اثر کلرید سدیم بر خصوصیات فیزیولوژیکی، بیوشیمیایی و بیان دو ژنADS و CYP71AV1دخیل در مسیر بیوسنتزی آرتمیزینین در گیاه افسنطین (Artemisia absinthium)
محورهای موضوعی : ژنتیک
سارا سلیمیان ریزی
1
,
زهرا رضایتمند
2
,
منیره رنجبر
3
,
نسرین یزدان پناهی
4
,
زرین دخت امامی
5
1 - گروه زیست شناسی، واحد فلاورجان، دانشگاه آزاد اسلامی، اصفهان، ایران
2 - گروه زیست شناسی، واحد فلاورجان، دانشگاه آزاد اسلامی، اصفهان، ایران
3 - گروه زیست شناسی، واحد فلاورجان، دانشگاه آزاد اسلامی، اصفهان، ایران
4 - گروه بیوتکنولوژی، واحد فلاورجان، دانشگاه آزاد اسلامی، اصفهان، ایران
5 - گروه میکروبیولوژی، واحد فلاورجان، دانشگاه آزاد اسلامی، اصفهان، ایران.
کلید واژه: تنش شوری, بیان ژن, افسنطین, آرتمیزینین, آنزیمهای آنتی اکسیدان,
چکیده مقاله :
تنش شوری یکی از عوامل مهم در رابطه با کاهش میزان رشد و تغییر در فرآیند‌های فیزیولوژیکی و متابولیسمی گیاهان می‌باشد. در این تحقیق جهت بررسی اثر تنش شوری بر عملکرد فیزیولوژی، بیوشیمیایی و بیان ژن در گیاه افسنطین، آزمایشی در سه سطح شوری(0، 75، 150 میلی‌مولار کلرید سدیم) در قالب طرح کاملاً تصادفی با سه تکرار در شرایط گلخانه ای انجام گرفت. بررسی نتایج نشان داد که تنش شوری باعث کاهش میزان پارامتر‌های رشدی گیاه مانند طول ساقه، طول ریشه، وزن تر ساقه، وزن تر ریشه، وزن خشک ساقه، خشک ریشه شد، همچنین شوری سبب کاهش میزان یون‌های پتاسیم، کلسیم، منیزیم و آهن و افزایش میزان سدیم در گیاه گردید. افزایش تنش شوری میزان پرولین، مالون دی آلدهید، ترکیبات فنلی و فعالیت برخی آنزیمهای آنتی اکسیدان را افزایش و میزان پروتئین در گیاه را کاهش داد. میزان بیان ژن‌های CYP71AV1 و ADS نیز به‌ترتیب در غلظت‌های 150 میلی‌مولار و 75 میلی‌مولار کلرید سدیم بیشترین میزان کاهش را نشان داد که این امر باعث کاهش میزان آرتمیزینین در گیاه افسنطین گشت. با توجه به نتایج این پژوهش می توان عنوان نمود که گیاه افسنطین بــرای مقــابله با تنـش شوری حاصل از کلرید سدیم از سیستم افزایش فعالیت آنزیم آنتی اکسیدانی و مواد تنطیم کننده پتانسیل اسمزی و ترکیبات فنلی استفاده نموده است وکاهش بیان ژن ADS می‌تواند عامل موثر در کاهش مقدارآرتمیزینین گیاه افسنطین باشد.
Salinity stress is one of the important factors in decreasing the rate of growth and changing physiologic and metabolic processes of plants. In the present study to investigate the effect of salinity stress on physiological and biochemical performances and also gene expressions of Artemisia absinthium plant, an experiment was conducted with three level of salinity (0, 75, and 15 Mmol NaCl) in a completely randomized design with three replications under greenhouse conditions. Results showed that salinity stress decreased the rate of growth parameters in the plants including shoot length, root length, wet shoot weight, wet root weight, dry shoot weight, and dry root weight. Also, salinity decreased the levels of potassium, calcium, magnesium, and iron ions while increasing sodium levels in the plants. Increased salinity stress increased levels of proline, malondialdehyde, phenolic compounds, and activities of some antioxidant enzymes while it led to protein reduction in the plants under study. The expression of CYP71AV1 and ADS genes reduced to minimum at 150 Mmol and 75 Mmol NaCl treatments, respectively leading to reduced level of artemisinin in the Artemisia absinthium plants. According to the findings of this study, it might be argued that in its attempt to confront salinity stress induced fromsodium chloride, Artemisia absinthium employs the system of increased level of antioxidant enzymes activity, osmotic potential regulators, and phenolic compounds. Also, decreased expression of ADS gene can be an effective factor in reducing artemisinin contents in Artemisia absinthium.
Abdallah, II., Van Merkerk, R., Klumpenaar, E., Quax, J.W. (2018). Catalysis of amorpha-4, 11-diene synthase unraveled and improved by mutability landscape guided engineering. Scientific Reports. DOI: 10.1038/s41598-018-28177-4.
