Physiological responses of mycorrhizal symbiosis to drought stress in white clover


  • Sheng-Min LIANG Yangtze University, College of Horticulture and Gardening, Jingzhou, Hubei 434025 (CN)
  • Dao-Ju JIANG Jingzhou Natural Resources and Planning Bureau, Shashi Substation, Jingzhou, Hubei 434000 (CN)
  • Miao-Miao XIE Yangtze University, College of Horticulture and Gardening, Jingzhou, Hubei 434025 (CN)
  • Ying-Ning ZOU Yangtze University, College of Horticulture and Gardening, Jingzhou, Hubei 434025 (CN)
  • Qiang-Sheng WU Yangtze University, College of Horticulture and Gardening, Jingzhou, Hubei 434025; University of Hradec Kralove, Faculty of Science, Department of Chemistry, Hradec Kralove 50003 (CN)
  • Kamil KUČA University of Hradec Kralove, Faculty of Science, Department of Chemistry, Hradec Kralove 50003 (CZ)



ABA; antioxidant; drought stress; root architecture; white clover


The aim of the present study was to analyze the effects of two arbuscular mycorrhizal fungi (AMF), Funneliformis mosseae and Paraglomus occultum, on leaf water status, root morphology, root sugar accumulation, root abscisic acid (ABA) levels, root malondialdehyde (MDA) content, and root antioxidant enzyme activities in white clover (Trifolium repens L.) exposed to well-watered (WW) and drought stress (DS) conditions. The results showed that root colonization by F. mosseae and P. occultum was significantly decreased by 7-week soil drought treatment. Under drought stress conditions, mycorrhizal fungal treatment considerably stimulated root total length, surface area and volume, as compared with non-mycorrhizal controls. In addition, inoculation with arbuscular mycorrhizal fungi also increased leaf relative water content and accelerated the accumulation of root glucose and fructose under drought stress. Mycorrhizal plants under drought stress registered higher activities of superoxide dismutase (SOD), catalase (CAT), and peroxidase (POD) and ABA levels in roots, while lower MDA contents, relative to non-mycorrhizal plants. As a result, mycorrhiza-inoculated plants represented better physiological activities (e.g. antioxidant defense systems, root morphology, and sugar accumulation) than non-inoculated plants in response to soil drought, whilst P. occultum had superior effects than F. mosseae.


Asner GP, Elmore AJ, Olander LP, Martin RE, Harris AT (2004). Grazing system, ecosystem responses, and global change. Annual Review of Environment and Resources 29:261-299.

Bajji M, Lutts S, Kinet JM (2001). Water deficit effects on solute contribution to osmotic adjustment as a function of leaf ageing in three durum wheat (Triticum durum Desf.) cultivars performing differently in arid conditions. Plant Science 160:669-681.

Baslam M, Goicoechea N (2012). Water deficit improved the capacity of arbuscular mycorrhizal fungi (AMF) for inducing the accumulation of antioxidant compounds in lettuce leaves. Mycorrhiza 22: 347-359.

Chatzistathis T, Orfanoudakis M, Alifragis D, Therios I (2013). Colonization of Greek olive cultivars' root system by arbuscular mycorrhiza fungus: root morphology, growth, and mineral nutrition of olive plants. Scientia Agricola 70:185-194.

Chen Q, Qi WB, Reiter RJ, Wei W, Wang BM (2009). Exogenously applied melatonin stimulates root growth and raises endogenous indoleacetic acid in roots of etiolated seedlings of Brassica juncea. Journal of Plant Physiology 166:324-328.

Francis D (1992). The cell cycle in plant development. New Phytologist 122(1):1-20.

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.

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.

Kozlowski TT, Pallardy SG (2002). Acclimation and adaptive responses of woody plants to environmental stresses. Botanical Review 68:270-334.[0270:AAAROW]2.0.CO;2

Kunert KJ, Vorster BJ, Fenta B A, Kibido T, Dionisio G, Foyer CH (2016). Drought stress responses in soybean roots and nodules. Frontiers in Plant Science 7:1-7.

