Evaluation of some root growth traits and activity of enzyme and nonenzyme antioxidants of different cultivars of durum wheat (Triticum turgidum var. durum) effected by phosphorous fertilizer and mycorrhizal fungi in rainfed condition
Subject Areas : GeneticHoushang Naseri Rad 1 , Rahim Naseri 2
1 - Department of Agriculture, Payame Noor University, PO Box 3697-19395 Tehran, Iran
2 - 2. Department of Plant Production Technology, Dehloran Faculty of Agriculture and Engineering, Ilam University, Ilam, Iran.
Keywords: Malondialdehyde, superoxide dismutase, Glutathione synthetase, Root length density, Root water content,
Abstract :
In order to evaluate the effect of mycorrhizal fungi and phosphorous fertilizer on some root growth traits and activity of enzyme and nonenzyme antioxidants of durum wheat in rainfed conditions, an experiment was carried out as factorial based on a randomized complete block design with three replications at Sarableh Agricultural Research station during growing season 2018-2019. Four cultivars of durum wheat (Dehdasht, Zahab, Savarz and Saji) as the first factor and five levels of fertilizer source (control, 25 and 50 kg.ha-1 P, mycorrhizal fungi (GM), mycorrhizal fungi + 25 kg.ha-1 P) as the second factor were considered. The average comparison results of simple effects indicated that Zahab and Saji cultivars among cultivars and combination treatment of mycorrhizal + 25 kg / ha P and then 50 kg / ha P had the greatest effect on improving the studied traits. The interaction effect of cultivars and fertilizer sources revealed that the combined use of phosphorous fertilizer and mycorrhizal fungi had better results compared to their use alone. So that, the highest fresh and dry weight, length density, and root water content and activity of ascorbate peroxidase, peroxidase, catalase, superoxide dismutase and glutathione synthetase was obtained in combined treatment of mycorrhizal and phosphorus fertilizer at Zahab and Saji cultivars. However, the lowest specific root length, and malondialdehyde and hydrogen peroxide activity were obtained in the same treatment and cultivars. In general, the results showed that inoculation with mycorrhizal fungi in rainfed conditions, especially in Zahab and Saji cultivars, in addition to reducing the application of phosphorus fertilizer can improve root growth characteristics and activity of enzyme and nonenzyme antioxidants. As a result, it reduces the peroxidation of membrane lipids (the decline in production of malondialdehyde and hydrogen peroxide) and increases drought stress tolerance.
Abaye, A.O., Brann, D.E., Alley, M.M. and Griffey, C.A. (1997). Winter durum wheat: Do we have all the answer. Crop Soil Environment Science. 424-802.
Adhya, T.K., Kumar, N., Reddy, G., Podile, A.R., Bee, H. and Samantaray, B. (2015). Microbial mobilization of soil phosphorus and sustainable P management in agricultural soils. Current Science. 108: 1280–1287.
Aebi, H. (1984). Catalase in vitro. Methods in Enzymology. 105: 121-126.
Agarwal, S. and Pandy, V. (2004). Antioxidant enzyme responses to NaCl stress in Cassia angustifolia. Biologia Plantarum. 48: 555-560.
Alguacil, M., Caravaca, F., Dı´az-Vivancos, P., Herna´ndez, J.A. and Roldan, A. (2006). Effect of arbuscular mycorrhizae and induced drought stress on antioxidant enzyme and nitrate reductase activities in niperus oxycedrus L. grown in a composted sewage sludge-amended semi-arid soil. Plant and Soil. 279: 209–218.
Aroca, R., Porcel, R. and Ruiz Lozano, J.M. (2007). How does arbuscular mycorrhizal symbiosis regulate root hydraulic properties and plasma membrane aquaporins in Phaseolus vulgaris under drought, cold or salinity stresses?. New Phytologist. 173: 808–816.
Attarzadeh, M., Balouchi, H., Rajaie, M. and Movahhedi Dehnavi, M. (2019). Growth and nutrient content of Echinacea purpurea as affected by the combination of phosphorus with arbuscular mycorrhizal fungus and Pseudomonas florescent bacterium under different irrigation regimes. Journal of Environmental Management. 231: 182–188.
