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Piriformospora indica Promotes Growth and Antioxidant Activities of Wheat Plant under Cadmium Stress

Year 2016, Volume: 26 Issue: 3, 333 - 340, 30.09.2016

Abstract

The influence of root endophytic fungus Piriformospora indica on growth, proline content, photosynthetic pigments and activity of antioxidant enzymes in wheat plant under 0.3 mM cadmium stress (Cd) was investigated. Cd exposure significantly reduced stem diameter, leaf area, chlorophyll a, carotenoid contents, activity of catalase (CAT) and ascorbate peroxidase (APX) in control plants, however, it notably increased malondialdehyde (MDA), proline and superoxide dismutase (SOD) activity.Inoculation of P. indica significantly increased the plant growth parameters, all photosynthetic pigments and proline contents. Also, the activity of CAT, APX and glutathione reductase (GR) were positivity influenced by fungus treatment. Under the stress, Cd contents markedly increased in stem and root organs (particularly at roots) but its accumulation was significantly decreased at both organs by P. indica. Our results suggest that the increased concentrations of antioxidant enzymes, and pigments and proline contents found in P. indica-inoculated plants may serve to protect wheat plants against oxidative damage, enhancing Cd tolerance.

References

  • Aebi H (1984) Catalase in vitro. Method of Enzymology. 105: 121-126.
  • Andrade SAL, Gratão PL, Silveira APD, Schiavinato MA, Azevedo RA, Mazzafera P (2009) Zn uptake, physiological response and stress attenuation in mycorrhizal jack bean growing in soil with increasing Zn concentrations. Chemosphere. 75: 1363–1370.
  • Andresen E, Küpper H (2013) Cadmium toxicity in plants. In Cadmium: From Toxicity to Essentiality (pp. 395-413). Springer Netherlands.
  • Baltruschat H, Fodor J, Harrach BD, Niemczyk E, Barna B, Gullner G (2008) Salt tolerance of barley induced by the root endophyte Piriformospora indica is associated with a strong increase in antioxidants. New Phytol. 180: 501–10.
  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil. 39: 205-207.
  • Bradford MM (1976) A rapid and sensitive method for the quantization of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochm. 72: 248-254.
  • Chen X, Wang J, Shi Y, Zhao MQ, Chi GY (2011) Effects of cadmium on growth and photosynthetic activities in pakchoi and mustard. Botanical studies. 52: 41-46.
  • Choudhury S, Panda P, Sahoo L, Panda S K (2013) Reactive oxygen species signaling in plants under abiotic stress. Plant signaling & behavior. 8(4): e23681.
  • Del Rio D, Stewart AJ, Pellegrini N (2005) A review of recent studies on malondialdehyde as toxic molecule and biological marker of oxidative stress. Nutr. Metabol. Cardiovasc. Dis. 15: 316–28.
  • Deshmukh S, Huckelhoven R, Schafer P, Imani J, Sharma M, Weiss M, Waller F, Kogel K (2006) The root endophytic fungus Piriformospora indica requires host cell death for proliferation during mutualistic symbiosis with barley. Proc. Nat. Acad. Sci. 103: 18450–18457.
  • Dias MC, Monteiro C, Moutinho-Pereira J, Correia C, Gonçalves B, Santos C (2013) Cadmium toxicity affects photosynthesis and plant growth at different levels. Acta physiologiae plantarum. 35: 1281-1289.
  • Esfandiari E, Shekari F, Esfandiari M (2007) The effect of water stress on the antioxidant content, protective enzyme activities, proline content and lipid peroxidation in wheat seedling. Not. Bot. Hort. Agro. Bot. 35: 48-56.
  • Fariduddin Q, Yusuf M, Hayat S, Ahmad A (2009) Effect of 28-homobrassinolide on antioxidant capacity and photosynthesis in Brassica juncea plants exposed to different levels of copper. Environ. Exp. Bot. 66: 418–424.
  • Gara LD, de Pinto MC and Tommasi F (2003) The antioxidant systems vis-a `vis reactive oxygen species during plant-pathogen interaction. Plant Physiol. Biochem. 41: 863–70.
