Abstract
Piriformospora indica, a root endophytic fungus, has been reported to promote growth of many plants under normal condition and allow the plants to survive under stress conditions. However, its impact on an important medicinal plant Aloe vera L. has not been well studied. Therefore, this study was undertaken to investigate the effect of P. indica on salinity stress tolerance of A. vera plant. P. indica inoculated and non-inoculated A. vera plantlets were subjected to four levels of salinity treatment- 0, 100, 200 and 300 mM NaCl. The salinity stress decreased the ability of the fungus to colonize roots of A. vera but the interaction of A. vera with P. indica resulted in an overall increase in plant biomass and greater shoot and root length as well as number of shoots and roots. The photosynthetic pigment (Chl a, Chl b and total Chl) and gel content were significantly higher for the fungus inoculated A. vera plantlets, at respective salinity concentrations. Furthermore, the inoculated plantlets had higher phenol, flavonoid, flavonol, aloin contents and radical scavenging activity at all salinity concentrations. The higher phenolic and flavonoid content may help the plants ameliorate oxidative stress resulting from high salinity.
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Abbreviations
- HPLC:
-
High Performance Liquid Chromatography
- DPPH:
-
1,1-diphenyl-2-picryl hydrazyl
- NaCl:
-
Sodium Chloride
- BSA:
-
Bovine serum albumin
- TFA:
-
Trifluoroacetic acid
- MQ:
-
Milli Q
- UV:
-
Ultraviolet
- MS:
-
Murashige and Skoog
- MAT:
-
Months after treatment
References
Akram NA, Ashraf M (2011) Improvement in growth, chlorophyll pigments and photosynthetic performance in salt-stressed plants of sunflower (Helianthus annuus L.) by foliar application of 5-aminolevulinic acid. Agrochimica 55:94–104
Ammar NM, Singab ANB, Ahmady SH, Anssary AA, Haggag EG, Shabban RS (2010) Phytochemical and biological studies of some polysaccharides isolated from Aloe, Tamarindus, Opuntia and citrus. JASMR 5:141–152
Arnon DI (1949) A copper enzyme is isolated chloroplast polyphenol oxidase in Beta vulgaries. Plant Physiol 24:1–15
Ashraf M, Harris PJC (2004) Potential biochemical indicators of salinity tolerance in plants. Plant Sci 166:3–16
Ashraf M, Harris PJC (2013) Photosynthesis under stressful environments: An overview. Photosynthetica 51:163–190
Ashwell G (1957) Colorimetric analysis of sugars. Methods Enzymol 3:73–105
Bagde US, Prasad R, Varma A (2010) Interaction of mycobiont: Piriformospora indica with medicinal plants and plants of economic importance. Afr J Biotechnol 9:9214–9226
Bajaj R, Agarwal A, Rajpal K, Asthana S, Prasad R, Kharkwal AC, Kumar R, Sherameti I, Oelmüller R, Varma A (2014) Co-cultivation of Curcuma longa with Piriformospora indica enhances the yield and active ingredients. Am J Curr Microbiol 2:6–17
Baltruschat H, Fodor J, Borbála D, Harrach NE, Barna B, Gullner G, Janeczko A, Kogel KH, Schäfer P, Schwarczinger I, Zuccaro A, Skoczowski A (2008) Salt tolerance of barley induced by the root endophyte Piriformospora indica is associated with a strong increase in antioxidants. New Phytol 180:501–510
Bheemareddy VS, Byatanal MB, Lakshman Libyan HC (2010) Effect of salt and acid stress on Triticum aestivum L. Var. inoculated with Glomus fasciculatum. Int J Agric Res 1:325–331
Bhuvana KB, Hema NG, Patil RT (2014) Review on Aloe vera. Int J Adv Res 2:677–691
Bolton MD (2009) Primary metabolism and plant defence fuel for the fire. Mol Plant Microbe In 22:487–497