Augé, R.M. (2004). Arbuscular mycorrhizae and soil/plant water relations. Canadian Journal of Soil Science. 84: 373–381.
Augé, R.M., Toler, H.D., Moore, J.L., Cho, K. and Saxton, A.M. (2007). Comparing contributions of soil versus root colonization to variations in stomatal behavior and soil drying in mycorrhizal Sorghum bicolor and Cucurbita pepo. Journal of Plant Physiology. 164:1289–1299.
Bagayoko, M., George, E., Romheld, V. and Buerkert, A. (2000). Journal of Agricultural Science, Cambridge, 135: 399–407.
Bárzana, G., Aroca, R., Bienert, G.P., Chaumont, F. and Ruiz-Lozano, J.M. (2014). New insights into the regulation of aquaporins by the arbuscular mycorrhizal symbiosis in maize plants under drought stress and possible implications for plant performance. Molecular Plant-Microbe Interactions Journal. 27: 349–363.
Baum, C., El-Tohamy, W. and Gruda, N. (2015). Increasing the productivity and product quality of vegetable crops using arbuscular mycorrhizal fungi: a review. Scientia Horticulturae. 187: 131–141.
Bayani, R., Saateyi, A. and Faghani, E. (2016). Some root traits of barley (Hordeum vulgare L.) as affected by mycorrhizal symbiosis under drought stress. Journal of Crop production and processing. 6(19):125-135.
Beutler, E. and Gelbart, T. (1986). Improved assay of the enzymes of glutathione synthesis: y- lutamylcysteine synthetase and glutathione synthetase. Clinica Chimica Acra. 158: 115-123.
Bompadre, M.J., Silvani, V.A., Bidondo, L.F., Ríosde Molina, M.D.C., Colombo, R.P., Pardo, A.G. and Godeas, A.M. (2014). Arbuscular mycorrhizal fungi alleviate oxidative stress in pomegranate plants growing under different irrigation conditions. Botany. 92: 187–193.
Cheynier, V., Comte, G., Davies, K.M., Lattanzio, V. and Martens, S. (2013). Plant phenolics: recent advances on their biosynthesis, genetics, and ecophysiology. Plant Physiology and Biochemistry. 72: 1–20.
Chu, X.T., Fu, J.J., Sun, Y.F., Xu, Y.M., Miao, Y.J., Xu, Y.F. and Hu, T.M. (2016). Effect of arbuscular mycorrhizal ungus inoculation on cold stress-induced oxidative damage in leaves of Elymus nutans Griseb. South African Journal of Botany. 104: 21–29.
Erdogan, U., Cakmakci, R., Varmazyari, A., Turan, M., Erdogan, Y. and Kitir, N. (2016). Role of inoculation with multi-trait rhizobacteria on strawberries under water deficit stress. Zemdirbyste-Agriculture. 103(1): 67–76.
Evelin, H., Kapoor, R. and Giri, B. (2009). Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Annals of Botany. 104:1263–1280.
Fadaee, E., Parvizi, Y., Gerdakane, M. and Khan-ahmadi, M. (2018). The effects of mycorhiza (Glomus mosseae and Glomus intraradiceae) and phosphorus on growth and phytochemical traits of dracocephalum moldavica l. under drought stress. Journal of Medicinal Plants. 17(66): 117-130.
Gholinezhad, E., Darvishzadeh, R., Siavash Moghaddam, S. and Popovi ć-Djordjević, J. (2020). Effect of mycorrhizal inoculation in reducing water stress in sesame (Sesamum indicum L.): The assessment of agrobiochemical traits and enzymatic antioxidant activity. Agricultural Water Management. 238: 106234.
Hasanabadi, T., Ardakani, M.R., Rejali, F., Paknejad, F., Eftekhari, S.A. and Zargari K. (2010). Response of barley root characters to co-inoculation with Azospirillum lipoferum and Pseudomonas flouresence under different levels of nitrogen. American-Eurasian Journal of Agriculture and Environmental Science. 9(2): 156-162.
