The effects of arbuscular mycorrhizal fungus and water stress on some antioxidant enzymes activities and nutrients uptake of two citrus rootstocks

Document Type : Full Article


Department of Soil Science, College of Agriculture, Shiraz University, Shiraz, I. R. Iran


ABSTRACT-Water stress is the main cause for crop yield reduction in the majority of agricultural regions of the world because it affects almost all plant functions. The effects of Glomus mosseae on growth, nutrients uptake, and antioxidant enzymes of sour orange (Citrus aurantium) and rough lemon) Citrus jambheri) rootstocks were assessed in sterilized soil under greenhouse conditions.  A three-factor experiment was set up in a completely randomized design with three replicates of each treatment. Treatments consisted of water stress at four levels (irrigation intervals of 2, 4, 6, and 8 days) and mycorrhizal treatments at two levels (inoculation with G. mosseae and non-mycorrhizal control). Mycorrhizal seedlings of two citrus rootstocks were successfully infected by G. mosseae. As water stress increased, root colonization, shoot dry weight, shoot N, P, Mn, Cu, and Fe uptake of two citrus rootstocks significantly decreased but shoot Zn uptake and the antioxidant enzymes [superoxide dismutase (SOD), catalase (CAT), glutathione peroxidase (G-POD) and ascorbate peroxidase (APX)] activities of two citrus rootstocks leaves increased. With inoculation of seedlings by G. mosseae compared with control, shoot dry weight, N and P uptake, and antioxidant enzymes activities increased. It may be concluded that mycorrhizal inoculation notably influenced shoot nutrients uptake and leaves antioxidant enzymes activities in citrus and an increase in these parameters alleviated water stress.


Main Subjects

Article Title [Persian]

اثر قارچهای میکوریز آربوسکولار و تنش آبی بر فعالیت برخی آنزیمهای آنتی اکسیدان و جذب عناصر غذای دو پایه مرکبات

Authors [Persian]

  • مهدی زارعی
  • زهرا پیمانه
  • عبدالمجید رونقی
بخش علوم خاک، دانشکده کشاورزی، دانشگاه شیراز، شیراز، ج. ا. ایران.
Abstract [Persian]

چکیده- تنش خشکی از مهمترین فاکتورهای کاهش تولید در کشاورزی است زیرا بر تمام فعالیت‌های گیاه اثر دارد. در این پژوهش گلخانه‌ای اثر تنش خشکی و قارچ گلوموس موسه بر روی رشد، جذب عناصر غذایی و انزیم‌های آنتی اکسیدان دو پایه مرکبات ‌نارنج و رافلمون) در خاک استریل بررسی شد. در این مطالعه از سه فاکتور در قالب طرح کاملاً تصادفی با سه تکرار استفاده شد. فاکتور‌ها شامل سه سطح تنش خشکی (‌دور های آبیاری 2، 4، 6 و 8 روز)، میکوریز در 2 سطح ( تلقیح قارچ گلوموس موسه و شاهد) و دوپایه مرکبات ( نارنج و رافلمون) بودند. دانهال‌های میکوریزی دو پایه مرکبات به خوبی توسط قارچ گلوموس موسه کلنیزه شده بودند. با افزایش سطح تنش خشکی درصد کلنیزاسیون ریشه، عملکرد ماده خشک اندام هوایی، جذب نیتروژن، فسفر، منگنز، مس و آهن در اندام هوایی دو پایه مرکبات به طور معنی‌داری کاهش ولی جذب روی اندام هوایی و فعالیت آنزیم‌های آنتی اکسیدان ‌سوپراکسید دسموتاز، کاتالاز، گلوتاتیون پراکسیداز و آسکوربیک پراکسیداز) در برگ در هر دو پایه مرکبات افزایش یافت. با تلقیح دو پایه مرکبات با قارچ در مقایسه با گیاهان بدون قارچ عملکرد ماده خشک اندام هوایی، جذب نیتروژن، فسفر و آنزیم‌های آنتی اکسیدان افزایش یافت. ممکن است قارچ های میکوریز آربوسکولار با افزایش جذب عناصر غذایی  در اندام هوایی و فعالیت آنزیم‌های آنتی اکسیدان برگ  مرکبات اثرات تنش خشکی را تعدیل نماید.

