Effects of phenology on the activity and gene expression of phenolic acid -biosynthetic enzymes in Salvia leriifolia Benth.

- Abrishamchi, P., Khaje Karamadini, M., Houshyar Sarjami, R., Zaker, A., Asili, J., Porsa H. and Zarif, R., 2016. Antibacterial effect of essential oils from Salvia leriifolia Benth. against some oral pathogens. Journal of Microbial World, 9(3): 215-225.

- Achakzai, A.K.K., Achakzai, P., Masood, A., Kayani, S.A. and Bakhsh Tareen, R., 2009. Response of plants parts and age on the distribution of secondary metabolites on plants found in Quetta. Pakistan Journal of Botany, 41(5): 2129-2135.

- Adomako-Bonsu, A.G., Chan, S.L., Pratten, M. and Fry, J.R., 2017. Antioxidant activity of rosmarinic acid and its principal metabolites in chemical and cellular systems: Importance of physico-chemical characteristics. Toxicology in vitro, 40(1): 248-255.

- Alagawany, M., Abd El-Hack, M.E., Farag, M.R., Gopi, M., Karthik, K., Malik, Y.S. and Dhama, K., 2017. Rosmarinic acid: modes of action, medicinal values and health benefits. Animal Health Research Reviews, 18(2): 167-176.

- Alizadeh, A., Alizadeh, O., Amari, G. and Zare, M., 2013. Essential oil composition, total phenolic content, antioxidant activity and antifungal properties of Iranian Thymus daenensis subsp. daenensis Celak. as in influenced by ontogenetical variation. Journal of Essential Oil Bearing Plants, 16(1): 59-70.

- Amiri, M.S. and Joharchi, M.R., 2013. Ethnobotanical investigation of traditional medicinal plants commercialized in the markets of Mashhad, Iran. Avicena Journal of Phytomedicine, 3(3): 254-271.

- Baâtour, O., Tarchoun, I., Nasri, N., Kaddour, R., Harrathi, J., Drawi, E., Ben Nasri-Ayachi, M., Marzouk, B. and Lachaâl, M., 2012. Effect of growth stages on phenolics content and antioxidant activities of shoots in sweet marjoram (Origanum majorana L.) varieties under salt stress. African Journal of Biotechnology, 11(99): 16486-16493.

- Bączek, K., Przybyl, J.L., Kosakowska, O. and Węglarz, Z., 2017. Accumulation of phenolics in eleuthero (Eleutherococcus senticosus (Rupr. et Maxim.) Maxim.) as affected by plant development. Acta Scientiarum Polonorum Hortorum Cultus, 16(4): 89-99.

- Bradford, M.M., 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72(1-2): 248-254.

- Brahmi, F., Mechri, B., Dhibi, M. and Hammami, M., 2015. Effect of growth stage and solvent extract on the antioxidant potential of olive leaves. Journal of Plant Sciences, 3(3-1): 1-7.

- Brasileiro, B.G., Leite, J.P.V., Casali, V.W.D., Pizziolo, V.R. and Coelho, O.G.L., 2015. The influence of planting and harvesting times on the total phenolic content and antioxidant activity of Talinum triangulare Jacq. wild. Acta Scientiarum, 37(2): 249-255.

- Chen, Y., Zhu, Z., Guo, Q., Zhang, L. and Zhang, X., 2012. Variation in concentrations of major bioactive compounds in Prunella vulgaris L. related to plant parts and phenological stages. Biological Research, 45(2): 171-175.

- Cirak, C., Radusiene, J., Janulis, V. and Ivanauskas, L., 2007. Secondary metabolites in Hypericum perfoliatum: variation among plant parts and phonological stages. Botanica Helvetica, 117(1): 29-36.

- Di, P., Zhang, L., Chen, J., Tan, H., Xiao, Y., Dong, X., Zhou, X. and Chen, W., 2013. ¹³C tracer reveals phenolic acids biosynthesis in hairy root cultures of Salvia miltiorrhiza. ACS Chemical Biology, 8(7): 1537-1548.

