Morphological, physiological, and enzymatic responses of Caucasian alder (Alnus subcordata C. A. Mey) seedlings to water deficit conditions by inoculation of Rhizophagus irregularis
Subject Areas : GeneticZahra Boor 1 , Ghasem Ali Parad 2 , Seyed Mohsen Hosseini 3 , Ehsan Ghanbary 4
1 - Deoartmaent of Forestry, Faculty of Natural Resources, Tarbiat Modarres University, Noor, Iran
2 - Deoartmaent of Forestry, Faculty of Natural Resources, Tarbiat Modarres University, Noor, Iran
3 - Deoartmaent of Forestry, Faculty of Natural Resources, Tarbiat Modarres University, Noor, Iran
4 - Deoartmaent of Forestry, Faculty of Natural Resources, Tarbiat Modarres University, Noor, Iran
Keywords: water potential, Field capacity, total biomass, Antioxidant activities, photosynthetic rate,
Abstract :
This study was conducted in greenhouse condition to investigate the growth, morphological and physiological changes and some antioxidant enzyme activities of one-year-old seedlings of Alnus subcordata C. A. Mey. inoculated with Rhizophagus irregularis mycorrhizal fungi under water deficit stress in a period of 70 days. The experiment was carried out at two inoculation levels (control or non-inoculated seedlings and inoculated with R. irregularismycorrhizal fungi) and with two levels of irrigation including irrigation at field capacity (control treatment) and irrigation at 30% of field capacity (water deficit treatment) in a completely randomized design with four treatments and 10 replications. Results revealed that morphological and physiological characteristics of A. subcordata seedlings significantly decreased under water deficit stress at 99% level while all enzymatic activities significantly increased. Although the morphological characteristics such as height and diameter growth, root length, leaf area, and leaf, stem, root, and total biomass significantly increased by 20-30% in R. irregularis mycorrhiza treatment of the irrigation control plants, these features increased by 55, 40, 46, 47, 37, 35, 50 and 37%, respectively when the plants under water deficit treatment were added R. irregularis mycorrhiza compared to non-mycorrhiza water deficit treatment. The meancomparisonresults indicated that the photosynthesis rate, stomatal conductance, transpiration, and leaf water potential reduced by 57, 54, 53, and 65%, respectively under water deficit regime whereas addition of R. irregularis mycorrhizal fungi in soil alleviated the effects of water deficit. Also, under water deficit condition, activities of catalase, peroxidase, superoxide dismutase, and ascorbate peroxidase significantly increased in comparison with field capacity irrigated seedlings while treatment of soil with mycorrhiza mitigated the destructive effects of water deficit. In general, the present study showed that inoculation of R. irregularis mycorrhizal fungi can alleviate physiological indexes and antioxidant enzyme and consequently leading to an increased tolerance of A. subcordata seedlings during the first year.
Abbaspour, H., Saeidi-Sar, S., Afshari, H. and Abdel-Wahhab, M. (2012).Tolerance of mycorrhiza infected pistachio (Pistacia vera L.) seedling to drought stress under glasshouse conditions. Journal of Plant Physiology. 169(7): 704-709.
Alguacil, M., Hernández, J.A., Caravaca, F., Portillo, B. and Roldan, A. (2003). Antioxidant enzyme activities in shoots from three mycorrhizal shrub species afforested in a degraded semi‐arid soil. Physiologia Plantarum. 118(4): 562-570.
Aroca, R., Vernieri P. and Ruiz-Lozano J.M. (2008). Mycorrhizal and non-mycorrhizal Lactuca sativa plants exhibit contrasting responses to exogenous ABA during drought stress and recovery. Journal of Experimental Botany. 59(8): 2029-2041.
Augé, R.M. (2001). Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza. 11(1): 3-42.
