Abstract
The tea plant [Camellia sinensis (L.) O. Kuntze] is an evergreen crop with a shallow root system that predominantly grows in acidic soil, strongly dependent on arbuscular mycorrhizal fungi. The present study evaluated the effects of a proven effective arbuscular mycorrhizal fungus (AMF), Claroideoglomus etunicatum, on plant growth performance, root morphology, root hair variables, root endogenous hormones, and root nutrient contents of Camellia sinensis cv. ‘Fuding Dabaicha’ seedlings under well-watered (WW) and drought stress (DS) conditions. After 8 weeks of DS treatment, root AMF colonization was decreased by 58.77%. AMF inoculation significantly increased plant height, leaf biomass, and root biomass, irrespective of soil moisture status. Mycorrhizal fungal colonization also significantly increased root volume, number of lateral roots, length of lateral roots in different classes, and root hair variables (e.g., density, length, and diameter) under both WW and DS conditions. AMF-colonized roots had higher concentrations of abscisic acid, brassinosteroids, gibberelins, and indole-3-acetic acid, which were significantly correlated with changes in root morphological parameters. AMF-inoculated plants represented higher root P, K, Ca, Mg, Fe, Mn, and Zn concentrations as compared with non-AMF-inoculated plants, regardless of the soil moisture status. These results concluded that arbuscular mycorrhizal plants under DS had superior adaptability of root morphology to promote nutrient acquisition, which was associated with higher hormone levels in roots induced by AMF.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
AbdElgawad H, Ahmed M, Mohammed AE, Alotaibi MO, Yehia RS, Selim S, Saleh AM, Beemster GTS, Sheteiwy MS (2022) Increasing atmospheric CO2 differentially supports arsenite stress mitigating impact of arbuscular mycorrhizal fungi in wheat and soybean plants. Chemosphere 296:134044. https://doi.org/10.1016/j.chemosphere.2022.134044
Alotaibi MO, Saleh AM, Sobrinho RL, Sheteiwy MS, El-Sawah AM, Mohammed AE, Elgawad HA (2021) Arbuscular mycorrhizae mitigate aluminum toxicity and regulate proline metabolism in plants grown in acidic soil. J Fungi 7:531. https://doi.org/10.3390/jof7070531
Belimov AA, Dodd IC, Safronova VI, Dumova VA, Shaposhnikov AI, Ladatko AG, Davies WJ (2014) Abscisic acid metabolizing rhizobacteria decrease ABA concentrations in planta and alter plant growth. Plant Physiol Biochem 74:84–91. https://doi.org/10.1016/j.plaphy.2013.10.032
Bisht A, Garg N (2022) AMF species improve yielding potential of cd stressed pigeonpea plants by modulating sucrose-starch metabolism, nutrients acquisition and soil microbial enzymatic activities. Plant Growth Regul 96:409–430. https://doi.org/10.1007/s10725-021-00791-9
Cheng HQ, Giri B, Wu QS, Zou YN, Kuča K (2021) Arbuscular mycorrhizal fungi mitigate drought stress in citrus by modulating root microenvironment. Arch Agron Soil Sci 57:1–12. https://doi.org/10.1080/03650340.2021.1878497
Cheng YW, Zhu WJ, Chen YX, Ito S, Asami T, Wang XL (2014) Brassinosteroids control root epidermal cell fate via direct regulation of a MYB-bHLH-WD40 complex by GSK3-like kinases. eLife 3:69–76. https://doi.org/10.7554/eLife.02525
Dai FJ, Rong ZY, Wu QS, Abd-Allah EF, Liu CY, Liu SR (2022) Mycorrhiza improves plant growth and photosynthetic characteristics of tea plants in response to drought stress. BIOCELL 46(5):1339–1346. https://doi.org/10.32604/biocell.2022.018909
