|Year : 2019 | Volume
| Issue : 1 | Page : 72-77
High-temperature condition increases lignanoid biosynthesis of Schisandra chinensis seeds via reactive oxygen species
Guo Huimin, Wang Jiahui, Gao Huiru, Meng Xiangcai
Department of Pharmacognosy, Heilongjiang University of Chinese Medicine, Harbin, China
|Date of Web Publication||20-Feb-2019|
Prof. Meng Xiangcai
School of Pharmaceutical Sciences, Heilongjiang University of Chinese Medicine, 24 Heping Road, Harbin 150040
Source of Support: None, Conflict of Interest: None
| Abstract|| |
Introduction: The herbal medicine used in many countries came mainly from the wild in the past; now, declining yield resource and laborious gathering result in prevailing cultivated medicine, with a result of prevailing inferior quality of herbal medicine. The contents of major functional ingredients varies greatly in the fruits of Schisandra chinensis, a herbal medicine in many Asian countries. Materials and Methods: These fruits were placed at 20°C, 35°C, 45°C, and 55°C for 1–6 days, respectively, covered with plastics to prevent cells from anhydration during treating. The contents of H2O2, phenylalanine, and lignanoids and activities of antioxidant enzymes and phenylalanine ammonia lyase (PAL) were monitored. Results: The fresh seeds were exposed to 35°C, 45°C, and 55°C for 1 week; the H2O2 was rose sharply at 1 day and then declined but still with a higher level. The superoxide dismutase, catalase, and peroxidase activities were lowered, with inefficient antioxidant capacity. The PAL activities had a certain degree of high-temperature tolerance, remained largely unchanged at 35°C, but reduced gradually as temperature increased. High temperature activated the glycolytic pathway and rose the phenylalanine contents, which increased sharply at 1 day for 35°C and 45°C and at the 2 days for the 55°C and then maintained a stable level with almost 1–3 times than the 0 day. Conclusions: The increased phenylalanine as substrate accelerated the synthesis of lignanoids; the contents of five lignanoids were increased by as much as 31.2%–81.5%, respectively.
Abbreviations Used: ROS: Reactive oxygen species; SOD: Superoxide dismutase; CAT: Catalase; POD: Peroxidase; PAL: Phenylalanine ammonia lyase.
Keywords: Environmental stress, lignanoids, phenylalanine, Schisandra chinensis, secondary metabolism
|How to cite this article:|
Huimin G, Jiahui W, Huiru G, Xiangcai M. High-temperature condition increases lignanoid biosynthesis of Schisandra chinensis seeds via reactive oxygen species. Phcog Res 2019;11:72-7
|How to cite this URL:|
Huimin G, Jiahui W, Huiru G, Xiangcai M. High-temperature condition increases lignanoid biosynthesis of Schisandra chinensis seeds via reactive oxygen species. Phcog Res [serial online] 2019 [cited 2019 Nov 12];11:72-7. Available from: http://www.phcogres.com/text.asp?2019/11/1/72/252569
- The abscised fresh fruits of Schisandra chinensis are live organisms and remain intrinsic total metabolic system. The fresh fruits were exposed to high-temperature condition, the antioxidase was lowered, the phenylalanine ammonia lyase activities also did gradually as temperature increased, but the glycolytic pathway was activated, and the phenylalanine contents were increased, enhancing the synthesis of lignanoids. “↑” and “↓” represent activity or content “up” and “down,” respectively.
| Introduction|| |
The herbal medicine used in many countries came mainly from the wild in the past; now, declining yield resource and laborious gathering result in prevailing cultivated medicine. The major functional ingredients of herbal medicine, usually the secondary metabolites, are to prevent plant from stress environment; therefore, its contents varies depending on the environment, with a result of prevailing inferior quality of herbal medicine, even have a word, “traditional Chinese medicine would come down,” “the traditional Chinese medicine would be destroyed by herbal medicine.” China has used the herbal medicine for several years; the conversion of herbal medicine from wild to cultivation threatened to the survival of traditional Chinese medicine. The Chinese Government promulgated “Good Agriculture Practice for Chinese crude drugs” to control various factors affecting the production quality of medicinal plant materials and further to ensure that traditional Chinese medicine herbs are authentic, safe, effective, and consistent in quality. Besides China, many countries have taken a series of standardized measures concerning quality control of production of raw materials for natural medicines, but all these pay attention to production procedure, not to specific active ingredient relevant to the effect, with a little success. How to improve the quality of herbal medicine is emphasis and difficulty. The clarification of herbal medicine ingredients' biosynthesis may be a reasonable way to improve cultivated herbal medicine.
