Effects of mycorrhizal fungi on plant growth, nutrient absorption and phytohormones levels in tea under shading condition
DOI:
https://doi.org/10.15835/nbha48412082Keywords:
AMF; nutrient; phytohormones; root hair; shading; teaAbstract
High temperature and strong light could induce bitterness and astringency of tea (Camellia sinensis (L.) O. Kuntze) in summer. Arbuscular mycorrhizal (AM) fungus and shading could change tea growth surroundings and improve its quality. The present study evaluated the inoculated effects of an arbuscular mycorrhizal fungus (AMF), Glomus etunicatum, on plant growth, root morphology, leaf nutrient status, phytohormones and the relative expression of root CsCPC, CsTTG1, CsAUX1, CsYUCCA1, CsNCED2, CsGA3OX1, CsDWF4 and CsAOS genes in Camellia sinensis ‘Xinyang population’ seedlings in sands under shading conditions. After 14 weeks of AMF inoculation, root mycorrhizal colonization ranged from 18.5% to 48.00%. AMF inoculation and shading heavily increased plant height, shoot and root biomass, total root length and volume, leaf nutrients content (except Fe), respectively. Both mycorrhizal inoculation and shading significantly increased root hair growth respectively, in company with up-regulation gene CsCPC and down-regulation gene CsTTG1. Root auxin level and its transport gene CsAUX1 was both up-regulated by mycorrhizal inoculation and shading. Interestingly, auxin biosynthesis gene CsYUCCA1 has not been affected, which suggested that both mycorrhizal and shading mainly regulate auxin transport but not biosynthesis pathway. The contents of gibberellin (GA) and brassinosteroid (BR) in root were notably increased by mycorrhizal inoculation and shading, accompanied with up-regulation of its biosynthesis genes, CsGA3OX1 and CsDWF4. With regard to the growth inhibiting phytohormones abscisic acid (ABA) and jasmonic acid (JA), mycorrhizal inoculation and shading significantly decreased their levels in root, in company with down-regulation of biosynthesis genes, CsNCED2 and CsAOS. These results implied that both AMF inoculation and shading could enhance the tea plant stress resistance and increase nutrient absorption, root biomass and the contents of root phytohormones by up-regulating its transport and biosynthesis pathway.
References
Aliasgharzad N, Hajiboland R, Olsson PA (2011). Lack of arbuscular mycorrhizal colonisation in tea (Camellia sinensis L.) plants cultivated in Northern Iran. Symbiosis 55:91-95.
Bray DF, Bagu J, Koegler P (1993). Comparison of hexamethyldisilazane (HMDS), Peldri II, and critical-point drying methods for scanning electron microscopy of biological specimens. Microscopy Research and Technique 26:489-495. https://doi.org/10.1002/jemt.1070260603
Bennett MJ, Marchant A, Green HG, May ST, Ward SP, ... Feldmann KA (1996). Arabidopsis AUX1 gene: a permease-like regulator of root gravitropism. Science 273:948-950. https://doi.org/10.1126/science.273.5277.948
Choe S, Dilkes BP, Fujioka S, Takatsuto S, Sakurai A, Feldmann KA (1998). The DWF4 gene of Arabidopsis encodes a cytochrome P450 that mediates multiple 22alpha-hydroxylation steps in brassinosteroid biosynthesis. The Plant Cell 10:231-244. https://doi.org/10.1105/tpc.10.2.231
Estrada-Melo AC, Reid MS, Jiang CZ (2015). Overexpression of an ABA biosynthesis gene using a stress-inducible promoter enhances drought resistance in petunia. Horticulture Research 2:15013. https://doi.org/10.1038/hortres.2015.13
Gutierrez L, Mongelard G, Flokova K, Pacurar DI, Novák O, ... Bellini C (2012). Auxin controls Arabidopsis adventitious root initiation by regulating jasmonic acid homeostasis. The Plant Cell 24:2515-2527. https://doi.org/10.1105/tpc.112.099119
Hashem A, Alqarawi AA, Al-Huqail AA, AbdAllah EF (2018). Biodiversity of arbuscular mycorrhizal fungi associated with Acacia gerrardii Benth in different habitats of Saudi Arabia. Pakistan Journal of Botany 50:1211-1217.