El-Sawah AM, El-Keblawy A, Ali DFI, Ibrahim HM, El-Sheikh MA, Sharma A, Hamoud YA, Shaghaleh H, Brestic M, Skalicky M, Xiong YC, Sheteiwy MS (2021) Arbuscular mycorrhizal fungi and plant growth-promoting rhizobacteria enhance soil key enzymes, plant growth, seed yield, and qualitative attributes of guar. Agriculture 11:194. https://doi.org/10.3390/agriculture11030194
Erice G, Louahlia S, Irigoyen JJ, Sanchez-Diaz M, Avice JC (2010) Biomass partitioning, morphology and water status of four alfalfa genotypes submitted to progressive drought and subsequent recovery. J Plant Physiol 167:114–120. https://doi.org/10.1016/j.jplph.2009.07.016
Gupta S, Bharalee R, Bhorali P, Das SK, Bhagawati P, Bandyopadhyay T, Gohain B, Agarwal N, Ahmed P, Borchetia S, Kalita MC, Handique AK, Das S (2013) Molecular analysis of drought tolerance in tea by cDNA-AFLP based transcript profiling. Mol Biotechnol 53:237–248. https://doi.org/10.1007/s12033-012-9517-8
Huang GM, Zou YN, Wu QS, Xu YJ, Kuča K (2020) Mycorrhizal roles in plant growth, gas exchange, root morphology, and nutrient uptake of walnuts. Plant Soil Environ 66:295–302, https://doi.org/10.17221/240/2020-PSE
Hui HS, Lin LH, Qi JC, Liao L, Wang CL, Cheng HT (2015) Effect of drought stress on the roots of barley seedling. J Triticeae Crops 35:1291–1297. https://doi.org/10.7606/j.issn
Ibrahim HM, El-Sawah AM (2022) The mode of integration between azotobacter and rhizobium affect plant growth, yield, and physiological responses of pea (Pisum sativum L.). J Soil Sci Plant Nutr 22:1238–1251, https://doi.org/10.1007/s42729-021-00727-2
Izumo M, Ridge RW, Katsumi M (1995) Hormonal control of root hair growth in clover. Abstracts of the 15th international conference on plant growth substances, Minneapolis, MN, pp 452
Li T, Lin G, Zhang X, Chen YL, Zhang SB, Chen BD (2014) Relative importance of an arbuscular mycorrhizal fungus (Rhizophagus intraradices) and root hairs in plant drought tolerance. Mycorrhiza 24:595–602, https://doi.org/10.1007/s00572-014-0578-3
Lin ZH, Chen LS, Chen RB, Zhang FZ, Jiang HX, Tang N, Smith BR (2011) Root release and metabolism of organic acids in tea plants in response to phosphorus supply. J Plant Physiol 168:644–652. https://doi.org/10.1016/j.jplph.2010.09.017
Liu CY, Huang YM, Zou YN, Wu QS (2014) Regulation of root length and lateral root number in trifoliate orange applied by peroxide hydrogen and arbuscular mycorrhizal fungi. Not Bot Horti Agrobo 42:94–98. https://doi.org/10.15835/nbha4219442
Liu CY, Wang YJ, Wu QS, Yang TY, Kuča K (2020a) Arbuscular mycorrhizal fungi improve the antioxidant capacity of tea (Camellia sinensis) seedlings under drought stress. Not Bot Horti Agrobo 48:1993–2005. https://doi.org/10.15835/nbha48412066
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. Sci Rep 8:1978, https://doi.org/10.1038/s41598-018-20456-4
Liu CY, Zhang F, Zhang DJ, Zou YN, Shu B, Wu QS (2020b) Transcriptome analysis reveals improved root hair growth in trifoliate orange seedlings by arbuscular mycorrhizal fungi. Plant Growth Regul 92:195–203. https://doi.org/10.1007/s10725-020-00630-3
Liu SC, Jin JQ, Ma JQ, Yao MZ, Ma CL, Li CF, Ding ZT, Chen L (2016) Transcriptomic analysis of tea plant responding to drought stress and recovery. PLoS ONE 11:e0147306. https://doi.org/10.1371/journal.pone.0147306
Lv SF, Yu DY, Sun QQ, Jiang J (2018) Activation of gibberellin 20-oxidase 2 undermines auxin dependent root and root hair growth in NaCl-stressed Arabidopsis seedlings. Plant Growth Regul 84:225–236. https://doi.org/10.1007/s10725-017-0333-9
Man D, Bao YX, Han LB, Zhang XZ (2011) Drought tolerance associated with proline and hormone metabolism in two tall fescue cultivars. HortScience 46:1027–1032. https://doi.org/10.1016/j.scienta.2011.06.002
