Photosynthetica 2012, 50(2):305-316 | DOI: 10.1007/s11099-012-0024-8

Improving growth, flower yield, and water relations of snapdragon (Antirhinum majus L.) plants grown under well-watered and water-stress conditions using arbuscular mycorrhizal fungi

A. A. Asrar1, G. M. Abdel-Fattah1,*, K. M. Elhindi1
1 Plant production Department, College of Food and Agriculture Sciences, King Saud University, Riyadh, Riyadh, Saudi Arabia

The influence of arbuscular mycorrhizal (AM) fungus Glomus deserticola (Trappe and John) on plant growth, nutrition, flower yield, water relations, chlorophyll (Chl) contents and water-use efficiency (WUE) of snapdragon (Antirhinum majus cv. butterfly) plants were studied in potted culture under well-watered (WW) and water-stress (WS) conditions. The imposed water stress condition significantly reduced all growth parameters, nutrient contents, flower yield, water relations, and Chl pigment content and increased the electrolyte leakage of the plants comparing to those of nonstressed plants. Regardless of the WS level, the mycorrhizal snapdragon plants had significantly higher shoot and root dry mass (DM), WUE, flower yield, nutrient (P, N, K, Mg, and Ca) and Chl contents than those nonmycorrhizal plants grown both under WW or WS conditions. Under WS conditions, the AM colonization had greatly improved the leaf water potential (Ψw), leaf relative water content (RWC) and reduced the leaf electrolyte leakage (EL) of the plants. Although the WS conditions had markedly increased the proline content of the leaves, this increase was significantly higher in nonmycorrhizal than in mycorrhizal plants. This suggests that AM colonization enhances the host plant WS tolerance. Values of benefit and potential dry matter for AM-root associations were highest when plants were stressed and reduced under WW conditions. As a result, the snapdragon plants showed a high degree of dependency on AM fungi which improve plant growth, flower yield, water relations particularly under WS conditions, and these improvements were increased as WS level had increased. This study confirms that AM colonization can mitigate the deleterious effect of water stress on growth and flower yield of the snapdragon ornamental plant.

Additional key words: arbuscular mycorrhiza; flower yield; snapdragon; water relations; water stress

Received: August 9, 2011; Accepted: February 3, 2012; Published: June 1, 2012  Show citation

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Asrar, A.A., Abdel-Fattah, G.M., & Elhindi, K.M. (2012). Improving growth, flower yield, and water relations of snapdragon (Antirhinum majus L.) plants grown under well-watered and water-stress conditions using arbuscular mycorrhizal fungi. Photosynthetica, 50(2), 305-316. doi: 10.1007/s11099-012-0024-8
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    References

    1. Abdel-Fattah, G.M.: Functional activity of VA-mycorrhiza (Glomus mosseae) in the growth and productivity of soybean plants grown in sterilized soil. - Folia Microbiol. 42: 495-502, 1997. Go to original source...
    2. Abdel-Fattah, G.M.: Measurement of the viability of arbuscular-mycorrhizal fungi using three different stains; relation to growth and metabolic activities of soybean plants. - Microbiol. Res. 156: 359-367, 2001. Go to original source...
    3. Abdel-Fattah, G.M., Asrar, A.A.: Arbuscular mycorrhizal fungal application to improve growth and tolerance of wheat (Triticum aestivum L.) plants grown in saline soil. - Acta Physiol. Plant. 34: 267-277, 2012. Go to original source...
    4. Abdel-Fattah, G.M., Migahed, F.F., Ibrahim, A.H.: Interactive effects of endomycorrhizal fungus Glomus etunicatum and phosphorus fertilization on growth and metabolic activities of broad bean plants under drought stress conditions. - Pakist. J. Biol. Sci. 5: 835-841, 2002. Go to original source...
    5. Aboul-Nasr, A.: Effects of vesicular-arbuscular mycorrhizal on Tagetes erecta and Zinnia elegans. - Mycorrhiza 6: 61-64, 1996. Go to original source...
    6. Al-Karaki, G.N.: Benefit, cost and water-use efficiency of arbuscular mycorrhizal durum wheat grown under drought stress. - Mycorrhiza 8: 41-45, 1998. Go to original source...
