Chromium-induced alkaloid production in Catharanthus roseus (L.) G.Don in vitro cultured shoots and related gene expression patterns particularly for the novel gene GS

Elham KHATAEE; Farah KARIMI; Khadijeh RAZAVI

doi:10.14720/aas.2019.113.1.09

Authors

Elham KHATAEE Dep. of Biology, Faculty of Basic Sciences, Shahed University, 3319118651, Tehran, Iran
Farah KARIMI Medicinal Plant Research Center, Shahed University, 3319118651, Tehran, Iran
Khadijeh RAZAVI National Institute of Genetic Engineering and Biotechnology, 1497716316 Tehran, Iran

DOI:

https://doi.org/10.14720/aas.2019.113.1.09

Keywords:

antioxidative responses, chromium, GS, MAPK3, ORCA3, real time PCR

Abstract

This study aimed to determine the effects of methyl jasmonate (Mj) combined with chromium (Cr) as elicitor on production of medicinal alkaloids, its antioxidant potential, and its effects on the expression of signaling and biosynthetic enzymes. Combined treatment had positive effects on secondary metabolism and changed genes expression levels of mitogen-activated protein kinase 3 (MAPK3), a transcription factor (TF) known as octadecanoid-responsive Catharanthus AP2-domain 3 (ORCA3) upstream of plant alkaloids biosynthetic pathway. Maximum expression levels of peroxidase1 (PRX1), geissoschizine synthase (GS) (24 h-treatment), MAPK3 and ORCA3 (8 h-treatment), were 6.25−, 4.87-, 7.67-, and 5.38-fold higher than control, respectively, in response to 100 µM Mj + 50 µM Cr. This value was 5.92-fold for strictosidine synthase (STR) in response to 100 µM Mj + 100 µM Cr after 24 h. The maximum total yield of vincristine was 1.52-fold more than control in response to 100 µM Mj after one week. This increase was 2.16, 4.01, 2.39 and 1.97-fold for ajmalicine, vinblastine, vindoline and catharanthine respectively, in response to 100 µM Mj + 50 µM Cr. Mj + Cr can elevate alkaloid production by induction of MAPK3 and ORCA3 signaling pathway, which induces expression of downstream terpenoid indole alkaloids (TIAs) biosynthetic enzymes.

References

Aftab, T., Khan, M. M. A., Idrees, M., Naeem, M., & Hashmi, N. (2011). Methyl jasmonate counteracts boron toxicity by preventing oxidative stress and regulating antioxidant enzyme activities and artemisinin biosynthesis in Artemisia annua L. Protoplasma, 248(3), 601-612. https://doi.org/10.1007/s00709-010-0218-5

DalCorso, G., Farinati, S., Maistri, S., & Furini, A. (2008). How plants cope with cadmium: staking all on metabolism and gene expression. Journal of integrative plant biology, 50(10), 1268-1280. https://doi.org/10.1111/j.1744-7909.2008.00737.x

Dewanto, V., Wu, X., Adom, K. K., & Liu, R. H. (2002). Thermal processing enhances the nutritional value of tomatoes by increasing total antioxidant activity. Journal of agricultural and food chemistry, 50(10), 3010-3014. https://doi.org/10.1021/jf0115589

Dubey, S., Misra, P., Dwivedi, S., Chatterjee, S., Bag, S. K., Mantri, S. & Tripathi, P. (2010). Transcriptomic and metabolomic shifts in rice roots in response to Cr (VI) stress. BMC genomics, 11(1), 648. https://doi.org/10.1186/1471-2164-11-648

Eleftheriou, E. P., Adamakis, I. D. S., Panteris, E., & Fatsiou, M. (2015). Chromium-induced ultrastructural changes and oxidative stress in roots of Arabidopsis thaliana. International journal of molecular sciences, 16(7), 15852-15871. https://doi.org/10.3390/ijms160715852

Emamverdian, A., Ding, Y., Mokhberdoran, F., & Xie, Y. (2015). Heavy metal stress and some mechanisms of plant defense response. The Scientific World Journal, 2015. http://dx.doi.org/10.1155/2015/756120

Gao, F., Su, Q., Fan, Y., & Wang, L. (2010). Expression pattern and core region analysis of AtMPK3 promoter in response to environmental stresses. Science China Life Sciences, 53(11), 1315-1321. https://doi.org/10.1007/s11427-010-4079-0