Augé, R.M., Moore, J.L., Cho, K., Stutz, J.C., Sylvia, D.M., Al-Agely, A.K. and Saxton, A.M. (2003). Relating foliar dehydration tolerance of mycorrhizal Phaseolus vulgaris to soil and root colonization by hyphae. Journal of Plant Physiology. 160(10): 1147-1156.
Azimi, R. and Kianian, M.K. (2018). Effects of Drought Stress and Mycorrhiza on Viability and Vegetative Growth Characteristics of Ziziphora clinopodioides Lam. Journal of Rangeland Science. 8(3): 253-263.
Bahadur, A., Batool, A., Nasir, F., Jiang, S., Mingsen, Q., Zhang, Q., Pan, J., Liu, Y. and Feng, H. (2019). Mechanistic insights into arbuscular mycorrhizal fungi-mediated drought stress tolerance in plants. International Journal of Molecular Sciences. 20(17): 4199.
Bartels, D. (2001). Targeting detoxification pathways: an efficient approach to obtain plants with multiple stress tolerance?. Trends in Plant Science. 6(7): 284-286.
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. 27(4): 349-363.
Borde, M., Dudhane, M. and Jite, P. (2011). Growth photosynthetic activity and antioxidant responses of mycorrhizal and non-mycorrhizal bajra (Pennisetum glaucum) crop under salinity stress condition. Crop Protection. 30(3): 265-271.
Chance B. and Maehly, A. (1955). [136] Assay of catalases and peroxidases.
Chitarra, W., Pagliarani, C., Maserti, B., Lumini, E., Siciliano, I., Cascone, P., Schubert, A., Gambino, G., Balestrini, R. and Guerrieri, E. (2016). Insights on the impact of arbuscular mycorrhizal symbiosis on tomato tolerance to water stress. Plant Physiology. 171(2): 1009-1023.
Fracasso, A., Telò, L., Lanfranco, L., Bonfante, P. and Amaducci, S. (2020). Physiological beneficial effect of Rhizophagus intraradices inoculation on tomato plant yield under water deficit conditions. Agronomy.10(1): 71-91.
Gao, D., Gao, Q., Xu, H.-Y., Ma, F., Zhao, C.-M. and Liu, J.-Q. (2009). Physiological responses to gradual drought stress in the diploid hybrid Pinus densata and its two parental species. Trees. 23(4): 717-728.
Ghanbary, E., Fathizadeh, O., Pazhouhan, I., Zarafshar, M., Tabari, M., Jafarnia, S., Parad, G.A., Bader, MK.-F. (2021). Drought and Pathogen Effects on Survival, Leaf Physiology, Oxidative Damage, and Defense in Two Middle Eastern Oak Species. Forests. 12(2): 247.
Gholamhoseini, M., Ghalavand, A., Dolatabadian, A., Jamshidi, E. and Khodaei-Joghan, A. (2013). Effects of arbuscular mycorrhizal inoculation on growth, yield, nutrient uptake and irrigation water productivity of sunflowers grown under drought stress. Agricultural Water Management. 117: 106-114.
Guha, A., Rasineni, G.K. and Reddy, A.R. (2010). Drought tolerance in mulberry (Morus spp.): a physiological approach with insights into growth dynamics and leaf yield production. Experimental Agriculture. 46 (4): 471-488.
Jia-Dong, H., Tao, D., Hui-Hui, W., Ying-Ning, Z., Qiang-Sheng, W. and Kamil, K. (2019). Mycorrhizas induce diverse responses of root TIP aquaporin gene expression to drought stress in trifoliate orange. Scientia Horticulturae. 243: 64-69.
Latef, A.A.H.A. and Chaoxing, H. (2011). Effect of arbuscular mycorrhizal fungi on growth, mineral nutrition, antioxidant enzymes activity and fruit yield of tomato grown under salinity stress. Scientia Horticulturae. 127(3): 228-233.