    7. Al-Karaki, G.N., Al-Raddad, A.: Effects of arbuscular mycorrhizal fungi and drought stress on growth and nutrient uptake of two wheat genotypes differing in drought resistance. - Mycorrhiza 7: 83-88, 1997. Go to original source...
    8. Allen, E.B., Cunningham, G.L.: Effects of vesicular mycorrhiza on Distichlis spicata under three salinity levels. - New Phytol. 93: 227-236, 1983. Go to original source...
    9. Allen, M.F.: Influence of vesicular mycorrhizae on water movement through Bouteloua gracilis (H.B.K.) lag ex Steud. - New Phytol. 91: 191-196, 1982. Go to original source...
    10. Allen, S.E.: Chemical Analysis of Ecological Materials. 2nd Ed. - Blackwell Sci. Publ., Osney 1989.
    11. Al-Qarawi, A.A.: Efficiency of arbuscular mycorrhizal (AM) fungi for improving growth, root system architecture, nutrient uptake, leaf hydraulic conductance and photosynthetic pigments of maize and pea plants. - J. Environ. Sci. 39: 67-82, 2010.
    12. Asrar, A.A., Elhindi, K.M.: Alleviation of drought stress of marigold (Tagetes erecta) plants by using arbuscular mycorrhizal fungi. - Saudi J. Biol. Sci. 19: 38-46, 2011. Go to original source...
    13. Auge, R.M.: Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. - Mycorrhiza 11: 3-42, 2001. Go to original source...
    14. Auge, R.M., Schekel, K.A., Wample, R.L.: Osmotic adjustment in leaves of VA mycorrhizal rose plants in response to drought stress. - Plant Physiol. 82: 765-770, 1986. Go to original source...
    15. Auge, R.M., Schekel, K.A., Wample, R.L.: leaf water and carbohydrate status of VA mycorrhizal rose exposed to drought stress. - Plant Soil 99: 291-302, 1987. Go to original source...
    16. Auge, R.M., Toler, H.D., Sams, C.E., Nasim, G.: Hydraulic conductance and water potential gradients in squash leaves showing mycorrhiza-induced increases in stomatal conductance. - Mycorrhiza 18: 115-121, 2008. Go to original source...
    17. Azcon-Aguilar, C., Barcelo, A., Vidal, M.T., de la Vina, G.: Further studies in the growth and development of microprogated avocado plants. - Agronomie 12: 837-840, 1992. Go to original source...
    18. Azcón, R., Gomez, M., Tobar, R.: Effects of nitrogen source on growth, nutrition, photosynthetic rate and nitrogen metabolism of mycorrhizal and phosphorus fertilized plants of Lactuca sativa L. - New Phytol. 121: 227-234, 1992. Go to original source...
    19. Berta, G., Fusconi, A., Trotta, A.: VA mycorrhizal infection and the morphology and function of root systems. - Environ. Exp. Bot. 33: 159-173, 1993. Go to original source...
    20. Bethlenfalvay, G.J., Brown, M.S., Ames, R.N., Thomas, R.S.: Effects of drought on host and endophyte development in mycorrhizal soybeans in relation to water use and phosphate uptake. - Physiol. Plant. 72: 565-571, 1988. Go to original source...
    21. Bryla, D.R., Duniway, J.M.: Growth, phosphorus uptake and water relations of safflower and wheat infected with an arbuscular mycorrhizal fungus. - New Phytol. 136: 581-590, 1997. Go to original source...
    22. Bulir, P.: Testing method applied for evaluation of ornamental trees in the Czech Republic. - Hort. Sci. 36: 154-161, 2009. Go to original source...
    23. Chapman, H.D., Pratt, P.F.: Ammonium vandate-molybdate method for determenation of phosphorus. - In: Methods of Analysis for Soils, Plants and Water. 1st Ed. Pp. 184-203. California Univ., California 1961.
    24. Cho, K., Toler, H., Lee, J., Ownley, B., Stutz, J., Moore, J., Auge, R.: Mycorrhizal symbiosis and responses of sorghum plants to combined drought and salinity stresses. - J. Plant Physiol. 163: 517-528, 2006. Go to original source...
