Increased Growth Rate, Lignin, and Shikonin Levels in Onosma dichroantha Bioss. as Affected by Silicon Treatment

Authors
Z. Koolabadi
M. B. Bagherieh
A. Abdolzadeh
Department of Biology, Faculty of Sciences, Golestan University, Gorgan, Islamic Republic of Iran.
Abstract
Onosma dichroantha Boiss. is a local medicinal herb in Iran, belonging to the Boraginaceae family that is used mainly for wound healing due to the presence of shikonin in its root cortex. Optimization of Onosma spp. in vitro cultures and shikonin production is encouraged as an alternative to harvesting the plant from its natural habitats. The present study evaluates the growth rate, several biochemical properties, and shikonin content of O. dichroantha plants treated with various concentrations of silicon (in the form of potassium silicate) in a hydroponic medium. Silicon application up to 0.5 mM increased the fresh mass, chlorophyll a/b, carotenoids, soluble proteins in shoots, and the lignin content in roots; however, phenolic compound contents were not significantly affected. In addition, silicon nutrition increased catalase and soluble ascorbate peroxidase activities, whereas polyphenol oxidase activity was not affected in roots and shoots. Interestingly, the shikonin content of O. dichroantha roots treated with increased concentrations of Si was 2-fold higher than that in the control plants, while the activity of phenylalanine ammonia lyase, a key enzyme in shikonin biosynthesis, was not affected. This suggests that the observed increase in shikonin in response to the silicon treatment could be due to increased stability or more accumulation sites of shikonin in roots. These data may be used for improvement of shikonin production in cell cultures of O. dichroantha under experimental or industrial conditions.

Keywords

Subjects

1. Al-aghabary, K., Zhu, Z. and Shi, Q. 2005. Influence of Silicon Supply on Chlorophyll Content, Chlorophyll Fluorescence, and Antioxidative Enzyme Activities in Tomato Plants under Salt Stress. J. Plant Nutr., 27: 2101–2115.
2. Alberto Moldes, C., Fontao De Lima Filho, O., Manuel Camina, J., Gabriela Kiriachek, S., Lia Molas, M. and Mui Tsai, S. 2013. Assessment of the Effect of Silicon on Antioxidant Enzymes in Cotton Plants by Multivariate Analysis. J. Agric. Food Chem., 61: 11243–11249.
3. Arnon, D.I. 1949. Copper Enzymes in Isolated Chloroplasts. Polyphenoloxidase in Beta Vulgaris. Plant Physiol., 24: 1–15.
4. Bagherieh-Najjar, M. B. and Nezamdoost, T. 2016. Optimization of Shikonin Production in Onosma dichroantha Callus Using Response Surface Methodology. Plant Cell Tissue Organ Cult., 126: 399–409.
5. Bradford, M. M. 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.
6. Cai, K., Gao, D., Luo, S., Zeng, R., Yang, J. and Zhu, X. 2008. Physiological and Cytological Mechanisms of Silicon-Induced Resistance in Rice Against Blast Disease. Physiol. Plant., 134: 324–333.
7. Carver, T. L. W., Robbins, M. P., Thomas, B. J., Troth, K., Raistrick, N. and Zeyen, R. J. 1998. Silicon Deprivation Enhances Localized Autofluorescent Responses and Phenylalanine Ammonia-Lyase Activity in Oat Attacked by Blumeria graminis. Physiol. Mol. Plant Pathol., 52: 245–257.
8. Chen, J., Xie, J., Jiang, Z., Wang, B., Wang, Y. and Hu, X. 2011. Shikonin and Its Analogs Inhibit Cancer Cell Glycolysis by Targeting Tumor Pyruvate Kinase-M2. Oncogene., 30: 4297–4306.
9. Chen, X., Yang, L., Oppenheim, J. J. and Zack Howard, O.M. 2002. Cellular Pharmacology Studies of Shikonin Derivatives. Phyther. Res., 16: 199–209.
10. Delavar, K., Enteshari, S., Gagoonani, S. and Kamali, S. 2016. Effect of Silicon on the Mineral Content of Borage (Borago Officinalis L.) under Aluminum Stress. J. Biol. Sci., 16: 128–135.
11. Fukuda, T., Ito, H. and Yoshida, T. 2003. Antioxidative Polyphenols from Walnuts (Juglans regia L.). Phytochemistry, 63: 795–801.
