci 164:301-306. doi:10.1016/S0168-9452(02)00414-4
10.1016/S0168-9452(02)00414-4
20
Kadioglu A, Saruhan N, Sağlam A, Terzi R, Acet T (2011) Exogenous salicylic acid alleviates effects of long term drought stress and delays leaf rolling by inducing antioxidant system. Plant Growth Regul 64:27-37. doi:10.1007/s10725-010-9532-3
10.1007/s10725-010-9532-3
21
Kazemi N, Khavari-Nejad RA, Fahimi H, Saadatmand S, Nejad-Sattari T (2010) Effects of exogenous salicylic acid and nitric oxide on lipid peroxidation and antioxidant enzyme activities in leaves of Brassica napus L. under nickel stress. Sci Hortic 126:402-407. doi:10.1016/j.scienta.2010.07.037
10.1016/j.scienta.2010.07.037
22
Khan MIR, Fatma M, Per TS, Anjum NA, Khan NA (2015) Salicylic acid-induced abiotic stress tolerance and underlying mechanisms in plants. Front Plant Sci 6:462. doi:10.3389/fpls.2015.00462
10.3389/fpls.2015.00462
23
Khan MIR, Iqbal N, Masood A, Per TS, Khan NA (2013a) Salicylic acid alleviates adverse effects of heat stress on photosynthesis through changes in proline production and ethylene formation. Plant Signal Behav 8:e26374. doi:10.4161/psb.26374
10.4161/psb.2637424022274PMC4091357
24
Khan MIR, Khan NA (2013b) Salicylic acid and jasmonates: Approaches in abiotic stress. J Plant Biochem Physiol 1:e113. doi:10.4172/2329-9029.1000e113
10.4172/2329-9029.1000e113
25
Khan NA, Nazar R, Iqbal N, Anjum NA (2012) Phytohormones and Abiotic Stress Tolerance in Plants. Springer Science and Business Media. doi:10.1007/978-3-642-25829-9
10.1007/978-3-642-25829-9
26
Kocsy G, Tari I, Vanková R, Zechmann B, Gulyás Z, Poór P, Galiba G (2013) Redox control of plant growth and development. Plant Sci 211:77-91. doi:10.1016/j.plantsci.2013.07.004
10.1016/j.plantsci.2013.07.00423987814
27
Kono Y, Fridovich I (1982) Superoxide radical inhibits catalase. J Biol Chem 257:5751-5754
28
Landberg T, Greger M (2002) Differences in oxidative stress in heavy metal resistant and sensitive clones of Salix viminalis. J Plant Physiol 159:69-75. doi:10.1078/0176-1617-00504
10.1078/0176-1617-00504
29
Laughton MJ, Halliwel B, Evans PJ, Robin J, Hoult S (1989) Antioxidant and pro-oxidant actions of the plant phenolics quercetin, gossypol and myricetin: Effects on lipid peroxidation, hydroxyl radical generation and bleomycin-dependent damage to DNA. Biochem Pharmacol 38:2859-2865. doi:10.1016/0006-2952(89)90442-5
10.1016/0006-2952(89)90442-5
30
Lee G, Lee G, Yu J, Kim Y, Park Y (2018) Correlation network analysis of abiotic stress-related genes reveals the coordinated regulation of transcription in Chinese cabbage. Hortic Sci Technol 36:266-279. doi:10.12972/kjhst.20180027
10.12972/kjhst.20180027
31
Lee G, Park Y (2017) A co-expression network of drought stress-related genes in Chinese cabbage. Hortic Sci Technol 35:243-251. doi:10.12972/kjhst.20170027
10.12972/kjhst.20170027
32
Mathur S, Jajoo A, Mehta P, Bharti S (2011) Analysis of elevated temperature‐induced inhibition of photosystem II using chlorophyll a fluorescence induction kinetics in wheat leaves (Triticum aestivum). Plant Biol 13:1-6. doi:10.1111/j.1438-8677.2009.00319.x
10.1111/j.1438-8677.2009.00319.x21143718
33
Metwally A, Finkemeier I, Georgi M, Dietz KJ (2003) Salicylic acid alleviates the cadmium toxicity in barley seedlings. Plant Physiol 132:272-281. doi:10.1104/pp.102.018457
10.1104/pp.102.01845712746532PMC166972
34
Mignolet-Spruyt L, Xu E, Idä nheimo N, Hoeberichts FA, Mü hlenbock P, Brosché M, Van Breusegem F, Kangasjä rvi J (2016) Spreading the news: Subcellular and organellar reactive oxygen species production and signaling. J Exp Bot 67:3831-3844. doi:10.1093/jxb/erw080
10.1093/jxb/erw08026976816
35
Misra N, Dwivedi UN (2004) Genotypic difference in salinity tolerance of green gram cultivars. Plant Sci 166:1135-1142. doi:10.1016/j.plantsci.2003.11.028
10.1016/j.plantsci.2003.11.028
36
Miyashita K, Tanakamaru S, Maitani T, Kimura K (2005) Recovery responses of photosynthesis, transpiration, and stomatal conductance in kidney bean following drought stress. Environ Exp Bot 53:205-214. doi:10.1016/j.envexpbot.2004.03.015
10.1016/j.envexpbot.2004.03.015
37
Møller IM (2001) Plant mitochondria and oxidative stress: Electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annu Rev Plant Biol 52:561-591. doi:10.1146/annurev.arplant.52.1.561
10.1146/annurev.arplant.52.1.56111337409
38
Møller IM, Sweetlove LJ (2010) ROS signalling - specificity is required. Trends Plant Sci 15:370-374. doi:10.1016/j.tplants.2010.04.008