Giri, C. C., & Zaheer, M. (2016). Chemical elicitors versus secondary metabolite production in vitro using plant cell, tissue and organ cultures: recent trends and a sky eye view appraisal. Plant Cell, Tissue and Organ Culture (PCTOC), 126(1), 1-18. https://doi.org/10.1007/s11240-016-0985-6

Heath, R. L., & Packer, L. (1968). Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Archives of biochemistry and biophysics, 125(1), 189-198. https://doi.org/10.1016/0003-9861(68)90654-1

Jung, S. (2004). Effect of chlorophyll reduction in Arabidopsis thaliana by methyl jasmonate or norflurazon on antioxidant systems. Plant Physiology and Biochemistry, 42(3), 225-231. https://doi.org/10.1016/j.plaphy.2004.01.001

Kumari, P., Reddy, C. R. K., & Jha, B. (2015). Methyl jasmonate-induced lipidomic and biochemical alterations in the intertidal macroalga Gracilaria dura (Gracilariaceae, Rhodophyta). Plant and Cell Physiology, 56(10), 1877-1889. https://doi.org/10.1093/pcp/pcv115

Kupper, F. C., Gaquerel, E., Cosse, A., Adas, F., Peters, A. F., Müller, D. G. & Potin, P. (2009). Free fatty acids and methyl jasmonate trigger defense reactions in Laminaria digitata. Plant and Cell Physiology, 50(4), 789-800. https://doi.org/10.1093/pcp/pcp023

Liu, D. H., Jin, H. B., Chen, Y. H., Cui, L. J., Ren, W. W., Gong, Y. F., & Tang, K. X. (2007). Terpenoid indole alkaloids biosynthesis and metabolic engineering in Catharanthus roseus. Journal of integrative plant biology, 49(7), 961-974. https://doi.org/10.1111/j.1672-9072.2007.00457.x

Livak, K. J., & Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods, 25(4), 402-408. https://doi.org/10.1006/meth.2001.1262

Miranda‐Ham, L., & Islas‐Flores, I. (2007). Accumulation of monoterpenoid indole alkaloids in periwinkle seedlings (Catharanthus roseus) as a model for the study of plant–environment interactions. Biochemistry and Molecular Biology Education, 35(3), 206-210. https://doi.org/10.1002/bmb.60

Mourato, M., Reis, R., & Martins, L. L. (2012). Characterization of plant antioxidative system in response to abiotic stresses: a focus on heavy metal toxicity. In Advances in selected plant physiology aspects. InTech. https://doi.org/10.5772/34557

Ncube, B., & Van Staden, J. (2015). Tilting plant metabolism for improved metabolite biosynthesis and enhanced human benefit. Molecules, 20(7), 12698-12731. https://doi.org/10.5772/34557

Ozturk, B., Yıldız, K., & Ozkan, Y. (2015). Effects of pre-harvest methyl jasmonate treatments on bioactive compounds and peel color development of ‘Fuji’ apples. International journal of food properties, 18(5), 954-962. https://doi.org/10.1080/10942912.2014.911312

Pan, Y. J., Liu, J., Guo, X. R., Zu, Y. G., & Tang, Z. H. (2015). Gene transcript profiles of the TIA biosynthetic pathway in response to ethylene and copper reveal their interactive role in modulating TIA biosynthesis in Catharanthus roseus. Protoplasma, 252(3), 813-824. https://doi.org/10.1007/s00709-014-0718-9

Pan, Q., Mustafa, N. R., Tang, K., Choi, Y. H., & Verpoorte, R. (2016). Monoterpenoid indole alkaloids biosynthesis and its regulation in Catharanthus roseus: a literature review from genes to metabolites. Phytochemistry reviews, 15(2), 221-250. https://doi.org/10.1007/s11101-015-9406-4

Peebles, C. A., Hughes, E. H., Shanks, J. V., & San, K. Y. (2009). Transcriptional response of the terpenoid indole alkaloid pathway to the overexpression of ORCA3 along with jasmonic acid elicitation of Catharanthus roseus hairy roots over time. Metabolic engineering, 11(2), 76-86. https://doi.org/10.1016/j.ymben.2008.09.002