Chang CC, Yang M, Wen H, Chern J (2002) Estimation of total flavonoid content in Propolis by two complementary colorimetric methods. J Food Drug Anal 10:178–182
Das A, Kamal S, Shakil NA, Sherameti I, Oelmuller R, Dua M, Tuteja N, Johri AK, Varma A (2012) The root endophyte fungus Piriformospora indica leads to early flowering, higher biomass and altered secondary metabolites of the medicinal plant, Coleus forskohlii. Plant Signal Behav 7:103–112
Dong S, Tian Z, Chen PJ, Kumar RS, Shen CH, Cai D, Oelmüller R, Yeh KW (2013) The maturation zone is an important target of Piriformospora indica in Chinese cabbage roots. J Exp Bot 64:4529–4540
Eckardt NA (2009) A new chlorophyll degradation pathway. Plant Cell 21:700
Evelin H, Kapoor R (2014) Arbuscular mycorrhizal symbiosis modulates antioxidant response in salt-stressed Trigonella foenum graecum plants. Mycorrhiza 24:197–208
Fletcher AL, Sinclair TR, Allen LH (2007) Transpiration responses to vapour pressure deficit in well watered ‘slow-wilting’ and commercial soybean. Environ Exp Bot 61:145–151
Franken P (2012) The Plant strengthening root endophyte Piriformospora indica: potential application and the biology behind. Appl Microbiol Biotechnol 96:1455–1464
Gao FK, Dai CC, Liu XZ (2010) Mechanisms of fungal endophytes in plant protection against pathogens-Review. Afr J Microbiol Res 4:1346–1351
Hamman JH (2008) Composition and applications of Aloe vera leaf gel. Mol 13:1599–1616
Hare PD, Cress WA, Staden JV (1998) Dissecting the roles of osmolyte accumulation during stress. Plant Cell Environ 21:535
Harrach BD, Baltruschat H, Barna B, Fodor J, Kogel KH (2013) The Mutualistic Fungus Piriformospora indica protects barley roots from a loss of antioxidant capacity caused by the necrotrophic pathogen Fusarium culmorum. Mol Plant-Microbe Interact 26:599–605
Hill TW, Kaefer E (2001) Improved protocols for Aspergillus medium: trace elements and minimum medium salt stock solution. Fungal Genet News 148:20–21
Jin ZM, Wang CH, Liu ZP, Gong WJ (2007) Physiological and ecological characters studies on Aloe vera under soil salinity and sea water irrigation. Process Biochem 42:710–714
Kapoor R, Giri B, Mukerji KG (2002) Glomus macrocarpum: a potential bioinoculant to improve essential oil quality and concentration in Dill (Anethum graveolens L.) and Carum (Trachyspermum ammi (Linn.) Sprague). World J Microbiol Biotechnol 18:459–463
Kilam D, Saifi M, Abdin MZ, Agnihotri A, Varma A (2015) Combined effects of Piriformospora indica and Azotobacter chroococcum enhance plant growth, antioxidant potential and steviol glycoside content in Stevia rebaudiana. Symbiosis 66:149–156
Kispotta A, Srivastava MK, Dutta M (2012) Free radical scavenging activity of ethanolic extracts and determination of aloin from Aloe vera L. leaf extract. Int J Med Arom Plants 2:612–618
Kumaran A, Karunakaran RJ (2007) In vitro antioxidant activities of methanolic extracts of five phyllanthus species from India. LWT Food Sci Technol 40:344–352
Lee MC, Liao JD, Huang WL, Jiang FY, Jheng YZ, Jin YY, Tseng YS (2014) Aloin-induced cell growth arrest, cell apoptosis, and autophagy in human non-small cell lung cancer cells. Biom Genom Med 6:144–149
McDonald S, Prenzler PD, Autolovich M, Robards K (2001) Phenolic content and antioxidant activity of olive extracts. Food Chem 73:73–84
Nelson N (1944) A photometric adaptation of the Somogyi method for the determination of glucose. J Biol Chem 153:315–380