Hegazi, A.M., El-Shraiy, A.M. and Ghoname, A.A. (2017). Mitigation of salt stress negative effects on sweet pepper using arbuscular mycorrhizal fungus (AMF), Bacillus megaterium and Brassinosteroids (BRs). Gesunde Pflanzen. 69: 91–102.
Heydari, A., Nasri, M. and Ghoshchi, F. (2014). The study of Symbiotic of mycorrhizae and phosphorus fertilizer on yield and yield components of corn in Robat karim region. Agronomic Research in Semi Desert Regions. 11: 161-170.
Jaleel, C.A., Riadh, K., Gopi, R., Manivannan, P., Inès, J., AI-Juburi, H.J., Zhao, C.X., Shao, H.B. and Panneerselvam, R. (2009). Antioxidant defense responses: physiological plasticity in higher plants under abiotic constraints. Acta Physiologiae Plantarum. 31:427–436.
Khalafallah, A.A. and Abo-Ghalia, H.H. (2008). Effect of arbuscular mycorrhizal fungi on the metabolic products and activity of antioxidant system in wheat plants subjected to short-term water stress, followed by recovery at different growth stages. Journal of Applied Sciences Research. 4: 559-569.
Khalvati, M.A., Mzafar, A. and Schmidhalter, U. (2005). Quantification of water uptake by arbuscular mycorrhizal hypha and its signification for leaf growth, water relations and gas exchange of barley subjected to drought stress. Plant Biology Stuttgart. 7(6): 706-712.
Koide, R. and Kabir, Z. (2000). Extraradical hyphae of the mycorrhizal fungus Glomus intraradices can hydrolyse organic phosphate. New Phytologist. 148: 511 –517.
Li, X.L., George, E. and Marschner, H. (1991). Extension of the phosphorus depletion zone in VA-mycorrhizal white clover in a calcareous soil. Plant and Soil. 136: 41–48.
Loreto, F. and Velikova, V. (2001). Isoprene produced by leaves protects the photosynthetic apparatus against ozone damage, quenches ozone products, and reduces lipid peroxidation of cellular membranes. Plant Physiology. 127(4): 1781-1787.
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(2): 248-258.
Mac-Adam, J.W., Nelson, C.J. and Sharp, R.E. (1992). Peroxidase activity in the leaf elongation zone of tall fescue I. Spatial distribution of ionically bound peroxidase activity in genotypes differing in length of the elongation zone. Plant Physiology. 9 (3): 872-878.
Mahanta, D., Rai, R.K., Mishra, S.D., Raja, A., Purakayastha, T.J. and Varghese, E. (2014). Influence of phosphorus and biofertilizers on soybean and wheat root growth and properties. Field Crops Research. 166: 1-9.
Mashhadi Akbar Bojar, M. (2011). Heavy metals and oxidative stress in plants. The first oxidative stress workshop. Karaj Islamic Azad University. Faculty of Agriculture and Natural Resources.
Minami, M. and Yoshikawa, H. (1979). A simplified assay method of superoxide dismutase activity for clinical use. Clinica Chimica Acta. 92: 337–342.
Ministry of Agriculture- Jahad. Agricultural statistic. 2016-17.
Mittler, R. (2002). Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science. 7: 405–410
Nakano, Y. and Asada, K. (1981). Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiology. 22: 867-880.
Oleson, B.T. (1996). World wheat production utilization and trade. In:Bushuk , W. and Rasper. V.F (eds ). Wheat production, properties and quality. Chapman and Hall, 1 -11.
Omirou, M., Ioannides, I.M. and Ehaliotis, C. (2013). Mycorrhizal inoculation affects arbuscular mycorrhizal diversity in watermelon roots, but leads to improved colonization and plant response under water stress only. Applied Soil Ecology. 63: 112–119.
Poulton, P.R., Johnston, A.E. and White, R.P. (2013). Plant – available soil phosphorus. Part I: the response of winter wheat and spring barley to Olsen P on a silty clay loam. Soil Use and Management. 29: 4–11.