Pang J, Bansal R, Zhao H, Bohuon E, Lambers H, Ryan MH, Ranathunge K, Siddique KHM (2018) The carboxylate-releasing phosphorus-mobilizing strategy can be proxied by foliar manganese concentration in a large set of chickpea germplasm under low phosphorus supply. New Phytol 219:518–529. https://doi.org/10.1111/nph.15200
Phillips JM, Hayman D (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–161. https://doi.org/10.1016/S0007-1536(70)80110-3
Plassard C, Becquer A, Garcia K (2019) Phosphorus transport in mycorrhiza: how far are we? Trends Plant Sci 24:794–801. https://doi.org/10.1016/j.tplants.2019.06.004
Quiroga G, Erice G, Aroca R, Zamarreño ÁM, García-Mina JM (2020) Radial water transport in arbuscular mycorrhizal maize plants under drought stress conditions is affected by indole-acetic acid (IAA) application. J Plant Physiol 246:153115. https://doi.org/10.1016/j.jplph.2020.153115
Rowe JH, Topping JF, Liu JL, Lindsey K (2016) Abscisic acid regulates root growth under osmotic stress conditions via an interacting hormonal network with cytokinin, ethylene and auxin. New Phytol 211:225–239. https://doi.org/10.1111/nph.13882
Shao YD, Hu XC, Wu QS, Yang TY, Srivastava AK, Zhang DJ, Gao XB, Kuča K (2021) Mycorrhizas promote P acquisition of tea plants through changes in root morphology and P transporter gene expression. S Afr J Bot 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, Gao XB, Kuča K (2018) Mycorrhiza-induced changes in root growth and nutrient absorption of tea plants. Plant Soil Environ 64:283–289. https://doi.org/10.17221/126/2018-PSE
Sheteiwy MS, Ali DFI, Xiong YC, Brestic M, Skalicky M, Hamoud YA, Ulhassan Z, Shaghaleh H, AbdElgawad H, Farooq M, Sharma A, El-Sawah AM (2021a) Physiological and biochemical responses of soybean plants inoculated with arbuscular mycorrhizal fungi and bradyrhizobium under drought stress. BMC Plant Biol 21:195. https://doi.org/10.1186/s12870-021-02949-z
Sheteiwy MS, Abd Elgawad H, Xiong YC, Macovei A, Brestic M, Skalicky M, Shaghaleh H, Hamoud YA, El-Sawah AM (2021b) Inoculation with Bacillus amyloliquefaciens and mycorrhiza confers tolerance to drought stress and improve seed yield and quality of soybean plant. Physiol Plant 172:2153–2169. https://doi.org/10.1111/ppl.13454
Szentpéteri V, Mayer Z, Posta K (2022) Mycorrhizal symbiosis-induced abiotic stress mitigation through phosphate transporters in Solanum lycopersicum L. Plant Growth Regul. https://doi.org/10.1007/s10725-022-00906-w
Tyagi J, Varma A, Pudake RN (2017) Evaluation of comparative effects of arbuscular mycorrhiza (Rhizophagus intraradices) and endophyte (Piriformospora indica) association with finger millet (Eleusine coracana) under drought stress. Eur J Soil Biol 81:1–10. https://doi.org/10.1016/j.ejsobi.2017.05.007
Upreti KK, Bhatt RM, Panneerselvam P, Varalakshmi LR (2016) Morpho-physiological responses of grape rootstock ‘Dogridge’ to arbuscular mycorrhizal fungi inoculation under salinity stress. Int J Fruit Sci 16:191–209. https://doi.org/10.1080/15538362.2015.1111185
Wang Y, Fan K, Wang J, Ding ZT, Wang H, Bi CH, Zhang YW, Sun HW (2017) Proteomic analysis of Camellia sinensis (L.) reveals a synergistic network in the response to drought stress and recovery. J Plant Physiol 219:91–99. https://doi.org/10.1016/j.jplph.2017.10.001
Wang Y, Zou YN, Shu B, Wu QS (2023) Deciphering molecular mechanisms regarding enhanced drought tolerance in plants by arbuscular mycorrhizal fungi. Sci Hortic 308:111591. https://doi.org/10.1016/j.scienta.2022.111591
