Biologia Plantarum 63: 411-417, 2019 | DOI: 10.32615/bp.2019.053
Growth, secondary metabolism, and related gene expression in response to interactions of nitrogen and sulfur in Isatis indigotica
- 1 College of Horticulture, Nanjing Agricultural University, Nanjing, 210095, P.R. China
- 2 Institute of Food Crops, Jiangsu Academy of Agricultural Sciences, Nanjing 210014, P.R. China
Nitrogen and sulfur are major elements influencing plant growth and production of secondary metabolites. They interact to each other, but little is known about it in Isatis indigotica Fort. plants. In this study, 15 different treatments representing all possible combinations of 3 N treatments (N1, N2, and N3, corresponding to 5, 15, and 25 mM N, respectively) and five S treatments (S0, S1, S2, S3, and S4, corresponding to 0.00, 1.25, 2.50, 5.00 and 7.50 mM S, respectively) were used, and plant growth, indigo and indirubin yields, and expressions of genes encoding enzymes involved in N and S metabolisms were measured. The results show that the highest dry biomass was observed in N2S2 treatment. Moreover, net photosynthetic rate in the N2S2 treatment was significantly higher than under other treatments (except for N3S2 treatment). A low nitrogen concentration (5 mM) was beneficial to the accumulation of alkaloids, and the N1S1 and N2S2 treatments resulted in the highest yields of indigo and indirubin, respectively. Additionally, the yields of indigo and indirubin were positively correlated with the expression of APS reductase and glutamine synthetase genes, respectively.
Keywords: indigo, indirubin, photosynthetic rate, RT-qPCR, stomatal conductance, transpiration rate
Received: July 24, 2018; Revised: December 11, 2018; Accepted: December 13, 2018; Prepublished online: February 11, 2019; Published online: January 19, 2019Show citation
ACS | AIP | APA | ASA | Harvard | Chicago | IEEE | ISO690 | MLA | NLM | Turabian | Vancouver |
Supplementary files
Download file | MIAO5901Suppl.pdf File size: 142.7 kB |
References
- Aharoni, A., Galili, G.: Metabolic engineering of the plant primary-secondary metabolism interface. - Curr. Opin. Biotechnol. 22: 239-244, 2011. Go to original source...
- Davidian, J.C., Kopriva, S.: Regulation of sulfate uptake and assimilation-the same or not the same? - Mol. Plant. 3: 314-25, 2010. Go to original source...
- De Bona, F.D., Fedoseyenko, D., Von Wirén, N, Monteiro, F.A.: Nitrogen utilization by sulfur-deficient barley plants depends on the nitrogen form. - Environ. exp. Bot. 74: 237-244, 2011. Go to original source...
- Fernández, E., Galván, A., Quesada, A.: Nitrogen assimilation and its regulation. - In: Rochaix, J.D., Goldschmidt-Clermont, M., Merchant, S. (ed.): The Molecular Biology of Chloroplasts and Mitochondria in Chlamydomonas. Advances in Photosynthesis and Respiration. Vol. 7. Pp. 637-659. Springer-Verlag, Dordrecht 1998. Go to original source...
- Gerhards, N., Neubauer, L., Tudzynski, P., Li, S.M.: Biosynthetic pathways of ergot alkaloids. - Toxins 6: 3281-3295, 2014. Go to original source...
- Giordano, M., Raven, J.A.: Nitrogen and sulfur assimilation in plants and algae. - Aquat. Bot. 118: 45-61, 2014. Go to original source...
- Guan, J.L., Wang, G., Chen, X., Zhang M.R., Miao, Y.J., Tang X.Q.: Effect of low nitrogen nutrition on the growth and active components of Isatis indigotica Fort. seedlings. - Chin. J. Ecol. 37: 2331-2338, 2018.
- Herms, D.A., Mattson, W.J.: The dilemma of plants: to grow or defend. - Quarterly Rev. Biol. 67: 282-335, 1992. Go to original source...
- Hesse, H., Nikiforova, V., Gakière, B., Hoefgen, R.: Molecular analysis and control of cysteine biosynthesis: integration of nitrogen and sulphur metabolism. - J. exp. Bot. 55: 1283-1292, 2004. Go to original source...
- Hoagland, D. R., Arnon, D. I.: The water-culture method for growing plants without soil. - Calif. Agr. Exp. Sta. Bull. 50: 463-485, 1950.
- Hol, W.H.G., Vrieling, K., Van Veen, J.A.: Nutrients decrease pyrrolizidine alkaloid concentrations in Senecio jacobaea. - New Phytol. 158: 175-181, 2003. Go to original source...
- Kopriva, S., Calderwood, A., Weckopp, S.C., Koprivova, A.: Plant sulfur and big data. - Plant Sci. 241: 1-10, 2015. Go to original source...
- Leustek, T., Martin, M.N., Bick, J.A.: Pathways and regulation of sulfur metabolism revealed through molecular and genetic studies. - Annu. Rev. Plant Biol. 51: 141-165, 2000. Go to original source...
- Leustek, T., Saito, K.: Sulfate transport and assimilation in plants. - Plant Physiol. 120: 637-644, 1999. Go to original source...
- Livak, K.J., Schmittgen, T.D.: Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. - Methods 25: 402-408, 2001. Go to original source...
