Amelioration of water deficiency stress in roselle (Hibiscus sabdariffa) by arbuscular mycorrhizal fungi and plant growth-promoting rhizobacteria


  • Sara SANAYEI University of Mohaghegh Ardabili, Faculty of Agriculture, Department of Agronomy and Plant Breeding, Ardabil (IR)
  • Morteza BARMAKI University of Mohaghegh Ardabili, Faculty of Agriculture, Department of Agronomy and Plant Breeding, Ardabil (IR)
  • Ali EBADI University of Mohaghegh Ardabili, Faculty of Agriculture, Department of Agronomy and Plant Breeding, Ardabil (IR)
  • Mousa TORABI-GIGLOU University of Mohaghegh Ardabili, Faculty of Agriculture, Department of Horticultural Sciences, Ardabil (IR)



antioxidant enzyme activities, limited irrigation, osmotic adjustment, photosynthetic pigments, proline content, root colonization, Roselle, sepals’ dry weight


Belowground interactions between plant roots, arbuscular mycorrhizal fungi (AMFs), and plant growth-promoting rhizobacteria (PGPR) can improve growth and yield under abiotic stress conditions. A pot factorial experiment based on completely randomized design with three replications was conducted to investigate the effects of AMFs (without inoculation as control, inoculation with Funneliformis mosseae and Funneliformis intraradices) and PGPRs (without inoculation as control Pseudomonas fluorescens p-169 inoculation) on roselle (Hibiscus sabdariffa L.) grown under water deficiency stress (WDS) [90% (I1), 75% (I2), 50% (I3), and 25% (I4) of field capacity as well-watered, mild, moderate, and severe stress, respectively]. The results showed that by applying WDS, the plant growth properties such as root and sepals’ dry weight, 1000-seed weight, seed yield, chlorophyll a, b, and total, carotenoids, and leaf water content was significantly reduced. The application of AMFs and PGPR under WDS conditions increased 1000-seed weight, seed yield. In response to WDS osmotic adjustment were provided in Roselle and under stress conditions. The highest seed yield was found under well-watered treatment by inoculation of F. mosseae without PGPR and the application of Pseudomonas fluorescens (6.37 and 6.51 g/plant, respectively). These results suggesting the antagonistic effects of AMFs and PGPR. AMFs inoculation under severe stress increased sepals dry weight compared to the non-inoculation. In conclusion, increased activity of enzymatic antioxidants and higher production of non-enzymatic antioxidant compounds, as well as photosynthetic pigments in symbiotic association with AMFs, can alleviate reactive oxygen species damage resulting in increased growth and yield parameters and improve water stress tolerance.


Metrics Loading ...


Agami R, Medani R, Abd El-Mola I, Taha R (2016). Exogenous application with plant growth-promoting rhizobacteria (PGPR) or proline induces stress tolerance in basil plants (Ocimum basilicum L.) exposed to water stress. International Journal of Environmental and Agriculture Research 2:78-82.

Aghighi Shahverdi M, Omidi H, Tabatabaei SJ (2019). Stevia (Stevia rebaudiana Bertoni) responses to NaCl stress: Growth, photosynthetic pigments, diterpene glycosides and ion content in root and shoot. Journal of the Saudi Society of Agricultural Sciences 18:355-360.

Ahanger MA, Tomar NS, Tittal M, Argal S, Agarwal RM (2017). Plant growth under water/salt stress: ROS production; antioxidants and significance of added potassium under such conditions. Physiology and Molecular Biology of Plants 23:731-744.

Ahmad N, Sharma S, Alam MK, Singh V, Shamsi S, Mehta B, Fatma A (2010). Rapid synthesis of silver nanoparticles using the dried medicinal plant of basil. Colloids, and Surfaces B: Biointerfaces 81:81-86.

Ahmadi SAK, Ebadi A, Daneshian J, Jahanbakhsh S, Siadat SA, Tavakoli H (2015). Effects of irrigation deficit and application of some growth regulators on defense mechanisms of canola. Notulae Botanicae Horti Agrobotanici Cluj-Napoca 43:124-130.

Al-Arjani AF, Hashem A, Abd Allah EF (2020). Arbuscular mycorrhizal fungi modulate dynamics tolerance expression to mitigate drought stress in Ephedra foliata Boiss. Saudi Journal of Biological Sciences 27:380-394.

Amiri R, Nikbakht A, Etemadi N, Sabzalian MR (2016). Nutritional status, essential oil changes, and water-use efficiency of rose geranium in response to arbuscular mycorrhizal fungi and water deficiency stress. Symbiosis 73:15-25.

Arnon A (1967). Method of extraction of chlorophyll in the plants. Agronomy Journal 23:112-121.