- Dong, J., Wan, G. and Liang, Z., 2010. Accumulation of salicylic acid-induced phenolic compounds and raised activities of secondary metabolic and antioxidative enzymes in Salvia miltiorrhiza cell culture. Journal of Biotechnology, 148(2-3): 99-104.

- Döring, A.S., Pellegrini, E., Della Batola, M., Nali, C., Lorenzini, G. and Petersen M., 2014. How do background ozone concentrations affect the biosynthesis of rosmarinic acid in Melissa officinalis? Journal of Plant Physiology, 171(5): 35-41.

- Erish, S., Mohammadzadeh, M., Ilkhanipour, M. and Babaei, F., 2018. The effect of hydroalcoholic extract of Salvia leriifolia root and fluvoxamine on the spatial memory in male rats under immobilization stress. Qom University Medical Sciences Journal, 11(11): 22-32.

- Espindola, K.M.M., Ferreira, R.G., Narvaez, L.E.M., Silva Rosario, A.C.R., da Silva, A.H.M, Silva, A. G.B., Vieira, A.P.O. and Monteiro, M.C., 2019. Chemical and pharmacological aspects of caffeic acid and its activity in hepatocarcinoma. Frontiers in Oncology, 9: 1-10.

- Fazly-Bazzaz, B.S. and Izadyar, A.R., 2002. Antimutagenic activity of different fractions of Salvia leriifolia extract. Iranian Journal of Basic Medical Sciences, 4(4/12): 241-250.

- Fletcher, R.S., Slimmon, T. and Kott, L.S., 2010. Environmental factors affecting the accumulation of rosmarinic acid in spearmint (Mentha spicata L.) and peppermint (Mentha piperita L.). The Open Agriculture Journal, 4(1): 10-16.

- Fotovvat, M., Radjabian, T. and Saboora, A., 2019. HPLC fingerprint of important phenolic compounds in some Salvia L. species from Iran. Records of Natural Products, 13(1): 37-49.

- Fritz, R.S., Hochwender, C.G., Lewkiewicz, D.A., Bothwell, S. and Orians, C.M., 2001. Seedling herbivory by slugs in a willow hybrid system: Developmental changes in damage, chemical defense and plant performance. Oecologia, 129(1): 87-97.

- Ghasemzadeh, A., Jaafar, H.Z.E., Ashkani, S., Rahmat, A., Juraimi, A.S., Puteh, A. and Muda Mohamed, M.T., 2016. Variation in secondary metabolite production as well as antioxidant and antibacterial activities of Zingiber zerumbet (L.) at different stages of growth. BMC Complementary and Alternative Medicine, 16(1): 1-10.

- Habtemariam, S., 2018. Molecular pharmacology of rosmarinic and salvianolic acids: Potential seeds for alzheimer’s and vascular dementia drugs. International Journal of Molecular Scinces, 19(2): 1-25.

- Hao, W., Guo, H., Zhang, J., Hu, G., Yao, Y. and Dong, J., 2014. Hydrogen peroxide is involved in salicylic acid-elicited rosmarinic acid production in Salvia miltiorrhiza cell cultures. The Scientific World Journal, 2014: 1-7.

- Hao, D.C., Gu, X.J. and Xiao, P.G., 2015. Medicinal Plants: Chemistry, Biology and Omics. Cambridge, UK, Woodhead Publishing, 664p.

- Ho, J.H.C. and Hong, C.Y., 2011. Salvianolic acids: small compounds with multiple mechanisms for cardiovascular protection. Journal of Biomedical Science, 18(30): 1-5.

- Holander-Czytko, H., Grabowski, J., Sandorf, I., Weckermann, K. and Weiler, E. W., 2005. Tocopherol content and activities of tyrosine aminotransferase and cysteine lyase in Arabidopsis thaliana under stress conditions. Journal of Plant Physiology, 162(7): 767-770.

- Hosseinzadeh, H., Sadeghnia, H.R., Imenshahidi, M. and Fazly Bazzaz, B.S., 2009. Review of the pharmacological and toxicological effects of Salvia leriifolia. Iranian Journal of Basic Medical Sciences, 12(1): 1-8.