Poonam, S., Kaur, H., & Geetika, S. (2013). Effect of jasmonic acid on photosynthetic pigments and stress markers in Cajanus cajan (L.) Millsp. Seedlings under copper stress. American Journal of Plant Sciences, 4(04), 817. https://doi.org/10.4236/ajps.2013.44100

Qu, Y., Easson, M. E., Simionescu, R., Hajicek, J., Thamm, A. M., Salim, V., & De Luca, V. (2018). Solution of the multistep pathway for assembly of corynanthean, strychnos, iboga, and aspidosperma monoterpenoid indole alkaloids from 19E-geissoschizine. Proceedings of the National Academy of Sciences, 115(12), 3180-3185. https://doi.org/10.1073/pnas.1719979115

Raina, S. K., Wankhede, D. P., Jaggi, M., Singh, P., Jalmi, S. K., Raghuram, B. & Sinha, A. K. (2012). CrMPK3, a mitogen activated protein kinase from Catharanthus roseus and its possible role in stress induced biosynthesis of monoterpenoid indole alkaloids. BMC plant biology, 12(1), 134. https://doi.org/10.1186/1471-2229-12-134

Sanchez-Rojo, S., Cerda-García-Rojas, C. M., Esparza-García, F., Plasencia, J., Poggi-Varaldo, H. M., Ponce-Noyola, T., & Ramos-Valdivia, A. C. (2015). Long-term response on growth, antioxidant enzymes, and secondary metabolites in salicylic acid pre-treated Uncaria tomentosa microplants. Biotechnology letters, 37(12), 2489-2496. https://doi.org/10.1007/s10529-015-1931-0

Sharmin, S. A., Alam, I., Kim, K. H., Kim, Y. G., Kim, P. J., Bahk, J. D., & Lee, B. H. (2012). Chromium-induced physiological and proteomic alterations in roots of Miscanthus sinensis. Plant science, 187, 113-126. https://doi.org/10.1016/j.plantsci.2012.02.002

Singh, K. B., Foley, R. C., & Oñate-Sánchez, L. (2002). Transcription factors in plant defense and stress responses. Current opinion in plant biology, 5(5), 430-436. https://doi.org/10.1016/S1369-5266(02)00289-3

Singh, S., Parihar, P., Singh, R., Singh, V. P., & Prasad, S. M. (2016). Heavy metal tolerance in plants: role of transcriptomics, proteomics, metabolomics, and ionomics. Frontiers in plant science, 6, 1143. https://doi.org/10.3389/fpls.2015.01143

Trinh, N. N., Huang, T. L., Chi, W. C., Fu, S. F., Chen, C. C., & Huang, H. J. (2014). Chromium stress response effect on signal transduction and expression of signaling genes in rice. Physiologia plantarum, 150(2), 205-224. https://doi.org/10.1111/ppl.12088

Van der Fits, L., & Memelink, J. (2000). ORCA3, a jasmonate-responsive transcriptional regulator of plant primary and secondary metabolism. Science, 289(5477), 295-297. https://doi.org/10.1126/science.289.5477.295

Van Moerkercke, A., Steensma, P., Schweizer, F., Pollier, J., Gariboldi, I., Payne, R. & Kellner, F. (2015). The bHLH transcription factor BIS1 controls the iridoid branch of the monoterpenoid indole alkaloid pathway in Catharanthus roseus. Proceedings of the National Academy of Sciences, 201504951. https://doi.org/10.1073/pnas.1504951112

Wójciak-Kosior, M., Sowa, I., Blicharski, T., Strzemski, M., Dresler, S., Szymczak, G. & Świeboda, R. (2016). The stimulatory effect of strontium ions on phytoestrogens content in Glycine max (L.) Merr. Molecules, 21(1), 90. https://doi.org/10.3390/molecules21010090

Zhang, H., Hedhili, S., Montiel, G., Zhang, Y., Chatel, G., Pré, M. & Memelink, J. (2011). The basic helix‐loop‐helix transcription factor CrMYC2 controls the jasmonate‐responsive expression of the ORCA genes that regulate alkaloid biosynthesis in Catharanthus roseus. The Plant Journal, 67(1), 61-71. https://doi.org/10.1111/j.1365-313X.2011.04575.x