Aebi, H. (1984). Catalase in vitro. Methods in Enzymology. 105: 121-126.
Aftab, T., A. Khan, M.M., Idrees, M., Naeem, M., Hashmi, N. and Moinuddin. (2010). Effect of Salt Stress on Growth, Membrane Damage, Antioxidant Metabolism and Artemisinin Accumulation in Artemisia annua L. Plant Stress. 4 (1): 36-43.
Aghai, K., Tayei, N., Kanaani, M.R. and Yazdani, M. (2014). The effect of salinity stress on some physiological and biochemical traits of two species of Salvia. Plant Process and Function. 3 (9): 96-85.
Ahmed, H. A.A., Koçak Şahin, N., Akdoğan, G., Yaman, C., Köm, D. and Uranbey, S. )2020(.Variability in salinity stress tolerance of potato (Solanum tuberosum L.) varieties using in vitro screening. Ciência e Agrotecnologia. http://dx.doi.org/10.1590/1413-7054202044004220
Ahmed, S., Ahmed, Sh., Roy, S.K., Woo, S.H., Sonawane, K.D. and Shohael, A.M. (2019). Effect of salinity on the morphological, physiological and biochemical properties of lettuce (Lactuca sativa L.) in Bangladesh. De Gruyter. 4: 361–373.
Alam, P., Kiran, U., Ahmad, M.M., Kamaluddin., Ali Khan, M., Jhanwar, Sh. and Abdin, M.Z. (2010). Isolation, characterization and structural features of amorpha- 4, 11-diene synthase (ADS3963) from Artemisia annu L. Bioinformation. 4(9): 421-429.
Amini, F. and Ehsanpour, A.A. (2005). Soluble proteins,proline, carbohydrates and Na+/K+ changes intwo tomato (Lycopersicon esculentum Mill.) cultivars under in vitro salt stress. American Journal of Biochemistry and Biotechnology. 1(4): 212-216.
Appel, K. and Hirt, H. (2004). Reactive oxygen species: metabolism, oxidative stress and signal transduction. Annual Review of Plant Biology. 55(1): 373-399.
Asada, K. (1999). The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons, Annual Review of Plant Biology. 50: 601–639.
Bates, L.S. )1973(. Rapid determination of free proline for water stress studies. Plant Soil. 39: 205-207.
Board, R., Reza Zadeh, Sh.Gh., Omidi, M., Torabi, S., Hariri Akbari, Ph., Parvaneh, S. and Taghizad Farid, R. (2013). Investigation of Quantitative diversity Artemisinin of Artemisia annua in plant populations native in northern Iran. Scientific-Research Quarterly of Plant and Ecosystem. 9 (35): 50-43.
Boughalleb, F., Abdellaoui, R., Mahmoudi, M. and Bakhshandeh, E. (2020). Changes in phenolic profile, soluble sugar, proline, and antioxidant enzyme activities of Polygonum equisetiforme in response to salinity. Turkish Journal of Botany. 44(1): 25-35.
Box, S. and Schachtman, D. P. (2011).The effect of low concentrations of sodium on potassium uptake and growth of wheat. Australian Journal of Plant Physiology. 27: 175-182.
Bradford, M.M. )1976(. Arapid and sensitive method for the quantitation of microgram quantities of protein uti-lizing the principle of protein day binding. Analytical Biochemistry. 72: 248-254.
Chance, B. and Maehly, A.C.)1995(. Assay of catalase and peroxidases. Methods of Enzymology. 11: 764-775.
Daneshmand, F., Arvin, M.J. and Kalantari, Kh.M. (2009).Effect of Acetylsalicylic Acid (Aspirin) on Salt and Osmotic Stress Tolerance in Solanum bulbocastanum in Vitro: Enzymatic Antioxidants. American-Eurasian Journal Agriculture and Environmental Science. 6 (1): 92-99.
Dash, M. and Panda, S. (2001). Salt Stress Induced Changes in Growth and Enzyme Activities in Germinating Phaseolus Mungo Seeds. Biologia Plantarum. 44(4): 587–589.
Dhindsa, R.A., Plumb-Dhindsa, P. and Thorpe, T.A. (1981). Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. Journal of Experimental Botany. 126: 93-101.
Davey, M.W., Stals, E., Panis, B., Keulemans, J. and Swennen, R.L. (2005). High-throughput determination of malondialdehyde in plant tissues. Analytical Biochemistry. 347: 201-207.
Doğan, M. (2011). Antioxidative and proline potentials as a protective mechanism in soybean plants under salinity stress. African Journal of Biotechnology. 10(32): 5972-5978.
Demiral, T. and Turkan, I. (2005). Comparative lipid peroxidation, antioxidant defense systems and proline content in roots of two rice cultivars differing in salt tolerance. Environmental and Experimental Botany. 53(3): 247–257.
