Document Type : Original Article


1 M.Sc student at Horticulture Faculty of Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran

2 Assisstance Professor at Horticulture Faculty of Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran

3 Assisstance Professor at Plant Protection Faculty of Sari University of Agricultural Sciences and Natural Resources, Sari, Iran


Piriformospora indica, a cultivable root colonizing endophytic fungus of Sebacinales, promotes plant growth and confers resistance against biotic and abiotic stress. The fungus has also the ability to colonize the roots of many varieties of plant species. The goal of present study was to clarify the colonization ability of P.indica in artichoke roots and the respond of plant to water stress. Results showed that Globe artichoke (Cynara scolymus L.) was strongly colonized by the fungus. The fungus retarded the drought-induced malfunctioning in the photosynthetic pigments. Proline, an osmotic signal adjustment was clearly increased during water stress in colonized plants. Total phenol, flavonoid contents, radical scavenging activities, and photosynthetic pigments were influenced by treatments. Based on the obtained results and observations, it can be concluded that P.indica as an elicitor enhances the plant growth efficiency under sever conditions. Thus, P.indica- colonized Cynara scolymus L., provides a good model system to study root-to-shoot communication in secondary metabolites production.


Ali, G.M., Komatsu, S. (2006). Proteomic analysis of rice leaf sheath during drought stress. Journal of proteomic research. 2:396-403.
Arnon, DJ., (1956). Chlorophyll absorption spectrum and quantitative determination. Biochemical and biophysical Acta.20: 449-461.
Ashraf, M., Foolad, MR.,(2007). Roles of Glycine betaine and proline in improving to abiotic plant resistance, Environmental and experimental botany.59: 206-216.
Bagheri, AA., Saadatmand, S., Niknam, V., Nejadsatari, T., Babaeizad, V. (2013). Effect of endophytic fungus, Piriformospora indica on growth and activity of antioxidant enzymes of rice (Oryzae sativa L.) under salinity stress. International journal of advanced biology and biomedical research.11:1337-1350
Bates, LS., Waldron, RP., Teare, I.D. (1973). Rapid determination of free proline for water stress studies. Plant soil. 39:205-208.
Baltruscht, H., Fodor, J., Harrach, BD., Niemczyk, E., Barna, B., Gullner, G., et al.(2008). Salt tolerance of barely induced by the root endophyte Piriformospora indica is associated with a strong increase in antioxidants. New phytol. 180: 501-510.
Barazani, O., Von Dahl, C., Baldwin, IT.(2007). sebacina vermifera promotes the growth at the expense of herbivore and fitness of Nicotiana attenuate by inhibiting ethylene signaling. Plant physiol, 144:1223- 1232.
Bousquet, J., Simon, L., LaLonde, M. (1990). DNA amplificationfrom vegetative and sexual tissues of trees using polymerase chainreaction. Can J Res 20: 254ñ257.
Catchpole WR, Wheeler CJ(1992). Estimating plant biomass: a review of techniques. Australian Journal of Ecology. 17(2): 121-131.
Chapman ,H., Pratt, PE. (1961). Methods of analysis for soils, plants, and waters. University of California, Division of Agricultural sciences. California. USA. Riverside Press.
Delauney, AJ., Verma, DPS.(1993). Proline biosynthesis and osmoregulation in plants. Plant J. 4:215-223.
Ebrahimzade, MA., Hossinimehr, SJ., Hamidinia, A., Jafari, M. (2008a). Antioxidant and free radical scavenging activity of Fijoa sallowiana. Fruits peel and leaves. Pharmacology online. 1: 7-14.