12. Frew, A., Weston, L. A., Reynolds, l. A. and Gurr, G. M. 2018. The Role of Silicon in Plant Biology: A Paradigm Shift in Research Approach, Annals of Botany, mcy009, https://doi.org/10.1093/aob/mcy009
13. Gaisser, S. and Heide, L. 1996. Inhibition and Regulation of Shikonin Biosynthesis in Suspension Cultures of Lithospermum. Phytochemistry., 41: 1065–1072.
14. Gali, H. U. and Smith, C. C. 1992. Effect of Silicon Supply on Growth, Fertility, and Mineral Composition of an Annual Brome, Bromus secalinus L. (Gramineae). Am. J. Bot., 79: 1259–1263.
15. Guo, Z. G., Liu, H. X., Tian, F. P., Zhang, Z. H. and Wang, S.M. 2006. Effect of Silicon on the Morphology of Shoots and Roots of Alfalfa (Medicago sativa). Aust. J. Exp. Agric., 46: 1161–1166.
16. Gupta, K., Garg, S., Singh, J. and Kumar, M. 2014. Enhanced Production of Napthoquinone Metabolite (Shikonin) from Cell Suspension Culture of Arnebia Sp. and Its Up-Scaling Through Bioreactor. 3 Biotech., 4: 263–273.
17. Hajiboland, R., Bahrami-Rad, S. and Poschenrieder, C. 2017. Silicon Modifies both a Local Response and a Systemic Response to Mechanical Stress in Tobacco Leaves. Biol. Plant., 61: 187–191.
18. Hashemi, A., Abdolzadeh, A. and Sadeghipour, H.R. 2010. Beneficial Effects of Silicon Nutrition in Alleviating Salinity Stress in Hydroponically Grown Canola, Brassica napus L., Plants. Soil Sci. Plant Nutr., 56: 244–253.
19. Hossain, M. T., Mori, R., Soga, K., Wakabayashi, K., Kamisaka, S., Fujii, S., Yamamoto, R. and Hoson, T. 2002. Growth Promotion and an Increase in Cell Wall Extensibility by Silicon in Rice and Some other Poaceae Seedlings. J. Plant Res., 115: 23–27.
20. Iwasaki, K., Maier, P., Fecht, M. and Horst, W.J. 2002. Effects of Silicon Supply on Apoplastic Manganese Concentrations in Leaves and Their Relation to Manganese Tolerance in Cowpea (Vigna unguiculata (L.) Walp.). Plant Soil., 238: 281–288.
21. Kar, M. and Mishra, D. 1976. Catalase, Peroxidase, and Polyphenoloxidase Activities during Rice Leaf Senescence. Plant Physiol., 57: 315–9.
22. Kim, S. G., Kim, K. W., Park, E. W. and Choi, D. 2002. Silicon-Induced Cell Wall Fortification of Rice Leaves: A Possible Cellular Mechanism of Enhanced Host Resistance to Blast. Phytopathology., 92: 1095–1103.
23. Kim Y. H, Khan, A. L, Waqas, M. and Lee I.J. 2017. Silicon Regulates Antioxidant Activities of Crop Plants under Abiotic-Induced Oxidative Stress: A Review. Front. Plant Sci. 8: 510-517.
24. Kumar, N., Kumar, R. and Kishore, K. 2013. Onosma L.: A review of Phytochemistry and Ethnopharmacology. Pharmacogn. Rev., 7: 140–51.
25. Lewin, J. and Reimann, B. E. F. 1969. Silicon and Plant Growth. Annu. Rev. Plant Physiol., 20: 289–304.
26. Liu, X. and Huang, B. 2000. Heat Stress Injury in Relation to Membrane Lipid Peroxidation in Creeping Bentgrass. Crop Sci., 40: 503–510.
27. Ma, J. F., Yamaji, N. and Mitani-Ueno, N. 2011. Transport of Silicon from Roots to Panicles in Plants. Proc. Jpn. Acad. Ser. B. Phys. Biol. Sci., 87: 377–385.
28. Ma, J. F., Yamaji, N., Mitani, N., Tamai, K., Konishi, S., Fujiwara, T., Katsuhara, M. and Yano, M. 2007. An Efflux Transporter of Silicon in Rice. Nature., 448: 209–212.
29. Markovich, O., Steiner, E., Kouřil, Š., Tarkowski, P., Aharoni, A., and Elbaum, R. 2017. Silicon Promotes Cytokinin Biosynthesis and Delays Senescence in Arabidopsis and Sorghum. Plant, Cell & Environment, 40: 1189–1196.