  • Garnier L, Francoise SP, Thuleau P, Agnel JP, Blein JP, Ranjeva R, Montillet JL (2006) Cadmium affects tobacco cells by a series of three waves of reactive oxygen species that contribute to cytotoxicity. Plant Cell Environ. 29 1956–1969.
  • Guo B, Liang Y, Zhu Y (2009) Does salicylic acid regulate antioxidant defense system, cell death, cadmium uptake and partitioning to acquire cadmium tolerance in rice? J. Plant Physiol. 166: 20–31.
  • Islam MM, Hoque A, Okuma E, Banu NA, Shimoishi Y, Nakumura Y, Murata Y (2009) Exogenous proline and glycinebetaine increase antioxidant enzyme activities and confer tolerance to cadmium stress in cultured tobacco cells. J. Plant Physiol. 166: 1587-1597.
  • Jiang HM, Yang JC, Zhang JF (2007) Effects of external phosphorus on the ultrastructure and the chlorophyll content of maize under cadmium and zinc stress. Environ. Pollution 147: 750-756.
  • Kataria S, Baghel L, Dubey A, Sahu S, Aanam S (2015) Effect of cadmium on growth, nitrogen metabolism, photosynthesis and yield of soybean. International Journal of Tropical Agriculture. 33: 993-1001.
  • Kumar K, Yadav V, Tuteja N, Johri AK (2009) Antioxidant enzyme activities in maize plants colonized with Piriformospora indica. Microbiology. 155: 780-790.
  • Lopez-Millan AF, Sagardoy R, Solanas M, Abadia A, Abadia J (2009) Cadmium toxicity in tomato (Lycopersicon esculentum) plants grown in hydroponics. Environ. Exp. Botany. 65: 376-385.
  • Mandyam K, Jumpponen A (2014) Unraveling the dark septate endophyte functions: insights from the Arabidopsis model. In Advances in Endophytic Research (pp. 115-141). Springer India.
  • Mori S, Uraguchi S, Ishakawa S, Arao T (2009) Xylem loading process is a critical factor in determining Cd accumulation in the shoots of Solanum melongena and Solanum torvum. Environ. Exp. Botany. 67: 127-132.
  • Murphy B R, Doohan FM, Hodkinson TR (2014) Yield increase induced by the fungal root endophyte Piriformospora indica in barley grown at low temperature is nutrient limited. Symbiosis. 62: 29-39.
  • Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49: 249–79.
  • Oelmüller R, Sherameti I, Tripathi S, Varma A (2009) Piriformospora indica, a cultivable root endophyte with multiple biotechnological applications. Symbiosis. 19: 1–19.
  • Pan J, Plant JA, Voulvoulis N, Oates CJ, Ihlenfeld C (2010) Cadmium levels in Europe: implications for human health. Environmental geochemistry and health. 32: 1-12.
  • Philips J, Hayman DS (1970) Improved procedure for cleaning roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans. Br. Mycol. Soc. 55: 158–61.
  • Popova LP, Maslenkova LT, Yordanova RY, Ivanova AP, Krantev AP, Szalai G (2009) Exogenous treatment with salicylic acid attenuates cadmium toxicity in pea seedlings. Plant Physiol. Biochem. 47: 224–31.
  • Pozo MJ, López‐Ráez JA, Azcón‐Aguilar C, García‐Garrido JM (2015) Phytohormones as integrators of environmental signals in the regulation of mycorrhizal symbioses. New Phytologist. 205: 1431-1436.
  • Saha J, Brauer EK, Sengupta A, Popescu SC, Gupta K, Gupta B (2015) Polyamines as redox homeostasis regulators during salt stress in plants. Frontiers in Environmental Science 3: 21.
  • Sairam RK, Rao KV, Srivastava GC (2002) Differential response of wheat genotypes to long term salinity stress in relation to oxidative stress, antioxidant activity and osmolyte concentration. Plant Sci. 163: 1037-1046.
  • Sen Gupta A, Webb RP, Holaday AS and Allen RD (1993) Overexpression of superoxide dismutase protects plants from oxidative stress. Plant Physiol. 103: 1067-1073.
  • Sharma S, Singh B, Manchanda VK (2015) Phytoremediation: role of terrestrial plants and aquatic macrophytes in the remediation of radionuclides and heavy metal contaminated soil and water. Environmental Science and Pollution Research. 22: 946-962.