Ruiz-Lozano, J.M. (2003). Arbuscular mycorrhizal symbiosis and alleviation of osmotic stress: new perspectives for molecular studies. Mycorrhiza. 13: 309–317.
Sheteiwy, S. Fathi Ismail Ali, M., Xiong, D., Brestic, Y.C., Skalicky, M., Alhaj Hamoud, M., Ulhassan, Y., Shaghaleh, Z., AbdElgawad, H., Farooq, H., Sharma, M., and El-Sawah, M.A. (2021). Physiological and biochemical responses of soybean plants inoculated with Arbuscular mycorrhizal fungi and Bradyrhizobium under drought stress. BMC Plant Biology. 21: 195.
Salah, M.S., Guan, Y., Cao, D., Li, J., Nawaz, A., Hu, Q., Weimin, H., Mimgyu, N. and Jin, H. (2015). Seed priming with polyethylene glycol regulating the physiological and molecular mechanism in rice (Oryza sativa L.) under nano-ZnO stress. Scientific Reports. 5:14278.
Shao, Y.D., Hu, X.C., Wu, Q.S., Yang, T.Y., Srivastava, A.K., Zhang, D.J., Gao, X.B. and Kuca, K. (2021). Mycorrhizas promote P acquisition of tea plants through changes in root morphology and P transporter gene expression. South African Journal of Botany. 137: 455 462.
Sims, J.T. and Sharpley, A.N. (2005). Phosphorus: agriculture and the environment. American Society of Agronomy, Wisconsin USA.
Smith, S.E., Facelli, E., Pope, S. and Smith, A. (2010). Plant performance in stressful environments: interpreting new and established knowledge of the roles of arbuscular mycorrhizas. Plant and Soil. 326(1 -2): 3-20
Stewart, R.R. and Bewley, J.D. (1980). Lipid peroxidation associated with accelerated aging of soybean axes. Plant Physiology. 65(2): 245-248.
Tisdale, S., Nelson, W., Beaton, J. and Havlin, J. (1993). Soil Fertility and Fertilizers, fifth ed. Macmillan Publication Company, New York.
Todd, R.L., Giddens, J.E., Kral, D.M. and Hawkins, S.L. (1984). Microbial–Plant Interactions. In ASA Special Publication Number 47. Proceedings of the Symposium held at Fort Collins, Colorado, USA, 5–10 August 1979. Madison, WI, USA: SSSA-ASA-SSA.
Wu, Q.S., Xia, R.X. and Zou, Y.N. (2006). Reactive oxygen metabolism in mycorrhizal and non-mycorrhizal citrus (Poncirus trifoliata) seedlings subjected to water stress. Journal of Plant Physiology. 163:1101–1110.
Wu, Q.S., Li, Y., Zou, Y.N. and He, X.H. (2015). Arbuscular mycorrhiza mediates glomalin-related soil protein production and soil enzyme activities in the rhizosphere of trifoliate orange grown under different P levels. Mycorrhiza. 25: 121–130.
Xie, X., Weng, B., Cai, B., Dong, Y. and Yan, C. (2014). Effects of arbuscular mycorrhizal inoculation and phosphorus supply on the growth and nutrient uptake of Kandelia obovata (Sheue, Liu & Yong) seedlings in autoclaved soil. Applied Soil Ecology. 75: 162– 171.
Yaghoubian, Y., Mohammadi Goltapeh, E., Pirdashti, H., Esfandiari, E., Feiziasl, V., Kari Dolatabadi, H., Varma, A. and Haryani Hassim, M. (2014). Effect of Glomus mosseae and Piriformospora indica on growth and antioxidant defense responses of wheat plants under drought stress. Agricultural Research. 3(3):239–245.
Yar Mahmoodi, Z., Ariana, L. and Alizadeh, O. (2012). Investigation of morphological properties of maize under stable agricultural conditions. Crop Production in Environmental Stress. 4(2): 15-20.
