Document Type : Original Article


1 Department of Forestry, Faculty of Natural Resources, Sari University of Agricultural Sciences and Natural Resources, Sari, Iran

2 Soil and Water Research Institute, Agricultural Education and Extension Research Organization, Karaj, Iran

3 Agricultural Researches and Natural Resources Center, Lorestan, Khoramabad, Iran


Unfavorable environmental conditions result in stress in plants and so disrupt their growth and survival. Today, soil microorganisms, especially fungi and growth-promoting bacteria, involved in various biological processes in plant growth and soil nutrient cycling, are suggested to reduce the effects of environmental stress.
Materials and methods:
In order to investigate the effect of drought stress and biological inputs on vegetative characteristics of Celtis caucasica (diameter and height growth, root length, fresh and dry weight of root and shoot, and seedling colonization), a factorial experiment (Mycorrhizal factors in two levels of inoculation with arbuscular mycorrhizal fungi and without inoculation (control), bacteria in four levels of Pseudomonas, Azpyrilum, Azotobacter and control treatments, and drought stress at three levels of field capacity (80, 60 and 40%) was performed in a complete randomized block design and four replications in the greenhouse of the Natural Resources Office in Lorestan Province.
Results and discussion:
The results showed that the highest diameter growth of Celtis caucasica L. seedlings was observed at moderate drought stress in Pseudomonas-fungi and Azotobacter-fungi treatments with an average of 0.554 and 0.525 mm, respectively. The highest height growth was observed at moderate drought stress in Pseudomonas-fungi and Azotobacter-fungi treatments with an average of 21.55 and 20.55 cm, respectively. The highest leaf area was observed at low drought stress in Pseudomonas-fungi and then with Azotobacter-fungi with an average of 116 and 116/75 cm2, respectively. The least of these traits was observed in high drought stress in the control group and azosperyllium treatment. The highest and lowest root length was observed at moderate drought stress in Pseudomonas and Azotobacter treatments, and at low drought stress in the control group and Pseudomonas-fungi treatments, respectively. The highest root fresh weight was observed at moderate drought stress in Azotobacter and Pseudomonas with an average of 16.7916 and 16.7941 g, respectively. The lowest values were obtained at low and moderate drought stress for the control group. The highest and lowest root dry weight was observed at high drought stress in Azotobacter and Pseudomonas treatments, and at low drought stress in control and Azospirillum-fungi treatments, respectively. The highest fresh and dry weight of shoot were obtained at moderate drought stress in Pseudomonas-fungi and Azotobacter-fungi treatments, and the lowest was observed at low drought stress in control and azosperyllium treatments. The highest percentage of colonization was observed in low drought stress in Pseudomonas-fungi and Azotobacter-fungi treatments with an average of 44. 175 and 42.675%, respectively; and the lowest was observed at high drought stress in the control group with 26.42% and azosperyllium treatments, with 26.695%.
Microbial and fungal factors and their interactions increase root colonization, plant growth characteristics, and water uptake and thus increase plant tolerance to adverse environmental conditions such as drought stress.


Abduelafez, I., Moragues, M., Elamari, A.A., Buchleiter, G. and Stromberger, M., 2011. Growth promotion of winter wheat under drought stress by ACC deaminase positive bacteria. Annual Meeting of the Soil Science Society of America, October 16-19. San Antonio, TX. USA.
Ahemad, M. and Kibret, M., 2014. Mechanisms and applications of plant growth promoting rhizobacteria: Current perspective. Journal of King Saud University –Science. 26, 1-20.
Ali Ahmad Korruri, S., Khoshnevis, M., Matinzade, M. and Moraghebi F., 2000. Ecological and environmental studies of Juniperus polycarpus stand in Iran. 1th National Conference of Northern Forests Management and Sustainable Development, 6 September, Ramsar, Iran. 327-357. (In Persian with English abstract).
Aliasgharzad, N., Neyshabouri, M.R. and Salimi, G., 2006. Effects of arbuscular mycorrhizal fungi and Bradyrhizobium japonicum on drought stress of soybean. Biologia. 61, 324-328.
Andersen, M.N., Asch, F., Wu, Y., Jensen, C.R., Næsted, H., Mogensen, V.O. and Koch, K.E., 2015. Soluble invertase expression is an early target of drought stress during the critical, abortion-sensitive phase of young ovary development in maize. Plant Physiology. 130, 591–604.