    25. Davies, F.T., Potter, J.R., Linderman, R.G.: Mycorrhiza and repeated drought exposure affect drought reistance and extraradical hyphae of pepper plants independent of plant size and nutrient content. - J. Plant Physiol. 139: 289-294, 1992. Go to original source...
    26. Davies, F.T., Svenson, S.E., Cole, J.C., Phavaphutanon, L., Duray, S.A., Olalde-Portugal, V., Meier, C.E., Bo, S.H.: Nonnutritional stress acclimation of mycorrhizal woody plants exposed to drought. - Tree Physiol. 16: 985-993, 1996. Go to original source...
    27. Davies, W.J., Tardieu, F., Trejo, C.L.: How do chemical signals work in plants that grow in drying soil? - Plant Physiol. 104: 309-314, 1994. Go to original source...
    28. De Miranda, J.C.C., Harris, P.J.: The effect of soil phosphorus on the external mycelium growth of arbuscular-mycorrhizal fungi during early stages of mycorrhiza formation. - Plant Soil 166: 271-280, 1994. Go to original source...
    29. Dionisio-Sese, M.L., Tobita, S.: Antioxidant responses of rice seedlings to salinity stress. - Plant Sci. 135: 1-9, 1998. Go to original source...
    30. Ellis. J.R., Larsen, H.J., Boosalis, M.G.: Drought resistance of wheat plants inoculated with vesicular-arbuscular mycorrhizae. - Plant Soil 86: 369-378, 1985. Go to original source...
    31. Faber, B.A., Zasoski, R.J., Munns, D.N., Shackel, K.: A method for measuring hyphal nutrient and water uptake in mycorrhizal plants. - Can. J. Bot. 96: 87-94, 1991. Go to original source...
    32. Feng, G., Zhang, F.S., Li, X.L., Tian, C.Y., Tang, C., Rengel, Z.: Improved tolerance of maize plants to salt stress by arbuscular mycorrhiza is related to higher accumulation of soluble sugars in roots. - Mycorrhiza 12: 185-190, 2002. Go to original source...
    33. George, E., Haussler, K., Vetterrlein, D., Gorgus, E., Marschner, H.: Water nutrient translocation by hyphae of Glomus mosseae. - Can. J. Bot. 70: 2130-2137, 1992. Go to original source...
    34. Giri, B., Kapoor, R., Mukerji, K.G.: Improved tolerance of Acacia nilotica to salt stress by arbuscular mycorrhiza, Glomus fasciculatum may be partly related to elevated K:Na ratios in root and shoot tissues. - Microbial Ecol. 54: 753-760, 2007. Go to original source...
    35. Goicoechea, N., Dolezal, K., Antolin, M.C., Sanchez-Diaz, M.: Root cytokinins, acid phosphorus and nodule activity in drought-stressed mycorrhizal or nitrogen-fixing alfalfa plants. - J. Exp. Bot. 47: 683-686, 1996. Go to original source...
    36. Hanson, A.D., Hitz, W.D.: Metabolic responses of mesophytes to plant water deficits. Annuals review - Plant Physiol. 33: 161-203, 1982. Go to original source...
    37. Hiscox, J.D., Israelstam, G.F.: A method for the extraction of chlorophyll from leaf tissue without maceration. - Can. J. Bot. 57: 1332-1234, 1979. Go to original source...
    38. Hoque, M.D.A., Arima, S.: Evaluation of salt damage through cell membrane stability monitored by electrolyte leakage in water chestnut (Trapa sp.). - Bull. Fac. Agric. Saga Univ. 85: 141-146, 2000.
    39. Ibrahim, H.A., Abdel-Fattah, G.M., Eman, F.M., Abd El-Aziz. M.H., Shohr, A.E.: Arbuscular mycorrhizal fungi and spermine alleviate the adverse effects of salinity stress on electrolyte leakage and productivity of wheat plants. - Phyton-Ann. Rei Bot. 51: 261-276, 2011.
    40. Kaya, C., Ashraf, M., Sonmez, O., Aydemir, S., Tuna, A., Cullu, M.: The influence of arbuscular mycorrhizal colonization on key growth parameters and fruit yield of pepper plants grown at high salinity. - Sci. Hort. 121: 1-6, 2009. Go to original source...
