Selenium improves the flavor-promoting substances of summer tea (Camellia sinensis) by altering the expression of flavonoid and amino acids metabolic genes

Abstract

Summer tea (Camellia sinensis) is less favored due to its inferior taste compared to spring tea. The application of selenium (Se) has proven effective in enhancing tea flavor. However, the specific mechanisms underlying the Se-mediated improvement of summer tea quality remain unclear. This study examines the alteration of trace elements, the metabolome, and the transcriptome in tea plants subjected to Se treatment. Se application increased the concentrations of B, Fe, Zn, and Se in the summer tea shoots of certain cultivars. Metabolomic analysis revealed that exogenous Se elevated the levels of theanine and flavonoids while reducing the catechin bitterness taste index in most of the selected cultivars. Transcriptomic analysis further demonstrated that Se treatment modulated the expression of CsSULTRs, CsPHTs, CsIRTs, CsZIPs, and CsBOTs, indicating a potential link between the accumulation of these elements and the corresponding transporter genes. Based on qRT-PCR results, CsSULTR1.1, 1.2, and 4.1 are likely involved in Se transport. Additionally, differentially expressed genes (DEGs) were predominantly enriched in the flavonoid and amino acid biosynthesis pathways following Se treatment. In conclusion, the addition of Se enhances the flavor profile of summer tea by modulating genes participating in flavonoid and amino acid metabolism, underpinning its potential for improving summer tea quality.

References

[1] Dai W, Qi D, Yang T, Lv H, Guo L, Zhang Y, et al. Nontargeted analysis using ultraperformance liquid chromatography-quadrupole time-of-flight mass spectrometry uncovers the effects of harvest season on the metabolites and taste quality of tea (Camellia sinensis L.). J Agric Food Chem. 2015;63:9869–78. https://doi.org/10.1021/acs.jafc.5b03967.

[2] Fan Z, Wang Y, Yang M, Cao J, Khan A, Cheng G. UHPLC-ESI-HRMS/MS analysis on phenolic compositions of different E Se tea extracts and their antioxidant and cytoprotective activities. Food Chem. 2020;318:126512. https://doi.org/10.1016/j.foodchem.2020.126512.

[3] Fernández-Martínez A, Charlet L. Selenium environmental cycling and bioavailability: a structural chemist point of view. Rev Environ Sci Biotechnol, 2009, 8: 81-110.

[4] Gao T, Hou B, Shao S, Xu M, Zheng Y, Jin S, et al.. Differential metabolites and transcriptional regulation of seven major tea cultivars (Camellia sinensis) in China. J Integr Agric, 2023, 22: 3346-63.

[5] Gupta M, Gupta S. An overview of selenium uptake, metabolism, and toxicity in plants. Front Plant Sci, 2017, 7: 2074. 5225104

[6] Hu Q, Xu J, Pang G. Effect of selenium on the yield and quality of green tea leaves harvested in early spring. J Agric Food Chem, 2003, 51: 3379-3381.

[7] Huang Y, Xu J, Hu Q. Effect of selenium on preservation quality of green tea during autumn tea-processing season. J Agric Food Chem, 2005, 53: 7444-7447.

[8] Huang S, Zuo T, Zheng X, Zhuo C, Hou Q, Yao L, et al. Foliar application of glycinebetaine and Zn fertilizer improves both the apparent and functional qualities of albino tea [Camellia sinensis (L.) O. Kuntze]. Food Funct. 2021;12:9476–85.https://doi.org/10.1039/d1fo01398j.

[9] Jiang C, Moon DG, Ma J, Chen L. Characteristics of non-volatile metabolites in fresh shoots from tea plant (Camellia sinensis) and its closely related species and varieties. Beverage Plant Research. 2022;2:9. https://doi.org/10.48130/BPR-2022-0009.

[10] Karak T, Bhagat RM. Trace elements in tea leaves, made tea and tea infusion: a review. Food Res Int, 2010, 43: 2234-2252.

[11] Kaur N, Sharma S, Kaur S, Nayyar H. Selenium in agriculture: a nutrient or contaminant for crops?. Arch Agron Soil Sci, 2014, 60: 1593-1624.

[12] Li J, Fu B, Huo D, Hou C, Yang M, Shen C, et al.. Discrimination of Chinese teas according to major amino acid composition by a colorimetric IDA sensor. Sensors and Actuators b: Chemical, 2017, 240: 770-778.

[13] Li D, Zhou C, Zou N, Wu Y, Zhang J, An Q, et al. Nanoselenium foliar application enhances biosynthesis of tea leaves in metabolic cycles and associated responsive pathways. Environ Pollut. 2021;273:116503. https://doi.org/10.1016/j.envpol.2021.116503.