Hoyerova K, Hosek P, Quareshy M, Li J, Klima P, Kubes M, ... Napier RM (2018). Auxin molecular field maps define AUX1 selectivity: many auxin herbicides are not substrates. New Phytologist 217:1625-1639. https://doi.org/10.1111/nph.14950
Huang S, Raman AS, Ream JE, Fujiwara H, Cerny RE, Brown SM (1998). Overexpression of 20-oxidase confers a gibberellin-overproduction phenotype in Arabidopsis. Plant Physiologist 118:773-781. https://doi.org/10.1104/pp.118.3.773
Jia F, Cheng D, Huifeng L, Yafan H, Zhongchi L, Chunying K (2019). Reporter gene expression reveals precise auxin synthesis sites during fruit and root development in wild strawberry. Journal of Experimental Botany 70:563-574. https://doi.org/10.1093/jxb/ery384
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 Science 4:53-58. http://dx.doi.org/10.4067/S0718-95162014005000016
Kalcsits L, Asteggiano L, Schmidt T, Musacchi S, Serra S, Layne DR, ... Mupambi G (2018). Shade netting reduces sunburn damage and soil moisture depletion in ‘Granny Smith’ apples. Acta Horticulturae 1228:85-90. https://doi.org/10.17660/ActaHortic.2018.1228.11
Kato-Noguchi H, Kobayashi K (2009). Jasmonic acid, protein phosphatase inhibitor, metals and UV-irradiation increased momilactone A and B concentrations in the moss Hypnum plumaeforme. Journal of Plant Physiology 166:1118-1122. https://doi.org/10.1016/j.jplph.2008.12.012
Kojima M, Sakakibara H (2012). Highly sensitive high-throughput profiling of six phytohormones using MS-probe modification and liquid chromatography-tandem mass spectrometry. Methods in Molecular Biology 918:151-164. https://doi.org/10.1007/978-1-61779-995-2_11
Ohashi-Ito K, Iwamoto K, Nagashima Y, Kojima M, Sakakibara H, Fukuda H (2019). A positive feedback loop comprising LHW-TMO5 and local auxin biosynthesis regulates initial vascular development in Arabidopsis roots. Plant and Cell Physiology 60(12):2684-2691. https://doi.org/10.1093/pcp/pcz156
Lagad RA, Alamelu D, Laskar AH, Rai VK, Singhb SK, Aggarwal SK (2013). Isotope signature study of the tea samples produced at four different regions in India. Analytical Methods 5:1604-1611.
Leng P, Yuan B, Guo Y (2014). The role of abscisic acid in fruit ripening and responses to abiotic stress. Journal of Experimental Botany 65:4577-4588. https://doi.org/10.1093/jxb/eru204
Li Q, Yu JW, Lu J, Fei HY, Luo M, Cao BW, ... Liu QQ (2018a). Seed-specific expression of OsDWF4, a rate-limiting gene involved in BR biosynthesis, improves both grain yield and quality in rice. Journal of Agricultural and Food Chemistry 66:3759-3772. https://doi.org/10.1021/acs.jafc.8b00077
Li T, Dai J, Zhang Y, Kong X, Li C, Dong H (2019). Topical shading substantially inhibits vegetative branching by altering leaf photosynthesis and hormone contents of cotton plants. Field Crops Research 238:18-26. https://doi.org/10.1016/j.fcr.2019.04.019
Li X, Wei JP, Ahammed GJ (2018b). Brassinosteroids attenuate moderate high temperature-caused decline in tea quality by enhancing the anine biosynthesis in Camellia sinensis L. Frontiers in Plant Science 9:1016. https://doi.org/10.3389/fpls.2018.01016
Li YX, Tang DY, Li L, Zhao XY, Lin JZ, Liu XM (2018c). Plant stature related receptor-like Kinanse2 (PSRK2) acts as a factor that determines stem elongation toward gibberellins response in rice. Bioscience Biotechnology and Biochemistry 82:1931-1941. https://doi.org/10.1080/09168451.2018.1501266
Li Z, Takahashi Y, Scavo A, Brandt B, Nguyen D, Rieu P, Schroeder JI (2018d). Abscisic acid-induced degradation of Arabidopsis guanine nucleotide exchange factor requires calcium-dependent protein kinases. Proceedings of the National Academy of Sciences 115:4522-4531. https://doi.org/10.1073/pnas.1719659115
Lian QL, Xin HB, Li XX, Zhong XH, Yin YL, Yi MF (2013). Isolation, characterization and expression analysis of the genes-GhAOS, GhAOC and GhOPR3: Encoding the key enzymes involved in jasmonic acid biosynthesis in Gladiolus hybridus. Scientia Horticulturae 154:88-95.
Lin ZH, Qi YP, Chen RB, Zhang FZ, Chen LS (2010). Effects of phosphorus supply on the quality of green tea. Food Chemistry 130:908-914.
Liu CY, Zhang F, Zhang DJ, Srivastava AK, Wu QS, Zou YN (2018). Mycorrhiza stimulates root-hair growth and IAA synthesis and transport in trifoliate orange under drought stress. Scientific Reports 8:1978.