  • Sherameti I, Shahollari B, Venus Y, Altschmied L, Varma A, Oelmuller R (2005) The endophytic fungus Piriformospora indica stimulates the expression of nitrate reductase and the starch-degrading enzyme glucan-water dikinase in tobacco and Arabidopsis roots through a homeodomain transcription factor that binds to a conserved motif in their promoters. J. Biol. Chem. 280: 26241–26247.
  • Shi G, Cai Q (2009) Leaf plasticity in peanut in response to heavy metal stress. Environ. Exp. Botany. 67: 112-117.
  • Shrivastava S, Varma A (2014) From Piriformospora indica to Rootonic: A review. African Journal of Microbiology Research. 32: 2984-2992.
  • Sirrenberg ACG, Stephanie G, Czempinski N, Karlovsky ARP, Santos P, Katharina IF. 2007. Piriformospora indica affects plant growth by auxin production. Physiologia Plantarum. 131: 581–589.
  • Smeets K, Ruytinx J, Semane B, Belleghem FV, Remans, T, Sanden SV, Vangronsveld J, Cuypers A (2008) Cadmium-induced transcriptional and enzymatic alterations related to oxidative stress. Environ. Exp. Botany. 63: 1-8.
  • Stewart RRC and Bewley JD. 1980. Lipid peroxidation associated aging of soybean axes. Plant Physiol. 65: 245-248.
  • Sun C, Johnson JM, Cai D, Sherameti I, Oelmüller R, Lou B (2010) Piriformospora indica confers drought tolerance in Chinese cabbage leaves by stimulating antioxidant enzymes, the expression of drought-related genes and the plastid-localized CAS protein. J. Plant Physiol. 167: 1009-1017.
  • Thapar R, Srivastava AK, Bhargava P, Mishra Y, Rai LC (2008) Impact of different abiotic stress on growth, photosynthetic electron transport chain, nutrient uptake and enzyme activities of Cu-acclimated Anabaena doliolum. J. Plant Physiol. 165: 306-316.
  • Tuan A, Popova LP (2013) Functions and toxicity of cadmium in plants: recent advances and future prospects. Turkish Journal of Botany. 37: 1-13.
  • Ueno D, Iwashita T, Zhao FJ, Ma JF. 2008. Characterization of Cd translocation and identification of the Cd form in xylem sap of the Cd-hyperaccumulator Arabidopsis halleri. Plant Cell Physiol. 49: 540–548.
  • Vadassery J, Ritter C, Venus Y, Camehl I, Varma A, Shahollari B, Novák O, Strnad M, Ludwig-Müller J, Oelmüller R (2008) The role of Auxins and Cytokinins in the mutualistic interaction between Arabidopsis and Piriformospora indica. Mol. Plant-Microbe Interact. 21: 1371–1383.
  • Vadassery J, Tripathi S, Prasad R, Varma A, Oelmüller R (2009) Monodehydroascorbate reductase 2 and dehydroascorbate reductase 5 are crucial for a mutualistic interaction between Piriformospora indica and Arabidopsis. J. Plant Physiol. 166: 1263–74.
  • Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M (2005) The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc. Natl. Acad. Sci. USA. 102: 86–91
  • Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J. Plant Physiol. 144: 307–313.
  • Weyens N, Van der Lelie D, Taghavi S, Vangronsveld J (2009) Phytoremediation: plant–endophyte partnerships take the challenge. Curr. Opin. Biotechnol. 20: 248–254.
  • Xu J, Yin HX, Li X (2009) Protective effects of proline against cadmium toxicity in micropropagated hyperaccumulator, Solanum nigrum L. Plant Cell Rep. 28: 325–33.
  • Yan Z, Li X, Chen J, Tam NFY (2015) Combined toxicity of cadmium and copper in Avicennia marina seedlings and the regulation of exogenous jasmonic acid. Ecotoxicology and environmental safety. 113: 124-132.
  • Ye W, Shen CH, Lin Y, Chen PJ, Xu X, Oelmüller R, Lai Z (2014) Growth promotion-related miRNAs in Oncidium orchid roots colonized by the endophytic fungus Piriformospora indica. Plos one. 9: e84920.
  • Yoshimura K, Yabute Y, Ishikawa T, Shigeoka S (2000) Expression of spinach ascorbate peroxidase isoenzymes in response to oxidative stresses. Plant Physiol. 123: 223-233.
  • Zhao FJ, Mc Grath SP and Crosland AR (1994) Comparison of three wet digestion methods for the determination of plant sulphur by inductively coupled plasma atomic emission spectroscopy (ICP AES). Commun. Soil Sci. Plant 25: 407–418.