[14] Li J, Wen T, Zhang R, Hu X, Guo F, Zhao H, et al. Metabolome profiling and transcriptome analysis unveiling the crucial role of magnesium transport system for magnesium homeostasis in tea plants. Hortic Res. 2024;11(7):uhae152. https://doi.org/10.1093/hr/uhae152.

[15] Li J, Li Q, Zhang X, Zhang L, Zhao P, Wen T, et al. Exploring the effects of magnesium deficiency on the quality constituents of hydroponic-cultivated tea (Camellia sinensis L.) leaves. J Agric Food Chem. 2021;69(47):14278–86. https://doi.org/10.1021/acs.jafc.1c05141.

[16] Li J, Hu X, Zhang R, Li Q, Xu W, Zhang L, et al. The plasma membrane magnesium transporter CsMGT5 mediates magnesium uptake and translocation under magnesium limitation in tea plants (Camellia sinensis L.). Sci Hortic. 2022;310:111711. https://doi.org/10.1016/j.scienta.2022.111711.

[17] Liang G. Iron uptake, signaling, and sensing in plants. Plant Commun. 2022;3:100349. https://doi.org/10.1016/j.xplc.2022.100349.

[18] Liang J, Puligundla P, Ko S, Wan X. A review on selenium-enriched green tea: fortification methods, biological activities and application prospect. Sains Malays, 2014, 43: 1685-92

[19] Liao Y, Zhou X, Zeng L. How does tea (Camellia sinensis) produce specialized metabolites which determine its unique quality and function: a review. Crit Rev Food Sci Nutr, 2022, 62: 3751-3767.

[20] Liu C, Zhou G, Qin H, Guan Y, Wang T, Ni W, et al. Metabolomics combined with physiology and transcriptomics reveal key metabolic pathway responses in apple plants exposure to different selenium concentrations. J Hazard Mater. 2024;464:132953. https://doi.org/10.1016/j.jhazmat.2023.132953.

[21] Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2^–ΔΔCT method. Methods, 2001, 25: 402-408.

[22] Navarro-Alarcon M, Cabrera-Vique C. Selenium in food and the human body: a review. Sci Total Environ, 2008, 400: 115-141.

[23] Peng Y, Jin T, Yang R, Chen R, Wang J. Distribution of mineral elements in the soil and in tea plants (Camellia sinensis). J Elem, 2022, 27: 765-796.

[24] Rashid MH, Chowdhury MAZ, Fardous Z, Tanvir EM, Pramanik MK, Jahan I, et al.. Microbial decontamination of gamma irradiated black tea and determination of major minerals in black tea, fresh tea leaves and tea garden soil. LWT- Food Sci Technol, 2016, 73: 185-190.

[25] Ren H, Li X, Guo L, Wang L, Hao X, Zeng J. Integrative transcriptome and proteome analysis reveals the absorption and metabolism of selenium in tea plants [Camellia sinensis (L.) O. Kuntze]. Front Plant Sci. 2022;13:848349. https://doi.org/10.3389/fpls.2022.848349.

[26] Ruan J, Ma L, Shi Y, Han W. The impact of pH and calcium on the uptake of fluoride by tea plants (Camellia sinensis L.). Ann Bot. 2004;93:97–105. https://doi.org/10.1093/aob/mch010.

[27] Sun M, Wang J, Liu W, Yin P, Guo G, Tong C, et al. Effect and mechanism of exogenous selenium on selenium content and quality of fresh tea leaves. Not Bot Horti Agrobot Cluj-Na. 2022;50:128143. https://doi.org/10.15835/nbha50312814.

[28] Tangjaidee P, Swedlund P, Xiang J, Yin H, Quek SY. Selenium-enriched plant foods: Selenium accumulation, speciation, and health functionality. Front Nutr. 2023;9:962312. https://doi.org/10.3389/fnut.2022.962312.

[29] Tavallali V. Interactive effects of zinc and boron on growth, photosynthesis, and water relations in pistachio. J Plant Nutr, 2017, 40: 1588-1603.

[30] Ullah H, Liu G, Yousaf B, Ali MU, Irshad S, Abbas Q, et al.. A comprehensive review on environmental transformation of selenium: recent advances and research perspectives. Environ Geochem Health, 2019, 41: 1003-1035.

[31] Upadhyaya H, Dutta BK, Panda SK. Zinc modulates drought-induced biochemical damages in tea [Camellia sinensis (L) O Kuntze]. J Agric Food Chem, 2013, 61: 6660-6670.

[32] Wang Y, Chen J, Zhang D, Zhang Y, Wen Y, Li L, et al.. Tumoricidal effects of a selenium (Se)-polysaccharide from Ziyang green tea on human osteosarcoma U-2 OS cells. Carbohydr Polym, 2013, 98: 1186-1190.