Anna, L.B., Alessandra, S., Claudia, E., Paola, C. and Maddalena, D.G., 2013. In vitro and in vivo inoculation of four endophytic bacteria on Lycopersicon esculentum. New Biotechnology. 30, 666–674.
Aroca, R., Ruiz-Lozano, J.M., Zamarreno, A.M., Paz, J.A., Garcia-Mina, J.M. and Pozo, M.J., 2013. Arbuscular mycorrhizal symbiosis influences strigolactone production under salinity and alleviates salt stress in lettuce plants. Journal of Plant Physiology. 170, 47-55.
Ashrafuzzaman, M., Hossen, F.A., Razi, I.M., Anamul, H.M., Zahurul, I.M., Shahidullah, S.M. and Sariah, M., 2009. Efficiency of plant growth- promoting rhizobacteria (PGPR) for the enhancement of rice growth. African Journal of Biotechnology. 8, 1247-1252.
Askary, M., Mostajeran, A. and Amooaghaei, R., 2009. Influence of the co-inoculation Azospirillum brasilense and Rhizobum meliloti plus 24-D on grain yield and N P K content of Triticum aestivum (Cv Baccros and mahdavi). American-Eurasian Journal of Agriculture and Environment Science. 5, 296-307.
Awari, V.R. and Mate, S.N., 2015. Effect of drought stress on early seedling growth of chickpea (Cicer arietinum L.) genotypes. International Journal of Life Sciences Research. 2, 356–361.
Bano, A. and Fatima, M., 2009. Salt tolerance in Zea mays (L.) following inoculation with Rhizobium and Pseudomonas. Biology and Fertility of Soils. 45, 405–413.
Bashan, Y. and de-Bashan, L.E., 2010. Chapter two—How the plant growth-promoting bacterium Azospirillum promotes plant growth–a critical assessment. Advances in Agronomy. 108, 77–136.
Bashan, Y., de-Bashan, L.E., Prabhu, S.R. and Hernandez, J.P., 2014. Advances in plant growth-promoting bacterial inoculant technology: formulations and practical perspectives (1998–2013). Plant Soil. 378, 1–33.
Bechtold, U., 2018. Plant life in extreme environments: How do you improve drought tolerance? Frontiers in Plant Science. 9, 543.
Bethlenfalvay, G.J., Brown, M.S., Ames, R.N. and Thomas, R.E., 1988. Effects of drought on host and endophyte development in mycorrhizal soybeans in relation to water use and phosphate uptake. Physiologia Plantarum. 11, 565-S71.
Bhattacharyya, P.N. and Jha, D.K., 2012. Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World Journal of Microbiology and Biotechnology. 28, 1327–1350.
Bianco, C. and Defez, R., 2011. Soil bacteria support and protect plants against abiotic stresses. In: Shanker, A. (Ed.), Abiotic Stress in Plants—Mechanisms and Adaptations. In TechOpen, Rijeka, Italy. pp. 143-170.
Borzoei, A., Kafe, M., Khazaei, H.R. and Mosavi Shelmani, M.A., 2012. Effects of saline irrigation water on root traits of two saline sensitive and resistance wheat cultivars and its relationship with grain yield in greenhouse condition. Journal of Science and Technology of Greenhouse Culture. 8, 95-106.
Cakmaci, R., Akmakc, I.A., Figen, B., Adil, A., Fikrettin, S. and Ahin, B.C., 2005. Growth promotion of plants by plant growth promoting rhizobacteria under greenhouse and two different field soil conditions. Biochemistry. 38, 1482-1487.
Cheng, Z., Park, E. and Glick, B.R., 2007. 1- Aminocyclopropane-1-carboxylate deaminase from Pseudomonas putida UW4 facilitates the growth of canola in the presence of salt. Canadian Journal of Microbiology. 53, 912-918.
Cooper, K.M., 1984. Physiology of VA mycorrhizal associations. In: VA Mycorrhiza, Powell, C. L., and D. J. Bagyaraj (eds). CRC Press, Boca Raton, Fl, pp. 155-186.
Copetta, A., Lingua, G., Berta, G., 2006. Effects of three AM fungi on growth, distribution of glandular hairs, and essential oil production in Ocimum basilicum L. var. Genovese. Mycorrhiza. 16, 485-494.