Keywords [Persian]

  • واژه های کلیدی:
  • مرکبات
  • جذب عناصر غذایی
  • آنزیم‌های آنتی اکسیدان
  • تنش آبی
  • گلوموس موسه
Abedi, T., & Pakniyat, H. (2010). Antioxidant enzyme changes in response to drought stress in ten cultivars of oilseed rape (Brassica napus L.). Czech Journal of Genetics and Plant Breeding, 46(1), 27–34.
Alguacil, M.M., Hernandez, J. A., Caravaea, F., Portillo, B., & Roldan, A. (2003). Antioxidant enzyme activities in shoots from three mycorrhizal shrub species afforested in a degraded semi-arid soil. Physiologia Plantarum, 118, 562–570.
Aliasgharzadeh, N., SalehRastin, N., Towfighi, H., & Alizadeh, A. (2001). Occurrence of arbuscular mycorrhizal fungi in saline soils of the Tabriz Plain of Iran in relation to some physical and chemical properties of soil. Mycorrhiza, 11 (3), 119-122.
AlKhaliel, A.S. (2010). Effects of arbuscular mycorrhization in sterile and non-sterile soils. Tropical Life Sciences Research, 21(1), 55–70.
Amiri, M.J., & Eslamian, S.S. (2010). Investigation of climate change in Iran. Journal of Environmental Science and Technology, 3(4), 208-216.
Arora, A., Sairam, R.K., & Srivastava, G.C. (2001). Oxidative stress and antioxidative system in plants. Current science, 82 (10), 1227–1238
Asada, K. (1999). The water–water cycle in chloroplasts: scavenging of active oxygen and dissipation of excess photons. Annual Review of Plant Physiology and Plant Molecular Biology, 50, 601–39.
Augé, R.M. (2001). Water relations, drought and VA mycorrhizal symbiosis. Mycorrhiza, 11, 3–42.
Bates, L.W., Waldern, R., & Tearal, P. (1973). Rapid determination of free proline for salt water stress studies. Plant and Soil, 39, 205-207.
Beauchamcp, C., & Fridovich, I. (1971). Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Analytical Biochemistry, 44, 276-287.
Bor, M., Ozdemir, F., & Turkan, I. (2003). The effect of salt stress on lipid peroxidation and antioxidants inleaves of sugar beet Beta vulgaris L. and wild beet Beta maritima L. Plant Science, 164, 77–84.
Bradford, M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principles of protein dye binding. Analytical Biochemistry, 72, 248-245.
Bremner, J.M. (1965). Total nitrogen. In: C.A. Black et al (ed). Methods of Soil Analysis. Part 2. Agronomy 9:1149-1178. American Society of Agronomy, Inc. Madison, Wisconsin, USA.
Chance, B., & Maehly, A.C. (1955). Assay of catalase and peroxidase. Methods in Enzymology, 2, 764-775.
Chapman,  H.D. (1965). Cation exchange capacity. In: Black, C.A.,Evans, D.D.,Ensminger, L.E.,White, J.L., & Clark, F.E. (ed).  Methods of soil analysis part 2. Chemical and microbiological properties. Monogr. 9. 2nd Edition. Agron. Monogr. 9. ASA and SSSA, Madison, WI.
Chapman, H.D., & Pratt, D.F. (1961). Methods of analysis of soil, plant and water. University California Division Agricultural Science.
Cottenie, A. (1980). Soil and plant testing as a basis of fertilizer recommendation. FAO Soils Bulletin, no. 38/2. Rome: FAO, Land and Water Development Division.
Daniels, B.A., & Trappe, J.M. (1980). Factors affecting spore germination of the vesicular-arbuscular mycorrhizal fungus, Glomus epigaeus. Mycologia, 72, 457-471.
Dhindsa, R.S., PlumbDhindsa, P., & Thorpe, T.A. (1981). Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation and deceased levels of superoxide desmutase and catalase. Journal of Experimental Botany, 32, 93-101.
Gaber Gomaa, S., OsamaKansowa, A., & HossamSaad, E. (2010). Effects of various chemical agents for alleviation of drought stress in rice plants (Oryza sativa L.). Notulae Botanicae Horti Agrobotanici Cluj, 38(1), 139-148
