Arbuscular Mycorrhiza Improves Leaf Food Quality of Tea Plants
Tea (Camellia sinensis) plants inhabit arbuscular mycorrhizal fungi (AMF) in rhizosphere, whereas it is not clear whether AMF improves leaf food quality of tea plants. A potted study was conducted to determine effects of Claroideoglomus etunicatum, Diversispora spurca, D. versiformis and a mixture of the three AMF species on leaf sugar, amino acid, soluble protein, tea polyphenol, catechuic acid, and flavonoid contents of Camellia sinensis ‘Fuding Dabaicha’ seedlings. After 12 weeks of AMF inoculation, mycorrhizal plants recorded significantly higher shoot biomass and total leaf area, whilst the effect was ranked as C. etunicatum > D. spurca > mixed-AMF > D. versiformis in the decreasing order. AMF treatments significantly increased leaf total amino acid concentrations, accompanied with up-regulation of amino acid synthetic enzymes genes glutamine synthetase (CsGS), glutamate synthase (CsGOGAT) and glutamate dehydrogenase (CsGDH). Leaf glucose, sucrose, total soluble protein, tea polyphenol, catechuic acid, and flavonoid contents were significantly higher in AMF- than in non-AMF-inoculated plants. In addition, mycorrhizal inoculation notably up-regulated the expression level of leaf 3-hydroxy-3-methylglutaryl coenzyme gene (CsHMGR), ascorbate peroxidase gene (CsAPX), and tea caffeine synthase 1 gene (CsTCS1). These results implied that AMF inoculation had positive effects on leaf food quality partly by means of up-regulation of relevant gene expression in ‘Fuding Dabaicha’ seedlings.
In press - Online First. Article has been peer reviewed, accepted for publication and published online without pagination. It will receive pagination when the issue will be ready for publishing as a complete number (Volume 47, Issue 3, 2019). The article is searchable and citable by Digital Object Identifier (DOI). DOI link will become active after the article will be included in the complete issue.
Aliasgharzad N, Hajiboland R, Olsson PA (2011). Lack of arbuscular mycorrhizal colonisation in tea (Camellia sinensis, L.) plants cultivated in Northern Iran. Symbiosis 55(2):91-95.
Baslam M, Garmendia I, Goicoechea N (2013). The arbuscular mycorrhizal symbiosis can overcome reductions in yield and nutritional quality in greenhouse-lettuces cultivated at inappropriate growing seasons. Scientia Horticulturae 164:145-154.
Bradford MM (1976). A rapid and sensitive method for the quantification of microgram quantities of proteins utilizing the principle-dye binding. Analytical Biochemistry 72(1-2):248-252.
Burgess PJ, Carr MKV (1996). Responses of young tea (Camellia sinensis) clones to drought and temperature. I. yield and yield distribution. Experimental Agriculture 32(3):357-372.
Camenzind T, Rillig MC (2013). Extraradical arbuscular mycorrhizal fungal hyphae in an organic tropical montane forest soil. Soil Biology and Biochemistry 64:96-102.
Cely MVT, de Oliveira, AG, de Freitas VF, de Luca MB, Barazetti AR, … Andrade G (2016). Inoculant of arbuscular mycorrhizal fungi (Rhizophagus Clarus) increase yield of soybean and cotton under field conditions. Frontiers in Microbiology 7:720.
Chen S, Jin W, Liu A, Zhang S, Liu D, … He C (2013). Arbuscular mycorrhizal fungi (AMF) increase growth and secondary metabolism in cucumber subjected to low temperature stress. Scientia Horticulturae 160: 222-229.
Chen X, Li H, Chan WF, Wu C, Wu F, … Wong MH (2012). Arsenite transporters expression in rice (Oryza sativa L.) associated with arbuscular mycorrhizal fungi (AMF) colonization under different levels of arsenite stress. Chemosphere 89(10):1248-1254.
Cheng SY, Wang Y, Fei Y, Zhu G (2004). Studies on the effects of different treatments on flavonoids contents in Ginkgo biloba leaves and their regulating mechanism. Journal of Fruit Science 21(2): 116-119.
Cicatelli A, Lingua G, Todeschini V, Biondi S, Torrigiani P, Castiglione S (2012). Arbuscular mycorrhizal fungi modulate the leaf transcriptome of a Populus alba, L. clone grown on a zinc and copper-contaminated soil. Environmental & Experimental Botany 75:25-35.