Yazdani, M., Bahmanyar, M., Pirdashti, H. and Esmaili, M.A. (2009). Effect of phosphate solubilization microorganisms (PSM) and plant growth promoting rhizobacteria (PGPR) on yield and yield components of corn (Zea mays L.). World Academy of Science, Engineering and Technology. 37: 90-92.
Zahir, Z.A., Arshad, M. and Khalid, A. (2006). Phytohormones: microbial production and applications. In: Andrew, S., Ball, E.F. (Eds.), Norman Uphoff, Hans Herren, Olivier Husson, Mark Laing, Cheryl Palm, Jules Pretty, Pedro Sanchez, Nteranya Sanginga, Janice Thies (Ed.), Biological Approaches to Sustainable Soil System, first ed. CRC Press, Boca Raton, pp. 207 –220.
Zhu, X., Song, F. and Xu, H. (2010). Influence of arbuscular mycorrhiza on lipid peroxidation and antioxidant enzyme activity of maize plants under temperature stress. Mycorrhiza. 20:325–332.
Zhu, X., Song, F. and Liu, S. (2011). Arbuscular mycorrhiza impacts on drought stress of maize plants by lipid peroxidation, proline content and activity of antioxidant system. Journal of Food, Agriculture and Environment. 9: 583-587.
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Abaye, A.O., Brann, D.E., Alley, M.M. and Griffey, C.A. (1997). Winter durum wheat: Do we have all the answer. Crop Soil Environment Science. 424-802.
Adhya, T.K., Kumar, N., Reddy, G., Podile, A.R., Bee, H. and Samantaray, B. (2015). Microbial mobilization of soil phosphorus and sustainable P management in agricultural soils. Current Science. 108: 1280–1287.
Aebi, H. (1984). Catalase in vitro. Methods in Enzymology. 105: 121-126.
Agarwal, S. and Pandy, V. (2004). Antioxidant enzyme responses to NaCl stress in Cassia angustifolia. Biologia Plantarum. 48: 555-560.
Alguacil, M., Caravaca, F., Dı´az-Vivancos, P., Herna´ndez, J.A. and Roldan, A. (2006). Effect of arbuscular mycorrhizae and induced drought stress on antioxidant enzyme and nitrate reductase activities in niperus oxycedrus L. grown in a composted sewage sludge-amended semi-arid soil. Plant and Soil. 279: 209–218.
Aroca, R., Porcel, R. and Ruiz Lozano, J.M. (2007). How does arbuscular mycorrhizal symbiosis regulate root hydraulic properties and plasma membrane aquaporins in Phaseolus vulgaris under drought, cold or salinity stresses?. New Phytologist. 173: 808–816.
Attarzadeh, M., Balouchi, H., Rajaie, M. and Movahhedi Dehnavi, M. (2019). Growth and nutrient content of Echinacea purpurea as affected by the combination of phosphorus with arbuscular mycorrhizal fungus and Pseudomonas florescent bacterium under different irrigation regimes. Journal of Environmental Management. 231: 182–188.
Augé, R.M. (2004). Arbuscular mycorrhizae and soil/plant water relations. Canadian Journal of Soil Science. 84: 373–381.
Augé, R.M., Toler, H.D., Moore, J.L., Cho, K. and Saxton, A.M. (2007). Comparing contributions of soil versus root colonization to variations in stomatal behavior and soil drying in mycorrhizal Sorghum bicolor and Cucurbita pepo. Journal of Plant Physiology. 164:1289–1299.
Bagayoko, M., George, E., Romheld, V. and Buerkert, A. (2000). Journal of Agricultural Science, Cambridge, 135: 399–407.
Bárzana, G., Aroca, R., Bienert, G.P., Chaumont, F. and Ruiz-Lozano, J.M. (2014). New insights into the regulation of aquaporins by the arbuscular mycorrhizal symbiosis in maize plants under drought stress and possible implications for plant performance. Molecular Plant-Microbe Interactions Journal. 27: 349–363.
Baum, C., El-Tohamy, W. and Gruda, N. (2015). Increasing the productivity and product quality of vegetable crops using arbuscular mycorrhizal fungi: a review. Scientia Horticulturae. 187: 131–141.