GianinazziPearson, V., Branzanti, B., & Gianinazzi, S. (1989). In vitro enhancement of spore germination and early hyphal growth of a vesicular-arbuscular mycorrhizal fungus by host root exudates and plant flavonoids. Symbiosis, 7, 243-255.
Gupta, S., & Gupta, N.K. (2005). High temperature induced antioxidative defense mechanism in contrasting wheat seedlings. Indian Journal of Plant Physiology, 10, 73-75.
Hassan, S., & Mathesius, U. (2012). The role of flavonoids in root–rhizosphere signalling: opportunities and challenges for improving plant–microbe interactions. Journal of Experimental Botany, 63(9), 3429–3444.
Helal, R.M., & Samir, M.A.A. (2008). Comparative response of drought tolerant and drought sensitive maize genotypes to water stress. Australian Journal of Crop Science, 1(1), 31-36.
Kariman, K., Goltapeh, E.M., & Minassian, V. (2005). Arbuscular mycorrhizal fungi from Iran. Journal of Agricultural Technology, 1 (2), 301-313.
Klute, A. (1986). Water retention: Laboratory methods. p. 635–662. In: A. Klute (ed.) Methods of soil analysis. Part 1. Physical and mineralogical methods. 2nd ed. Agron. Monogr. 9. ASA and SSSA, Madison, WI.
Koo, R.C.J. (1980). Results of citrus fertigation studies. Proceedings of the Florida State. Horticultural Society, 93, 33-36. 
Kormanik, P.P., & McGraw, A.C. (1982). Quantification of vesicular-arbuscular mycorrhizae in plant root. In: Methods and principles of mycorrhizal reseach,ed. By N .C. Schenk, The American Phytopathological Society. St.Paul.
Lambais, M.R., RiosRuiz, W.E., & Andrade, R.M. (2003). Antioxidant responses in bean (Phaseolus vulgaris) roots colonized by arbuscular mycorrhizal fungi. New Phytologist,160, 421-428.
Lindsay, W.L., & Norvell, W.A. (1978). Development of a DTPA soil test for zinc, iron, manganese, and copper. Soil Science Society of American Journal, 42, 241-428.
Marschner, H. (1986). Mineral Nutrition of Higher Plants. 2nd. edition Academic Press, London.
Mousavi S.R, Galavi, M., & Rezaei, M. (2012). The interaction of zinc with other elements in plants: a review. International Journal of Agriculture and Crop Sciences, 4 (24), 1881-1884.
Nahar, K., & Gretzmacher, R. (2002). Effect of water stress on nutrient uptake, yield and quality of tomato (Lycoperscon esculentum Mill.) under subtropical conditions. Die Bodenkultur, 53 (1), 45-51.
Nakano, Y., & Asada, K. (1981). Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplast. Plant Cell Physiology, 22, 867-880.
Neill, S., Desikan, R., Clarke, S., Hurs, A.R., & Hancock, J.T. (2002). Hydrogen peroxide and nitric oxide as signaling molecules in plants. Journal of Experimental Botany, 53, 1237–1247.
Nelson, D.W., & Sommers, L.E. (1996). Total carbon, organic carbon, and organic matter. Methods of Soil Analysis: Part 3.Chemical Methods. Sparks‚ D. L. (Ed.). Soil Science Society of America and American Society of Agronomy. Madison WI.
Nonami, H., & Boyer, J.S. (1990). Wall extensibility and cell wall hydraulic conductivity decrease in enlarging stem tissues at low water potentials. Plant Physiology, 93, 1601–1609.
Olsen, S.R., Cole, C.V.,Watanabe, F.S., & Dean, L.A. (1954). Estimation of available phosphorus in soils by extraction with sodium bicarbonate. U.S. Dep. of Agric. Circ.
Rhoades‚ J.D. (1996). Salinity: Electrical conductivity and total dissolved solids‚ In: Methods of Soil Analysis‚ Part 3. Chemical Methods. Sparks‚ D. L. (Ed.). Soil Science Society of America and American Society of Agronomy. Madison WI.