Piriformospora indica’nın Kadmiyum Stresi altındaki Buğday Bitkisinin Büyüme ve Antioksidan Etkinliklerini Teşviki

Year 2016, Volume: 26 Issue: 3, 333 - 340, 30.09.2016

Abstract

Bir kök endofitik fungusu olan Piriformospora indica’nın 0.3 mM kadmiyum (Cd) stresi altındaki buğday bitkisinin büyüme, prolin içeriği, fotosentetik pigmentler ve antioksidan enzim aktiviteleri üzerindeki etkisi araştırılmıştır. Cd’ye maruz bırakılma, kontrol bitkilerinde önemli ölçüde gövde çapı, yaprak alanı, klorofil a, karotenoid içeriği, katalaz (CAT) ve askorbat peroksidaz (APX) aktivitesini azaltmış; bununla birlikte, özellikle de malondialdehit (MDA), prolin ve süperoksit dismutaz (SOD) aktivitelerini de artırmıştır. P. indica inokülasyonu, önemli ölçüde bitki büyüme parametreleri, tüm fotosentetik pigmentleri ve prolin içeriğini artmıştır. Ayrıca, KAT APX ve glutatyon redüktaz (GR) aktiviteleri de fungus uygulamasında pozitif şekilde etkilenmişlerdir. Stres altında Cd içerikleri, belirgin bir şekilde kök ve kök organlarda artmış (özellikle köklerde), ancak Her iki organda da Cd birikimi, P. indica tarafından önemli ölçüde azaltılmıştır. Elde edilen sonuçlar, P. indica-inoküle edilmiş bitkilerde bulunan antioksidan enzimler, pigmentler ve prolin içeriklerinin artan konsantrasyonlarının Cd toleransının güçlendirilmesinde, oksidatif hasara karşı buğday bitkileri korumak için hizmet edebileceğini düşündürmektedir.