Oelmuller R, Sherameti I, Tripathi S, Varma A (2009) Piriformospora indica, a cultivable root endophyte with biotechnological applications. Symbiosis 49:1–17
Perveen S, Shahbaz M, Ashraf M (2010) Regulation in gas exchange and quantum yield of photosystem II (PSII) in salt stressed and non-stressed wheat plants raised from seed treated with triacontanol. Pak J Bot 42:3073–3081
Peškan-Berghöfer T, Shahollari B, Giang PH, Hehl S, Markert C, Blanke V, Varma AK, Oelmuller R (2004) Association of Piriformospora indica with Arabidopsis thaliana roots represents a novel system to study beneficial plant microbe interactions and involves early plant protein modifications in the endoplasmic reticulum and at the plasma memberane. Physiol Plant 122:465–477
Pham HG, Singh A, Malla R, Kumari R, Prasad R, Sachdev M, Rexer KH, Kost G, Luis P, Kaldorf M, Buscot F, Herrmann S, Peŝkan T, Oelmüller R, Saxena AK, Declerck S, Mittag M, Stabentheiner E, Hehl S, Varma A (2004) Interaction of Piriformospora indica with diverse microorganisms and plants. In: Varma A, Abbott LK, Werner D, Hampp R (eds) Plant surface microbiology. Springer, Germany, pp. 237–265
Phillips JM, Hayman DS (1970) Improved procedure of clearing roots and staining parasitic and vesicular Arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:159–161
Pinheiro HA, Silva JV, Endres L et al (2008) Leaf gas exchange, chloroplastic pigments and dry matter accumulation in castor bean (Ricinus communis L.) seedlings subjected to salt stress conditions. Ind Crop Prod 27:385–392
Ramachandra CT, Rao PS (2008) Processing of Aloe vera leaf gel: a review. Am J Agric Biol Sci 3:502–510
Rodriguez RJ, Redman RS, Henson J (2004) The role of fungal symbioses in the adaptation of plants to high stress environments. Mitig Adapt Strat Gl 9:261–272
Satheesan J, Narayanan AK, Sakunthala M (2012) Induction of root colonization by Piriformospora indica leads to enhanced asiaticoside production in Centella asiatica. Mycorrhiza 22:195–202
Serfling A, Wirsel SGR, Lind V, Deising HB (2007) Performance of the biocontrol fungus Piriformospora indica on wheat under greenhouse and field conditions. J Phytopathol 97:523–531
Shannon MC (1997) Adaptation of plants to salinity. Adv Agron 60:75–120
Sharma M, Schmid M, Rothballer M, Hause G, Zuccaro A, Imani J, Kampfer P, Domann E, Schäfer P, Hartmann A, Kogel KH (2008) Detection and identification of bacteria intimately associated with fungi of the order Sebacinales. Cell Microbiol 11:2235–2246
Sharma P, Kharkwal AC, Abdin MZ, Varma A (2014a) Piriformospora indica improves micro propagation, growth and phyto chemical content of Aloe vera L. Plants Symbiosis 64:11–23
Sharma P, Kharkwal AC, Kharkwal H, Abdin MZ, Varma A (2014b) A review on pharmacological properties of Aloe vera. Int J Pharm Sci Rev Res 29:31–37
Sharma P, Abdin MZ, Kharkwal AC, Varma A (2015) Salt Stress Alleviation Using Mycorrhizal Fungi- A Short Review. The Botanica 64(65):1–8
Silveira JAG, Viegas RA, Rocha IMA, Moreira ACDM, Moreira RA, Oliveira JTA (2003) Proline accumulation and glutamine synthetase activity are increased by salt-induced proteolysis in cashew leaves. J Plant Physiol 160:115–123
Sirrenberg A, Gobel C, Grond S, Czempinski N, Ratzinger A, Karlovsky P, Santos P, Feussner I, Pawlowski K (2007) Piriformospora indica affects plant growth by auxin production. Physiol Plant 131:581–589
Tarro VE (1993) The honest herbal: A sensible guide to the use of herbs and related remedies 3rd ed., Pharmaceutical Products Press, New York, pp 25–28
