Inoculation with Clariodeoglomus etunicatum improves leaf food quality of tea exposed to P stress
DOI:
https://doi.org/10.15835/nbha49112166Keywords:
catechins; flavonoid; mycorrhiza; secondary metabolites; white teaAbstract
The present study aimed to evaluate the effect of an arbuscular mycorrhizal fungus (AMF), Clariodeoglomus etunicatum, on leaf food quality and relevant gene expression levels of tea (Camellia sinensis cv. ‘Fuding Dabaicha’) seedlings exposed to 0.5 μM P (P0.5) and 50 μM P (P50) levels. Twenty-four weeks later, the seedlings recorded higher root mycorrhizal fungal colonization in P50 than in P0.5. AMF-inoculated tea plants represented significantly higher leaf fructose and glucose contents and lower sucrose content than non-inoculated plants, irrespective of substate P levels. AMF treatment also increased total amino acids content in P0.5 and P50, accompanied with higher expression of glutamate dehydrogenase (CsGDH) and lower expression of glutamine synthetase (CsGS) and glutamine oxoglutarate aminotransferase (CsGOGAT). The total flavonoid content was higher in mycorrhizal versus non-mycorrhizal plants under P0.5 and P50, together with induced expression of phenylalanine ammonia-lyase (CsPAL) and cinnamic acid 4-hydroxylase (CsC4H). Mycorrhizal fungal inoculation improved catechins content, which is due to the up-regulated expression of flavanone 3-hydroxylase (CsF3H), flavonoid 3'-hydroxylase (CsF3'H), dihydroflavonol 4-reductase (CsDFR), leucoanthocyanidin reductase (CsLAR), anthocyanidin reductase (CsANR), and chalcone isomerase (CsCHI) under P0.5. However, under P50, the gene involved in catechins synthesis was not affected or down-regulated by mycorrhization, implying a complex mechanism (e.g. nutrient improvement). AMF also inhibited the tea caffeine synthase 1 (CsTCS1) expression regardless of P levels. Therefore, the results of this study concluded that inoculation with C. etunicatum improves leaf food quality of tea exposed to P stress, but the improved mechanisms were different between P0.5 and P50.
References
Ahmed S, Griffin TS, Kraner D, Schaffner MK, Sharma D, Hazel M, … Cash SB (2019). Environmental factors variably impact tea secondary metabolites in the context of climate change. Frontiers in Plant Science 10:939. https://doi.org/10.3389/fpls.2019.00939
Bradford MM (1970). A rapid and sensitive method for the quantification of microgram quantities of proteins utilizing the principle-dye binding. Analytical Biochemistry 72:248-252. https://doi.org/10.1016/0003-2697(76)90527-3
Ceasar SA (2020). Regulation of low phosphate stress in plants. In: Tripathi DK, Singh VP, Chauhan DK, Sharma S, Prasad SM, Dubey NK, Ramawat N (Eds). Plant Life under Changing Environment: Responses and Management. Academic Press, pp 123-156.
Cheng SY, Wang Y, Fei YJ, Zhu GC (2004). Studies on the effects of different treatments on flavonoids contents in Ginkgo biloba leaves and their regulating mechanism. Journal of Fruit Science 21:116-119 (in Chinese with English abstract).
de La Rosa LA, Alvarez-Parrilla E, Shahidi F (2011). Phenolic compounds and antioxidant activity of kernels and shells of Mexican pecan (Carya illinoinensis). Journal of Agricultural and Food Chemistry 59:152-162. https://doi.org/10.1021/jf1034306
Duan Y, Zhu XJ, Shen JZ, Xing HQ, Zou ZW, Ma YC, … Fang WP (2020). Genome-wide identification, characterization and expression analysis of the amino acid permease gene family in tea plants (Camellia sinensis). Genomics 112:2866-2874. https://doi.org/10.1016/j.ygeno.2020.03.026
He JD, Chi GG, Zou YN, Shu B, Wu QS, Srivastava AK, Kuča K (2020a). Contribution of glomalin-related soil proteins to soil organic carbon in trifoliate orange. Applied Soil Ecology 154:103592. https://doi.org/10.1016/j.apsoil.2020.103592
He JD, Zou YN, Wu QS, Kuča K (2020b). Mycorrhizas enhance drought tolerance of trifoliate orange by enhancing activities and gene expression of antioxidant enzymes. Scientia Horticulturae 262:108745. https://doi.org/10.1016/j.scienta.2019.108745
Huang JH, Luo SM, Zeng RS, Dong DF (2006). Effects of AMF on maize plant growth under phosphorus stress. Journal of Guangxi Agricultural and Biology Science 25:321-324 (in Chinese with English abstract).