- Hosseinzadeh, H. and Lari, P., 2000. Effect of Salvia leriifolia extract on morphine dependence in mice. Phytotherapy Research, 14(5): 384-387.

- Hou, J., Fu, J., Zhang, Z.M. and Zhu, H.L., 2011. Biological activities and chemical modifications of caffeic acid derivatives. Fudan University Journal of Medical Science, 38(6): 546-552.

- Hu, Y.S., Zhang, L., Di, P. and Chen, W.S., 2009. Cloning and induction of phenylalanine ammonia-lyase gene from Salvia miltiorrhiza and its effect on hydrophilic phenolic acids levels. Chinese Journal of Natural Medicines, 7(6): 0449-0457.

- Imtiyaz, M., Omi Laila, M., Abdin, M.Z., Parveen, K., Raja, T., Abid Ali, S. and Sharma, G., 2013. Maximum phenylalanine ammonia lyase (PAL) enzyme activity at mid stage of growth imparts highest hypoglycemic property to fenugreek. Current Trends in Biotechnology and Pharmacy, 7(4): 837-846.

- Ishikura, N., 1976. Seasonal changes in contents of phenolic compounds and sugar in Rhus, Euonymus and Acer leaves with special reference to anthocyanin formation in autumn. The Botanical Magazine Tokyo, 89(1016): 251-257.

- Jami, S., Esmaeilzadeh Bahabadi, S. and Modarres, M., 2018. Effect of chitosan on micropropagation, secondary metabolites content and antioxidant activity of Salvia leriifolia Benth. Journal of Plant Research (Iranian Journal of Biology), 31(3): 710-725.

- Jiang, R.W., Lau, K.M., Hon, P.M., Mak, T., Woo, K.S. and Fung, K.P., 2005. Chemistry and biological activities of caffeic acid derivatives from Salvia miltiorrhiza. Current Medicinal Chemistry, 12(2): 237-246.

- Jiang, X., Liu, Y., Li, W., Zhao, L., Meng, F., Wang, Y., Tan, H., Yang, H., Wei, C., Wan, X., Gao, L. and Xia, T., 2013. Tissue-specific, development-dependent phenolic compounds accumulation profile and gene expression pattern in tea plant (Camellia Sinensis). PLOS One, 8(4): 1-14.

- Jiao, M., Cao, R., Chen, H., Hao, W. and Dong, J., 2012. Effects of salicylic acid on synthesis of rosmarinic acid and related enzymes in the suspension cultures of Salvia miltiorrhiza. Chinese Journal of Biotechnology, 28(3): 320-328.

- Kamalizadeh, M., Bihamta, M., Peyghambari, S.A. and Hadian, J., 2014. Expression of genes involved in rosmarinic acid biosynthesis pathway in dragonhead affected by nanoparticles. Genetics in the Third Millennium, 12(1): 3428-3437.

- Kamatou, G.P.P., Viljoen, A.M., Gono-Bwalya, A.B., van Zyl, R.L., Van Vuuren, S.F., Lourens, A.C. U., Baser, K.H.C., Demirci, B., Lindsey, K.L. Van Staden, J. and Steenkamp, P., 2005. The in vitro pharmacological activities and a chemical investigation of three South African Salvia species. Journal of Ethnopharmacology, 102(3): 382-390.

- Khouei, A.R., Hosseinzadeh, H. and Imanshahidi, M., 2003. Pathologic evaluation of anti-ischemic effect of Salvia leriifolia Benth. seed and leaf extracts in rats after global cerebral ischemia. Iranian Journal of Basic Medical Sciences, 5(4): 200-205.

- Lavola, A., Julkunen-Tiitto, R., De La Rosa, T.M., Lehto, T. and Aphalo, P.J., 2000. Allocation of carbon to growth and secondary metabolites in birch seedlings under UV-B radiation and CO₂ exposure. Physiologia Plantarum, 109(3): 260-267.

- Li, M.H., Chen, J.M., Peng, Y. and Xiao, P.G., 2008. Distribution of phenolic acids in Chinese Salvia plants. Word Science and Technology, 10(5): 46-52.