References

  • Aebi H (1984) Catalase in vitro. Method of Enzymology. 105: 121-126.
  • Andrade SAL, Gratão PL, Silveira APD, Schiavinato MA, Azevedo RA, Mazzafera P (2009) Zn uptake, physiological response and stress attenuation in mycorrhizal jack bean growing in soil with increasing Zn concentrations. Chemosphere. 75: 1363–1370.
  • Andresen E, Küpper H (2013) Cadmium toxicity in plants. In Cadmium: From Toxicity to Essentiality (pp. 395-413). Springer Netherlands.
  • Baltruschat H, Fodor J, Harrach BD, Niemczyk E, Barna B, Gullner G (2008) Salt tolerance of barley induced by the root endophyte Piriformospora indica is associated with a strong increase in antioxidants. New Phytol. 180: 501–10.
  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil. 39: 205-207.
  • Bradford MM (1976) A rapid and sensitive method for the quantization of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochm. 72: 248-254.
  • Chen X, Wang J, Shi Y, Zhao MQ, Chi GY (2011) Effects of cadmium on growth and photosynthetic activities in pakchoi and mustard. Botanical studies. 52: 41-46.
  • Choudhury S, Panda P, Sahoo L, Panda S K (2013) Reactive oxygen species signaling in plants under abiotic stress. Plant signaling & behavior. 8(4): e23681.
  • Del Rio D, Stewart AJ, Pellegrini N (2005) A review of recent studies on malondialdehyde as toxic molecule and biological marker of oxidative stress. Nutr. Metabol. Cardiovasc. Dis. 15: 316–28.
  • Deshmukh S, Huckelhoven R, Schafer P, Imani J, Sharma M, Weiss M, Waller F, Kogel K (2006) The root endophytic fungus Piriformospora indica requires host cell death for proliferation during mutualistic symbiosis with barley. Proc. Nat. Acad. Sci. 103: 18450–18457.
  • Dias MC, Monteiro C, Moutinho-Pereira J, Correia C, Gonçalves B, Santos C (2013) Cadmium toxicity affects photosynthesis and plant growth at different levels. Acta physiologiae plantarum. 35: 1281-1289.
  • Esfandiari E, Shekari F, Esfandiari M (2007) The effect of water stress on the antioxidant content, protective enzyme activities, proline content and lipid peroxidation in wheat seedling. Not. Bot. Hort. Agro. Bot. 35: 48-56.
  • Fariduddin Q, Yusuf M, Hayat S, Ahmad A (2009) Effect of 28-homobrassinolide on antioxidant capacity and photosynthesis in Brassica juncea plants exposed to different levels of copper. Environ. Exp. Bot. 66: 418–424.
  • Gara LD, de Pinto MC and Tommasi F (2003) The antioxidant systems vis-a `vis reactive oxygen species during plant-pathogen interaction. Plant Physiol. Biochem. 41: 863–70.
  • Garnier L, Francoise SP, Thuleau P, Agnel JP, Blein JP, Ranjeva R, Montillet JL (2006) Cadmium affects tobacco cells by a series of three waves of reactive oxygen species that contribute to cytotoxicity. Plant Cell Environ. 29 1956–1969.
  • Guo B, Liang Y, Zhu Y (2009) Does salicylic acid regulate antioxidant defense system, cell death, cadmium uptake and partitioning to acquire cadmium tolerance in rice? J. Plant Physiol. 166: 20–31.
  • Islam MM, Hoque A, Okuma E, Banu NA, Shimoishi Y, Nakumura Y, Murata Y (2009) Exogenous proline and glycinebetaine increase antioxidant enzyme activities and confer tolerance to cadmium stress in cultured tobacco cells. J. Plant Physiol. 166: 1587-1597.
  • Jiang HM, Yang JC, Zhang JF (2007) Effects of external phosphorus on the ultrastructure and the chlorophyll content of maize under cadmium and zinc stress. Environ. Pollution 147: 750-756.
  • Kataria S, Baghel L, Dubey A, Sahu S, Aanam S (2015) Effect of cadmium on growth, nitrogen metabolism, photosynthesis and yield of soybean. International Journal of Tropical Agriculture. 33: 993-1001.