Johansen A, Finlay RD, Olsson PA (1996). Nitrogen metabolism of external hyphae of the arbuscular mycorrhizal fungus Glornus intraradices. New Phytologist 133:705-712.
Kato M, Mizuno K, Crozier A, Fujimura T, Ashihara H (2000). Caffeine synthase gene from tea leaves. Nature 406:956-957. https://doi.org/10.1038/35023072
Li CF, Zhu Y, Yu Y, Zhao QY, Wang SJ, Wang XC, … Yang YJ (2015). Global transcriptome and gene regulation network for secondary metabolite biosynthesis of tea plant (Camellia sinensis). BMC Genomics 16:560. https://doi.org/10.1186/s12864-015-1773-0
Liu YF, Jin JQ, Yao MZ, Chen L (2019). Screening, cloning and functional research of the rare allelic variation of caffeine synthase gene (TCS1g) in tea plants. Scientia Agricultura Sinica 52:1772-1783 (in Chinese with English abstract).
Livak KJ, Schmittgen TD (2002). Analysis of relative gene expression data using real-time quantitative PCR and 2-ΔΔCt method. Methods 25:402-408. https://doi.org/10.1006/meth.2001.1262
Mei LL, Yang X, Zhang SQ, Zhang T, Guo JX (2019). Arbuscular mycorrhizal fungi alleviate phosphorus limitation by reducing plant N:P ratios under warming and nitrogen addition in a temperate meadow ecosystem. Science of the Total Environment 686:1129-1139. https://doi.org/10.1016/j.scitotenv.2019.06.035
Phillips JM, Hayman DS (1970). Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Transactions of the British Mycological Society 55:158-161. https://doi.org/10.1016/S0007-1536(70)80110-3
Salehi SY, Hajiboland R (2008). A high internal phosphorus use efficiency in tea (Camellia sinensis L.) plants. Asian Journal of Plant Sciences 7:30-36. https://doi.org/10.3923/ajps.2008.30.36
Salvioli A, Zouari I, Chalot M, Bonfante P (2012). The arbuscular mycorrhizal status has an impact on the transcriptome profile and amino acid composition of tomato fruit. BMC Plant Biology 12:44. https://doi.org/10.1186/1471-2229-12-44
Shao YD, Hu XC, Wu QS, Yang TY, Srivastava AK, Zhang DJ, … Kuča K (2021). Mycorrhizas promote P acquisition of tea plants through changes in root morphology and P transporter gene expression. South African Journal of Botany 137:455-462. https://doi.org/10.1016/j.sajb.2020.11.028
Shao YD, Zhang DJ, Hu XC, Wu QS, Jiang CJ, Xia TJ, … Kuča K (2018). Mycorrhiza-induced changes in root growth and nutrient absorption of tea plants. Plant, Soil and Environment 64:283-289. https://doi.org/10.17221/126/2018-PSE
Singh S, Pandey A, Kumar B, Palni LMS (2010). Enhancement in growth and quality parameters of tea [Camellia sinensis (L.) O. Kuntze] through inoculation with arbuscular mycorrhizal fungi in an acid soil. Biology and Fertility of Soils 46:427-433. https://doi.org/10.1007/s00374-010-0448-x
Tchameni SN, Nwaga D, Wakam LN, Mangaptche Ngonkeu EL, Fokom R, Kuaté, J, Etoa FX (2012). Growth enhancement, amino acid synthesis and reduction in susceptibility towards phytophthora megakarya by arbuscular mycorrhizal fungi inoculation in cocoa plants. Journal of Phytopathology 160:220-228. https://doi.org/10.1111/j.1439-0434.2012.01888.x
Thokchom SD, Gupta S, Kapoor R (2020). Arbuscular mycorrhiza augments essential oil composition and antioxidant properties of Ocimum tenuiflorum L. – A popular green tea additive. Industrial Crops and Products 153:112418. https://doi.org/10.1016/j.indcrop.2020.112418
Tomanr DS, Bhuyan LP, Sabhapondit S, Sarmah SR, Borthakur BK, Jha DK (2012). Impact of inoculated arbuscular mycorrhizal (AM) fungi on metabolism of flavanols (catechins) and caffeine in tea shoots [Camellia sinensis (L) O. Kuntze]. Two and a Bud 59:106-111. https://www.researchgate.net/publication/259191607
Wang SG (2002). Influence of AM on the growth of vegetative tea seedling and the quality of tea. Chinese Bulletin of Botany 19:462-468 (in Chinese with English abstract).