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 Regul 68:27–35. https://doi.org/10.1007/s10725-012-9690-6
Wu QS, Liu CY, Zhang DJ, Zou YN, He XH (2016) Mycorrhiza alters the profile of root hairs in trifoliate orange. Mycorrhiza 26:237–247. https://doi.org/10.1007/s00572-015-0666-z
Xie MM, Wang Y, Li QS, Kuča K, Wu QS (2020) A friendly-environmental strategy: application of arbuscular mycorrhizal fungi to ornamental plants for plant growth and garden landscape. Not Bot Horti Agrobo 48:1100–1115. https://doi.org/10.15835/nbha48312055
Yao Q, Wang LR, Zhu HH, Chen JZ (2009) Effect of arbuscular mycorrhizal fungal inoculation on root system architecture of trifoliate orange (Poncirus trifoliata L. Raf.) Seedlings. Sci Hortic 121:45861. https://doi.org/10.1016/j.scienta.2009.03.013
Yasin M, Younis A, Javed T, Akram A, Ahsan M, Shabbir R, Ali MM, Tahir A, El-Ballat EM, Sheteiwy MS, Sammour RH, Hano C, Alhumaydhi FA, El-Esawi MA (2021) River tea tree oil: composition, antimicrobial and antioxidant activities, and potential applications in agriculture. Plants 10:2105. https://doi.org/10.3390/plants10102105
Ye H, Roorkiwal M, Valliyodan B, Zhou L, Chen P, Varshney RK, Nguyen HT (2018) Genetic diversity of root system architecture in response to drought stress in grain legumes. J Exp Bot 69:3267–3277. https://doi.org/10.1093/jxb/ery082
Zhang F, Zou YN, Wu QS, Kuča K (2020) Arbuscular mycorrhizas modulate root polyamine metabolism to enhance drought tolerance of trifoliate orange. Environ Exp Bot 171:103962. https://doi.org/10.1016/j. envexpbot.2019.103926
Zhang JH, Jia WS, Yang JC, Ismail AM (2006) Role of ABA in integrating plant responses to drought and salt stresses. Field Crops Res 97:111–119. https://doi.org/10.1016/j.fcr.2005.08.018
Zhang XQ, Zhou FY, Liang YF (2012) Review on the measures of drought prevention and drought resistance in the tea garden. Guizhou Tea 40:7–10
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. Sci Rep 7:41134. https://doi.org/10.1038/srep41134
Zou YN, Zhang DJ, Liu CY, Wu QS (2019) Relationships between mycorrhizae and root hairs. Pak J Bot 51:727–733. https://doi.org/10.30848/PJB2019-2(39)
Acknowledgements
This work was supported by the Open Fund of State Key Laboratory of Tea Plant Biology and Utilization (SKLTOF20200122) and the Hundred schools and hundred counties - Efficient service Rural Revitalization science and technology support action project of Hubei Provincial Department of Education, China (BXLBX0296). The authors would like to extend their sincere appreciation to the Researchers Supporting Project Number (RSP2023R134), King Saud University, Riyadh, Saudi Arabia.
Author information
Authors and Affiliations
Contributions
CYL, YH and QSW designed research and drafted the entire manuscript. CYL, XLW and FJD performed research and analyzed data. Material preparation and collection were performed by YH, XLW and FJD. Analysis were performed by CYL. The first draft of the manuscript was written by CYL, EFA and QSW, review and editing were performed by QSW, EFA and SRL, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Additional information
Communicated by Daolong Dou.
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Liu, CY., Hao, Y., Wu, XL. et al. Arbuscular mycorrhizal fungi improve drought tolerance of tea plants via modulating root architecture and hormones. Plant Growth Regul 102, 13–22 (2024). https://doi.org/10.1007/s10725-023-00972-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10725-023-00972-8