[33] Wang M, Zou Z, Li Q, Xin H, Zhu X, Chen X, et al.. Heterologous expression of three Camellia sinensis small heat shock protein genes confers temperature stress tolerance in yeast and Arabidopsis thaliana. Plant Cell Rep, 2017, 36: 1125-1135.

[34] Wang Y, Fan Z, Yang M, Wang Y, Cao J, Khan A, et al. Protective effects of E Se tea extracts against alcoholic fatty liver disease induced by high fat/alcohol diet: in vivo biological evaluation and molecular docking study. Phytomedicine. 2022;101:154113. https://doi.org/10.1016/j.phymed.2022.154113.

[35] Wei Y, Yin X, Wu H, Zhao M, Huang J, Zhang J, et al. Improving the flavor of summer green tea (Camellia sinensis L.) using the yellowing process. Food Chem. 2022;388:132982. https://doi.org/10.1016/j.foodchem.2022.132982.

[36] White PJ. Selenium accumulation by plants. Ann Bot, 2016, 117: 217-235.

[37] White PJ, Bowen HC, Parmaguru P, Fritz M, Spracklen WP, Spiby RE, et al.. Interactions between selenium and sulphur nutrition in Arabidopsis thaliana. J Exp Bot, 2004, 55: 1927-1937.

[38] Xiang J, Rao S, Chen Q, Zhang W, Cheng S, Cong X, et al.. Research progress on the effects of selenium on the growth and quality of tea plants. Plants (Basel), 2022, 11: 2491.

[39] Xu J, Zhang Y, Zhang M, Wei X, Zhou Y. Effects of foliar selenium application on Se accumulation, elements uptake, nutrition quality, sensory quality and antioxidant response in summer-autumn tea. Food Res Int. 2024;175:113618. https://doi.org/10.1016/j.foodres.2023.113618.

[40] Yang T, Li H, Hu X, Li J, Hu J, Liu R, et al.. Effects of fertilizing with N, P, Se, and Zn on regulating the element and functional component contents and antioxidant activity of tea leaves planted in red soil. J Agric Food Chem, 2014, 62: 3823-3830.

[41] Ye Y, Yan W, Peng L, He J, Zhang N, Zhou J, et al. Minerals and bioactive components profiling in Se-enriched green tea and the pearson correlation with Se. LWT-Food Sci Technol. 2023a;175:114470. https://doi.org/10.1016/j.lwt.2023.114470.

[42] Ye Y, Yan W, Peng L, Zhou J, He J, Zhang N, et al. Insights into the key quality components in Se-enriched green tea and their relationship with selenium. Food Res Int. 2023b;165:112460. https://doi.org/10.1016/j.foodres.2023.112460.

[43] Yu X, Hu S, He C, Zhou J, Qu F, Ai Z, et al. Chlorophyll metabolism in postharvest tea (Camellia sinensis L.) leaves: variations in color values, chlorophyll derivatives, and gene expression levels under different withering treatments. J Agric Food Chem. 2019;67(38):10624–36. https://doi.org/10.1021/acs.jafc.9b03477.

[44] Yuan Z, Long W, Hu H, Liang T, Luo X, Hu Z, et al.. Genome-wide identification and expansion patterns of SULTR gene family in gramineae crops and their expression profiles under abiotic stress in Oryza sativa. Genes (Basel), 2021, 12(5): 634.

[45] Zhang L, Cao Q, Granato D, Xu Y, Ho C. Association between chemistry and taste of tea: a review. Trends Food Sci Technol. 2020a;101:139–49. https://doi.org/10.1016/j.tifs.2020.05.015.

[46] Zhang M, Wilson L, Xing G, Jiang L, Tang S. Optimizing root architecture and increasing transporter gene expression are strategies to promote selenium uptake by high-se accumulating rice cultivar. Plant Soil, 2020, 447: 319-332.

[47] Zhang X, He H, Xiang J, Yin H, Hou T. Selenium-containing proteins/peptides from plants: a review on the structures and functions. J Agric Food Chem, 2020, 68: 15061-15073.

[48] Zhang H, Hao X, Zhang J, Wang L, Wang Y, Li N, et al.. Genome-wide identification of SULTR genes in tea plant and analysis of their expression in response to sulfur and selenium. Protoplasma, 2022, 259: 127-140.

[49] Zheng S, Dai H, Meng Q, Huang R, Tong H, Yuan L. Identification and expression analysis of the ZRT, IRT-like protein (ZIP) gene family in Camellia sinensis (L.) O. Kuntze. Plant Physiol Biochem. 2022;172:87–100. https://doi.org/10.1016/j.plaphy.2022.01.008.

Funding

Natural Science Foundation of Hubei Province(2023AFB877)

Knowledge Innovation Program of Wuhan-Shuguang Project,(2023020201020348)

National Key Research and Development Program of China,(2019YFD1001600)

RIGHTS & PERMISSIONS

The Author(s)