Bayani, R., Saateyi, A. and Faghani, E. (2016). Some root traits of barley (Hordeum vulgare L.) as affected by mycorrhizal symbiosis under drought stress. Journal of Crop production and processing. 6(19):125-135.
Beutler, E. and Gelbart, T. (1986). Improved assay of the enzymes of glutathione synthesis: y- lutamylcysteine synthetase and glutathione synthetase. Clinica Chimica Acra. 158: 115-123.
Bompadre, M.J., Silvani, V.A., Bidondo, L.F., Ríosde Molina, M.D.C., Colombo, R.P., Pardo, A.G. and Godeas, A.M. (2014). Arbuscular mycorrhizal fungi alleviate oxidative stress in pomegranate plants growing under different irrigation conditions. Botany. 92: 187–193.
Cheynier, V., Comte, G., Davies, K.M., Lattanzio, V. and Martens, S. (2013). Plant phenolics: recent advances on their biosynthesis, genetics, and ecophysiology. Plant Physiology and Biochemistry. 72: 1–20.
Chu, X.T., Fu, J.J., Sun, Y.F., Xu, Y.M., Miao, Y.J., Xu, Y.F. and Hu, T.M. (2016). Effect of arbuscular mycorrhizal ungus inoculation on cold stress-induced oxidative damage in leaves of Elymus nutans Griseb. South African Journal of Botany. 104: 21–29.
Erdogan, U., Cakmakci, R., Varmazyari, A., Turan, M., Erdogan, Y. and Kitir, N. (2016). Role of inoculation with multi-trait rhizobacteria on strawberries under water deficit stress. Zemdirbyste-Agriculture. 103(1): 67–76.
Evelin, H., Kapoor, R. and Giri, B. (2009). Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Annals of Botany. 104:1263–1280.
Fadaee, E., Parvizi, Y., Gerdakane, M. and Khan-ahmadi, M. (2018). The effects of mycorhiza (Glomus mosseae and Glomus intraradiceae) and phosphorus on growth and phytochemical traits of dracocephalum moldavica l. under drought stress. Journal of Medicinal Plants. 17(66): 117-130.
Gholinezhad, E., Darvishzadeh, R., Siavash Moghaddam, S. and Popovi ć-Djordjević, J. (2020). Effect of mycorrhizal inoculation in reducing water stress in sesame (Sesamum indicum L.): The assessment of agrobiochemical traits and enzymatic antioxidant activity. Agricultural Water Management. 238: 106234.
Hasanabadi, T., Ardakani, M.R., Rejali, F., Paknejad, F., Eftekhari, S.A. and Zargari K. (2010). Response of barley root characters to co-inoculation with Azospirillum lipoferum and Pseudomonas flouresence under different levels of nitrogen. American-Eurasian Journal of Agriculture and Environmental Science. 9(2): 156-162.
Hegazi, A.M., El-Shraiy, A.M. and Ghoname, A.A. (2017). Mitigation of salt stress negative effects on sweet pepper using arbuscular mycorrhizal fungus (AMF), Bacillus megaterium and Brassinosteroids (BRs). Gesunde Pflanzen. 69: 91–102.
Heydari, A., Nasri, M. and Ghoshchi, F. (2014). The study of Symbiotic of mycorrhizae and phosphorus fertilizer on yield and yield components of corn in Robat karim region. Agronomic Research in Semi Desert Regions. 11: 161-170.
Jaleel, C.A., Riadh, K., Gopi, R., Manivannan, P., Inès, J., AI-Juburi, H.J., Zhao, C.X., Shao, H.B. and Panneerselvam, R. (2009). Antioxidant defense responses: physiological plasticity in higher plants under abiotic constraints. Acta Physiologiae Plantarum. 31:427–436.
Khalafallah, A.A. and Abo-Ghalia, H.H. (2008). Effect of arbuscular mycorrhizal fungi on the metabolic products and activity of antioxidant system in wheat plants subjected to short-term water stress, followed by recovery at different growth stages. Journal of Applied Sciences Research. 4: 559-569.