Emami Bistgani, Z., Hashemi, M., DaCosta, M., Craker, L., Maggic, F. and Morshedloo, M.R. (2019). Effect of salinity stress on the physiological characteristics, phenolic compounds and antioxidant activity of Thymus vulgaris L. and Thymus daenensis Celak. Industrial Crops and Products. 135: 311-320.
Farhoudi, R. (2012). Effect of salinity stress on alpha-amylase enzyme activity, cell membrane permeability and seedling growth of rapeseed cultivars. Plant Process and Function. 1(1): 24-14.
Farhoudi, R. (2013). Investigation of the effect of salinity stress on growth and histological characteristics of nine wheat cultivars in vegetative growth stage. Journal of Crop Physiology - Islamic Azad University, Ahvaz Branch. 5 (20): 86-71.
Fabriky Aurang, S. and Davoodnia, B. (2018). Evaluation of changes in growth traits and secondary metabolites in Thymus vulgaris L.under mild salinity and drought stress. Journal of Ecophytic Chemistry of Medicinal Plants. 6(2): 40-27.
Gapinska, M., Sklodowska, M. and Gabara, B. (2008) . Effect of short- and long-term salinity on the activities of antioxidative enzymes and lipid peroxidation in tomato roots. Acta Physiologia Plantarum. 30: 11-18.
Gehanbazy Gojani, H., Hosseini Nasr, S., Saqib Talebi, Kh. and Hojjati, S. (2014). The Effect of salinity stress on vegetative factors, proline, plant pigments and nutrient uptake in shoots of four species of wild almonds. Journal of Plant Research (Iranian Journal of Biology). 27 (5): 787-777.
Golkar, P., Amooshahi, F. and Arzani, A. (2017). The effects of salt stress on physio-biochemical traits, total phenolic and mucilage content of Plantago ovata Forsk under in vitro conditions. Journal of Applied Botany and Food Quality. 90: 224 - 231.
Gupta, K.J., Stoimenova, M. and Kaiser, W.M. (2005). In higher plants, only root mitochondria, but not leaf mitochondria reduce nitrite to NO, in vitro and in situ, Journal of Experimental Botany. 56(420): 2601–2609.
Heath, R.L. and Packer, L. (1969). Photoperoxidation in isolated chloroplast. I. kinetics and stoichiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysics. 125: 189-198.
Hosseini, R., Yazdani, N., Garoosi, GA. (2011). The presence of amorpha-4, 11-diene synthase, a key enzyme in artemisinin production in ten Artemisia species. Daru. 19: 332-337.
Hussein, M.M., Balbaa, L.K. and Gaballah, M.S. )2007). Salicylic Acid and Salinity Effects onGrowth of Maize Plants. Research Journal of Agriculture and Biological Sciences. 3( 4): 321 - 328.
Jahanbakhsh GodehKahriz, S., Khadem Sedighi, S., Ebadi, Gh., Tavakoli, N. and Davari, M. (2017). The effect of salinity stress on the expression of salinity resistance proteins and antioxidant activity in Echium amoenum using calcium. Genetic Engineering and Biosafety. 6 (1): 129-117.
Jahantigh, O., Najafi, F., Naghdi badi, H.A., Khavari-nejad, R.A. and Sanjarian, F. (2015). Changes In Antioxidant Enzymes Activities and Proline, Total Phenol And Anthocyanine Contents In Hyssopus OfficinalisL. Plants Undersalt Stress. Acta Biologica Hungarica. 67(2): 195–204.
Kafi, M. and Rahimi, Z. (2011). Effect of salinity and silicon on root characteristics, growth, waterstatus, proline content and ion accumulation of purslane (Portulaca oleracea L.).Soil Science and Plant Nutrition. 57(2): 341-347.
Karmian, R. and Atai Barazandeh, S. (2012). Study of the effect of salinity stress on some growth indices in three species of sainfoin (Onobrychis) in Iran. Plant Biology. 5 (15): 82-69.
Khalid, H., Kumari, M., Grover, A. and Nasim, M. (2015). Salinity Stress Tolerance of Camelina InvestIgated in vitro. Scientia Agriculturae Bohemica. 46(4): 137–144.
Khan Kayani, W., Hafeez Kiani, B., Dilshad, E. and Mirza, B. (2018). Biotechnological approaches for artemisinin production in Artemisia. World Journal of Microbiology and Biotechnology. 34: 1-14.
Khan, M.A., A. Ungar, I. and M. Showalter, A. (2000). The effect of salinity on the growth, water status, and ion content of a leaf succulent perennial halophyte, Suaeda fruticosa (L.) Forssk. Journal of Arid Environments. 45: 73–84.
Koul, B., Taak, P., Kumar, A., Khatri, T. and Sanyal, I. (2017). The Artemisia Genus: A Review on Traditional Uses, Phytochemical Constituents, Pharmacological Properties and Germplasm Conservation. Journal of Glycomics and Lipidomics.7:1-7.