Ebrahimzade, MA., Pourmorad, F., Hafezi, S.(2008b). Antioxidant activities of Iranian corn silk. Turk.J.Biol. 32:43-49.
Ebrahimzade, MA., Pourmorad, F., Bekhradnia, AR. (2008c). Iron chelating activity screening, phenol and flavonoid content of some medicinal plants from Iran. Afr.J.Biotechnol. 7:3188-3192.
Flexas, J., Bota, J.,Loreto, FC., ornic, G., Sharkey, TD. (2004). Diffiusive and metabolic limitation to photosynthesis under drought and salinity in C3 plants. Plant biology6:249-279.
Graifenberg, A., Giustiniani, L., Temperini, O., Lipucci, DP. (1995). Allocation of Na, Cl, K and Ca within plant tissue in Globe Artichoke (Cynara scolymus L.) under Saline- sodiac condition.Scientia horticulture.63: 1-10.
Harrison, MJ.(2005). Signaling in the arbuscular mycorrhizal symbiosis. Annu Rev Microbiol 59:19ñ42 
Idrees, M., Khan, MA., Naeem, M., Aftab, T., Hashemi, N., Alam, M.(2011).Modulation of defense responses by improving photosynthetic activity. Antioxidant metabolism and vincristine and vinblastine accumulations in Catharenthus roseous(L.) G. Don through salicylic acid under water stress. Russian agricultural sciences. 6:474-483.
Jogwart, A., Saha, S., Bakshi, M., Dayaman, V., Dua, M., Varma, A. (2013). Piriformospora indica rescues growth diminution of rice seedlings during high salt stress. NCBI pub Med.9(1).
Kost, G., Rexer, KH. (2013). Piriformospora indica: Morphology and ultra structure of Piriformospora indica. Varma A Kost,G OelmullerR (Ed) Springer Marburg Germany.
Kulchesk, FR., Oliveira, L., Molina, LG., Almerag, P., Rodrigues, F., Margolino, J., Barbosa, J., StolfMoreira, R., Nepomuceno, A., Marcelino-Guimaraes,F., et al.(2011). Identification of noval soybean microRNA involved in abiotic and biotic stresses.BMC Genomics. 12:307.
Long, H.H., Schmidt, D.D., Baldwin, I.T.(2008). Native bacterial endophytes promote host growth in species-specific manner. Phytohormone manipulations do not result in common growth responses. PLoS ONE. 3,e2702.
Munns, R.(2003). Comparative physiology of salt and water stress. Plant cell Environ. 25: 239-250.
Murashige, T., Skoog, F.(1962). A revised medium for rapid growth and bioassay with tobacco tissue cultures, plant physiol. 15: 473-497.
Mattioni, C., Lacerenza, N., Troccoli, A., De Leonardis, A., Di Fonzo, M.(1997). Water and salt stress ñ induced alternation in proline metabolism of Triticum durum seedlings. Physiologia plantarum. 101:787-792.
Nascimento, NC., Cannes, N., Frett-Neto, AG. (2010). Plant secondary metabolisms and challenges in modifying its operation: an overview. In Plant secondary metabolism engineering. Human press. 1-13
Oldroyd, G. downie, J.A. (2006). Nuclear Calcium Changes at the Core of Symbiosis Signaling. current opinion. Plant biology. 9: 351ñ357.
Peng, Z., Verma, L.(1996). Reciprocal regulation of pyrroline-5-carboxylate synthetase and proline dehydrogenase genes controls proline levels during and after osmotic stress in plants. Mol Gen Genet. 253:334-341.
Peökan-Berghˆfer, T., Shahollari, B., Giang, PH., Hehl, S., Markert, C., Blanke, V., et al.(2004). Association of Piriformospora indica with Arabidopsis thaliana roots represents a noval system to study beneficial plant-microbe interactions and involves early plant protein modifications in the endoplasmatic
reticulum and at the plasma membrane. Physiol plant. 122:465-477.
Ragazzi, E., & Veronese, G. (1973). Quantitative analysis of phenolic compounds after thin-layer chromatographic separation. Journal of Chromatography A. 77:369-375.