Li, J., Meng, B., Chai, H., Yang, X., Song, W., Li, S., Lu, A., Zhang, T. and Sun, W. (2019). Arbuscular mycorrhizal fungi alleviate drought stress in C3 (Leymus chinensis) and C4 (Hemarthria altissima) grasses via altering antioxidant enzyme activities and photosynthesis. Frontiers in Plant Science. 10:499.
Liu, H., Wang, X., Wang, D., Zou, Z. and Liang, Z. (2011). Effect of drought stress on growth and accumulation of active constituents in Salvia miltiorrhiza Bunge. Industrial Crops and Products. 33(1): 84-88.
Monzón, A. and Azcón, R. (2001). Growth responses and N and P use efficiency of three Alnus species as affected by arbuscular-mycorrhizal colonisation. Plant Growth Regulation. 35(1): 97-104.
Morrissey, J.P., Dow, J.M., Mark, G.L. and O'Gara, F. (2004). Are microbes at the root of a solution to world food production? Rational exploitation of interactions between microbes and plants can help to transform agriculture. EMBO reports. 5(10): 922-926.
Munne-Bosch, S. and Penuelas, J. (2003). Photo-and antioxidative protection, and a role for salicylic acid during drought and recovery in field-grown Phillyrea angustifolia plants. Planta. 217(5): 758-766.
Nakano, Y. and Asada, K. (1981). Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant and Cell Physiology. 22(5): 867-880.
Parad, G.A., Ghobad-Nejhad, M., Tabari, M., Yousefzadeh, H., Esmaeilzadeh, O., Tedersoo, L. and Buyck, B. (2018). Cantharellus alborufescens and C. ferruginascens (Cantharellaceae, Basidiomycota) new to Iran Cryptogamie. Mycologie. 39(3): 299–310.
Parad, G.A., Tabari Kouchaksaraei, M., Striker, G.G., Sadati, S.E. and Nourmohammadi, K. (2016). Growth, morphology and gas exchange responses of two-year-old Quercus Castaneifolia seedlings to flooding stress. Scandinavian Journal of Forest Research. 31(5): 458-466.
Parad, G.A., Zarafshar, M., Striker, G.G. and Sattarian, A. (2013a). Some physiological and morphological responses of Pyrus boissieriana to flooding. Trees, Structure and Function. 27(5): 1387-1393.
Parad, G.A., Tabari, M., and Sadati, E. (2013b). Survival, Growth and Biomass Allocationin Seedlings of Common ash (Fraxinus excelsior L.) as affected by flooding Stress. 26(1): 9-20.
Parad, G.A., Tabari, M., and Sadati, E. (2014). Effect of permanent and periodic flooding treatments on growth, morphological and physiological characteristics of one-year old potted seedlings of Quercus castaneifolia in Noor lowland. Journal of Wood and Forest Science and Technology. 20(4): 167-181.
Polle, A., Otter, T. and Seifert, F. (1994). Apoplastic peroxidases and lignification in needles of Norway spruce (Picea abies L.). Plant Physiology. 106(1): 53-60.
Porcel, R., Barea, J.M. and Ruiz‐Lozano, J.M. (2003). Antioxidant activities in mycorrhizal soybean plants under drought stress and their possible relationship to the process of nodule senescence. New Phytologist. 157(1): 135-143.
Ruiz‐Lozano, J., Azcón, R. and Palma, J. (1996). Superoxide dismutase activity in arbuscular mycorrhizal Lactuca sativa plants subjected to drought stress. New Phytologist. 134(2): 327-333.
Ruiz-Lozano, J.M. (2003). Arbuscular mycorrhizal symbiosis and alleviation of osmotic stress. New perspectives for molecular studies. Mycorrhiza. 13(6): 309-317.
Ruíz-Sánchez, M., Armada, E., Muñoz, Y., de Salamone, I.E. G., Aroca, R., Ruíz-Lozano, J.M. and 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(10): 1031-1037.