Li, J., Zhao, G .Zh., Varma, A., Qin, Sh., Xiong, Zh., Huang, H.Y., Zhu, W.Y., Zhao, L.X., Xu, L. H., Zhang, S. and Li, W.J. (2012). An Endophytic Pseudonocardia Species Induces the Production of Artemisinin in Artemisia annua. Public Library of Science One. 7: 1-9.
Livak, K.J. and Schmittgen, Th.D. (2001). Analysis of Relative Gene Expression Data Using Real- Time Quantitative PCR and the 22DDCT Method, Methods. 25: 402–408.
Maqsoomi Holaso, S. and Pourakbar, L. (2014). Effects of salinity on growth and some physiological parameters of wheat seedlings. Plant Biology of Iran. 6(19):31-42.
Matysik, J., Alia, B.B. and Mohanty, P. (2002). Molecular mechanisms of quenching of reactive oxygen species by proline under stress in plants. Current Science. 82: 525–532.
Meloni, D.A., Oliva, M.A., Martinez, C.A. and Cambraia, J.)2003). Photosynthesis and ctivity of superoxide dismutase, peroxidase and gluthatione reductase in cotton under salt stress. Environmental and Experimental Botany. 49: 69-76.
Motamedi, M.and Farhoudi, R. (2010).Effect of Salt Stress on Antioxidant Activity and Seedling Growth of Safflower Cultivars. International Journal of Applied Agricultural Research. 5(3): 367-375.
Olofsson, L., Engstrom, A., Lundgren, A. and Brodelius, P.E. (2011). Relative expression of genes of terpene metabolism in different tissues of Artemisia annua L. BMC Plant Biology. 11: 1-12.
Omidi, M., Khandan-Mirkohi, A.Gh., Kafi, M. and Zamani, Z.A. (2021). Investigation of The effect of salinity stress on some morphological and physiological indices of Rosa damascena Kashan genotype. Iranian Horticultural Sciences. 51(1): 17-1.
Prasad, A., Kumar, D., Anwar, M., Singh, D.V. and Jain, D.C. (1996). Response of Artemisia annua L. to Soil Salinity. Journal of Herbs, Spices & Medicinal Plants. https://doi.org/10.1300/J044v05n02_07 .
Qian, Zh., Gong, K., Zhang, L., Lv, J., Jing, F., Wang ,Y., Guan, Sh., Wang, G. and Tang, K. (2007). A simple and efficient procedure to enhance artemisinin content in Artemisia annua L. by seeding to salinity stress. Full Length Research Paper. 6: 1410-1413.
Ranjan, R., Bohra, S.P. and Jeet, A.M. (2001). Book of plant senescence. Jodhpur Agrobios New York. 18-42.
Razavizadeh, R. and Ehsanpour, A.A. (2009). Effects of salt stress on proline content, expression of delta -1-pyrroline-5-carboxylate synthetase, and activities of catalase and ascorbate peroxidase in transgenic tobacco plants. Biological Plantarum. 46(2): 63-75.
Razavizadeh, R. and Mohagheghian, N. (2015). Investigation of changes in antioxidant enzyme activity and secondary metabolites of thyme seedlings (Thymus vulgaris) under salinity stress under in vitro culture conditions. Plant Biology of Iran. 8 (26): 58-41.
Ronald, S.F. and Laima, S.K. (1999). Phenolicsand cold tolerance of Brassica napus. Plant Agriculture. 1: 1-5.
Saeedipoor, S. (2017). Effect of salinity stress on yield, concentration and distribution of some elements in different organs of two cultivars Barbej (Oriza sativa L.). Journal of Crop Physiology - Islamic Azad University, Ahvaz Branch. 9 (36): 40-27.
Samia, M., Tahani, A., Hathout, A., R.Ahsour, A. and Abd Almalik, A. (2009). Brassinolide and Salinity Acid Induced Antioxidant Enzymes, Hormonal Balance and Protein Profile of Maize Plants Grown under Salt Stress. Research Journal of Agriculture and Biological Sciences. 5(4): 391-402.
Savarus, A., Ja Oua, S., Hua, X.J., Ardiles, W., Van.Montago, M. and Verbruggen, N. (1995). Isolation, Characterization, and Chromosomal Location of Gene Encoding the 1-pyroline-5-carboxylate Synthetase in Arbidobsis Thaliana. Federation of European Biochemical Societies. 372: 13-19.
Shahnazi, M., Azadmehr, A., Hajiaghaee, R., Mosalla, S. and Latifi, R. (2015). Effects of Artemisia Absinthium L. Extract on the Maturation and Function of Dendritic Cells. Jundishapur Journal of Natural Pharmaceutical Products. 10: 1-6.
Sharma, T., Dreyer, I., Riedelsberger, J. (2013). The role of K+ channels in uptake and redistribution of potassium in the model plant Arabidopsis thaliana. Frontiers in Plant Science. 4: 1-16.