    41. Kaya, C., Higgs, D.: Response of tomato (Lycopersicon esculentum L.) cultivars to foliar application of zinc when grown in sand culture at low zinc. - Sci. Hort. 93: 53-64, 2002. Go to original source...
    42. Kaya, C., Higgs, D., Kirnak, H., Tas, I.: Mycorrhizal colonization improves fruit yield and water use efficiency in watermelon (Citrulus lanatus Thunb.) grown under well-watered and water-stressed conditions. - Plant Soil 254: 287-292, 2003. Go to original source...
    43. Koide, R., Ellitott, G.: Cost, benefit and efficiency of vesiculararbuscular mycorrhizal symbiosis. - Func. Ecol. 3: 252-255, 1989.
    44. Lee, B.R., Kim, K.Y., Jung, W.J., Avice, J.C., Ourry, A., Kim, T.H.: Peroxidases and lignification in relation to the intensity of water-deficit stress in white clover (Trifolium repens L.). - J. Exp. Bot. 6: 1271-1279, 2007. Go to original source...
    45. Levitt, J.: Responses of plants to environmental stress. - In: Levitt, J.: Water, Radiation, Salt and Other Stresses. Vol. II. 2nd Ed., Pp. 3-53, Acad. Press, New York 1980.
    46. Levy, Y., Krikun, J.: Effect of vesicular-arbuscular mycorrhizal on Citrus jambhiri water relations. - New Phytol. 85: 25-31, 1980. Go to original source...
    47. Li, H.S.: Principles and Techniques of Plant Physiological Biochemical Experiment. - Higher Education Press, Beijing 2000.
    48. Linderman, R.G., Davis, E.: varied response of marigold (Tagetes spp.) genotypes to inoculation with different arbuscular mycorrhizal fungi. - Sci. Hort. 99: 67-78, 2004. Go to original source...
    49. Liu, G.H., Nada, K., Honda, C., Kitashiba, H., Wen, X., Pang, X., Moriguchi, T.: Polyamine biosynthesis of apple callus under salt stress: importance of the arginine decarboxylase pathway in stress response. - J. Exp. Bot. 57: 2589-2599, 2006. Go to original source...
    50. Maggio, A., Reddy, M.P., Joly, R.J.: leaf gas exchange and soluble accumulation in the halophyte Salvadora persica grown at moderate salinity. - Environ. Exp. Bot. 44: 31-38, 2000. Go to original source...
    51. Menge, J.A., Johnson, E.L.V., Platt, R.G.: Mycorrhizal dependency of several citrus cultivars under three nutrient regimes. - New Phytol. 81: 553-559, 1978. Go to original source...
    52. Morte, A., Lovisolo, C., Schubert, A.: Effect of drought stress on growth and water relations of the mycorrhizal association Helianthemum almeriense - Terfezia claveryi. - Mycorrhiza 10: 115-119, 2000. Go to original source...
    53. Munns, R., James, R.A., Lauchli, A.: Approaches to increasing the salt tolerance of wheat and other cereals. - J. Exp. Bot. 57: 1025-1043, 2006. Go to original source...
    54. Nelson, D.W., Sommers, L.E.: Determination of total nitrogen in plant material. - Agron. J. 65: 109-112, 1973. Go to original source...
    55. Phillips, J.M., Hayman, D.S.: Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. - Trans. Brit. Mycol. Soc. 55: 158-161, 1970. Go to original source...
    56. Porcel, R., Ruiz-Lozano, J.M.: Arbuscular mycorrhizal influence on leaf water potential, solute accumulation and oxidative stress in soybean plants subjected to drought stress. - J. Exp. Bot. 55: 1743-1750, 2004. Go to original source...
    57. Raju, P.S., Clark, R.B., Ellis, J.R.: Benefit and cost analysis and phosphorus mycorrhizal fungi colonization with sorghum (Sorghum bicolor) genotypes grown at varied phosphorus levels. - Plant Soil 124: 199-204, 1990. Go to original source...
    58. Richert, D.H., Sancho, F.O., Ananth, S.: Vesicular-arbuscular endomycorrhizal colonization of wetland plants. - J. Environ. Quality 23: 913-916, 1994. Go to original source...
    59. Ruiz-Lozano, J.M., Azcon, R.: Hyphal contribution to water uptake in mycorrhizal plants as affected by the fungal species and water status. - Physiol. Plant. 95: 472-478, 1995. Go to original source...