  • Kumar K, Yadav V, Tuteja N, Johri AK (2009) Antioxidant enzyme activities in maize plants colonized with Piriformospora indica. Microbiology. 155: 780-790.
  • Lopez-Millan AF, Sagardoy R, Solanas M, Abadia A, Abadia J (2009) Cadmium toxicity in tomato (Lycopersicon esculentum) plants grown in hydroponics. Environ. Exp. Botany. 65: 376-385.
  • Mandyam K, Jumpponen A (2014) Unraveling the dark septate endophyte functions: insights from the Arabidopsis model. In Advances in Endophytic Research (pp. 115-141). Springer India.
  • Mori S, Uraguchi S, Ishakawa S, Arao T (2009) Xylem loading process is a critical factor in determining Cd accumulation in the shoots of Solanum melongena and Solanum torvum. Environ. Exp. Botany. 67: 127-132.
  • Murphy B R, Doohan FM, Hodkinson TR (2014) Yield increase induced by the fungal root endophyte Piriformospora indica in barley grown at low temperature is nutrient limited. Symbiosis. 62: 29-39.
  • Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49: 249–79.
  • Oelmüller R, Sherameti I, Tripathi S, Varma A (2009) Piriformospora indica, a cultivable root endophyte with multiple biotechnological applications. Symbiosis. 19: 1–19.
  • Pan J, Plant JA, Voulvoulis N, Oates CJ, Ihlenfeld C (2010) Cadmium levels in Europe: implications for human health. Environmental geochemistry and health. 32: 1-12.
  • Philips J, Hayman DS (1970) Improved procedure for cleaning roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans. Br. Mycol. Soc. 55: 158–61.
  • Popova LP, Maslenkova LT, Yordanova RY, Ivanova AP, Krantev AP, Szalai G (2009) Exogenous treatment with salicylic acid attenuates cadmium toxicity in pea seedlings. Plant Physiol. Biochem. 47: 224–31.
  • Pozo MJ, López‐Ráez JA, Azcón‐Aguilar C, García‐Garrido JM (2015) Phytohormones as integrators of environmental signals in the regulation of mycorrhizal symbioses. New Phytologist. 205: 1431-1436.
  • Saha J, Brauer EK, Sengupta A, Popescu SC, Gupta K, Gupta B (2015) Polyamines as redox homeostasis regulators during salt stress in plants. Frontiers in Environmental Science 3: 21.
  • Sairam RK, Rao KV, Srivastava GC (2002) Differential response of wheat genotypes to long term salinity stress in relation to oxidative stress, antioxidant activity and osmolyte concentration. Plant Sci. 163: 1037-1046.
  • Sen Gupta A, Webb RP, Holaday AS and Allen RD (1993) Overexpression of superoxide dismutase protects plants from oxidative stress. Plant Physiol. 103: 1067-1073.
  • Sharma S, Singh B, Manchanda VK (2015) Phytoremediation: role of terrestrial plants and aquatic macrophytes in the remediation of radionuclides and heavy metal contaminated soil and water. Environmental Science and Pollution Research. 22: 946-962.
  • Sherameti I, Shahollari B, Venus Y, Altschmied L, Varma A, Oelmuller R (2005) The endophytic fungus Piriformospora indica stimulates the expression of nitrate reductase and the starch-degrading enzyme glucan-water dikinase in tobacco and Arabidopsis roots through a homeodomain transcription factor that binds to a conserved motif in their promoters. J. Biol. Chem. 280: 26241–26247.
  • Shi G, Cai Q (2009) Leaf plasticity in peanut in response to heavy metal stress. Environ. Exp. Botany. 67: 112-117.
  • Shrivastava S, Varma A (2014) From Piriformospora indica to Rootonic: A review. African Journal of Microbiology Research. 32: 2984-2992.
  • Sirrenberg ACG, Stephanie G, Czempinski N, Karlovsky ARP, Santos P, Katharina IF. 2007. Piriformospora indica affects plant growth by auxin production. Physiologia Plantarum. 131: 581–589.