- Li, M.H., Li, Q.Q., Liu, Y.Z., Cui, Z.H., Zhang, N., Huang, L.Q. and Xiao, P.G., 2013. Pharmacophylogenetic study on plants of genus Salvia L. from China. Chinese Herbal Medicines, 5(3): 164-181.

- Li, Q., Feng, J., Chen, L., Xu, Z., Zhu, Y., Wang, Y., Xiao, Y., Chen, J., Zhou, Y., Tan, H., Zhang, L. and Chen, W., 2019. Genome-wide identification and characterization of Salvia miltiorrhiza laccases reveal potential targets for salvianolic acid B biosynthesis. Frontiers in Plant Science, 10: 1-15.

- Loizzo, M.R., Tundis, R., Conforti, F., Menichini, F., Bonesi, M., Nadjafi, F., Giuseppe Frega, N. and Menichini, F., 2010. Salvia leriifolia Benth. (Lamiaceae) extract demonstrates in vitro antioxidant properties and cholinesterase inhibitory activity. Nutrition Research. 30(12): 823-830.

- Lu, Y. and Foo, L.Y., 2002. Polyphenolics of Salvia-a review. Phytochemistry, 59(2): 117-140.

- Ma, X.H., Ma, Y., Tang, J.F., He, Y.L., Liu, Y.C., Ma, X.J., Shen, Y., Cui, G.H., Lin, H.X., Rong, Q.X., Guo, J. and Huang, L.Q., 2015. The Biosynthetic pathways of tanshinones and phenolic acids in Salvia miltiorrhiza. Molecules, 20(9): 16235-16254.

- Ma, L., Tang, L. and Yi, Q., 2019. Salvianolic acids: Potential source of natural drugs for the treatment of fibrosis disease and cancer. Frontiers in Pharmacology, 10: 1-13.

- Matkowski, A., Zielinska, S., Oszmianski, J. and Lamer-Zarawska, E., 2008. Antioxidant activity of extracts from leaves and roots of Salvia miltiorrhiza Bunge, S. przewalskii Maxim., and S. verticillata L. Bioresource Technology, 99(16): 7892-7896.

- Mizukami, H. and Ellis, B.E., 1991. Rosmarinic acid formation and differential expression of tyrosine aminotransferase isoforms in Anchusa officinalis cell suspension cultures. Plant Cell Reports, 10(6-7): 321-324.

- Moridi Farimani, M., Miran, M. and Nejad Ebrahimi, S., 2019. New diterpenoids from the aerial parts of Salvia reuterana. Iranian Journal of Pharmaceutical Research, 18(1): 406-411.

- Mozaffarian, V., 2007. A Dictionary of Iranian Plant Names, Latin-English-Persian.Tehran, Iran, Farhang Mo’aser, 740p.

- Mutalib, L.Y., 2015. Effect of gowth age period on biochemical composition of Plantago major plant. International Journal of Current Research and Review, 7(19): 6-10.

- Naghiloo, S., Movafeghi, A., Delazar, A., Nazemiyeh, H., Asnaashari, S. and Dadpour, M.R., 2012. Ontogenetic variation of total phenolics and antioxidant activity in roots, leaves and flowers of Astragalus compactus Lam. (Fabaceae). BioImpacts, 2(2): 105-109.

- Ngo, Y.L. and Chua, L.S., 2018. Anti-diabetic activity of rosmarinic acid rich fractions from Orthosiphon stamineus. Current Enzyme Inhibition, 14(2): 97-103.

- Norouzi, E., Hosseini, B., Maleki, R. and Abdollahi Mandoulakani, B., 2019. Iron oxide nanoparticle a novel elicitor to enhancing anticancer flavonoid production and gene expression in Dracocephalum kotschyi hairy root cultures. Journal of the Science of Food and Agriculture, 99(14): 6418-6430.

- Ogata, A., Tsuruga, A., Matsuno, M. and Mizukami, H., 2004. Elicitor-induced rosmarinic acid biosynthesis in Lithospermum erythrorhizon cell suspension cultures: Activities of rosmarinic acid synthase and the final two cytochrome P450-catalyzed hydroxylations. Plant Biotechnology, 21(5): 393-396.