Shen, Q., Chen, Y.F., Wang, T., Wu, S.Y., Lu, X., Zhang, L., Zhang, F.Y., Jiang, W.M., Wang, G.F. and Tang, K.X. (2012). Overexpression of the cytochrome P450 monooxygenase (cyp71av1) and cytochrome P450 reductase (cpr) genes increased artemisinin content in Artemisia annua (Asteraceae).Genetics and Molecular Research. 11 (3): 3298-3309.
Teoh, K.H., Polichuk, D.R., Reed, D.W., Nowak, G., Covello, P.S. (2006). Artemisia annua L. (Asteraceae) trichome-specific cDNAs reveal CYP71AV1, a cytochrome P450 with a key role in the biosynthesis of the antimalarial sesquiterpene lactone artemisinin. The Federation of European Biochemical Societies Letters. 580:1411–1416.
Valifard, M., Mohsenzadeh, S., Kholdebarin, B. and Rowshan, V. (2014).Effects of salt stress on volatile compounds, total phenolic content and antioxidant activities of Salvia mirzayanii. South African Journal of Botany. 93: 92–97.
Wasim, A., hasan, A., Abdullah, A. and Tarannum, T. (2010). Medicinal I mportance of Artemisia absinthium Linn (Afsanteen) in Unani Medicine: A Review. Hippocratic Journal of Unani Medicine. 5: 117-125.
Wimmer, M.A., Muhiling, K.H., Lauchli, A., Brown, P.H. and Goldbach, H.E. (2003). The Interaction between Salinity and Boron Toxicity Effects the Subcellular Distribution of ions Proteins in Wheat Leaves. Plant Cell and Environmental. 26: 2567-1271.
Yarizadeh, K., Hosseini, R. and Moghaddami, M. (2015). Gene studyADS, DBR2 and SQS in five species of Different artemisia. Plant Biology of Iran .7 (25): 52-43.
Younis, A., Riaz, A., Hasan, S.U., Mustaq, N. and Hameed, M. (2014). Response of Hedera helix (English Ivy) to various salinity levels. Journal of Horticulture, Forestry and Biotechnology. 18(1): 1-6.
Zaidi, I. and Hanin, M. (2016). The wheat MAP kinase phosphatase 1 alleviates salt stress and increases antioxidant activities in Arabidopsis. Journal of Plant Physiology. 193: 12-21.
Zargari, A. (2011). Medicial Plants. University of Tehran press. P. 85. (In Persian).
Zhu, J.K. (2001). Plant salt tolerance. Trends in Plant Science. 6(2): 66–71.
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Abdallah, II., Van Merkerk, R., Klumpenaar, E., Quax, J.W. (2018). Catalysis of amorpha-4, 11-diene synthase unraveled and improved by mutability landscape guided engineering. Scientific Reports. DOI: 10.1038/s41598-018-28177-4.
Aebi, H. (1984). Catalase in vitro. Methods in Enzymology. 105: 121-126.
Aftab, T., A. Khan, M.M., Idrees, M., Naeem, M., Hashmi, N. and Moinuddin. (2010). Effect of Salt Stress on Growth, Membrane Damage, Antioxidant Metabolism and Artemisinin Accumulation in Artemisia annua L. Plant Stress. 4 (1): 36-43.
Aghai, K., Tayei, N., Kanaani, M.R. and Yazdani, M. (2014). The effect of salinity stress on some physiological and biochemical traits of two species of Salvia. Plant Process and Function. 3 (9): 96-85.
Ahmed, H. A.A., Koçak Şahin, N., Akdoğan, G., Yaman, C., Köm, D. and Uranbey, S. )2020(.Variability in salinity stress tolerance of potato (Solanum tuberosum L.) varieties using in vitro screening. Ciência e Agrotecnologia. http://dx.doi.org/10.1590/1413-7054202044004220
Ahmed, S., Ahmed, Sh., Roy, S.K., Woo, S.H., Sonawane, K.D. and Shohael, A.M. (2019). Effect of salinity on the morphological, physiological and biochemical properties of lettuce (Lactuca sativa L.) in Bangladesh. De Gruyter. 4: 361–373.
Alam, P., Kiran, U., Ahmad, M.M., Kamaluddin., Ali Khan, M., Jhanwar, Sh. and Abdin, M.Z. (2010). Isolation, characterization and structural features of amorpha- 4, 11-diene synthase (ADS3963) from Artemisia annu L. Bioinformation. 4(9): 421-429.
Amini, F. and Ehsanpour, A.A. (2005). Soluble proteins,proline, carbohydrates and Na+/K+ changes intwo tomato (Lycopersicon esculentum Mill.) cultivars under in vitro salt stress. American Journal of Biochemistry and Biotechnology. 1(4): 212-216.
Appel, K. and Hirt, H. (2004). Reactive oxygen species: metabolism, oxidative stress and signal transduction. Annual Review of Plant Biology. 55(1): 373-399.
Asada, K. (1999). The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons, Annual Review of Plant Biology. 50: 601–639.
Bates, L.S. )1973(. Rapid determination of free proline for water stress studies. Plant Soil. 39: 205-207.