Different species have a highly specific trait to acclimate various environment; even the different organs or tissues of the same species may vary significantly. Schisandra chinensis (Turcz.) Baill. is a deciduous, perennial vine from Magnoliaceae, habitat in the bushes. Its fruits ripen in the autumn, but the seeds, still in the heart-shaped embryo stage, will take another 3 months to further grow and develop after abscission  and have to undergo frequently various stresses such as high temperature, drought, and microbes, during germination. A simple change during this critical life stage may threaten germination. Therefore, S. chinensis is a better species to investigate into seeds against the environment.
There were two primary sides for plant damage by stress: physical and mechanical injury and chemical injury. The physical and mechanical injury derives mainly from the low temperature, pests, etc., whereas the chemical injury mainly from the high temperature, water deficit, saline-alkali soil, environmental contamination, etc., Animals can dodge dreadful conditions, but plants must be disturbed by various environmental stresses. One of the major consequences of stress is the excess generation of reactive oxygen species (ROS), with a result of oxidative stress., For this reason, the plant develops a exclusively secondary metabolism pathway to combating the stress. The secondary metabolites, responsible for the enhanced stress tolerance, are produced by induction of ROS. The lignanoids in S. chinensis fruit, such as schizandrol A, schizandrol B, shiandrin A, shiandrin B, and shiandrin C, with neuroregulation, liver protection, antioxidation, and anti-allergic effects, are used as medicine in most Asian countries. Therefore, an exhaustive research into the secondary metabolites has been done. The previous study showed the secondary metabolites of S. chinensis fruit are able to detoxify ROS,, biosynthesized by phenylalanine ammonia lyase (PAL). PAL, a typical of inducible enzymes, can respond to various unfavorable circumstance quickly; even within 10 min under 40°C, the hypericin biosynthesis in Hypericum perforatum L. cells can be enhanced. Thus, the phenylpropanoid metabolic pathway is far more susceptible to circumstance than any other pathways. The lignanoids relate to the temperature and rainfall, which vary greatly between producing areas.,,,
Plants are constantly challenged by various ever-changing abiotic stresses under which plants generate and accumulate ROS. The stresses are various, and their essence of influencing on plants are all ROS. One of them is H2O2, which plays a major role in tolerance. Earlier research has found some interesting facts that plants possess cross-resistance, meaning that one stress can result in increased tolerance of another stresses. Heat hock not only raises heat resistance but also induces tolerance to chilling, drought, and salinity and heavy metal in different plant species.,,, High-temperature stress can result in cellular damage and even cell death. At germination, seeds tolerate various environmental stresses such as drought, high temperature, and microbes, but the high temperature was manipulated easier. Plants can produce ROS during high-temperature stresses; therefore, exposure of S. chinensis seeds can easily promote the biosynthesis of lignanoids and provide an avenue for improved herbal medicine quality.
| Materials and Methods|| |
Medicinal material collection and treatment
Fresh fruits of S. chinensis were collected, on September 9, 2015, from the medicinal garden of Heilongjiang University of Chinese Medicine, China, homogenized. These fruits were divided into 20°C, 35°C, 45°C, and 55°C groups, each group into six parts, placed in thermostatic drying chamber for 1, 2, 3, 4, 5, and 6 days, respectively, and covered with plastics to prevent cells from anhydration during treating.
Determination of H2O2 content
H2O2 was determined using a plant H2O2 ELISA kit that was purchased from Shanghai Yu Ping Biotechnology Limited Company, China.
Determination of enzyme activities
Superoxide dismutase (SOD) activity (U), assayed based on the reduction of nitroblue tetrazolium (NBT), was defined as the activity of enzyme that caused 50% inhibition of NBT reduction. Catalase (CAT) activity, monitoring the decrease of H2O2 at 240 nm for 1 min at 25°C, was calculated as the activity of enzyme that caused a reduction in absorbance at 240 nm of 0.01 per min. Peroxidase (POD) activity, determined the absorbance changes at 470 nm and 25°C, was defined as the activity of enzyme that caused an increase in absorbance at 470 nm of 0.001 per min.