Wu QS, Gao WQ, Srivastava AK, Zhang F, Zou YN (2020). Nutrient acquisition and fruit quality of Ponkan mandarin in response to AMF inoculation. Indian Journal of Agricultural Sciences 90:1563-1567.
Wu QS, He JD, Srivastava AK, Zou YN, Kuča K (2019a). Mycorrhizas enhance drought tolerance of citrus by altering root fatty acid compositions and their saturation levels. Tree Physiology 39:1149-1158. https://doi.org/10.1093/treephys/tpz039
Wu QS, Lou YG, Li Y (2015). Plant growth and tissue sucrose metabolism in the system of trifoliate orange and arbuscular mycorrhizal fungi. Scientia Horticulturae 181:189-193. http://dx.doi.org/10.1016/j.scienta.2014.11.006
Wu QS, Shao YD, Gao XB, Xia TJ, Kuča K (2019b). Characterization of AMF-diversity of endosphere versus rhizosphere of tea (Camellia sinensis) crops. Indian Journal of Agricultural Sciences 89:348-352.
Wu QS, Peng YH, Zou YN, Liu CY (2010). Exogenous polyamines affect mycorrhizal development of Glomus mosseae-colonized citrus (Citrus tangerine) seedlings. ScienceAsia 36:254-258. https://doi.org/10.2306/scienceasia1513-1874.2010.36.254
Xiong LG, Li J, Li YH, Yuan L, Liu SQ, Huang JA, Liu ZH (2013). Dynamic changes in catechin levels and catechin biosynthesis-related gene expression in albino tea plants (Camellia sinensis L.). Plant Physiology and Biochemistry 71:132-143. https://doi.org/10.1016/j.plaphy.2013.06.019
Yang L, Zou YN, Tian ZH, Wu QS, Kuča K (2021). Effects of beneficial endophytic fungal inoculants on plant growth and nutrient absorption of trifoliate orange seedlings. Scientia Horticulturae 277:109815. https://doi.org/10.1016/j.scienta.2020.109815
Zhang F, Wang P, Zou YN, Wu QS, Kuča K (2019a). Effects of mycorrhizal fungi on root-hair growth and hormone levels of taproot and lateral roots in trifoliate orange under drought stress. Archives of Agronomy and Soil Science 65:1316-1330. https://doi.org/10.1080/03650340.2018.1563780
Zhang F, Zou YN, Wu QS, Kuča K (2020). Arbuscular mycorrhizas modulate root polyamine metabolism to enhance drought tolerance of trifoliate orange. Environmental and Experimental Botany 171:103962. https://doi.org/10.1016/j.envexpbot.2019.103926
Zhang YC, Zou YN, Liu LP, Wu QS (2019b). Common mycorrhizal networks activate salicylic acid defense responses of trifoliate orange (Poncirus trifoliata). Journal of Integrative Plant Biology 61:1099-1111. https://doi.org/10.1111/jipb.12743
Zhao (2010). Sulfuric acid-vanillin assay of the total amount of tea catechin. Journal of Anhui Agricultural Sciences 38:9766-9770 (in Chinese with English abstract).
Zhao QH, Sun LT, Wang Y, Ding ZT, Li M (2014). Effects of arbuscular mycorrhizal fungi and nitrogen regimes on plant growth, nutrient uptake and tea quality in Camellia sinensis (L.) O. Kuntze. Plant Physiology Journal 50:164-170.
Zou YN, Wu HH, Giri B, Wu QS, Kuča K (2019). Mycorrhizal symbiosis down-regulates or does not change root aquaporin expression in trifoliate orange under drought stress. Plant Physiology and Biochemistry 144:292-299. https://doi.org/10.1016/j.plaphy.2019.10.001
Zou YN, Wu QS, Kuča K (2020). Unravelling the role of arbuscular mycorrhizal fungi in mitigating the oxidative burst of plants under drought stress. Plant Biology http://dx.doi.org/10.1111/plb.13161.
Zou YN, Zhang F, Srivastava AK, Wu QS, Kuča K (2021). Arbuscular mycorrhizal fungi regulate polyamine homeostasis in roots of trifoliate orange for improved adaptation to soil moisture deficit stress. Frontiers in Plant Science 11:600792. https://doi.org/10.3389/fpls.2020.600792
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2021 Jin-Li CAO, Ya-Dong SHAO, Ying-Ning ZOU, Qiang-Sheng WU, Tian-Yuan YANG, Kamil KUČA

This work is licensed under a Creative Commons Attribution 4.0 International License.
License:
Open Access Journal:
The journal allows the author(s) to retain publishing rights without restriction. Users are allowed to read, download, copy, distribute, print, search, or link to the full texts of the articles, or use them for any other lawful purpose, without asking prior permission from the publisher or the author.