Board, R., Reza Zadeh, Sh.Gh., Omidi, M., Torabi, S., Hariri Akbari, Ph., Parvaneh, S. and Taghizad Farid, R. (2013). Investigation of Quantitative diversity Artemisinin of Artemisia annua in plant populations native in northern Iran. Scientific-Research Quarterly of Plant and Ecosystem. 9 (35): 50-43.
Boughalleb, F., Abdellaoui, R., Mahmoudi, M. and Bakhshandeh, E. (2020). Changes in phenolic profile, soluble sugar, proline, and antioxidant enzyme activities of Polygonum equisetiforme in response to salinity. Turkish Journal of Botany. 44(1): 25-35.
Box, S. and Schachtman, D. P. (2011).The effect of low concentrations of sodium on potassium uptake and growth of wheat. Australian Journal of Plant Physiology. 27: 175-182.
Bradford, M.M. )1976(. Arapid and sensitive method for the quantitation of microgram quantities of protein uti-lizing the principle of protein day binding. Analytical Biochemistry. 72: 248-254.
Chance, B. and Maehly, A.C.)1995(. Assay of catalase and peroxidases. Methods of Enzymology. 11: 764-775.
Daneshmand, F., Arvin, M.J. and Kalantari, Kh.M. (2009).Effect of Acetylsalicylic Acid (Aspirin) on Salt and Osmotic Stress Tolerance in Solanum bulbocastanum in Vitro: Enzymatic Antioxidants. American-Eurasian Journal Agriculture and Environmental Science. 6 (1): 92-99.
Dash, M. and Panda, S. (2001). Salt Stress Induced Changes in Growth and Enzyme Activities in Germinating Phaseolus Mungo Seeds. Biologia Plantarum. 44(4): 587–589.
Dhindsa, R.A., Plumb-Dhindsa, P. and Thorpe, T.A. (1981). Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. Journal of Experimental Botany. 126: 93-101.
Davey, M.W., Stals, E., Panis, B., Keulemans, J. and Swennen, R.L. (2005). High-throughput determination of malondialdehyde in plant tissues. Analytical Biochemistry. 347: 201-207.
Doğan, M. (2011). Antioxidative and proline potentials as a protective mechanism in soybean plants under salinity stress. African Journal of Biotechnology. 10(32): 5972-5978.
Demiral, T. and Turkan, I. (2005). Comparative lipid peroxidation, antioxidant defense systems and proline content in roots of two rice cultivars differing in salt tolerance. Environmental and Experimental Botany. 53(3): 247–257.
Emami Bistgani, Z., Hashemi, M., DaCosta, M., Craker, L., Maggic, F. and Morshedloo, M.R. (2019). Effect of salinity stress on the physiological characteristics, phenolic compounds and antioxidant activity of Thymus vulgaris L. and Thymus daenensis Celak. Industrial Crops and Products. 135: 311-320.
Farhoudi, R. (2012). Effect of salinity stress on alpha-amylase enzyme activity, cell membrane permeability and seedling growth of rapeseed cultivars. Plant Process and Function. 1(1): 24-14.
Farhoudi, R. (2013). Investigation of the effect of salinity stress on growth and histological characteristics of nine wheat cultivars in vegetative growth stage. Journal of Crop Physiology - Islamic Azad University, Ahvaz Branch. 5 (20): 86-71.
Fabriky Aurang, S. and Davoodnia, B. (2018). Evaluation of changes in growth traits and secondary metabolites in Thymus vulgaris L.under mild salinity and drought stress. Journal of Ecophytic Chemistry of Medicinal Plants. 6(2): 40-27.
Gapinska, M., Sklodowska, M. and Gabara, B. (2008) . Effect of short- and long-term salinity on the activities of antioxidative enzymes and lipid peroxidation in tomato roots. Acta Physiologia Plantarum. 30: 11-18.
Gehanbazy Gojani, H., Hosseini Nasr, S., Saqib Talebi, Kh. and Hojjati, S. (2014). The Effect of salinity stress on vegetative factors, proline, plant pigments and nutrient uptake in shoots of four species of wild almonds. Journal of Plant Research (Iranian Journal of Biology). 27 (5): 787-777.
Golkar, P., Amooshahi, F. and Arzani, A. (2017). The effects of salt stress on physio-biochemical traits, total phenolic and mucilage content of Plantago ovata Forsk under in vitro conditions. Journal of Applied Botany and Food Quality. 90: 224 - 231.
Gupta, K.J., Stoimenova, M. and Kaiser, W.M. (2005). In higher plants, only root mitochondria, but not leaf mitochondria reduce nitrite to NO, in vitro and in situ, Journal of Experimental Botany. 56(420): 2601–2609.
Heath, R.L. and Packer, L. (1969). Photoperoxidation in isolated chloroplast. I. kinetics and stoichiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysics. 125: 189-198.
Hosseini, R., Yazdani, N., Garoosi, GA. (2011). The presence of amorpha-4, 11-diene synthase, a key enzyme in artemisinin production in ten Artemisia species. Daru. 19: 332-337.