PAL activity was determined as per the method of Hussain et al. A total of 1.0 g of fresh seeds was ground in an ice bath with 10 ml 0.1 mol/L boric acid buffer solution (pH 8.8) containing 1.0 mmol/L EDTA, 5% glycerol, and 5% polyvinylpyrrolidone; the extracts were centrifuged at −4°C 10000 r/min for 20 min. Added above-mentioned 1.0 ml supernatant and 2.0 ml 0.1 mol/L boric acid buffer solution, then added 0.01 ml H2O, and 0.01 ml 0.4 mol/L H2O2 respectively. They were placed in 30°C water, 1 h later, inactivated with 0.2 ml 6 mol/L HCl, and centrifuged at 130,00 rpm for 15 min, and the change of 0.01 optical density values, measured at 290 nm by the spectrophotometer, was defined as one unit of enzyme activity.
The above-mentioned sample was determined at the same temperature as it was placed.
Determination of phenylalanine
A volume of 0.0, 0.5, 1.0, 1.5, 2.0, 2.5, and 3.0 ml of 40 μg/ml phenylalanine standards were added to test tubes, respectively; distillation water was added to 4.0 ml; afterward, 1 ml of 1.2% ninhydrin aqueous solution and 1 ml of pH 8.04 phosphate buffer solution were added to each of seven tubes, respectively, and blended. The reaction was performed in a water bath at a constant temperature of 90°C for 25 min, then cooled down, added loss, blended, and left to stand for 15 min. The absorbance at 570 nm was determined using ultraviolet spectrophotometry, drew the standard curves.
A total of 1.0 g fresh seeds was ground in 0.5 ml 10% ethylic acid solution, converted into 10 ml volumetric flask, water-volumed. The obtained solutions were centrifuged at 13,000 rpm for 20 min, and the absorbance of supernatant was determined. The phenylalanine was calculated as follows:
H2O2 was determined using 1,3-diphosphoglyceric acid ELISA kit that was purchased from Shanghai Fu Sheng Biotechnology Limited Company, China.
The 1.0 g seeds of 20°C and 45°C groups were ground into homogenates with an appropriate amount of saturated (NH4)2 SO4; then, saturated (NH4)2 SO4 was added to 10 ml and centrifuged at 13,000 rpm for 20 min. The liquid supernatant was used for the determination of 1,3-diphosphoglyceric acid.
The sediments were washed with saturated (NH4)2 SO4 twice and re-dissolved with pH 8.04 phosphate buffer, and the crude enzymes were obtained. Four test tubes were all numbered; the number 1 (for 20°C) and the number 2 (for 45°C) were added 1 ml liquid supernatant and 1 ml 0.16 nmol/ml glucose, while the number 3 (for 20°C) and the number 4 (for 45°C) were added 1 ml liquid supernatant and 1 ml soybean protein solution. They all were placed at 30°C for 2 h and then determined the contents of L-phenylalanine.
Above all solution and utensils were cooled to 4°C below during extracting. The procedure was repeated three times.
Determination of lignanoids
0.25 g of the dry S. chinensis fruit power (day <0.1 mm) was put in a 25 ml volumetric flask; then, ultrasonic extraction with 70% methanol for 30 min; finally, the supernatant was filtered with a 0.22-μm microporous filter for ultra-high performance liquid chromatography analysis.
The experimental samples were analyzed by a Waters ACQUITY HPLC. The trial samples were based on a BEH C18 column (2.1 mm × 50 mm, 1.7 μm). The mobile phases were composed of (A) H2O with 0.5% glacial acetic acid and (B) methanol. The gradient program as initial 20% B ~ 60% B from 0 to 10 min, 60% B from 10 to 30 min, 60% B ~ 70% B from 30 to 50 min, 70% B ~ 80% B from 50 to 60 min, 80% B for 60 ~ 70 min, 80% B ~ 100% B from 70 to 75 min, 100% B for 75 ~ 85 min, 100% B ~ 20% B from 85 to 86 min, and 20% B for 86 ~ 96 min. The flow rate was set at 1 ml/min, and the column temperature was set at 30°C. The detection wavelengths of schizandrol A, schizandrol B, shiandrin A, shiandrin B, and shiandrin C were 250 nm.