Marulanda A, Porcel R, Barea JM, Azcón R (2007). Drought tolerance and antioxidant activities in lavender plants colonized by native drought-tolerant or drought-sensitive Glomus species. Microbial Ecology 54:543-552.

Meng LL, He JD, Zou YN, Wu QS, Kuča K (2020). Mycorrhiza-released glomalin-related soil protein fractions contribute to soil total nitrogen in trifoliate orange. Plant, Soil and Environment 66:183-189.

Mirshad PP, Puthur JT (2016). Arbuscular mycorrhizal association enhances drought tolerance potential of promising bioenergy grass (Saccharum arundinaceum retz.). Environmental Monitoring and Assessment 188:5-20.

Mo YL, Wang YQ, Yang RP, Zheng JX, Liu CM, Li H, … Zhang X (2016). Regulation of plant growth, photosynthesis, antioxidation and osmosis by an arbuscular mycorrhizal fungus in watermelon seedlings under well-watered and drought conditions. Frontiers in Plant Science 7:644.

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 British Mycological Society 55:158-161.

Qiao G, Wen XP, Yu LF, Ji XB (2011). The enhancement of drought tolerance for pigeon pea inoculated by arbuscular mycorrhizae fungi. Plant, Soil and Environment 57:541-546.

Ruiz-Lozano JM, Collados C, Barea JM, Azcón R (2001). Cloning of cDNAs encoding SODs from lettuce plants which show differential regulation by arbuscular mycorrhizal symbiosis and by drought stress. Journal of Experimental Botany 55:2241-2242.

Ruiz-Sánchez M, Aroca R, Muñoz Y, Polón R, Ruiz-Lozano JM (2010). The arbuscular mycorrhizal symbiosis enhances the photosynthetic efficiency and the antioxidative response of rice plants subjected to drought stress. Journal of Plant Physiology 167:862-869.

Ruth B, Khalvati M, Schmidhalter U (2011). Quantification of mycorrhizal water uptake via high-resolution on-line water content sensors. Plant and Soil 342:459-468.

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, He JD, Srivastava AK, Zou YN, Kuča K (2019). Mycorrhizas enhance drought tolerance of citrus by altering root fatty acid compositions and their saturation levels. Tree Physiology 39:1149-1158.

Wu QS, Srivastava AK, Zou YN (2013). AMF-induced tolerance to drought stress in citrus: A review. Scientia Horticulturae 164:77-87.

Xie MM, Zou YN, Wu QS, Zhang ZZ, Kuča K (2020). Single or dual inoculation of arbuscular mycorrhizal fungi and rhizobia regulates plant growth and nitrogen acquisition in white clover. Plant, Soil and Environment 66:287-294.

Yadav A, Suri VK, Kumar A, Choudhary AK, Meena AL (2015). Enhancing plant water relations, quality, and productivity of pea (Pisum sativum L.) through arbuscular mycorrhizal fungi, inorganic phosphorus, and irrigation regimes in an Himalayan acid alfisol. Communications in Soil Science and Plant Analysis 46:80-93.

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.

Yooyongwech S, Phaukinsang N, Chaum S, Supaibuwatana K (2013). Arbuscular mycorrhiza improved growth performance in Macadamia tetraphylla L. grown under water deficit stress involves soluble sugar and proline accumulation. Plant Growth Regulation 69(3):285-293.

Zhang F, Wang P, Zou YN, Wu QS, Kuča 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.

Zhang F, Zou YN, Wu QS (2018). Quantitative estimation of water uptake by mycorrhizal extraradical hyphae in citrus under drought stress. Scientia Horticulturae 229:132-136.

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.

Zhang Z, Zhang J, Huang Y (2014). Effects of arbuscular mycorrhizal fungi on the drought tolerance of Cyclobalanopsis glauca seedlings under greenhouse conditions. New Forests 45:545-556.

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.

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.




How to Cite

LIANG, S.-M., JIANG, D.-J., XIE, M.-M., ZOU, Y.-N., WU, Q.-S., & KUČA, K. (2021). Physiological responses of mycorrhizal symbiosis to drought stress in white clover. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 49(1), 12209.



Research Articles
DOI: 10.15835/nbha49112209

Most read articles by the same author(s)

1 2 3 > >>