Hussein, M.M., Balbaa, L.K. and Gaballah, M.S. )2007). Salicylic Acid and Salinity Effects onGrowth of Maize Plants. Research Journal of Agriculture and Biological Sciences. 3( 4): 321 - 328.
Jahanbakhsh GodehKahriz, S., Khadem Sedighi, S., Ebadi, Gh., Tavakoli, N. and Davari, M. (2017). The effect of salinity stress on the expression of salinity resistance proteins and antioxidant activity in Echium amoenum using calcium. Genetic Engineering and Biosafety. 6 (1): 129-117.
Jahantigh, O., Najafi, F., Naghdi badi, H.A., Khavari-nejad, R.A. and Sanjarian, F. (2015). Changes In Antioxidant Enzymes Activities and Proline, Total Phenol And Anthocyanine Contents In Hyssopus OfficinalisL. Plants Undersalt Stress. Acta Biologica Hungarica. 67(2): 195–204.
Kafi, M. and Rahimi, Z. (2011). Effect of salinity and silicon on root characteristics, growth, waterstatus, proline content and ion accumulation of purslane (Portulaca oleracea L.).Soil Science and Plant Nutrition. 57(2): 341-347.
Karmian, R. and Atai Barazandeh, S. (2012). Study of the effect of salinity stress on some growth indices in three species of sainfoin (Onobrychis) in Iran. Plant Biology. 5 (15): 82-69.
Khalid, H., Kumari, M., Grover, A. and Nasim, M. (2015). Salinity Stress Tolerance of Camelina InvestIgated in vitro. Scientia Agriculturae Bohemica. 46(4): 137–144.
Khan Kayani, W., Hafeez Kiani, B., Dilshad, E. and Mirza, B. (2018). Biotechnological approaches for artemisinin production in Artemisia. World Journal of Microbiology and Biotechnology. 34: 1-14.
Khan, M.A., A. Ungar, I. and M. Showalter, A. (2000). The effect of salinity on the growth, water status, and ion content of a leaf succulent perennial halophyte, Suaeda fruticosa (L.) Forssk. Journal of Arid Environments. 45: 73–84.
Koul, B., Taak, P., Kumar, A., Khatri, T. and Sanyal, I. (2017). The Artemisia Genus: A Review on Traditional Uses, Phytochemical Constituents, Pharmacological Properties and Germplasm Conservation. Journal of Glycomics and Lipidomics.7:1-7.
Li, J., Zhao, G .Zh., Varma, A., Qin, Sh., Xiong, Zh., Huang, H.Y., Zhu, W.Y., Zhao, L.X., Xu, L. H., Zhang, S. and Li, W.J. (2012). An Endophytic Pseudonocardia Species Induces the Production of Artemisinin in Artemisia annua. Public Library of Science One. 7: 1-9.
Livak, K.J. and Schmittgen, Th.D. (2001). Analysis of Relative Gene Expression Data Using Real- Time Quantitative PCR and the 22DDCT Method, Methods. 25: 402–408.
Maqsoomi Holaso, S. and Pourakbar, L. (2014). Effects of salinity on growth and some physiological parameters of wheat seedlings. Plant Biology of Iran. 6(19):31-42.
Matysik, J., Alia, B.B. and Mohanty, P. (2002). Molecular mechanisms of quenching of reactive oxygen species by proline under stress in plants. Current Science. 82: 525–532.
Meloni, D.A., Oliva, M.A., Martinez, C.A. and Cambraia, J.)2003). Photosynthesis and ctivity of superoxide dismutase, peroxidase and gluthatione reductase in cotton under salt stress. Environmental and Experimental Botany. 49: 69-76.
Motamedi, M.and Farhoudi, R. (2010).Effect of Salt Stress on Antioxidant Activity and Seedling Growth of Safflower Cultivars. International Journal of Applied Agricultural Research. 5(3): 367-375.
Olofsson, L., Engstrom, A., Lundgren, A. and Brodelius, P.E. (2011). Relative expression of genes of terpene metabolism in different tissues of Artemisia annua L. BMC Plant Biology. 11: 1-12.
Omidi, M., Khandan-Mirkohi, A.Gh., Kafi, M. and Zamani, Z.A. (2021). Investigation of The effect of salinity stress on some morphological and physiological indices of Rosa damascena Kashan genotype. Iranian Horticultural Sciences. 51(1): 17-1.
Prasad, A., Kumar, D., Anwar, M., Singh, D.V. and Jain, D.C. (1996). Response of Artemisia annua L. to Soil Salinity. Journal of Herbs, Spices & Medicinal Plants. https://doi.org/10.1300/J044v05n02_07 .
Qian, Zh., Gong, K., Zhang, L., Lv, J., Jing, F., Wang ,Y., Guan, Sh., Wang, G. and Tang, K. (2007). A simple and efficient procedure to enhance artemisinin content in Artemisia annua L. by seeding to salinity stress. Full Length Research Paper. 6: 1410-1413.