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(1):152-162.
Fajardo L, Cáceres A, Arrindell P (2014). Arbuscular mycorrhizae, a tool to enhance the recovery and re-introduction of Juglans venezuelensis Manning, an endemic tree on the brink of extinction. Symbiosis 64(2):63-71.
Gachomo E, Allen JW, Pfeffer PE, Govindarajulu M, … Bücking H (2009). Germinating spores of Glomus intraradices can use internal and exogenous nitrogen sources for de novo biosynthesis of amino acids. New Phytologist 184(2):399-411.
Hartmann H, Trumbore S (2016). Understanding the roles of nonstructural carbohydrates in forest trees–from what we can measure to what we want to know. New Phytologist 211(2):386-403.
He JD, Dong T, Wu HH, Zou YN, Wu QS, Kuca K (2019). Mycorrhizas induce diverse responses of root TIP aquaporin gene expression to drought stress in trifoliate orange. Scientia Horticulturae 243:64-69.
Hu L, Li H, Pang H, Fu J (2012). Responses of antioxidant gene, protein and enzymes to salinity stress in two genotypes of perennial ryegrass (Lolium perenne) differing in salt tolerance. Journal of Plant Physiology 169(2):146-156.
Hui T, Drijber RA, Li X, Miller DN, Wienhold BJ (2013). Arbuscular mycorrhizal fungi differ in their ability to regulate the expression of phosphate transporters in maize (Zea mays L.). Mycorrhiza 23(6):507-514.
Jacob PT, Ana C, Concepción AA, Nuria F (2014). Transcriptional regulation of host NH4+ transporters and GS/GOGAT pathway in arbuscular mycorrhizal rice roots. Plant Physiology and Biochemistry 75:1-8.
Jin JQ, Yao MZ, Ma CL, Ma JQ, Chen L (2016). Natural allelic variations of TCS1 play a crucial role in caffeine biosynthesis of tea plant and its related species. Plant Physiology and Biochemistry 100:18-26.
Kahneh E, RamezanPour H, Tanha MRH, Shirinfekr A (2006). Effect of arbuscular mycorrhizal fungi and phosphorus supplement on leaf P, Zn, Cu and Fe concentrations of tea seedlings. Caspian Journal of Environmental Sciences 4(1):53-58.
Kerio LC, Wachira FN, Wanyoko JK, Rotich MK (2013). Total polyphenols, catechin profiles and antioxidant activity of tea products from purple leaf coloured tea cultivars. Food Chemistry 136(3-4):1405-1413.
Larose G, Chênevert R, Moutoglis P, Gagné S, Piché Y, Vierheilig H (2002). Flavonoid levels in roots of Medicago sativa, are modulated by the developmental stage of the symbiosis and the root colonizing arbuscular mycorrhizal fungus. Journal of Plant Physiology 159(12):1329-1339.
Li YH, Lu JL, Fan FY, Shi YT (2014). Gene cloning and expression analysis of HMGR in tea plant roots. Journal of Tea Science 34:583-590 (in Chinese with English abstract).
Lin ZH, Zhong QS, Chen CS (2012). Molecular cloning and quantitative analysis of GDH, GS and GOGAT genes from leave of tea plant. Journal of Tea Science 32:523-529 (in Chinese with English abstract).
Lingua G, Bona E, Manassero P, Marsano F, Todeschini V, … Berta G (2013). Arbuscular mycorrhizal fungi and plant growth-promoting pseudomonads increases anthocyanin concentration in strawberry fruits (Fragaria x ananassa var. Selva) in conditions of reduced fertilization. International Journal of Molecular Sciences 14(8):16207-16225.
Liu A, Chen S, Liu Y, Li Y, He C (2011). Effects of AM fungi on leaf photosynthetic physiological parameters and antioxidant enzyme activities under low temperature. Acta Ecologica Sinica 31:3497-3503 (in Chinese with English abstract).
Liu CY, Wang P, Zhang DJ, Zou YN, Kuca K, Wu QS (2018). Mycorrhiza-induced change in root hair growth is associated with IAA accumulation and expression of EXPs in trifoliate orange under two P levels. Scientia Horticulturae 234:227-235.
Livak KJ, Schmittgen TD (2001). Analysis of relative gene expression data using real-time quantitative PCR and 2-ΔΔCT method. Methods 25(4):402-408.