Rai, M., Acharya, D., singh, A. (2001). Positive growth response of the medicinal plants Spilanthes calva and Withania somnifera to inoculation by Piriformospora indica in a field trial. Mycorrhiza. 11: 123-128.
Rice-Evans, C., Miller, N., Paganga, G. (1997).Antioxidant properties of phenolic compounds. Trends in plant science.4 :152-159.
Rottenberg, A., Zohary,D. ( 1996). The wild ancestry of the cultivated artichoke. Genetic resources crop evolution.43:53-58.
Shahollari, B., Varma, A., Oelm¸ller, R.(2005). Expression of a receptor kinase in Arabidopsis roots stimulated by the basidiomycete Piriformospora indica and the protein accumulates in TritonX-100
insoluble plasma membrane microdomains. J plant physiol. 162:945-958.
Sherameti, I., Tripathi, S., Varma, A., Oelm¸ller, R. (2005). The root-colonizing endophyte Piriformospora indica confers drought tolerance in Arabidopsis by stimulating the expression of drought stress-related genes in leaves. Mol plant-Microb interact.21:799-807.
Schutz, K., Muks, E., Carle, R., Schieber, A. (2006). Quantitative determination of phenolic compounds in artichoke-based dietry supplements and pharmaceutical by high-performance liquid chromatography.
Journal of agricultural and food chemistry. 54: 8812-8817.
Singh, LP., Singh, Gill, S., Tuteja, N.(2011). Unrevealing the role of fungal symbionts in plant abiotic stress tolerance. Plant signaling and behavior. 6: 175-191.
Sun, C., Johnson, JM., Cai, D., Sheramti, I., Oelm¸llre, 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-locolized CAS protein. J plant physiol. 167:1009-1017.
Tanji, K.,K.(1990). Nature and extent of agricultural salinity.In: Tanji,K,K.(ed), Agricultural Salinity assessment and management .pp: 1-13. ASCE, New York. Varma, A., Verma, S., SudhaSahay, NA., Butehorn, B., Franken, P.(1999). Piriformospora indica a cultivable lant growth promotinh root endophyte. Appl Environ Microbiol. 65:2741-2744.
Verma, SA., Varma, A., Rexer, K-H., Hassel, A., Kost, G., Sarbhoy, A., et al.(1998). Piriformospora indica gen. et. Sp. nov., a new root- colonizing fungus. Mycologia. 90:898-965.
Vierheilig, H., coughlan, AP., Wyss, U., Piche, Y. (1998). Ink and vinegar, a simple staining technique for arbascular mycorrhizal fungi. Application of Environmental Microbiology. 64: 5004-5007.
Walker, A.F., Middleton, RW., Petrowicz, O. (2001). Artichoke leaf extract reduces symptoms of irritable bowel syndrome in a post marketing surveillance study. Phytotherapy Reasearch.15: 58-61.
Waller, F., Achatz, B., Bultruscht, H., Fodor, J., Becker, K., Fischer, M., et al.(2005). The endophytic fungus Piriformospora indica reprograms barely to salt-stress tolerance. Disease resistance and higher yield. Proc Natl Acad Sci USA. 102: 13386-13391.
Waller, F., Mukherjee, K., Deshmukh, SD., Achatz, B., Sharma, M., Schafer, P., et al.(2008). Systemic and local modulation of plant responses by Piriformospora indica and related Sebacinales species. J Plant Physiol. 179: 675-686.
Warcup, JH., Mcgee, PA.(1983). The mycorrhizal associations of some Australian Asteraceae. New Phytol. 4: 667-672.
Walton, E., Podivinsky, E.(1998). Regulation of proline biosynthesis in Kiwifruit buds with and without hydrogen cynammide treatment. Physiologia Plantarum. 102: 171-178.
Zuccaro, A., Lahrmann, U., Guldener, U., Langen, G., Pfiffi, S., Biedenkopf, D., Wong, P., Samans, P., Grimme, C., Basiewicz, M., et al.(2011). Endophytic life strategies decoded by genome and transcriptome analyses of the mutualistic root symbiont Piriformospora indica. PLoS Pathog. 7,