- Papageorgiou, V., Gardeli, C., Mallouchos, A., Papaioannou, M. and Komaitis, M., 2008. Variation of the chemical profile and antioxidant behavior of Rosmarinus officinalis L. and Salvia fruticosa Miller grown in Greece. Journal of Agricultural and Food Chemistry, 56(16): 7254-7264.

- Pasko, P., Barto, H., Zagrodzki, P., Gorinstein, S., Fota, M. and Zachwieja, Z., 2009. Anthocyanins, total polyphenols and antioxidant activity in amaranth and quinoa seeds and sprouts during their growth. Food Chemistry, 115(3): 994-998.

- Petersen, M., 2013. Rosmarinic acid: new aspects. Phytochemistry Reviews, 12(1): 207-227.

- Pourmorad, F., Hosseinimehr, S.J. and Shahabimajd, N., 2006. Antioxidant activity, phenol and flavonoid contents of some selected Iranian medicinal plants. African Journal of Biotechnology, 5(11): 1142-1145.

- Rechinger, K.H., 1996. Flora Iranica. Graz, Austria, Akademische Druck-und Verlagsanstalt, 234p.

- Reis, E., Batista, M.T. and Canhoto, J.M., 2008. Effect and analysis of phenolic compounds during somatic embryogenesis induction in Feijoa sellowiana Berg. Protoplasma, 232(3-4): 193-202.

- Ru, M., An, Y., Wang, K., Peng, L., Li, B., Bai, Z., Wang, B. and Liang, Z., 2016. Prunella vulgaris L. hairy roots: Culture, growth, and elicitation by ethephon and salicylic acid. Engineering in Life Sciences, 16(5): 494-502.

- Ru, M., Wang, K., Bai, Z., Peng, L., He, S., Wang, Y. and Liang, Z., 2017. A tyrosine aminotransferase involved in rosmarinic acid biosynthesis in Prunella vulgaris L. Scientific Reports, 7(1): 1-16.

- Sahu, R., Gangopadhyay, M. and Dewanjee, S., 2012. Elicitor-induced rosmarinic acid accumulation and secondary metabolism enzyme activities in Solenostemon scutellarioides. Acta Physiologiae Plantarum, 35(5): 1473-1481.

- Scarpati, M.L. and Oriente, G., 1958. Isolation and constitution of rosmarinic acid from Rosmarinus officinalis. La Ricerca Scientifica, 28(11): 2329-2333.

- Sharma, A., Shahzad, B., Rehman, A., Bhardwaj, R., Marco Landi, M. and Zheng, B., 2019. Response of phenylpropanoid pathway and the role of polyphenols in plants under abiotic stress. Molecules, 24(13): 1-22.

- Shokrollahi, S.H., Heshmatii, G.H.A. and Yosefzadeh, H., 2018. Study the phenolic compounds and antioxidant activity of the extract lily (Lilium ledebourii (Baker) Boiss.). Journal of Fasa University of Medical Sciences, 8(2): 727-734.

- Soltanabad, M.H., Bagherieh-Najjar, M.B. and Mianabadi, M., 2018. Seasonal variations in carnosic acid content of rosemary correlates with anthocyanins and soluble sugars. Journal of Medicinal Plants and By-products, 2: 163-171.

- Song, J., Ji, Y.Y., Xu, K. and Wang, Z.Z., 2012. An integrated analysis of the rosmarinic acid-biosynthetic genes to uncover the regulation of rosmarinic acid pathway in Salvia miltiorrhiza. Acta Physiologia Plantarum, 34(4): 1501-1511.

- Song, Z. and Li, X., 2015. Expression profiles of rosmarinic acid biosynthesis genes in two Salvia miltiorrhiza lines with differing water-soluble phenolic contents. Industrial Crops and Products, 71: 24-30.

- Suwa, R., Tajima, H., Gima, S., Uehara, N., Kenta Watanabe, K., Yabuta, S., Tominaga, J. and Kawamitsu, Y., 2018. Polyphenol production in Peucedanum japonicum Thunb. varies with soil type and growth stage. The Horticulture Journal, 87(3): 382-388.

- Topcu, G., 2006. Bioactive triterpenoids from Salvia species. Journal of Natural products, 69: 482-487.