Khalvati, M.A., Mzafar, A. and Schmidhalter, U. (2005). Quantification of water uptake by arbuscular mycorrhizal hypha and its signification for leaf growth, water relations and gas exchange of barley subjected to drought stress. Plant Biology Stuttgart. 7(6): 706-712.
Koide, R. and Kabir, Z. (2000). Extraradical hyphae of the mycorrhizal fungus Glomus intraradices can hydrolyse organic phosphate. New Phytologist. 148: 511 –517.
Li, X.L., George, E. and Marschner, H. (1991). Extension of the phosphorus depletion zone in VA-mycorrhizal white clover in a calcareous soil. Plant and Soil. 136: 41–48.
Loreto, F. and Velikova, V. (2001). Isoprene produced by leaves protects the photosynthetic apparatus against ozone damage, quenches ozone products, and reduces lipid peroxidation of cellular membranes. Plant Physiology. 127(4): 1781-1787.
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(2): 248-258.
Mac-Adam, J.W., Nelson, C.J. and Sharp, R.E. (1992). Peroxidase activity in the leaf elongation zone of tall fescue I. Spatial distribution of ionically bound peroxidase activity in genotypes differing in length of the elongation zone. Plant Physiology. 9 (3): 872-878.
Mahanta, D., Rai, R.K., Mishra, S.D., Raja, A., Purakayastha, T.J. and Varghese, E. (2014). Influence of phosphorus and biofertilizers on soybean and wheat root growth and properties. Field Crops Research. 166: 1-9.
Mashhadi Akbar Bojar, M. (2011). Heavy metals and oxidative stress in plants. The first oxidative stress workshop. Karaj Islamic Azad University. Faculty of Agriculture and Natural Resources.
Minami, M. and Yoshikawa, H. (1979). A simplified assay method of superoxide dismutase activity for clinical use. Clinica Chimica Acta. 92: 337–342.
Ministry of Agriculture- Jahad. Agricultural statistic. 2016-17.
Mittler, R. (2002). Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science. 7: 405–410
Nakano, Y. and Asada, K. (1981). Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiology. 22: 867-880.
Oleson, B.T. (1996). World wheat production utilization and trade. In:Bushuk , W. and Rasper. V.F (eds ). Wheat production, properties and quality. Chapman and Hall, 1 -11.
Omirou, M., Ioannides, I.M. and Ehaliotis, C. (2013). Mycorrhizal inoculation affects arbuscular mycorrhizal diversity in watermelon roots, but leads to improved colonization and plant response under water stress only. Applied Soil Ecology. 63: 112–119.
Poulton, P.R., Johnston, A.E. and White, R.P. (2013). Plant – available soil phosphorus. Part I: the response of winter wheat and spring barley to Olsen P on a silty clay loam. Soil Use and Management. 29: 4–11.
Ruiz-Lozano, J.M. (2003). Arbuscular mycorrhizal symbiosis and alleviation of osmotic stress: new perspectives for molecular studies. Mycorrhiza. 13: 309–317.
Sheteiwy, S. Fathi Ismail Ali, M., Xiong, D., Brestic, Y.C., Skalicky, M., Alhaj Hamoud, M., Ulhassan, Y., Shaghaleh, Z., AbdElgawad, H., Farooq, H., Sharma, M., and El-Sawah, M.A. (2021). Physiological and biochemical responses of soybean plants inoculated with Arbuscular mycorrhizal fungi and Bradyrhizobium under drought stress. BMC Plant Biology. 21: 195.
Salah, M.S., Guan, Y., Cao, D., Li, J., Nawaz, A., Hu, Q., Weimin, H., Mimgyu, N. and Jin, H. (2015). Seed priming with polyethylene glycol regulating the physiological and molecular mechanism in rice (Oryza sativa L.) under nano-ZnO stress. Scientific Reports. 5:14278.