    60. Ruiz-Lozano, J.M., Azcon, R., Gomez, M.: Effects of arbuscular mycorrhizal Glomus species on drought tolerance: physiological and nutritional plant responses. - Appl. Environ. Microbiol. 61: 456-460, 1995. Go to original source...
    61. Sadasivam, S., Manickam, A.: Biochemical methods. 2nd Ed. - Int. Publ. Ltd., New Delhi 1996.
    62. Safir, G.R., Boyer, J.S. Gerdemann, J.W.: Mycorrhizal enhancement of water transport in soybean. - Science 172: 581-583, 1971. Go to original source...
    63. Sanchez, F.J., Manzanares, M., Andres, E.F., Tenorio, J.L., Averbe, L.: Turgor maintenance, osmotic adjustment and soluble sugar and proline accumulation in 49 pea cultivars in response to water stress. - Field Crops Res. 59: 225-235, 1998. Go to original source...
    64. Stevens, K.J., Wall, C.B., Jansen, J.A.: Effects of arbuscular mycorrhizal fungi on seedling growth and development of two wetland plants, Bidens frondosa L., and Eclipta prostrata (L.) L., grown under three levels of water availability. - Mycorrhiza 21: 279-288, 2011. Go to original source...
    65. Subramanian, K.S., Charest, C.: Influence of arbuscular mycorrhizae on the metabolism of maize under drought stress. - Mycorrhiza 5: 273-278, 1995. Go to original source...
    66. Subramanian, K.S., Charest, C.: Arbuscular mycorrhizae and nitrogen assimilation in maize after drought and recovery. - Physiol. Plant. 102: 285-296, 1998. Go to original source...
    67. Subramanian, K.S., Santhanakrishnan, P., Balasubramanian, P.: Responses of field grown tomato plants to arbuscular mycorrhizal fungal colonization under varying intensities of drought stress. - Sci. Hort. 107: 245-253, 2006. Go to original source...
    68. Tang, M., Chen, H., Huang, J.C., Tian, Z.Q.: AM fungi effects on the growth and physiology of Zea mays seedlings under diesel stress. - Soil Biol. Biochem. 41: 936-940, 2009. Go to original source...
    69. Tarafdar, J.C.: Role of a VA mycorrhizal fungus on growth and water relations in wheat in presence of organic and inorganic phosphates. - J. Ind. Soc. Soil Sci. 43: 197-203, 1995.
    70. Tobar, R.M., Azcon, R., Barea J.M.: Improved nitrogen uptake and transport from N15-labeled nitrate by external hyphae of arbuscular mycorrhiza under water-stressed conditions. - New Phytol. 126: 119-122, 1994. Go to original source...
    71. Trouvelot, A., Kough, J., Gianinazzi-Pearson, V.: Evaluation of VA infection levels in root systems. Research for estimation methods having a functional significance. - In: Gianinazzi-Pearson, V., Gianinazzi, S. (ed.): Physiological and Genetical Aspects of Mycorrhizae. Pp. 217-221. INRA Press, Paris 1986.
    72. Wu, Q., Xia, R.X.: Arbuscular mycorrhizal fungi influence growth, osmotic adjustment and photosynthesis of citrus under well-watered and water stress conditions. - J. Plant physiol. 163: 417-425, 2006. Go to original source...
    73. Wu, Q.S., Xia, R.X., Zou, Y.N.: Improved soil structure and citrus growth after inoculation with three arbuscular mycorrhizal fungi under drought stress. - Eur. J. Soil Biol. 44: 122-128, 2008. Go to original source...
    74. Zandavalli, R.B., Dillenburg, L.R., de Souza, P.V.: Growth responses of Araucaria angustifolia (Araucariaceae) to inoculation with the mycorrhizal fungus Glomus clarum. - Appl. Soil Ecology 25: 245-255, 2004. Go to original source...
    75. Zhang, Q., Xu, L., Tang, J., Bai, M., Chen, X.: Arbuscular mycorrhizal mediation of biomass-density relationship of Medicago sativa L. under two water conditions in a field experiment. - Mycorrhiza 21: 269-277, 2011. Go to original source...

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