Livak KJ, Schmittgen TD (2001). 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
Long Y, Schiefelbein J (2020). Novel ttg1 mutants modify root-hair pattern formation in Arabidopsis. Frontiers in Plant Science 11:383. https://doi.org/10.3389/fpls.2020.00383
Martin MT, Pedranzani H, Garcia-Molinero P, Pando V, Sierra-de-Grado R (2009). Inhibitory effect of jasmonic acid and ethylene on epicotyl growth and bud induction in the maritime pine, Pinus pinaster Soland. in Ait. Biocell 33:141-148. https://doi.org/10.32604/biocell.2009.33.141
Mathur S, Sharma MP, Jajoo A (2018). Improved photosynthetic efficacy of maize (Zea mays) plants with arbuscular mycorrhizal fungi (AMF) under high temperature stress. Journal of Photochemistry and Photobiology B-Biology 180:149-154. https://doi.org/10.1016/j.jphotobiol.2018.02.002
Mathur S, Tomar RS, Jajoo A (2019). Arbuscular Mycorrhizal fungi (AMF) protects photosynthetic apparatus of wheat under drought stress. Photosynthesis Research 139:227-238. https://doi.org/10.1007/s11120-018-0538-4
Muleta D, Assefa F, Nemomissa S, Granhall U (2007). Composition of coffee shade tree species and density of indigenous arbuscular mycorrhizal fungi (AMF) spores in Bonga natural coffee forest, southwestern Ethiopia. Forest Ecology and Management 241:145-154. https://doi.org/10.1016/j.foreco.2007.01.021
Roumeliotis E, Kloosterman B, Oortwijn M, Lange T, Visser RGF, Bachem CWB (2013). Down regulation of StGA3ox genes in potato results in altered GA content and affect plant and tuber growth characteristics. Journal of Plant Physiology 170:1228-1234.
Savage N, Yang TJ, Chen CY, Lin KL, Monk NA, Schmidt W (2013). Positional signaling and expression of ENHANCER OF TRY AND CPC1 are tuned to increase root hair density in response to phosphate deficiency in Arabidopsis thaliana. PLoS One 8:e75452. https://doi.org/10.1371/journal.pone.0075452
Schomburg FM, Bizzell CM, Lee DJ, Zeevaart JAD, Amasino RM (2003). Overexpression of a novel class of gibberellin 2-oxidases decreases gibberellin levels and creates dwarf plants. The Plant Cell 15:151-163. https://doi.org/10.1105/tpc.005975
Shahnejat-Bushehri S, Tarkowska D, Sakuraba Y, Balazadeh S (2016). Arabidopsis NAC transcription factor JUB1 regulates GA/BR metabolism and signalling. Nature Plants 2:16013. https://doi.org/10.1038/nplants.2016.13
Shao YD, Zhang DJ, Hu XC, Wu QS, Jiang CJ, ... Kuca 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
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.
http://dx.doi.org/10.18006/2017.5(2).235.241
Sieberer T, Leyser O (2006). Auxin transport, but in which direction? Many aspects of plant growth depend on transport of the hormone auxin across tissues, directed by specific transporter proteins. Science 312:858-860. https://doi.org/10.1126/science.1123701
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 44:491-500. https://doi.org/10.1007/s00374-007-0231-9
Sun L, Yuan B, Zhang M, Wang L, Cui M (2012). Fruit-specific RNAi-mediated suppression of SlNCED1 increases both lycopene and β-carotene contents in tomato fruit. Journal of Experimental Botany 63:3097-3108. https://doi.org/10.1093/jxb/ers026
Tang H, Tang JC, Li JL (2008). Synthetical effects of shading on tea plantation during the high-temperature and drought season. Guangdong Agriculture Science 26:26-29 (in Chinese with English abstract).
Tominaga-Wada R, Wada T (2016). Analysis of TTG1 and CPC-like MYB genes during Arabidopsis epidermal cell differentiation. Plant Biotechnology 33:201-206. https://doi.org/10.5511/plantbiotechnology.16.0629a
Upreti KK, Bhatt RM, Panneerselvam P, Varalakshmi LR (2016). Morpho-physiological responses of grape rootstock ‘Dogridge’ to arbuscular mycorrhizal fungi inoculation under salinity stress. International Journal of Fruit Science 16:191-209.