All the experimental data were analyzed using Excel (Microsoft Corp) and expressed as the mean ± standard error of the mean. The 35°C, 45°C, and 55°C were chosen as high-temperature condition; the 20°C was chosen as nonstress condition. The high-temperature effect was determined by comparison with the 0 day.
| Results|| |
The amount of H2O2 was increased sharply in fresh fruit under 35°C, 45°C, and 55°C [Figure 1]. The 45°C and 55°C peaked at 1 day and the 45°C at 2 days; then, they all declined but still with a higher level than the 0 day. Among them, the 45°C had the sharpest rise, and the 55°C had the highest contents.
|Figure 1: Mount of H2O2 changed under high temperature. The 0 day and 20°C had not altered the H2O2, the high temperature increased the H2O2 remarkably, with a tendency of increases first, then decreases, but still with a higher level than the 0 day. Among them, the 55°C had the highest contents|
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The high temperature had various effects on the SOD activities, rose at the 55°C, lowered at 35°C, and changed little at the 45°C. The CAT activities of the 35°C, 45°C, and 55°C had been reduced in all stages. All the POD activities had been reduced only at the 1 day, then rose at the 35°C, lowered at 55°C, and changed little at the 45°C [Figure 2]. Altogether, the antioxidant action was lowered than the 0 day and the 20°C.
|Figure 2: Effect of high temperature on the antioxidant activities. The SOD rose at the 55°C and lowered at 35°C; the POD was the opposite and was changed little at the 45°C. The CAT activities of the 35°C, 45°C, and 55°C had been remarkably reduced in all stages, indicating that the antioxidant action was lowered than the 0 day and the 20°C. SOD: Superoxide dismutase; CAT: Catalase; POD: Peroxidase|
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Phenylalanine ammonia lyase activities
The PAL activities had a certain degree of resisting high temperature, remained largely unchanged at 35°C, but reduced gradually as temperature increased, 35°C > 45°C > 55°C [Figure 3]. Varying high temperature rose the phenylalanine contents, increased sharply at the 1 day for the 35°C and 45°C and at the 2 days for the 55°C and 45°C, and then maintained a stable level with almost 1–3 times than the 0 day and the 20°C [Figure 4].
|Figure 3: Change of the PAL activities. The PAL had a certain degree of resisting high temperature, remained largely unchanged at 20°C and 35°C, but reduced gradually as temperature increased, 35°C > 45°C > 55°C, indicating that the PAL did not work very well at all. PAL: Phenylalanine ammonia lyase|
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|Figure 4: Change of the phenylalanine contents. Varying high temperature rises the phenylalanine contents, increased sharply, then declined, but still with as much as 1–3 times higher than the 0 day and the 20°C, which stimulated the synthesis of lignanoids|
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The 1,3-diphosphoglyceric acid content of the 45°C was higher remarkably than that of the 20°C (P ≤ 0.01). For the glucose and protein group, the phenylalanine content from 45°C seeds were all higher than that of 20°C, but the statistically significant differences exist only in glucose group [Figure 5].
|Figure 5: Origin of phenylalanine. The 1,3-diphosphoglyceric acid content of the 45°C was higher remarkably than that of the 20°C (P < 0.05)* (P < 0.01)**. For the glucose and protein group, the phenylalanine content from 45°C seeds were all higher than that of 20°C, but the statistically significant differences exist only in glucose group, indicating phenylalanine derives mainly from the degradation of glucose under high-temperature condition|
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Varying high temperature rose the contents of schizandrol A, schizandrol B, shiandrinA, shiandrin B, and shiandrin C, with similar trends. The contents increased gradually as time goes on. At 6 days, the contents of schizandrol A, schizandrol B, shiandrin A, shiandrin B, and shiandrin C increased by 48.0%, 64.6%, 81.5%, 56.8%, and 31.2%, respectively, than the 0 day and the 20°C [Figure 6].