Sairam, R.K, Srivastava, G.C, Agarwal, S. and Meena, R.C. (2005). Differences in antioxidant activity in response to salinity stress in tolerant and susceptible wheat genotypes. Biologia Plantarum. 49(1): 85–91.
Schrader, J.A. and Graves, W.R. (2000). Seed germination and seedling growth of Alnus maritima from its three disjunct populations. Journal of the American society for Horticultural science. 125(1): 128-134.
Stewart, R.R. and Bewley, J.D. (1980). Lipid peroxidation associated with accelerated aging of soybean axes. Plant Physiology. 65(2): 245-248.
Subramanian, K.S. and Charest, C. (1997). Nutritional, growth, and reproductive responses of maize (Zea mays L.) to arbuscular mycorrhizal inoculation during and after drought stress at tasselling. Mycorrhiza. 7(1): 25-32.
Volpe, V., Chitarra, W., Cascone, P., Volpe, M.G., Bartolini, P., Moneti, G., Pieraccini, G., Di Serio, C., Maserti, B. and Guerrieri, E. (2018). The association with two different arbuscular mycorrhizal fungi differently affects water stress tolerance in tomato. Frontiers in plant science. 9:1480.
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(4): 417-425.
Wu, Q.-S., Xia, R.-X., Zou, Y.-N. and Wang, G.-Y. (2007). Osmotic solute responses of mycorrhizal citrus (Poncirus trifoliata) seedlings to drought stress. Acta Physiologiae Plantarum., 29(6): 543-549.
Wu, Q.-S., Zou, Y.-N., Xia, R.-X. and Wang, M.-Y. (2007). Five Glomus species affect water relations of Citrus tangerine during drought stress. Botanical Studies. 48(2): 147-154.
Xia, C., Christensen, M.J., Zhang, X. and Nan, Z. (2018). Effect of Epichloë gansuensis endophyte and transgenerational effects on the water use efficiency, nutrient and biomass accumulation of Achnatherum inebrians under soil water deficit. Plant and Soil. 424(1-2): 555-571.
Yamaguchi-Shinozaki, K. and Shinozaki, K. (2006). Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annual Review of Plant Biology. 57: 781–803.
Yang, Y., Tang, M., Sulpice, R., Chen, H., Tian, S. and Ban, Y. (2014). Arbuscular mycorrhizal fungi alter fractal dimension characteristics of Robinia pseudoacacia L. seedlings through regulating plant growth, leaf water status, photosynthesis, and nutrient concentration under drought stress. Journal of Plant Growth Regulation. 33(3): 612-625.
Zarik, L., Meddich, A., Hijri, M., Hafidi, M., Ouhammou, A., Ouahmane, L. and Boumezzough, A. (2016). Use of arbuscular mycorrhizal fungi to improve the drought tolerance of Cupressus atlantica G. Comptes Rendus Biologies. 339(5-6): 185-196.
Zhang, F., Jia-Dong, H., Qiu-Dan, N., Qiang-Sheng, W. and Ying-Ning Z. (2018). Enhancement of drought tolerance in trifoliate orange by mycorrhiza: changes in root sucrose and proline metabolisms. Notulae Botanicae Horti Agrobotanici Cluj-Napoca. 46(1): 270-276.
Zhang, Z., Zhang, J. and Huang, Y. (2014). Effects of arbuscular mycorrhizal fungi on the drought tolerance of Cyclo balanopsis glauca seedlings under greenhouse conditions. New Forests. 45(4): 545-556.
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Abbaspour, H., Saeidi-Sar, S., Afshari, H. and Abdel-Wahhab, M. (2012).Tolerance of mycorrhiza infected pistachio (Pistacia vera L.) seedling to drought stress under glasshouse conditions. Journal of Plant Physiology. 169(7): 704-709.
Alguacil, M., Hernández, J.A., Caravaca, F., Portillo, B. and Roldan, A. (2003). Antioxidant enzyme activities in shoots from three mycorrhizal shrub species afforested in a degraded semi‐arid soil. Physiologia Plantarum. 118(4): 562-570.