Mena-Violante HG, Ocampo-Jiménez O, Dendooven L, Martínez-Soto G, González-Castañeda J, … Olalde-Portugal V (2006). Arbuscular mycorrhizal fungi enhance fruit growth and quality of chile ancho (Capsicum annuum L. cv San Luis) plants exposed to drought. Mycorrhiza 16(4):261-267.
Mizuno K, Okuda A, Kato M, Yoneyama N, Tanaka H, … Fujimura T (2003). Isolation of a new dual-functional caffeine synthase gene encoding an enzyme for the conversion of 7-methylxanthine to caffeine from coffee (Coffea arabica, L.). FEBS Letters 534(1-3):75-81.
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(1):158-161.
Ravnskov S, Wu Y, Graham JH (2003). Arbuscular mycorrhizal fungi differentially affect expression of genes coding for sucrose synthases in maize roots. New Phytologist 157(3):539-545.
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(1):44.
Sanmartín C, Garmendia I, Romano B, Díaz M, Palop JA, Goicoechea N (2014). Mycorrhizal inoculation affected growth, mineral composition, proteins and sugars in lettuces biofortified with organic or inorganic selenocompounds. Scientia Horticulturae 180:40-51.
Sarowar S, Kim EN, Kim YJ, Ok SH, Kim KD, … Shin JS (2005). Overexpression of a pepper ascorbate peroxidase-like 1 gene in tobacco plants enhances tolerance to oxidative stress and pathogens. Plant Science 169(1):55-63.
Sharma D, Kayang H (2017). Effects of arbuscular mycorrhizal fungi (AMF) on Camellia sinensis (L.) O. Kuntze under greenhouse conditions. Journal of Experimental Biology 5:235-241.
Shao YD, Zhang DJ, Hu XC, Wu QS, Jiang CJ, … Kuča K (2018). Mycorrhiza-induced changes in root growth and nutrient absorption of tea plants. Plant Soil and Environment 64(6):283-289.
Singh S, Pandey A, Chaurasia B, Palni LMS (2008). Diversity of arbuscular mycorrhizal fungi associated with the rhizosphere of tea growing in ‘natural’ and ‘cultivated’ ecosites. Biology and Fertility of Soils 44(3):491-500.
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(5):427-433.
Tchameni SN, Nwaga D, Wakam LN, Ngonkeu ELM, … 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(5):220-228.
Van der Heijdan MGA, Kliromomos JN, Ursic M, Moutoglis P (1998). Mycorrhizal fungi diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396(6706):69-72.
Van Lelyveld LJ, Fraser C, Smith BL, Visse G (1990). Nitrogen fertilization of tea: effect of tea leaf plucking criteria on chlorophyll and quality parameters. South African Journal of Plant and Soil 7(3):188-191.
Vangelisti A, Natali L, Bernardi R, Sbrana C, Turrini A, … Giordani T (2018). Transcriptome changes induced by arbuscular mycorrhizal fungi in sunflower (Helianthus annuus L.) roots. Scientific Reports 8(1):4.
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.
Wu QS, Peng YH, Zou YN, Liu CY (2010). Exogenous polyamines affect mycorrhizal development of Glomus mosseae-colonized citrus (Citrus tangerine) seedlings. ScienceAsia 36(3):254-258.
Xia T, Gao LP (2009). Advances in biosynthesis pathways and regulation of flavonoids and catechins. Scientia Agricultura Sinica 42:2899-2908 (in Chinese with English abstract).
Zhang J, Zeng L, Sun H, Wu H, Chen S (2017). Adversity stress-related responses at physiological attributes, transcriptional and enzymatic levels after exposure to Cu in Lycopersicum esculentm seedlings. Scientia Horticulturae 222:213-220.
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 (in Chinese with English abstract).
Zhao XM (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).
Zou YN, Srivastava AK, Ni QD, Wu QS (2015). Disruption of mycorrhizal extraradical mycelium and changes in leaf water status and soil aggregate stability in rootbox-grown trifoliate orange. Frontiers in Microbiology 6:203.
Zubek S, Rola K, Szewczyk A, Majewska ML, Turnau K (2015). Enhanced concentrations of elements and secondary metabolites in Viola tricolor L. induced by arbuscular mycorrhizal fungi. Plant and Soil 390(1-2):129-142.
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.