|Figure 6: Change of the lignanoid contents. High temperature rises the contents of schizandrol A, schizandrol B, shiandrin A, shiandrin B, and shiandrin C, with similar trends. The contents increased gradually as time goes on. At 6 days, the contents of schisandrin, deoxyschizandrin, γ-shiandrin B, and shiandrin C increased by as much as 48.0%, 64.6%, 81.5%, 56.8%, and 31.2%, respectively, than the 0 day|
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| Discussion|| |
Plants can produce ROS during high-temperature stresses. The several locations that the chlorophyllous tissues produce ROS are mainly in chloroplasts and mitochondria and the other organs mainly in mitochondria, plasma membranes, peroxisomes, apoplast, endoplasmic reticulum, and cell walls. The most common ROS in the nonchlorophyllous tissues include O • −2, H2O2, and • OH. Activation of O2 occurs mainly by stepwise monovalent reduction; O2 is sequentially reduced to O • −2, H2O2, and • OH. H2O2 has a half-life of only 1 ms and is relatively stable as compared to O • −2 and •OH that have only 1 μs and 1 ns, respectively. Therefore, the contents of H2O2 generally present the level of whole ROS. Cell damage under stress condition results from ROS, and high level of ROS can modify adjacent molecular configuration, lower stability of lipid bilayer, and cross-link sulfur protein, with great damage to cell.
Contents of H2O2 in S. chinensis seeds under high-temperature condition increased rapidly at the 1 day and then decreased [Figure 1]. The high-temperature condition as a fountain of H2O2 was continuous, the decrease of H2O2 was a dissonant dilemma, and the reason that decreased of H2O2 probably was the result of antioxidant. Plants possess complex antioxidative defense system, comprising antioxidase, secondary metabolites, glutathione, Vitamin C, et al., to scavenge ROS. The antioxidants play an important role in scavenging ROS. The SOD of the 35°C and 45°C failed to increase, the CAT and the POD of the 45°C and 55°C did also, probably due to the damages of ROS to the antioxidase, a bioactive protein. The SOD cannot scavenge ROS without the help of CAT and POD et al., the POD has a typically slowly reductive step, the CAT does not require cellular reducing equivalent and has a very fast turnover rate, and the CAT therefore does excellent in scavenging ROS. These, in general, manifested that the antioxidant capacities were not increased but decreased [Figure 2], in spite of increase of SOD under 55°C and POD under 35°C. In this case, the ROS from high temperature were scavenged mainly by secondary metabolites.
Plants developed negative feedback self-regulation to eliminate ROS during the long-term evolution. Once the plants are subject to stresses, then ROS are rose and convert into more H2O2. The long-lived H2O2 as messenger of regulating metabolism acts as a central player in stress signal transduction pathways. These pathways can then activate multiple acclamatory responses that reinforce resistance to various stresses. With this, the secondary metabolism is upregulated by ROS, and in turn, the increased secondary metabolites scavenge the redundant ROS.
Biphenyl cyclooctene lignanoids are a class of chemical constituents with the capacity to eliminate ROS. PAL is a key enzyme for biosynthesis of lignanoids, whose optimal temperature is 30°C–65°C, higher than other enzymes. The PAL is a stress enzyme, used as a physiological marker for measuring the resistance of plants due to its strongly expressed under stresses. [Figure 3] shows that PAL had powerful resistance to high temperature. It was interesting that the PAL activities did not be increased but not decreased under high-temperature condition, while the contents of phenylalanine rose sharply and kept a high level [Figure 4]. The glycolytic pathway or the degradation of protein can be a major potential source of stress. The 1,3-diphosphoglyceric acid is one of the intermediates in glycolytic pathway. The increased 1,3-diphosphoglyceric acid revealed that the phenylalanine derives in the main from the degradation of glucose [Figure 5], which is sufficient in any tissue. High temperature can lead to protein degradation, the phenylalanine can also result from the degradation of protein [Figure 5], but the mount may seem fairly trifling, maybe due to small amounts of phenylalanine in protein. Heat stress causes alterations in expression of genes involved in direct protection from high-temperature stress. The biphenyl cyclooctene lignanoids are synthesized from phenylalanine; the increased phenylalanine stimulates lignanoids' synthesis. The exposure of the fresh fruit to 35°C, 45°C, and 55°C condition boosted the lignanoids, going on with time [Figure 5]. Under 55°C, both the PAL and the produced phenylalanine were the least, with a result of the least contents of total lignanoids, in this case more and more H2O2 probably damage the cells. Under 45°C conditions, although PAL activity was lower than the 35°C, the phenylalanine was the highest [Figure 4]; furthermore, SOD, CAT, and POD rose [Figure 3] and eliminated a great amount ROS, causing retention of more lignanoids than the 35°C.
| Conclusions|| |
Seeds as the pivotal organ for plant contain large quantities of stored carbohydrate, protein, and other reserves. The synthesis of lignanoids took advantage of phenylalanine from degraded glucose under high-temperature condition; the effectiveness of S. chinensis seeds could be improved heavily.