Aroca, R., Vernieri P. and Ruiz-Lozano J.M. (2008). Mycorrhizal and non-mycorrhizal Lactuca sativa plants exhibit contrasting responses to exogenous ABA during drought stress and recovery. Journal of Experimental Botany. 59(8): 2029-2041.
Augé, R.M. (2001). Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza. 11(1): 3-42.
Augé, R.M., Moore, J.L., Cho, K., Stutz, J.C., Sylvia, D.M., Al-Agely, A.K. and Saxton, A.M. (2003). Relating foliar dehydration tolerance of mycorrhizal Phaseolus vulgaris to soil and root colonization by hyphae. Journal of Plant Physiology. 160(10): 1147-1156.
Azimi, R. and Kianian, M.K. (2018). Effects of Drought Stress and Mycorrhiza on Viability and Vegetative Growth Characteristics of Ziziphora clinopodioides Lam. Journal of Rangeland Science. 8(3): 253-263.
Bahadur, A., Batool, A., Nasir, F., Jiang, S., Mingsen, Q., Zhang, Q., Pan, J., Liu, Y. and Feng, H. (2019). Mechanistic insights into arbuscular mycorrhizal fungi-mediated drought stress tolerance in plants. International Journal of Molecular Sciences. 20(17): 4199.
Bartels, D. (2001). Targeting detoxification pathways: an efficient approach to obtain plants with multiple stress tolerance?. Trends in Plant Science. 6(7): 284-286.
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. 27(4): 349-363.
Borde, M., Dudhane, M. and Jite, P. (2011). Growth photosynthetic activity and antioxidant responses of mycorrhizal and non-mycorrhizal bajra (Pennisetum glaucum) crop under salinity stress condition. Crop Protection. 30(3): 265-271.
Chance B. and Maehly, A. (1955). [136] Assay of catalases and peroxidases.
Chitarra, W., Pagliarani, C., Maserti, B., Lumini, E., Siciliano, I., Cascone, P., Schubert, A., Gambino, G., Balestrini, R. and Guerrieri, E. (2016). Insights on the impact of arbuscular mycorrhizal symbiosis on tomato tolerance to water stress. Plant Physiology. 171(2): 1009-1023.
Fracasso, A., Telò, L., Lanfranco, L., Bonfante, P. and Amaducci, S. (2020). Physiological beneficial effect of Rhizophagus intraradices inoculation on tomato plant yield under water deficit conditions. Agronomy.10(1): 71-91.
Gao, D., Gao, Q., Xu, H.-Y., Ma, F., Zhao, C.-M. and Liu, J.-Q. (2009). Physiological responses to gradual drought stress in the diploid hybrid Pinus densata and its two parental species. Trees. 23(4): 717-728.
Ghanbary, E., Fathizadeh, O., Pazhouhan, I., Zarafshar, M., Tabari, M., Jafarnia, S., Parad, G.A., Bader, MK.-F. (2021). Drought and Pathogen Effects on Survival, Leaf Physiology, Oxidative Damage, and Defense in Two Middle Eastern Oak Species. Forests. 12(2): 247.
Gholamhoseini, M., Ghalavand, A., Dolatabadian, A., Jamshidi, E. and Khodaei-Joghan, A. (2013). Effects of arbuscular mycorrhizal inoculation on growth, yield, nutrient uptake and irrigation water productivity of sunflowers grown under drought stress. Agricultural Water Management. 117: 106-114.
Guha, A., Rasineni, G.K. and Reddy, A.R. (2010). Drought tolerance in mulberry (Morus spp.): a physiological approach with insights into growth dynamics and leaf yield production. Experimental Agriculture. 46 (4): 471-488.
Jia-Dong, H., Tao, D., Hui-Hui, W., Ying-Ning, Z., Qiang-Sheng, W. and Kamil, K. (2019). Mycorrhizas induce diverse responses of root TIP aquaporin gene expression to drought stress in trifoliate orange. Scientia Horticulturae. 243: 64-69.