- Maeda, H., Dudareva, N.: The shikimate pathway and aromatic amino acid biosynthesis in plants. - Annu. Rev. Plant Biol. 63: 73-105, 2012. Go to original source...
- Marcinek, H., Weyler, W., Deus-Neumann, B., Zenk, M.H.: Indoxyl - UDPG - glucosyltransferase from Baphicacanthus cusia. - Phytochemistry 53: 201-207, 2000. Go to original source...
- Mentzen, W.I., Peng, J.L., Ransom, N., Nikolau, B.J., Wurtele, E.S.: Articulation of three core metabolic processes in Arabidopsis: fatty acid biosynthesis, leucine catabolism and starch metabolism. - BMC Plant Biol. 8: 76, 2008. Go to original source...
- Miflin, B.J.: The location of nitrite reductase and other enzymes related to amino acid biosynthesis in the plastids of root and leaves. - Plant Physiol. 54: 550-555, 1974. Go to original source...
- Murchie, E.H., Pinto, M., Horton, P.: Agriculture and the new challenges for photosynthesis research. - New Phytol. 181: 532-552, 2009. Go to original source...
- Parry, M.A.J., Reynolds, M., Salvucci, M.E., Raines, C., Andralojc, P.J., Zhu, X.G., Price, G.D., Condon, A.G., Furbank, R.T.: Raising yield potential of wheat. II. increasing photosynthetic capacity and efficiency. - J. exp. Bot. 62: 453-467, 2011. Go to original source...
- Raza, M.A., Feng, L.Y., Manaf, A., Wasayac, A., Ansar, M., Hussain, A., Khalid, M.H.B., Iqbal, N., Xi, Z.J., Chen, Y. K., Chen, J.X., Yang, F., Yang, W.Y. : Sulphur application increases seed yield and oil content in sesame seeds under rainfed condition. - Field Crops Res. 218: 51-58, 2018. Go to original source...
- Rentsch, D., Schmidt, S., Tegeder, M.: Transporters for uptake and allocation of organic nitrogen compounds in plants. - FEBS Lett. 581: 2281-2289, 2007. Go to original source...
- Rosales, E.P., Iannone, M.F., Groppa, M.D., Benavides, M.P.: Nitric oxide inhibits nitrate reductase activity in wheat leaves. - Plant Physiol. Biochem. 49: 124-130, 2011. Go to original source...
- Salvagiotti, F., Castellarin, J.M., Miralles, D.J., Pedrol, H.M.: Sulfur fertilization improves nitrogen use efficiency in wheat by increasing nitrogen uptake. - Field Crops Res. 113: 170-177, 2009. Go to original source...
- Salvagiotti, F., Miralles, D.J.: Radiation interception, biomass production and grain yield as affected by the interaction of nitrogen and sulfur fertilization in wheat. - Eur. J. Agron. 28: 282-290, 2008. Go to original source...
- Scherer, H.W.: Sulphur in crop production. - Eur. J. Agron. 14: 81-111, 2001. Go to original source...
- Singh, A., Pandey, B., Kumari, S., Agrawal, M.: Nitrogen availability modulates CO2-induced responses of Catharanthus roseus: biomass allocation, carbohydrates and alkaloids profile. - JARMAP 2: 160-167, 2015. Go to original source...
- Sorin, E., Etienne, P., Maillard, A., Zamarreño, A.M., Garcia-Mina, J.M., Arkoun, M., Jamois, F., Cruz, F., Yvin, J.C., Ourry, A.: Effect of sulphur deprivation on osmotic potential components and nitrogen metabolism in oilseed rape leaves: identification of a new early indicator. - J. exp. Bot. 66: 6175-6189, 2015. Go to original source...
- Tsujimoto, Y., Inusah, B., Katsura, K., Fuseini, A., Dogbe, W., Zakaria, A.I., Fujihara, Y., Oda, M., Sakagami, J.I.: The effect of sulfur fertilization on rice yields and nitrogen use efficiency in a floodplain ecosystem of northern Ghana. - Field Crops Res. 211: 155-164, 2017. Go to original source...
- Wink, M.: Evolution of secondary metabolites from an ecological and molecular phylogenetic perspective. - Phytochemistry 64: 3-19, 2003. Go to original source...
- Xiao, Y.H., Zhao, X.L., Wang, K.C., Shi, X.M., Tang, X.Q.: Effect of different nitrogen forms and concentrations on biomass and alkaloids of Isatidis Folium. - Chin. J. Chin. Master Med. 38: 2755-2760, 2013.
- Xu, W., Gavia, D.J., Tang, Y.: Biosynthesis of fungal indole alkaloids. - Nat. Prod. Rep. 31: 1474-1487, 2014. Go to original source...
- Zhao, J., Zhu, W.H., Hu, Q., Wang, W.K.: Regulation of indole alkaloids synthesis and related enzymes during callus initiation and culture of Madagascar periwinkle leaves (Catharanthus roseus). - Chin. tradit. herbal Drugs 7: 533-537, 1999.
- Zhou, W., Zhang, X.Y.: Research progress of Chinese herbal medicine Radix isatidis (banlangen). - Amer. J. Chinese Med. 41: 743-764, 2013. Go to original source...