- Truong, D.M., Thu, N.T.B. and Nghi, L.T., 2010. Accumulation and variation of rosmarinic acid content in Orthosiphon stamineus Benth. based on phonological stages. Academia Journal of Biology, 32(3): 65-71.

- Vagiri, M., Conner, S., Stewart, D., Andersson, S.C., Verrall, S., Johansson, E. and Rumpunen, K., 2015. Phenolic compounds in black currant (Ribes nigrum L.) leaves relative to leaf position and harvest date. Food Chemistry, 172: 135-142.

- Verma, V. and Kasera, P., 2007. Variations in secondary metabolites in some Arid zone medicinal plants in relation to season and plant growth. Indian Journal of Plant Physiology, 12(2): 203-206.

- Voght, T., 2010. Phenylpropanoid biosynthesis. Molecular Plant, 3(1): 2-20.

- Wam, H.K., Stolter, C. and Nybakken, L., 2017. Compositional changes in foliage phenolics with plant age, a natural experiment in Boreal forests. Journal of Chemical Ecology, 43(9): 920-928.

- Wang, B.Q., 2010. Salvia miltiorrhiza: Chemical and pharmacological review of a medicinal plant. Journal of Medicinal Plants Research, 4(25): 2813-2820.

- Wang, J., Xu, J., Gong, X., Yang, M., Zhang, C. and Li, M., 2019. Biosynthesis, chemistry, and pharmacology of polyphenols from Chinese Salvia species: A review. Molecules, 24(1): 132-155.

- Weitzel, C. and Petersen, M., 2011. Cloning and characterization of rosmarini aid synthase from Melissa officinalis L. Phytochemistry, 72: 572-578.

- Wu, W.Y. and Wang, Y.P., 2012. Pharmacological actions and therapeutic applications of Salvia miltiorrhiza depside salt and its active components, Acta Pharmacologica Sinica, 33(9): 1119-1130.

- Xiao, Y., Gao, S., Di, P., Chen, J., Chen, W. and Zhang, L., 2009. Methyl jasmonate dramatically enhances the accumulation of phenolic acids in Salvia miltiorrhiza hairy root cultures. Physiologia Plantarum, 137(1): 1-9.

- Xing, B., Yang, D., Guo, W., Liang, Z., Yan, X., Zhu, Y. and Liu, Y., 2015. Ag⁺ as a more effective elicitor for production of tanshinones than phenolic acids in Salvia miltiorrhiza hairy roots. Molecules, 20(1): 309-324.

- Yan, Q., Shi, M., Ng, J. and Wu, J.Y., 2006. Elicitor-induced rosmarinic acid accumulation and secondary metabolism enzyme activities in Salvia miltiorrhiza hairy roots. Plant Science, 170(4): 853-858.

- Yang, D., Huang, Z., Xing, B., Jin, W., Yan, X., Guo, Z. and Liang, Z., 2016. Regulation of folic acid on phenolic acids production in Salvia miltiorrhiza hairy roots. Plant Cell Tissue and Organ Culture, 127(1): 175-185.

- Zeng, H., Su, S., Xiang, X., Sha, X., Zhu, Z., Wang, Y., Guo, S., Yan, H., Qian, D. and Duan, J., 2017. Comparative analysis of the major chemical constituents in Salvia miltiorrhiza roots, stems, leaves and flowers during different growth periods by UPLC-TQ-MS/MS and HPLC-ELSD methods. Molecules, 22(5): 1-16.

- Zhang, S., Yan, Y., Wang, B., Liang, Z., Liu, Y., Liu, F. and Qi, Z., 2014. Selective responses of enzymes in two parallel pathways of rosmarinic acid biosynthetic pathway to elicitors in Salvia miltiorrhiza hairy root cultures. Journl of Bioscience and Bioengineering, 117(5): 645-651.

- Ziaei, M., Sharifi, M., Behmanesh, M. and Razavi, K., 2012. Gene expression and activity of phenyl alanine amonialyase and essential oil composition of Ocimum basilicum L. at different growth stages. Iranian Journal of Biotechnology, 10(1): 32-39.