Emadi, A., Jones, R.J. and Brodsky, R.A., 2009. Cyclophosphamide and cancer: golden anniversary. Nature Reviews Clinical Oncology. 6, 638-647.
Fahad, S., Hussain, S., Bano, A., Saud, S., Hassan, S., Shan, D., Ahmed Khan, F., Khan, F., Chen, Y., Wu, C., Tabassum, M.A., Chun, M.X., Afzal, M., Jan, A., Tariq Jan, M. and Huang, J., 2015. Potential role of phytohormones and plant growth-promoting rhizobacteria in abiotic stresses: consequences for changing environment. Environmental Science and Pollution Research. 22, 4907–4921.
Fitter, A.H., 1985. Functioning of vesicular-arbuscular mycorrhizas under field conditions. New Phytology. 99, 257-265.
Frolov, A., Bilova, T., Paudel, G., Berger, R., Balcke, G.U., Birkemeyer, C. and Wessjohann, L.A., 2017. Early responses of mature Arabidopsis thaliana plants to reduced water potential in the agar-based polyethylene glycol infusion drought model. Journal of Plant Physiology. 208, 70–83.
Gagne-Bourgue, F., Aliferis, K.A., Seguin, P., Rani, M., Samson, R. and Jabaji, S., 2013. Isolation and characterization of indigenous endophytic bacteria associated with leaves of switchgrass (Panicum virgatum L.) cultivars. Journal of Applied Microbiology. 2, 40-47.
Ghahraman, A., 1987. Plant systematic. Tehran University Press. 350 pp. (In Persian)
Ghorchiani, M., Akbari, G., Alikhani, H.A., Allahdadi, I. and Zarei, M., 2011. Effect of arbuscular mycorrhiza fungi and Pseudomonas florescence bacterium on the ear traits, chlorophyll content and yield of Zea mays L. under moisture stress conditions, Water and Soil Science. 21, 97-114 (In Persian with English abstract).
Giasson, P., Karam, A. and Jaouich, A., 2008. Arbuscular mycorrhizae and alleviation of soil stresses on plant growth. In: Siddiqui Z.A, Akhtar M. S. and Futai, K. (eds) Mycorrhizae: Sustainable Agriculture and Forestry. Springer, Dordrecht, The Netherlands, Pp. 99-134.
Giovannetti, M. and Mosse, B., 1980. An evaluation of techniques for measuring vesicular-arbescular mycorrhizal infection in roots. Journal of New Phytologist. 84, 489-500.
Greenvay, H. and Munns, R., 1980. Mechanism of salt tolerance of non-halophytes. Plant Physiology. 31, 149-190.
Hamayun, M., Khan, S.A., Khan, A.L., Shin, J.H. and Lee, I.J., 2010. Exogenous gibberellic acid reprograms soybean to higher growth, and salt stress tolerance. Journal of Agricultural and Food Chemistry. 58, 7226–7232.
Hamidi, A., Ghalavand, A., Dehghan Shoar, M., Malakooti, M. and Chogan, R., 2006. Effects of plant growth promoting rhizobacteria on yield of forage corn. Journal of Research and production. 70, 16-22.
Hardoim, P.R., Van Overbeek, S.V. and Van Elsas, J.D., 2008. Properties of bacterial endophytes and their proposed role in plant growth. Trends in Microbiology. 16, 463–471.
Hayat, R., Ali, S., Amara, U., Khalid, R. and Ahmed, I., 2010. Soil beneficial bacteria and their role in plant growth promotion: a review. Annals of Microbiology. 60, 579–598.
He, F., Sheng, M. and Tang, M., 2017. Effects of rhizophagus irregularis on photosynthesis and antioxidative enzymatic system in Robinia pseudoacacia L. under drought stress. Frontiers in Plant Science. 8,183.
Jay, P.V., Janardan, Y., Kavindra, N.T. and Ashok, K., 2013. Effect of indigenous Mesorhizobium spp. and plant growth promoting rhizobacteria on yields and nutrients uptake of chickpea (Cicer arietinum L.) under sustainable agriculture. Ecological Engineering. 51: 282–286.
Johnson, C.R. and Hummel, R.L., 1985. Influence of Mycorrhizal and drought stress on growth of poncirus X citrus seedlings. Horticultural Science. 20, 754-755.