Awasthi R, Tewari R, Nayyar H (2011). Synergy between plants and P-solubilizing microbes in soils: effects on growth and physiology of crops. International Research Journal of Microbiology 2:484-503.

Carrasco-Ríos L, Pinto M (2014). Effect of salt stress on antioxidant enzymes and lipid peroxidation in leaves in two contrasting corn, Jubilee. Chilean Journal of Agricultural Research 74:89-95.

Chakraborty U, Pradhan B (2012). Oxidative stress in five wheat varieties (Triticum aestivum L.) exposed to water stress and study of their antioxidant enzyme defense system, water stress responsive metabolites and H2O2 accumulation. Brazilian Journal of Plant Physiology 24:117-130.

Da-Costa-Rocha I, Bonnlaender B, Sievers H, Pischel I, Heinrich M (2014). Hibiscus sabdariffa L. - a phytochemical and pharmacological review. Food Chemistry 165:424-443.

Demir S (2005). Influence of arbuscular mycorrhiza on some physiological growth parameters of pepper. Turkish Journal of Biology 28:85-90.

Dutta S, Patel V, Viswanathan C, Singh S, Singh A (2015). Physiological and biochemical adaptation of arbuscular mycorhizal fungi (AMF) inoculated Citrus jambhiri (Jatti khatti) seedlings under water deficit stress conditions. Progressive Horticulture 47:229-236.

Erdogan U, Cakmakci R, Varmazyarı A, Turan M, Erdogan Y, Kıtır N (2016). Role of inoculation with multi-trait rhizobacteria on strawberries under water deficit stress. Zemdirbyste-Agriculture 103:67-76.

Esmaielpour B, Jalilvand P, Hadian J (2013). Effects of drought stress and arbuscular mycorrhizal fungi on some morphophysiological traits and yield of savoury (Satureja hortensis L.). Agroecology 5(2):169-177.

Fallahi HR, Ghorbany M, Aghhavani-Shajari M, Samadzadeh A, Asadian AH (2017). Qualitative response of roselle to planting methods, humic acid application, mycorrhizal inoculation and irrigation management. Journal of Crop Improvement 1:17-24.

Ghorbanpour M, Hatami M, Khavazi K (2013). Role of plant growth promoting rhizobacteria on antioxidant enzyme activities and tropane alkaloid production of Hyoscyamus niger under water deficit stress. Turkish Journal of Biology 37:350-360.

Giovannetti M, Mosse B (1980). An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytologist 489-500.

Gleason SM (2015). Evolutionary outcomes should inform strategies to increase drought tolerance. Nature Plants 1:15114.

Gouda S, Kerry RG, Das G, Paramithiotis S, Shin HS, Patra JK (2018). Revitalization of plant growth-promoting rhizobacteria for sustainable development in agriculture, Microbiological Research 206:131-140.

Gratão PL, Polle A, Lea PJ, Azevedo RA (2005). Making the life of heavy metal-stressed plants a little easier. Functional Plant Biology 32:481-494.

Hossain M, Fujita M (2012). Regulatory role of components of ascorbate-glutathione (AsA-GSH) pathway in plant tolerance to oxidative stress, oxidative stress in plants: causes, consequences and tolerance. IK International Publishing House Pvt. Ltd., India pp 81-147.

Irigoyen J, Einerich D, Sánchez‐Díaz M (1992). Water stress-induced changes in concentrations of proline and total soluble sugars in nodulated alfalfa (Medicago sativd) plants. Physiologia Plantarum 84:55-60.

Kapoor R, Sharma D, Bhatnagar A (2008). Arbuscular mycorrhizae in micropropagation systems and their potential applications. Scientia Horticulturae 116:227-239.

Kar M, Mishra D (1976). Catalase, peroxidase, and polyphenoloxidase activities during rice leaf senescence. Plant Physiology 57:315-319.

Kumar V, Kumar P, Khan A (2020). Optimization of PGPR and silicon fertilization using response surface methodology for enhanced growth, yield and biochemical parameters of French bean (Phaseolus vulgaris L.) under saline stress. Biocatalysis and Agricultural Biotechnology 23:22-27.

Kusvuran S (2012). Effects of drought and salt stresses on growth, stomatal conductance, leaf water and osmotic potentials of melon genotypes (Cucumis melo L.). African Journal of Agricultural Research 7:775-781.

Marasco R, Rolli E, Ettoumi B, Vigani G, Mapelli F, Borin S, … Cherif A (2012). A drought resistance-promoting microbiome is selected by root system under desert farming. PLoS One 7:e48479.

Misra A, Srivastava N (2000). Influence of water stress on Japanese mint. Journal of Herbs, Spices & Medicinal Plants 7:51-58.