Wada T, Tachibana T, Shimura Y, Okada K (1997). Epidermal cell differentiation in Arabidopsis determined by a Myb homolog, CPC. Science 277:1113-1116. https://doi.org/10.1126/science.277.5329.1113
Wang X, Zeng W, Ding Y, Wang Y, Niu L, Pan L, ... Wang ZQ (2019). PpERF3 positively regulates ABA biosynthesis by activating PpNCED2/3 transcription during fruit ripening in peach. Horticulture Research 6:19. https://doi.org/10.1038/s41438-018-0094-2
Wu QS, He JD, Srivastava AK, Zou YN, Kuca K (2019). 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, He XH, Zou YN, Liu CY, Xiao J, Li Y (2012). Arbuscular mycorrhizas alter root system architecture of Citrus tangerine through regulating metabolism of endogenous polyamines. Plant Growth Regulation 68:27-35. https://doi.org/10.1007%2Fs10725-012-9690-6
Wu QS, Liu CY, Zhang DJ, Zou YN, He XH, Wu QH (2016). Mycorrhiza alters the profile of root hairs in trifoliate orange. Mycorrhiza 26:237-247.
Wu QS, Srivastava AK, Zou YN (2013). AMF-induced tolerance to drought stress in citrus: A review. Scientia Horticulturae 164:77-87. https://doi.org/10.1016/j.scienta.2013.09.010
Wu QS, Zou YN, He XH, Luo P (2011). Arbuscular mycorrhizal fungi can alter some root characters and physiological status in trifoliate orange (Poncirus trifoliata L. Raf.) seedlings. Plant Growth Regulation 65:273-278. https://doi.org/10.1007/s10725-011-9598-6
Yang T, Lv R, Li J, Lin H, Xi D (2018). Phytochrome A and B negatively regulate salt stress tolerance of Nicotiana tabacum via ABA-Jasmonic acid synergistic cross-talk. Plant and Cell Physiology 59:2381-2393. https://doi.org/10.1093/pcp/pcy164
Yin Y, Wang ZY, Mora-Garcia S, Li JM, Yoshida S, Asami T, Chory J (2002). BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation. Cell 109:181-191. https://doi.org/10.1016/s0092-8674(02)00721-3
Zbigniew B, Agnieszka S, Zenon T, Kurtyka R, Karcz W (2018). Role of auxin (IAA) in the regulation of slow vacuolar (SV) channels and the volume of red beet taproot vacuole. BMC Plant Biology 18:102. https://doi.org/10.1186/s12870-018-1321-6
Zhang DJ, Xia RX, Cao X (2016). Ethylene modulates root hair development in trifoliate orange through auxin-signaling pathway. Scientia Horticulturae 213:252-259. https://doi.org/10.1016/j.scienta.2016.11.007
Zhang DJ, Xia RX, Cao X, Shu B, Chen CC (2013). Root hair development of Poncirus trifoliata grown in different growth cultures and treated with 3-indolebutyric acid and ethephon. Scientia Horticulturae 160:389-397. https://doi.org/10.1016/j.scienta.2013.06.007
Zhang DJ, Yang YJ, Liu CY, Zhang F, Hu W, ... Wu QS (2018). Auxin modulates root-hair growth through its signaling pathway in citrus. Scientia Horticulturae 236:73-78.
Zhang F, Wang P, Zou YN, Wu QS, Kuca K (2019). 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 J, Zhang X, Ye M, Li XW, Lin SB, Sun XL (2020). The jasmonic acid pathway positively regulates the polyphenol oxidase-based defense against tea geometrid caterpillars in the tea plant (Camellia sinensis). Journal of Chemical Ecology 46:308-316. https://doi.org/10.1007/s10886-020-01158-6
Zhang YC, Wang P, Wu QH, Zou YN, Bao Q, Wu QS (2017). Arbuscular mycorrhizas improve plant growth and soil structure in trifoliate orange under salt stress. Archives of Agronomy and Soil Science 63:491-500. https://doi.org/10.1080/03650340.2016.1222609
Zhao Y, Christensen SK, Fankhauser C, Cashman JR, Cohen JD, Chory J (2001). A role for flavin monooxygenase-like enzymes in auxin biosynthesis. Science 291:306-309. https://doi.org/10.1126/science.291.5502.306
Zou YN, Wang P, Liu CY, Ni QD, Zhang DJ, Wu QS (2017). Mycorrhizal trifoliate orange has greater root adaptation of morphology and phytohormones in response to drought stress. Scientific Reports 7:41134.
Zou YN, Wu HH, Giri B, Wu QS, Kuca 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, Zhang DJ, Liu CY, Wu QS (2019). Relationships between mycorrhizae and root hairs. Pakistan Journal of Botany 5:727-733.

Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2020 Mufang SUN, Ding YUAN, Xianchun HU, Dejian ZHANG, Yeyun LI

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.