10.1016/j.tplants.2010.04.00820605736
39
Moynihan MR, Ordentlich A, Raskin I (1995) Chilling-induced heat evolution in plants. Plant Physiol 108:995-999. doi:10.1104/pp.108.3.995
10.1104/pp.108.3.99512228523PMC157449
40
Munne-Bosch S, Penuelas J (2003) Photo-and antioxidative protection, and a role for salicylic acid during drought and recovery in field-grown Phillyrea angustifolia plants. Planta 217:758-766. doi:10.1007/s00425-003-1037-0
10.1007/s00425-003-1037-012698367
41
Pancheva TV, Popova LP, Uzunova AN (1996) Effects of salicylic acid on growth and photosynthesis in barley plants. J Plant Physiol 149:57-63. doi:10.1016/S0176-1617(96)80173-8
10.1016/S0176-1617(96)80173-8
42
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867-880
43
Ramel F, Birtic S, Ginies C, Soubigou-Taconnat L, Triantaphylidès C, Havaux M (2012) Carotenoid oxidation products are stress signals that mediate gene responses to singlet oxygen in plants. Proc Natl Acad Sci USA 109:5535-5540. doi:10.1073/pnas.1115982109
10.1073/pnas.111598210922431637PMC3325660
44
Raskin I (1992) Role of salicylic acid in plants. Annu Rev Plant Biol 43:439-463. doi:10.1146/annurev.pp.43.060192.002255
10.1146/annurev.pp.43.060192.002255
45
Saruhan N, Saglam A, Kadioglu A (2012) Salicylic acid pretreatment induces drought tolerance and delays leaf rolling by inducing antioxidant systems in maize genotypes. Acta Physiol Plant 34:97-106. doi:10.1007/s11738-011-0808-7
10.1007/s11738-011-0808-7
46
Sasaki R (2004) Characteristics and seedling establishment of rice nursling seedlings. JARQ-Jpn Agric Res Q 38:7-13. doi:10.6090/jarq.38.7
10.6090/jarq.38.7
47
Schurr U, Walter A, Rascher U (2006) Functional dynamics of plant growth and photosynthesis-from steady-state to dynamics-from homogeneity to heterogeneity. Plant Cell Environ 29:340-352. doi:10.1111/j.1365-3040.2005.01490.x
10.1111/j.1365-3040.2005.01490.x17080590
48
Schwachtje J, Baldwin IT (2008) Why does herbivore attack reconfigure primary metabolism? Plant Physiol 146:845-851. doi:10.1104/pp.107.112490
10.1104/pp.107.11249018316639PMC2259057
49
Sharma P, Dubey RS (2005) Drought induces oxidative stress and enhances the activities of antioxidant enzymes in growing rice seedlings. Plant Growth Regul 46:209-221. doi:10.1007/s10725-005-0002-2
10.1007/s10725-005-0002-2
50
Smirnoff N (1993) The role of active oxygen in the response of plants to water deficit and desiccation. New Phytol 125:27-58. doi:10.1111/j.1469-8137.1993.tb03863.x
10.1111/j.1469-8137.1993.tb03863.x
51
Siddique MRB, Hamid AIMS, Islam MS (2000) Drought stress effects on water relations of wheat. Bot Bull Acad Sinica 41
52
Shawon RA, Kang BS, Kim HC, Lee SG, Kim SK, Lee HJ, Bae JH, Ku YG (2018) Changes in free amino acid, carotenoid, and proline content in Chinese Cabbage (Brassica rapa subsp. Pekinensis) in Response to Drought Stress. Korean J Plant Res 31:622-633
53
Sun C, Li X, Hu Y, Zhao P, Xu T, Sun J, Gao X (2015) Proline, sugars, and antioxidant enzymes respond to drought stress in the leaves of strawberry plants. Korean J Hortic Sci Technol 33:625-632. doi:10.7235/hort.2015.15054
10.7235/hort.2015.15054
54
Swarbreck SM, Colaco R, Davies JM (2013) Plant calcium-permeable channels. Plant Physiol 163:514-522. doi:10.1104/pp.113.220855
10.1104/pp.113.22085523860348PMC3793033
55
Vurukonda SS, Vardharajula S, Shrivastava M, SkZ A (2016) Enhancement of drought stress tolerance in crops by plant growth promoting rhizobacteria. Microbiol Res 184:13-24. doi:10.1016/j.micres.2015.12.003
10.1016/j.micres.2015.12.00326856449
56
Wang H, Wu J, Sun S, Liu B, Cheng F, Sun R, Wang X (2011) Glucosinolate biosynthetic genes in Brassica rapa. Gene 487:135-142. doi:10.1016/j.gene.2011.07.021
10.1016/j.gene.2011.07.02121835231
57
War AR, Paulraj MG, War MY, Ignacimuthu S (2011) Role of salicylic acid in induction of plant defense system in chickpea (Cicer arietinum L.). Plant Signal Behav 6:1787-1792. doi:10.4161/psb.6.11.17685
10.4161/psb.6.11.1768522057329PMC3329353
58
Yang S, Vanderbeld B, Wan J, Huang Y (2010) Narrowing down the targets: Towards successful genetic engineering of drought-tolerant crops. Mol Plant 3:469-490. doi:10.1093/mp/ssq016
10.1093/mp/ssq01620507936
59
Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247-273. doi:10.1146/annurev.arplant.53.091401.143329
10.1146/annurev.arplant.53.091401.14332912221975PMC3128348
페이지 상단으로 이동하기