30. Mehraban, P., Zadeh, A. A. and Sadeghipour, H. R. 2008. Iron Toxicity in Rice (Oryza sativa L.), under Different Potassium Nutrition. Asian J. Plant Sci., 7: 251–259.
31. Miyake, Y. and Takahashi, E. 1985. Effect of Silicon on the Growth of Soybean Plants in a Solution Culture. Soil Sci. Plant Nutr., 31: 625–636.
32. Murashige, T. and Skoog, F. 1962. A Revised Medium for Rapid Growth and Bio Assays with Tobacco Tissue Cultures. Physiol. Plant., 15: 473–497.
33. Nakano, Y. and Asada, K. 1981. Hydrogen Peroxide Is Scavenged by Ascorbate-Specific Peroxidase in Spinach Chloroplasts. Plant Cell Physiol., 22: 867–880.
34. Neocleous, D. 2015. Grafting and Silicon Improve Photosynthesis and Nitrate Absorption in Melon (Cucumis melo L.) Plants. J. Agr. Sci. Tech. 17: 1815-1824.
35. Pavol, M., Mártonfiová, L. and Kolar, V. 2008. Karyotypes and Genome Size of Onosma Species from Northern Limits of the Genus in Carpathians. Caryologia, 61: 363–374.
36. Richmond, K. E. and Sussman, M. 2003. Got Silicon? The Non-Essential Beneficial Plant Nutrient. Curr. Opin. Plant Biol., 6: 268–272.
37. Sagratini, G., Cristalli, G., Giardinà, D., Gioventù, G., Maggi, F., Ricclutelli, M. and Vittori, S. 2008. Alkannin/Shikonin Mixture from Roots of Onosma Echioides (L.): Extraction Method Study and Quantification. J. Sep. Sci., 31: 945–952.
38. Shi, Q., Bao, Z., Zhu, Z., He, Y., Qian, Q. and Yu, J. 2005. Silicon-Mediated Alleviation of Mn Toxicity in Cucumis sativus in Relation to Activities of Superoxide Dismutase and Ascorbate Peroxidase. Phytochemistry., 66: 1551–1559.
39. Silva, O. N., Lobato, A. K. S., Ávila, F. W., Costa, R. C. L. Oliveira Neto, C. F., Santos Filho, B. G., Martins Filho, A. P., Lemos, R. P., Pinho, J. M., Medeiros, M. B. C. L., Cardoso, M. S. Andrade, I. P. 2012. Silicon-Induced Increase in Chlorophyll Is Modulated by the Leaf Water Potential in Two Water-Deficient Tomato Cultivars. Plant, Soil Environ., 58: 481–486.
40. Tabata, M., Mizukami, H., Hiraoka, N. and Konoshima, M. 1974. Pigment Formation in Callus Cultures of Lithospermum erythrorhizon. Phytochemistry., 13: 927–932.
41. Tahir, M. A., Aziz, T., Farooq, M. and Sarwar, G. 2012. Silicon-Induced Changes in Growth, Ionic Composition, Water Relations, Chlorophyll Contents and Membrane Permeability in Two Salt-Stressed Wheat Genotypes. Arch. Agron. Soil Sci., 58: 247–256.
42. Torabi, F., Majd, A. and Enteshari, S. 2015. The Effect of Silicon on Alleviation of Salt Stress in Borage (Borago officinalis L.). Soil Sci. Plant Nut. 61, 788–798.
43. Tripathi, D. K., Singh, S., Singh, V. P., Prasad, S. M., Dubey, N. K. and Chauhan, D. K. 2017. Silicon Nanoparticles more Effectively Alleviated UV-B Stress than Silicon in Wheat (Triticum aestivum) Seedlings. Plant Physiol. Biochem. 110, 70–81.
44. Wang, S. Y. and Galletta, G. J. 1998. Foliar Application of Potassium Silicate Induces Metabolic Changes in Strawberry Plants. J. Plant Nutr., 21: 157–167.
45. Whetten, R. W. and Sederoff, R. R. 1992. Phenylalanine Ammonia-Lyase from Loblolly pine : Purification of the Enzyme and Isolation of Complementary DNA Clones. Plant Physiol., 98: 380–386.
46. Zimmer, M. 1999. Combined Methods for the Determination of Lignin and Cellulose in Leaf Litter. Sci. Soils., 4: 14–21.
Journal of Agricultural Science and Technology
Volume 21, Issue 3
May and June 2019
Pages 671-681