Karthikeyan, B., Jaleel, C.A., Gopi, R. and Delveekasundarm, M., 2007. Alterations in seedling vigour and antioxidant enzyme activitvities in Catharanthus roseus under seed priming with native diazotrophs. Journal of Zhejiang University Science. 8, 453-457.
Kumar, D., 1984. The value of certain plant parameters as an index for salt tolerance in Indian mustard (Brassica juncea L.). Plant and Soil. 79, 261-272.
Laxa, M., Liebthal, M., Telman, W., Chibani, K. and Dietz, K.J., 2019. The Role of the plant antioxidant system in drought tolerance. Antioxidants. 8, 94, doi:10.3390/antiox8040094.
Li, P., Zhang, Y., Wu, X. and Liu, Y., 2018. Drought stress impact on leaf proteome variations of faba bean (Vicia faba L.) in the Qinghai–Tibet Plateau of China. 3 Biotech. 8, 110.
Ma, Y., Prasad, M.N.V., Rajkumar, M. and Freitas, H., 2011. Plant growth promoting rhizobacteria and endophytes accelerate phytoremediation of metalliferous soils. Biotechnology Advances. 29, 248-258.
Mahfouz, S.A. and Sharaf-Eldin, M.A., 2007. Effect of mineral vs biofertilizer on growth yield and essential oil content of fennel (Foeniculum vulgare). International Agrophysics. 21, 361-366.
Marinkovic, J., Dordevic, V., Balesevic-Tubic, S., Bjelic, D., Vucelic-Radovic, B. and Josic, D., 2013. Osmotic stress tolerance, PGP traits and RAPD analysis of Bradyrhizobium japonicum strains. Genetika. 45, 75–86.
Mishra, M., Kumar, U., Mishra, P.K. and Prakash, V., 2010. Efficiency of plant growth promoting rhizobacteria for the enhancement of Cicerarietinum L. growth and germination under salinity. Advances in Biological Research. 4, 92-96.
Munns, R., 2002. Comparative physiology of salt and water stress. Plant, Cell and Environment. 25, 239-250.
Nadeem, M., Li, J., Yahya, M., Sher, A., Ma, C., Wang, X. and Qiu, L., 2019. Research progress and perspective on drought stress in legumes: a review. International Journal of Molecular Sciences. 20, 25-41, doi:10.3390/ijms20102541.
Nadeem, S.M., Ahmad, M., Zahir, Z.A., Javaid, A. and Ashraf, M., 2014. The role of mycorrhizae and plant growth promoting rhizobacteria (PGPR) in improving crop productivity under stressful environments. Biotechnology Advances. 32, 429–448.
Nezarat, C. and Gholami, A., 2009. Effect of plant growth promoting rhizobacteria on agronomic traits of maize under water stress, 11th Iranian Soil Science Congress, Gorgan University of Agricultural Sciences and Natural Resources, 11th -13th June, Gorgan, Iran. (In Persian).
Ojaghloo, F., Farah wash, F., Hasanzadeh, A. and Pouryousef, M., 2007. Effect of inoculation with bio fertilizers (Azotobacter and phosphate solvent bacteria) on yield and yield components of safflower. Journal of Agricultural Sciences. Islamic Azad university, Branch of Tabriz. 1, 64-75.
Osmolovskaya, N., Shumilina, J., Kim, A., Didio, A., Grishina, T., Bilova, T., Keltsieva, O.A., Zhukov, V., Tikhonovich, I. and Tarakhovskaya, E., 2018. Methodology of drought stress research: experimental setup and physiological characterization. International Journal of Molecular Sciences. 19, 4089.
Parmar, N. and Dufresne, J., 2011. Beneficial interactions of plant growth promoting rhizosphere microorganisms. Soil Biology. 28, 27-42.
Patil, N.B., Gajbhiye, M., Ahiwale, S.S., Gunjal, A.B. and Kapadnis, B.P., 2011. Optimization of Indole 3acetic acid (IAA) production by Acetobacter diazotrophicus L1 isolated from Sugarcane. International Journal of Environmental Sciences. 2, 295-302.
Rojas-Tapias, D., Moreno-Galván, A., Pardo-Díaz, S., Obando, M., Diego Rivera, D. and Ruth Bonilla, R., 2012. Effect of inoculation with plant growth-promoting bacteria (PGPB) on amelioration of saline stress in maize (Zea mays). Applied Soil Ecology (Microorganisms and the Sustainable Management of Soil). 61, 264–272.