Ranjan, R., Bohra, S.P. and Jeet, A.M. (2001). Book of plant senescence. Jodhpur Agrobios New York. 18-42.
Razavizadeh, R. and Ehsanpour, A.A. (2009). Effects of salt stress on proline content, expression of delta -1-pyrroline-5-carboxylate synthetase, and activities of catalase and ascorbate peroxidase in transgenic tobacco plants. Biological Plantarum. 46(2): 63-75.
Razavizadeh, R. and Mohagheghian, N. (2015). Investigation of changes in antioxidant enzyme activity and secondary metabolites of thyme seedlings (Thymus vulgaris) under salinity stress under in vitro culture conditions. Plant Biology of Iran. 8 (26): 58-41.
Ronald, S.F. and Laima, S.K. (1999). Phenolicsand cold tolerance of Brassica napus. Plant Agriculture. 1: 1-5.
Saeedipoor, S. (2017). Effect of salinity stress on yield, concentration and distribution of some elements in different organs of two cultivars Barbej (Oriza sativa L.). Journal of Crop Physiology - Islamic Azad University, Ahvaz Branch. 9 (36): 40-27.
Samia, M., Tahani, A., Hathout, A., R.Ahsour, A. and Abd Almalik, A. (2009). Brassinolide and Salinity Acid Induced Antioxidant Enzymes, Hormonal Balance and Protein Profile of Maize Plants Grown under Salt Stress. Research Journal of Agriculture and Biological Sciences. 5(4): 391-402.
Savarus, A., Ja Oua, S., Hua, X.J., Ardiles, W., Van.Montago, M. and Verbruggen, N. (1995). Isolation, Characterization, and Chromosomal Location of Gene Encoding the 1-pyroline-5-carboxylate Synthetase in Arbidobsis Thaliana. Federation of European Biochemical Societies. 372: 13-19.
Shahnazi, M., Azadmehr, A., Hajiaghaee, R., Mosalla, S. and Latifi, R. (2015). Effects of Artemisia Absinthium L. Extract on the Maturation and Function of Dendritic Cells. Jundishapur Journal of Natural Pharmaceutical Products. 10: 1-6.
Sharma, T., Dreyer, I., Riedelsberger, J. (2013). The role of K+ channels in uptake and redistribution of potassium in the model plant Arabidopsis thaliana. Frontiers in Plant Science. 4: 1-16.
Shen, Q., Chen, Y.F., Wang, T., Wu, S.Y., Lu, X., Zhang, L., Zhang, F.Y., Jiang, W.M., Wang, G.F. and Tang, K.X. (2012). Overexpression of the cytochrome P450 monooxygenase (cyp71av1) and cytochrome P450 reductase (cpr) genes increased artemisinin content in Artemisia annua (Asteraceae).Genetics and Molecular Research. 11 (3): 3298-3309.
Teoh, K.H., Polichuk, D.R., Reed, D.W., Nowak, G., Covello, P.S. (2006). Artemisia annua L. (Asteraceae) trichome-specific cDNAs reveal CYP71AV1, a cytochrome P450 with a key role in the biosynthesis of the antimalarial sesquiterpene lactone artemisinin. The Federation of European Biochemical Societies Letters. 580:1411–1416.
Valifard, M., Mohsenzadeh, S., Kholdebarin, B. and Rowshan, V. (2014).Effects of salt stress on volatile compounds, total phenolic content and antioxidant activities of Salvia mirzayanii. South African Journal of Botany. 93: 92–97.
Wasim, A., hasan, A., Abdullah, A. and Tarannum, T. (2010). Medicinal I mportance of Artemisia absinthium Linn (Afsanteen) in Unani Medicine: A Review. Hippocratic Journal of Unani Medicine. 5: 117-125.
Wimmer, M.A., Muhiling, K.H., Lauchli, A., Brown, P.H. and Goldbach, H.E. (2003). The Interaction between Salinity and Boron Toxicity Effects the Subcellular Distribution of ions Proteins in Wheat Leaves. Plant Cell and Environmental. 26: 2567-1271.
Yarizadeh, K., Hosseini, R. and Moghaddami, M. (2015). Gene studyADS, DBR2 and SQS in five species of Different artemisia. Plant Biology of Iran .7 (25): 52-43.
Younis, A., Riaz, A., Hasan, S.U., Mustaq, N. and Hameed, M. (2014). Response of Hedera helix (English Ivy) to various salinity levels. Journal of Horticulture, Forestry and Biotechnology. 18(1): 1-6.
Zaidi, I. and Hanin, M. (2016). The wheat MAP kinase phosphatase 1 alleviates salt stress and increases antioxidant activities in Arabidopsis. Journal of Plant Physiology. 193: 12-21.
Zargari, A. (2011). Medicial Plants. University of Tehran press. P. 85. (In Persian).
Zhu, J.K. (2001). Plant salt tolerance. Trends in Plant Science. 6(2): 66–71.