Shao, Y.D., Hu, X.C., Wu, Q.S., Yang, T.Y., Srivastava, A.K., Zhang, D.J., Gao, X.B. and Kuca, K. (2021). Mycorrhizas promote P acquisition of tea plants through changes in root morphology and P transporter gene expression. South African Journal of Botany. 137: 455 462.
Sims, J.T. and Sharpley, A.N. (2005). Phosphorus: agriculture and the environment. American Society of Agronomy, Wisconsin USA.
Smith, S.E., Facelli, E., Pope, S. and Smith, A. (2010). Plant performance in stressful environments: interpreting new and established knowledge of the roles of arbuscular mycorrhizas. Plant and Soil. 326(1 -2): 3-20
Stewart, R.R. and Bewley, J.D. (1980). Lipid peroxidation associated with accelerated aging of soybean axes. Plant Physiology. 65(2): 245-248.
Tisdale, S., Nelson, W., Beaton, J. and Havlin, J. (1993). Soil Fertility and Fertilizers, fifth ed. Macmillan Publication Company, New York.
Todd, R.L., Giddens, J.E., Kral, D.M. and Hawkins, S.L. (1984). Microbial–Plant Interactions. In ASA Special Publication Number 47. Proceedings of the Symposium held at Fort Collins, Colorado, USA, 5–10 August 1979. Madison, WI, USA: SSSA-ASA-SSA.
Wu, Q.S., Xia, R.X. and Zou, Y.N. (2006). Reactive oxygen metabolism in mycorrhizal and non-mycorrhizal citrus (Poncirus trifoliata) seedlings subjected to water stress. Journal of Plant Physiology. 163:1101–1110.
Wu, Q.S., Li, Y., Zou, Y.N. and He, X.H. (2015). Arbuscular mycorrhiza mediates glomalin-related soil protein production and soil enzyme activities in the rhizosphere of trifoliate orange grown under different P levels. Mycorrhiza. 25: 121–130.
Xie, X., Weng, B., Cai, B., Dong, Y. and Yan, C. (2014). Effects of arbuscular mycorrhizal inoculation and phosphorus supply on the growth and nutrient uptake of Kandelia obovata (Sheue, Liu & Yong) seedlings in autoclaved soil. Applied Soil Ecology. 75: 162– 171.
Yaghoubian, Y., Mohammadi Goltapeh, E., Pirdashti, H., Esfandiari, E., Feiziasl, V., Kari Dolatabadi, H., Varma, A. and Haryani Hassim, M. (2014). Effect of Glomus mosseae and Piriformospora indica on growth and antioxidant defense responses of wheat plants under drought stress. Agricultural Research. 3(3):239–245.
Yar Mahmoodi, Z., Ariana, L. and Alizadeh, O. (2012). Investigation of morphological properties of maize under stable agricultural conditions. Crop Production in Environmental Stress. 4(2): 15-20.
Yazdani, M., Bahmanyar, M., Pirdashti, H. and Esmaili, M.A. (2009). Effect of phosphate solubilization microorganisms (PSM) and plant growth promoting rhizobacteria (PGPR) on yield and yield components of corn (Zea mays L.). World Academy of Science, Engineering and Technology. 37: 90-92.
Zahir, Z.A., Arshad, M. and Khalid, A. (2006). Phytohormones: microbial production and applications. In: Andrew, S., Ball, E.F. (Eds.), Norman Uphoff, Hans Herren, Olivier Husson, Mark Laing, Cheryl Palm, Jules Pretty, Pedro Sanchez, Nteranya Sanginga, Janice Thies (Ed.), Biological Approaches to Sustainable Soil System, first ed. CRC Press, Boca Raton, pp. 207 –220.
Zhu, X., Song, F. and Xu, H. (2010). Influence of arbuscular mycorrhiza on lipid peroxidation and antioxidant enzyme activity of maize plants under temperature stress. Mycorrhiza. 20:325–332.
Zhu, X., Song, F. and Liu, S. (2011). Arbuscular mycorrhiza impacts on drought stress of maize plants by lipid peroxidation, proline content and activity of antioxidant system. Journal of Food, Agriculture and Environment. 9: 583-587.