Teshome T, Sintayehu B, Yohannes H, Gebrelibanos M, Karim A, Gomathi P, Yarlagadda R (2015) Radical scavenging activity and preliminary phytochemical screening on aerial part extracts of Cineraria abyssinica sch. bip. EXA. J Pharmacogn Phytochem 3:239–243
Toussaint JP, Smith FA, Smith SE (2007) Arbuscular mycorrhizal fungi can induce the production of phytochemicals in sweet basil irrespective of phosphorus nutrition. Mycorrhiza 17:291–297
Varma A, Verma S, Sudha Sahay N, Bütehorn B, Franken P (1999) Piriformospora indica, a cultivable plant-growth-promoting root endophyte. Appl Environ Microbiol 65:2741–2744
Varma A, Sherameti I, Tripathi S, Prasad R, Das A, Sharma M, Bakshi M, Johnson JM, Bhardwaj S, Arora M, Rastogi K, Agrawal A, Kharkwal AC, Talukdar S, Bagde US, Bisaria VS, Upadhyaya CP, Won PS, Chen Y et al (2012a) The Symbiotic Fungus Piriformospora indica: Review. Mycota 9:231–254
Varma A, Sherameti I, Tripathi S, Prasad R, Das A, Sharma M, Bakshi M, Johnson JM, Bhardwaj S, Arora M, Rastogi K, Agrawal A, Kharakwal AC, Talukdar S, Bagde US, Bisaria VS, Upadhyay CP, Won PS, Chen Y, Ma J, Kumar M, Dua M, Lou B, Adya A, Zhong L, Meghvansi MK, Sree KS, Gosal SK, Srivastava RB, Johri AK, Cruz C, Oelmueller R (2012b) The symbiotic fungus Piriformospora indica: review. In: Hock B (ed) The Mycota IX, Fungal Associations, Springer-Verlag, Germany, Chapter, vol 13, pp. 231–254
Varma A, Bajaj R, Agarwal A, Asthana S, Rajpal K, Das A, Prasad R, Kharkwal AC (2013) Memoirs of ‘Rootonic’- the magic fungus. Amity University Press, Noida
Verma S, Varma A, Rexer K, Hassel A, Kost G, Sarbhoy A, Bisen P, Butehorn B, Franken P (1998) Piriformospora indica, gen. et sp. nov., a new root-colonizing fungus. Mycologia 90:896–903
Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M, Heier T, Huckelhoven R, Neumann C, Wettstein DV, Franken P, Kogel KH (2005) The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc Natl Acad Sci 102:13386–13391
Williams WB, Cuvelier M, Berset C (1995) Use of a free radical method to evaluate antioxidant activity. Lebensm Wiss Technol 28:25–30
Xu YJ, Li N, Gu W, Shi PJ, Cui WJ (2006) A study on the technology of sea ice desalination in solid state by freezing and melting through temperature control. J Basic Sci Eng 14:470–477 in Chinese
Yadav V, Kumar M, Deep DK, Kumar H, Sharma R, Tripathi T, Tuteja N, Saxena AK, Johri AK (2010) A phosphate transporter from the root endophytic fungus Piriformospora indica plays a role in phosphate transport to the host plant. J Biol Chem 285:26532–26544
Zarea MJ, Hajinia S, Karimi N, Mohammadi Goltapeh E, Rejali F, Varma A (2011) Effect of Piriformospora indica and Azospirillum strains from saline or non-saline soil on mitigation of the effects of NaCl. Soil Biol Biochem 45:139–146
Acknowledgments
Authors are thankful to Dr. Ashok K Chauhan, Founder President, Ritanand Balved Educational Foundation for support. They are also thankful to Shri. Atul Chauhan, Chancellor, Amity University Uttar Pradesh and Prof. Dr. (Mrs.) Balvinder Shukla, Vice Chancellor, Amity University Uttar Pradesh for their constant support and guidance. PS acknowledge Ministry of Environment and Forest and University Grant Commision, Government of India for financial support.
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Sharma, P., Kharkwal, A.C., Abdin, M.Z. et al. Piriformospora indica-mediated salinity tolerance in Aloe vera plantlets. Symbiosis 72, 103–115 (2017). https://doi.org/10.1007/s13199-016-0449-0
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DOI: https://doi.org/10.1007/s13199-016-0449-0