We wish to thank for providing financial support from the Heilongjiang province Science Foundation (H2016065).
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Ren DQ, Zhou RH. The significance and role of GAP. In: Good agricultural practice (GAP) implementation guide for Chinese crude drug. Beijing: China Agricultural Practices; 2003. p. 44-6.
Zhang B, Peng Y, Zhang Z, Liu H, Qi Y, Liu S, et al.
GAP production of TCM herbs in China. Planta Med 2010;76:1948-55.
Xiao X, Chen S, Huang L, Xiao P. Survey of investigations on daodi Chinese medicinal materials in China since 1980s. Zhongguo Zhong Yao Za Zhi 2009;34:519-23.
Hasanuzzaman M, Nahar K, Alam MM, Roychowdhury R, Fujita M. Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. Int J Mol Sci 2013;14:9643-84.
Wang Y, Zhao M, Yu J. A study on the dormancy characteristic and inner inhibitory substances of Fructus schisandrae
. J Chin Mater Med 1997;22:10-4.
Anne C. Modelling seed germination response to temperature in Eucalyptus
) species in the context of global warming. Seed Sci Res 2017;27:99-109.
Hasanuzzaman M, Hossain MA, Silva JA, Fujita M. Plant responses and tolerance to abiotic oxidative stress: Antioxidant defenses is a key factor. Crop Stress and its Management: Perspectives and Strategies. Netherlands: Springer; 2012. p. 261-315.
Hasanuzzaman M, Nahar K, Fujita M. Extreme temperature responses, oxidative stress and antioxidant defense in plants. J Natl Cancer Inst 2013;65:81-93.
Simontacchi M, Galatro A, Ramos-Artuso F, Santa-María GP. Survival in a changing environment: the role of nitric oxide in plant responses to abiotic stress. Front Plant Sci 2015;63:260-8.
Kim YJ, Lee HJ, Kim CY, Han SY, Chin YW, Choi YH, et al.
Simultaneous determination of nine lignans from Schisandra chinensis
extract using ultra-performance liquid chromatography with tandem mass spectrometry in rat plasma, urine, and gastrointestinal tract samples: Application to the pharmacokinetic study of Schisandra chinensis
. J Sep Sci 2014;37:2851-63.
Szopa A, Ekiert R, Ekiert H. Current knowledge of Schisandra chinensis
(Turcz.) baill. (Chinese magnolia vine) as a medicinal plant species: A review on the bioactive components, pharmacological properties, analytical and biotechnological studies. Phytochem Rev 2017;16:195-218.
Hou W, Gao W, Wang D, Liu Q, Zheng S, Wang Y, et al.
The protecting effect of deoxyschisandrin and schisandrin B on HaCaT cells against UVB-induced damage. PLoS One 2015;10:e0127177.
Pi Z, Hou G, Ai J, Song F, Liu Z, Liu S, et al.
Correlation of lignans content and antioxidant activities of Schisandra chinensis
fruits by using stoichiometry method. Zhongguo Zhong Yao Za Zhi 2012;37:1133-9.
Zhang N, Sun Q, Li H, Li X, Cao Y, Zhang H, et al.
Melatonin improved anthocyanin accumulation by regulating gene expressions and resulted in high reactive oxygen species scavenging capacity in cabbage. Front Plant Sci 2016;7:197.
Xu M, Dong J, Zhang X. Signal interaction between nitric oxide and hydrogen peroxide in heat shock-induced hypericin production of Hypericum perforatum
suspension cells. Sci China C Life Sci 2008;51:676-86.
Lin HM, Han HX, Li YH, Yang LM. Correlation study on lignin contents of Schisandra chinensis
and ecological factors. Zhongguo Zhong Yao Za Zhi 2013;38:4281-6.
Yang J, Duan JA, Li GL, Zhu ZH, Zhu TL, Qian DW, et al.
Determination of lignans in Schisandrae Sphenantherae Fructus
from different regions. Zhongguo Zhong Yao Za Zhi 2014;39:4647-52.
Lee DK, Yoon MH, Kang YP, Yu J, Park JH, Lee J, et al.