Roldán, A., DíazVivancos, P., Herníndez, J.A., Carrasco, L., & Caravaca, F. (2008). Superoxide dismutase and total peroxidase activities in relation to drought recovery performance of mycorrhizal shrub seedlings grown in an amended semiarid soil. Journal of Plant Physiology, 165, 715–722.
Saab, I.N., Sharp, R.E., Pritchard, J., & Voetberg, G.S. (1990). Increased endogenous abscisic acid maintains primary root growth and inhibits shoot growth of maize seedlings at low water potentials. Journal of Plant Physiology, 93, 1329-1336.
Safir, G.R., Boyer, J.S., & Gerdemann, J.W. (1972). Nutrient status and mycorrhizal enhancement of water transport in soybean. Journal of Plant Physiology, 49, 700–703.
Sairam, R.K., Srivastava, G.C., & Saxena, D.C. (2000). Increased antioxidant activity under elevated temperature: a mechanism of heat stress tolerance in wheat genotypes. Biologia Plantarum, 43, 245-251.
Sangtarash, M.H., Qaderi, M.M., Chinnappa, C.C., & Reid, D.M. (2009). Differential responses of two Stellaria longipes ecotypes to Ultraviolet-B radiation and drought stress Flora-Morphology, Distribution. Flora Morphology Functional Ecology of Plants, 204(8), 593-603.
Scandalios, J.G. (1993). Oxygen stress and superoxide dismutases. Plant Physiology, 101, 7–12.
Schnepf, A., Jones, D., & Roose, T.(2011). Modelling nutrient uptake by individual hyphae of arbuscular mycorrhizal fungi: temporal and spatial scales for an experimental design. Bulletin of Mathematical Biology, 73, 2175-2200.
Sepaskhah, A.R., & Yarami, N. (2009). Interaction effects of irrigation regime and salinity on flower yield and growth of saffron. The Journal of Horticultural Science and Biotechnology, 84(2), 216-222.
Singh, N.B., Singh, D., & Singh, A. (2009). Modification of physiological responses of water stressed Zea mays seedlings by leachate of Nicotiana plumbaginifolia. General and Applied Plant Physiology, 35(1,2), 51–63.
Syvertsen, J.P. (1985). Integration of water stress in fruit trees. Horticultural Science, 20, 1039-1043.
Thomas, G.W. (1996). Soil pH and soil acidity. In: J. M. Bigham (ed). Methods of soil analysis: Part 3. Chemical methods. Sparks‚ D.L. (Ed.). Soil Science Society of America and American Society of Agronomy. Madison WI.
Tommerup, I.C. (1984). Effect of soil water potential on spore germination by vesicular-arbuscular mycorrhizal fungi. Transactions of the British Mycological Society, 83(2), 193-202.
Wu, Q.R., & Xia, 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.
Wu, Q.S., & Zou, Y.N. (2009a). Mycorrhiza has a direct effect on reactive oxygen metabolism of drought-stressed citrus plant. Soil and Environment, 55 (10), 436–442.
Wu, Q.S., & Zou, Y.N. (2009b). Mycorrhizal influence on nutrient uptake of citrus exposed to drought stress. The Philippine Agricultural Scientist, 92(1), 33-38.
Wu, Q.S., Xia, R.X., & 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., Zou, Y.N., Xia, R.X., & Wang, M.Y. (2007). Five Glomus species affect water relations of Citrus tangerine during drought stress. Botanical Studies, 48, 147-154.
Wutscher, H.K. (1989). Alternation of fruit tree nutrition through rootstocks. Horticultural Science, 24, 578- 584.
Zarei, M., König, S., Hempel, S., Nekouei, M.K., Savaghebi, G., & Buscot, F. (2008). Community structure of arbuscular mycorrhizal fungi associated to Veronica rechingeri at the Anguran zinc and lead mining region. Environmental Pollution, 156(3), 1277-1283.