Latef, A.A.H.A. and Chaoxing, H. (2011). Effect of arbuscular mycorrhizal fungi on growth, mineral nutrition, antioxidant enzymes activity and fruit yield of tomato grown under salinity stress. Scientia Horticulturae. 127(3): 228-233.
Li, J., Meng, B., Chai, H., Yang, X., Song, W., Li, S., Lu, A., Zhang, T. and Sun, W. (2019). Arbuscular mycorrhizal fungi alleviate drought stress in C3 (Leymus chinensis) and C4 (Hemarthria altissima) grasses via altering antioxidant enzyme activities and photosynthesis. Frontiers in Plant Science. 10:499.
Liu, H., Wang, X., Wang, D., Zou, Z. and Liang, Z. (2011). Effect of drought stress on growth and accumulation of active constituents in Salvia miltiorrhiza Bunge. Industrial Crops and Products. 33(1): 84-88.
Monzón, A. and Azcón, R. (2001). Growth responses and N and P use efficiency of three Alnus species as affected by arbuscular-mycorrhizal colonisation. Plant Growth Regulation. 35(1): 97-104.
Morrissey, J.P., Dow, J.M., Mark, G.L. and O'Gara, F. (2004). Are microbes at the root of a solution to world food production? Rational exploitation of interactions between microbes and plants can help to transform agriculture. EMBO reports. 5(10): 922-926.
Munne-Bosch, S. and Penuelas, J. (2003). Photo-and antioxidative protection, and a role for salicylic acid during drought and recovery in field-grown Phillyrea angustifolia plants. Planta. 217(5): 758-766.
Nakano, Y. and Asada, K. (1981). Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant and Cell Physiology. 22(5): 867-880.
Parad, G.A., Ghobad-Nejhad, M., Tabari, M., Yousefzadeh, H., Esmaeilzadeh, O., Tedersoo, L. and Buyck, B. (2018). Cantharellus alborufescens and C. ferruginascens (Cantharellaceae, Basidiomycota) new to Iran Cryptogamie. Mycologie. 39(3): 299–310.
Parad, G.A., Tabari Kouchaksaraei, M., Striker, G.G., Sadati, S.E. and Nourmohammadi, K. (2016). Growth, morphology and gas exchange responses of two-year-old Quercus Castaneifolia seedlings to flooding stress. Scandinavian Journal of Forest Research. 31(5): 458-466.
Parad, G.A., Zarafshar, M., Striker, G.G. and Sattarian, A. (2013a). Some physiological and morphological responses of Pyrus boissieriana to flooding. Trees, Structure and Function. 27(5): 1387-1393.
Parad, G.A., Tabari, M., and Sadati, E. (2013b). Survival, Growth and Biomass Allocationin Seedlings of Common ash (Fraxinus excelsior L.) as affected by flooding Stress. 26(1): 9-20.
Parad, G.A., Tabari, M., and Sadati, E. (2014). Effect of permanent and periodic flooding treatments on growth, morphological and physiological characteristics of one-year old potted seedlings of Quercus castaneifolia in Noor lowland. Journal of Wood and Forest Science and Technology. 20(4): 167-181.
Polle, A., Otter, T. and Seifert, F. (1994). Apoplastic peroxidases and lignification in needles of Norway spruce (Picea abies L.). Plant Physiology. 106(1): 53-60.
Porcel, R., Barea, J.M. and Ruiz‐Lozano, J.M. (2003). Antioxidant activities in mycorrhizal soybean plants under drought stress and their possible relationship to the process of nodule senescence. New Phytologist. 157(1): 135-143.
Ruiz‐Lozano, J., Azcón, R. and Palma, J. (1996). Superoxide dismutase activity in arbuscular mycorrhizal Lactuca sativa plants subjected to drought stress. New Phytologist. 134(2): 327-333.