Comparison of primary and secondary metabolites for suitability to discriminate the origins of Schisandra chinensis
by GC/MS and LC/MS. Food Chem 2013;141:3931-7.
Qin YD, Wang YQ, Wang RB, Wang CQ, Liu XL, Zhou Z, et al.
Quality assessment on Schisandrae fructus
from different habitats. Zhong Yao Cai 2014;37:210-4.
Han ZF, Hu GS, Li N, Fan X, Jia JM. Quality evaluation and antioxidant activity research of Schisandra chinensis
from various habitats. Zhong Yao Cai 2012;35:1904-9.
Driedonks N, Xu J, Peters JL, Park S, Rieu I. Multi-level interactions between heat shock factors, heat shock proteins, and the redox system regulate acclimation to heat. Front Plant Sci 2015;6:999.
You J, Chan Z. ROS regulation during abiotic stress responses in crop plants. Front Plant Sci 2015;6:1092.
Hossain MA, Bhattacharjee S, Armin SM, Qian P, Xin W, Li HY, et al.
Hydrogen peroxide priming modulates abiotic oxidative stress tolerance: Insights from ROS detoxification and scavenging. Front Plant Sci 2015;6:420.
Sabehat A, Weiss D, Lurie S. The correlation between heat-shock protein accumulation and persistence and chilling tolerance in tomato fruit. Plant Physiol 1996;110:531-7.
Kadyrzhanova DK, Vlachonasios KE, Ververidis P, Dilley DR. Molecular cloning of a novel heat induced/chilling tolerance related cDNA in tomato fruit by use of mRNA differential display. Plant Mol Biol 1998;36:885-95.
Kuznetsov VV. Rakitin VY, Zholkevich VN. Effects of preliminary heat-shock treatment on accumulation of osmolytes and drought resistance in cotton plants during water deficiency. Physiol Plantarum 1999;107: 399-406.
Neumann D, Lichtenberger O, Günther D, Tschiersch K, Nover L. Heat shock proteins induce heavy-metal tolerance in higher plants. Planta 1994;194:360-7.
Giannopolitis CN, Ries SK. Superoxide dismutases: II. Purification and quantitative relationship with water-soluble protein in seedlings. Plant Physiol 1977;59:315-8.
Zeng SX, Wang YR, Liu HX. Some enzymatic reactions related to chlorophyll degradation in cucumber cotyledons under chilling in the light. Acta Phytophysiol Sin 1991;17:177-82.
Zhang L, Han S, Li Z, Nan L, Li L, Luo L, et al
. Effects of the infestation by Actinote thalia
pyrrha (Fabricius) on the physiological indexes of Mikania micranth
leaves. Acta Ecol Sinica 2006;26:1330-6.
Hussain PR, Wani AM, Meena RS, Dar MA. Gamma irradiation induced enhancement of phenylalanine ammonia-lyase (PAL) and antioxidant activity in peach (Prunus persica
Bausch, Cv. Elberta). Radiat Phys Chem 2010;79:982-9.
Rachana S, Samiksha S, Parul P, Mishra RK, Tripathi DK, Singh VP. Reactive oxygen species (ROS): Beneficial companions of plants' developmental processes. Front Plant Sci 2016;9:1-19.
Møller IM, Jensen PE, Hansson A. Oxidative modifications to cellular components in plants. Annu Rev Plant Biol 2007;58:459-81.
Sharma P, Jha AB, Dubey RS, Pessarakli M. Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot 2012;32:243-7.
Mishra S, Imlay J. Why do bacteria use so many enzymes to scavenge hydrogen peroxide? Arch Biochem Biophys 2012;525:145-60.
Crawford DR, Davies KJ. Adaptive response and oxidative stress. Environ Health Perspect 1994;102 Suppl 10:25-8.
Zhang C, Wang X, Zhang F, Dong L, Wu J, Cheng Q, et al.
Phenylalanine ammonia-lyase2.1 contributes to the soybean response towards Phytophthora sojae
infection. Sci Rep 2017;7:7242.
Bokszczanin KL, Fragkostefanakis S. Perspectives on deciphering mechanisms underlying plant heat stress response and thermotolerance. Front Plant Sci 2013;8:1-20.
Shinozaki K, Yamaguchi-Shinozaki K. Gene networks involved in drought stress response and tolerance. J Exp Bot 2007;58:221-7.
[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6]