Narula N, Kumar V, Behl RK, Deubel A, Gransee A, Merbach W (2000). Effect of P‐solubilizing Azotobacter chroococcum on N, P, K uptake in P‐responsive wheat genotypes grown under greenhouse conditions. Journal of Plant Nutrition and Soil Science 163:393-398.<393::AID-JPLN393>3.0.CO;2-W

Ortiz N, Armada E, Duque E, Roldán A, Azcón R (2015). Contribution of arbuscular mycorrhizal fungi and/or bacteria to enhancing plant drought tolerance under natural soil conditions: effectiveness of autochthonous or allochthonous strains. Journal of Plant Physiology 174:87-96.

Pan J, Wang Q, Snell WJ (2005). Cilium-generated signaling and cilia-related disorders. Laboratory Investigation 85:452-463.

Phillips JM, Hayman D (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.

Pirzad A, Shakiba MR, Zehtab-Salmasi S, Mohammadi SA, Darvishzadeh R, Samadi A (2011). Effect of water stress on leaf relative water content, chlorophyll, proline and soluble carbohydrates in Matricaria chamomilla L. Journal of Medicinal Plants Research 5:2483-2488.

Qiao Y, Ren J, Yin L, Liu Y, Deng X, Liu P, Wang S (2020). Exogenous melatonin alleviates PEG-induced short-term water deficiency in maize by increasing hydraulic conductance. BMC Plant Biology 20:218.

Rahimzadeh S, Pirzad A (2017). Arbuscular mycorrhizal fungi and Pseudomonas in reduce drought stress damage in flax (Linum usitatissimum L.): a field study. Mycorrhiza 27:537-552.

Riaz G, Chopra R (2018). A review on phytochemistry and therapeutic uses of Hibiscus sabdariffa L. Biomed Pharmacother 102:575-586.

Rouphael Y, Franken P, Schneider C, Schwarz D, Giovannetti M, Agnolucci M, … Colla G (2015). Arbuscular mycorrhizal fungi act as biostimulants in horticultural crops. Scientia Horticulturae 196:91-108.

Ruíz-Sánchez M, Armada E, Muñoz Y, de Salamone IEG, Aroca R, Ruíz-Lozano JM, Azcón R (2011). Azospirillum and arbuscular mycorrhizal colonization enhance rice growth and physiological traits under well-watered and drought conditions. Journal of Plant Physiology 168:1031-1037.

Sbrana C, Avio L, Giovannetti M (2014). Beneficial mycorrhizal symbionts affecting the production of health-promoting phytochemicals. Electrophoresis 35:1535-1546.

Selvaraj T, Chellappan P (2006). Arbuscular mycorrhizae: a diverse personality. Journal of Central European Agriculture 7:349-358.

Sharma A, Shahzad B, Kumar V, Kohli SK, Sidhu GPS, Bali AS, … Zheng B (2019). Phytohormones regulate accumulation of osmolytes under abiotic stress. Biomolecules 9(7):285.

Shoresh M, Harman GE, Mastouri F (2010). Induced systemic resistance and plant responses to fungal biocontrol agents, Annual Review of Phytopathology 48:21-43.

Soengas P, Rodriguez VM, Velasco P, Cartea ME (2018). Effect of temperature stress on antioxidant defenses in Brassica oleracea. ACS Omega 3:5237-5243.

Verma P, Saxena R, Tomar RS (2016). Rhizobacteria: A promising tool for drought tolerance in crop plants. International Journal of Pahrma and Bio Science (Int-BIONANO-2016) 116-125.

Vurukonda SS, Vardharajula S, Shrivastava M, Sk ZA (2016). Enhancement of drought stress tolerance in crops by plant growth-promoting rhizobacteria. Microbiological Research 184:13-24.

Wang CJ, Yang W, Wang C, Gu C, Niu DD, Liu HX, … Guo JH (2012). Induction of drought tolerance in cucumber plants by a consortium of three plant growth-promoting rhizobacterium strains. PLoS One 7:e52565.

Weisany W, Sohrabi Y, Heidari G, Siosemardeh A, Ghassemi-Golezani K (2012). Changes in antioxidant enzymes activity and plant performance by salinity stress and zinc application in soybean (Glycine max L.). Plant Omics 5:60-68.

Young LS, Hameed A, Peng SY, Shan YH, Wu SP (2013). Endophytic establishment of the soil isolate Burkholderia sp. CC-Al74 enhances growth and P-utilization rate in maize (Zea mays L.). Applied Soil Ecology 66:40-47.




How to Cite

SANAYEI, S., BARMAKI, M., EBADI, A., & TORABI-GIGLOU, M. (2021). Amelioration of water deficiency stress in roselle (Hibiscus sabdariffa) by arbuscular mycorrhizal fungi and plant growth-promoting rhizobacteria. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 49(2), 11987.



Research Articles
DOI: 10.15835/nbha49211987