Ruiz-Lozano, J.M. (2003). Arbuscular mycorrhizal symbiosis and alleviation of osmotic stress. New perspectives for molecular studies. Mycorrhiza. 13(6): 309-317.
Ruíz-Sánchez, M., Armada, E., Muñoz, Y., de Salamone, I.E. G., Aroca, R., Ruíz-Lozano, J.M. and 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(10): 1031-1037.
Sairam, R.K, Srivastava, G.C, Agarwal, S. and Meena, R.C. (2005). Differences in antioxidant activity in response to salinity stress in tolerant and susceptible wheat genotypes. Biologia Plantarum. 49(1): 85–91.
Schrader, J.A. and Graves, W.R. (2000). Seed germination and seedling growth of Alnus maritima from its three disjunct populations. Journal of the American society for Horticultural science. 125(1): 128-134.
Stewart, R.R. and Bewley, J.D. (1980). Lipid peroxidation associated with accelerated aging of soybean axes. Plant Physiology. 65(2): 245-248.
Subramanian, K.S. and Charest, C. (1997). Nutritional, growth, and reproductive responses of maize (Zea mays L.) to arbuscular mycorrhizal inoculation during and after drought stress at tasselling. Mycorrhiza. 7(1): 25-32.
Volpe, V., Chitarra, W., Cascone, P., Volpe, M.G., Bartolini, P., Moneti, G., Pieraccini, G., Di Serio, C., Maserti, B. and Guerrieri, E. (2018). The association with two different arbuscular mycorrhizal fungi differently affects water stress tolerance in tomato. Frontiers in plant science. 9:1480.
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(4): 417-425.
Wu, Q.-S., Xia, R.-X., Zou, Y.-N. and Wang, G.-Y. (2007). Osmotic solute responses of mycorrhizal citrus (Poncirus trifoliata) seedlings to drought stress. Acta Physiologiae Plantarum., 29(6): 543-549.
Wu, Q.-S., Zou, Y.-N., Xia, R.-X. and Wang, M.-Y. (2007). Five Glomus species affect water relations of Citrus tangerine during drought stress. Botanical Studies. 48(2): 147-154.
Xia, C., Christensen, M.J., Zhang, X. and Nan, Z. (2018). Effect of Epichloë gansuensis endophyte and transgenerational effects on the water use efficiency, nutrient and biomass accumulation of Achnatherum inebrians under soil water deficit. Plant and Soil. 424(1-2): 555-571.
Yamaguchi-Shinozaki, K. and Shinozaki, K. (2006). Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annual Review of Plant Biology. 57: 781–803.
Yang, Y., Tang, M., Sulpice, R., Chen, H., Tian, S. and Ban, Y. (2014). Arbuscular mycorrhizal fungi alter fractal dimension characteristics of Robinia pseudoacacia L. seedlings through regulating plant growth, leaf water status, photosynthesis, and nutrient concentration under drought stress. Journal of Plant Growth Regulation. 33(3): 612-625.
Zarik, L., Meddich, A., Hijri, M., Hafidi, M., Ouhammou, A., Ouahmane, L. and Boumezzough, A. (2016). Use of arbuscular mycorrhizal fungi to improve the drought tolerance of Cupressus atlantica G. Comptes Rendus Biologies. 339(5-6): 185-196.
Zhang, F., Jia-Dong, H., Qiu-Dan, N., Qiang-Sheng, W. and Ying-Ning Z. (2018). Enhancement of drought tolerance in trifoliate orange by mycorrhiza: changes in root sucrose and proline metabolisms. Notulae Botanicae Horti Agrobotanici Cluj-Napoca. 46(1): 270-276.
Zhang, Z., Zhang, J. and Huang, Y. (2014). Effects of arbuscular mycorrhizal fungi on the drought tolerance of Cyclo balanopsis glauca seedlings under greenhouse conditions. New Forests. 45(4): 545-556.