  • Smeets K, Ruytinx J, Semane B, Belleghem FV, Remans, T, Sanden SV, Vangronsveld J, Cuypers A (2008) Cadmium-induced transcriptional and enzymatic alterations related to oxidative stress. Environ. Exp. Botany. 63: 1-8.
  • Stewart RRC and Bewley JD. 1980. Lipid peroxidation associated aging of soybean axes. Plant Physiol. 65: 245-248.
  • Sun C, Johnson JM, Cai D, Sherameti I, Oelmüller R, Lou B (2010) Piriformospora indica confers drought tolerance in Chinese cabbage leaves by stimulating antioxidant enzymes, the expression of drought-related genes and the plastid-localized CAS protein. J. Plant Physiol. 167: 1009-1017.
  • Thapar R, Srivastava AK, Bhargava P, Mishra Y, Rai LC (2008) Impact of different abiotic stress on growth, photosynthetic electron transport chain, nutrient uptake and enzyme activities of Cu-acclimated Anabaena doliolum. J. Plant Physiol. 165: 306-316.
  • Tuan A, Popova LP (2013) Functions and toxicity of cadmium in plants: recent advances and future prospects. Turkish Journal of Botany. 37: 1-13.
  • Ueno D, Iwashita T, Zhao FJ, Ma JF. 2008. Characterization of Cd translocation and identification of the Cd form in xylem sap of the Cd-hyperaccumulator Arabidopsis halleri. Plant Cell Physiol. 49: 540–548.
  • Vadassery J, Ritter C, Venus Y, Camehl I, Varma A, Shahollari B, Novák O, Strnad M, Ludwig-Müller J, Oelmüller R (2008) The role of Auxins and Cytokinins in the mutualistic interaction between Arabidopsis and Piriformospora indica. Mol. Plant-Microbe Interact. 21: 1371–1383.
  • Vadassery J, Tripathi S, Prasad R, Varma A, Oelmüller R (2009) Monodehydroascorbate reductase 2 and dehydroascorbate reductase 5 are crucial for a mutualistic interaction between Piriformospora indica and Arabidopsis. J. Plant Physiol. 166: 1263–74.
  • Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M (2005) The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc. Natl. Acad. Sci. USA. 102: 86–91
  • Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J. Plant Physiol. 144: 307–313.
  • Weyens N, Van der Lelie D, Taghavi S, Vangronsveld J (2009) Phytoremediation: plant–endophyte partnerships take the challenge. Curr. Opin. Biotechnol. 20: 248–254.
  • Xu J, Yin HX, Li X (2009) Protective effects of proline against cadmium toxicity in micropropagated hyperaccumulator, Solanum nigrum L. Plant Cell Rep. 28: 325–33.
  • Yan Z, Li X, Chen J, Tam NFY (2015) Combined toxicity of cadmium and copper in Avicennia marina seedlings and the regulation of exogenous jasmonic acid. Ecotoxicology and environmental safety. 113: 124-132.
  • Ye W, Shen CH, Lin Y, Chen PJ, Xu X, Oelmüller R, Lai Z (2014) Growth promotion-related miRNAs in Oncidium orchid roots colonized by the endophytic fungus Piriformospora indica. Plos one. 9: e84920.
  • Yoshimura K, Yabute Y, Ishikawa T, Shigeoka S (2000) Expression of spinach ascorbate peroxidase isoenzymes in response to oxidative stresses. Plant Physiol. 123: 223-233.
  • Zhao FJ, Mc Grath SP and Crosland AR (1994) Comparison of three wet digestion methods for the determination of plant sulphur by inductively coupled plasma atomic emission spectroscopy (ICP AES). Commun. Soil Sci. Plant 25: 407–418.
There are 54 citations in total.

Details

Journal Section Articles
Authors

Ali Asghar Aliloo

Saleh Shahabıvand This is me

Publication Date September 30, 2016
Published in Issue Year 2016 Volume: 26 Issue: 3

Cite

APA Aliloo, A. A., & Shahabıvand, S. (2016). Piriformospora indica Promotes Growth and Antioxidant Activities of Wheat Plant under Cadmium Stress. Yuzuncu Yıl University Journal of Agricultural Sciences, 26(3), 333-340.
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