Saadat, A., Savaghebi, G.H.R., Rejali, F., Khavazei, K. and Shirmardi, M., 2009. The evaluation of some plant growth promoting Pseudomonas fluorescence strains and arbuscular mycorrhizal fungi on root colonization of wheat (Cistan and Chamran cultivars).11th Iranian Soil Science Congress, Gorgan University of Agricultural Sciences and Natural Resources, 11th -13th June, Gorgan, Iran. (In Persian).
Sabeti, H., 2007. Forests, trees and shrubs of Iran. Yazd University Press, Yazd, Iran.
Safapour, M., Ardakani, M.R., Khaghani, S., Teymoori, M. and Hezaveh, H., 2012. The influence of mycorrhizal fungi and rhizobium bacteria on nutrient uptake and phytohormonal fluctuations of three red been (Phaseolus vulgaris L.) Genotypes. Archives Des Sciences Journal. 5, 465-473.
Saikia, S.P., Dutta, S.P., Goswami, A., Bahau, B.S. and Kanjilal, P.B., 2010. Role of Azospirillum in the improvement of legumes. Microbes for Legume Improvement. 389-408. doi:10.1007/978-3-211-99753-6-16.
Sehgal, A., Sita, K., Siddique, K.H.M., Kumar, R. and Oliver, M.J., 2018. Drought or/and heat-stress effects on seed filling in food crops: Impacts on functional biochemistry, seed yields, and nutritional quality. Frontiers in Plant Science. 9, 1705.
Shirinbayana, S., Khosravi, H. and Malakouti, M.J., 2019. Alleviation of drought stress in maize (Zea mays) by inoculation with Azotobacter strains isolated from semi-arid regions. Applied Soil Ecology. 133, 138–145
Singh, A.K., Hamel, C., DePauw, R.M. and Knox, R.E., 2012. Genetic variability in arbuscular mycorrhizal fungi compatibility supports the selection of durum wheat genotypes for enhancing soil ecological services and cropping systems in Canada. Canadian Journal Microbiology. 58, 293-302.
Sturz, A.V. and Christie, B.R., 2003. The management of soil quality and plant disease with rhizobacteria. Soil and Tillage Research. 72, 107- 123.
Talaat, N.B., Ghoniem, A.E., Abdelhamid, M.T. and Shawky, B.T., 2015. Effective microorganisms improve growth performance, alter nutrients acquisition and induce compatible solutes accumulation in common bean (Phaseolus vulgaris L.) plants subjected to salinity stress. Plant Growth Regulation. 75, 281–295.
Tavili, A., Zare, S., Moosavi, S.A. and Enayati, A., 2011. Effects of seed priming on germination characteristics of Bromus species under salt and drought conditions. American-Eurasian Journal of Agricultural and Environmental Sciences. 10, 163–168.
Vyas, P. and Gulati, A., 2009. Stress tolerance and genetic variability of phosphate solubilizing Pseudomonas fluorescens from the cold deserts of the trans-Himalayas. Microbial Ecology. 58: 425-434.
Whittemore, A.T., 2005. genetic structure, lack of introgression and taxonomic status in the celtis laevigata-c. reticulata complex (Cannabaceae). Journal of Systematic Botany. 30, 809–817.
Wu, Q.S. and Xia, R.X., 2006. Arbuscular mycorrhizal fungi influence growth, osmotic adjustment and photosynthesis of Citrus under well-watered and water stress conditions. Journal of Plant Physiology. 163, 417-425.
Yordanov, V. and Tsoev, T., 2000. Plant responses to drought, acclimation and stress tolerance. Photosynthica. 38, 171-186.
Zaidi, A. and Mohammad, S., 2006. Co-inoculation effects of phosphate solubilizing micro- organisms and Glomus fasciculatum on green gram-bradyrhizobium symbiosis. Agricultural Science. 30, 223 -230.
Zawoznik, M.S., Ameneiros, M., Benavides, M.P., Vázquez, S. and Groppa, M.D., 2011. Response to saline stress and aquaporin expression in Azospirillum-inoculated barley seedlings. Applied Microbiology and Biotechnology. 90, 1389–1397.