Document Type : Original Article

Authors

Department of Horticultural Sciences, Gorgan University of Agricultural Sciences and Natural Resources, Iran

Abstract

Purpose: Due the importance of taxol and based on the confirmed role of certain endophytes of Yew tree in the production of this vital compound, the present study was designed to investigate the effect of isolated endophytic fungi on vegetative and qualitative characteristics of stevia plant. Research method: The experiment included five different endophytic fungi isolated from Yew tree. In order to do that, rooted cuttings of stevia were transferred to the pot after being inoculated with different isolated endophytic fungi (TB2, TB2-3, TB20, TB55) of Yew tree in four replications as a completely randomized design and were kept in outdoor conditions. To isolate endophytic fungi, root samples were collected from the yew trees in the Ziyarat forest located in Golestan province, Iran. Main findings: The results of the study revealed the positive effect of Yew tree endophytes as biotic agents on the growth and physiological parameters of stevia. Also, the fungal pathogenicity effect on stevia was not observed. In addition, the main stem diameter, internode spacing, leaf area and other measured parameters were affected by studied endophytes. Among of the five used isolates fungi, three were classified as stevia plant grows stimulator. Also, due to the highest total sugar and antioxidant activity of stevia, rest two isolates were classified as “bio-elicitor”. Limitations: There was no limitation to report. Originality/Value: The findings of the present study suggest that stevia, as a medicinal and economical herb, is capable of coexistence with yew endophytes. If taxol producer endophytes successfully transfer to stevia, it is possible to study the production of taxol in herbaceous plants, thereby opening the new door to easier and cheaper access to Taxol.

Keywords

Main Subjects

Ajikumar, P. K., Xiao, W. H., Tyo, K. E., & Wang, Y. (2010). Isoprenoid pathway optimization for taxol precursor overproduction in Escherichia coli. Science, 330(6000), 70-74. https://doi.org/10.1126/science.1191652
Ali, S. K. Z., Sandhya, V., Grover, M., Kishore, N., Rao, L. V., & Venkateswarlu, B. (2009). Pseudomonas sp. strain AKM-P6 enhances tolerance of sorghum seedlings to elevated temperatures. Biology and Fertility of Soils, 46, 45-55. https://doi.org/10.1007/s00374-009-0404-9
Alkaraki, G. N., & Hamnad, R. (2001). Mycorrhizal influence on fruit yield and mineral content of tomato grown under salt stress. Journal of Plant Nutrition, 24, 1311-1323. https://doi.org/10.1081/PLN-100106983
Ansari, M. W., Kumar Trivedi, D., Kumar Sahoo, R., Singh Gill, S., & Tuteja, N. (2013). A critical review on fungi mediated plant responses with special emphasis to Piriformospora indica on improved production and protection of crops. Plant Physiology and Biochemistry, 70, 403-410. https://doi.org/10.1016/j.plaphy.2013.06.005
Auge, R. M., Stodola, A. J. W., Tims, J. E., & Saxton, A. M. (2001). Moisture retention properties of a mycorrhizal soil. Journal of Plant and Soil, 230, 87-97. https://doi.org/10.1023/A:1004891210871
Azcon-Aguilar, C., & Barea, J. M. (1996). Arbuscular mycorrhizas and biological control of soil- borne plant pathogens - an overview of the mechanisms involved. Mycorrhiza, 6, 457-464.  https://doi.org/10.1007/s005720050147
Bacon, C. W., & White, J. F. (2000). An Overview of Endophytic Microbes: Endophytism Definition. Microbial Endophytes, Marcel Dekker, New York, pp. 3-5.
Bandyopadhyay, U., Das, D., & Banerjee, R. K. (1999). Reactive oxygen species: Oxidative damage and pathogenesis. Current Science, 77, 658-666.
Bearden, B. N. (2001). Influence of Arbuscular mycorrhizal fungi on soil structure and soil water characteristics of vertisols. Plant and Soil, 229, 245-258. https://doi.org/10.1023/A:1014923911324
Brand-Williams, W., Cuvelier, M. E., & Berset, C. (1995). Use of a free radical method to evaluate antioxidant activity. LWT-Food Science and Technology, 28, 25-30. https://doi.org/10.1016/S0023-6438(95)80008-5
Chang, C., Yang, M., Wen, H., & Chern, J. (2006). Estimation of total flavonoid content in propolis by two complementary colorimetric methods. Journal of Food and Drug Analysis, 10, 178 -182.
Chliyeh, M., Touhami, A. Q., Filali-Maltouf, A., Modafar, C., Moukhli, A., Oukabli, A., Benkirane, R., & Douira, A. (2014). Effect of a composite endomycorrhizal inoculum on the growth of olive trees under nurseries conditions in Morocco. International Journal of Pure and Applied Bioscience, 2(2), 1-14. https://doi.org/10.22161/ijeab/2.3.9
Das, A., Kamal, Sh., Shakil, N. A., Sherameti, I., Oelmüller, R., Dua, M., Tuteja, N., Johri, A. K., & 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 Signaling and Behavior, 7(1), 1-10. https://doi.org/10.4161/psb.7.1.18472
Demir, S. (2004). Influence of Arbuscular mycorrhiza on some physiological growth parameters of pepper. Turkish Journal of Biology, 28, 85-90.
Dolatabadi, H. K., Goltapeh, E. M., Moieni, A., Jaimand, K., Sardrood, B. P., & Varma, A. (2011). Effect of Piriformospora indica and Sebacina vermifera on plant growth and essential oil yield in Thymus vulgaris invitro and invivo experiments. Journal of Symbiosis, 53, 29-35.
Dolatabadi, H. K., Mohammadi Goltapeh, E. M., Moieni, A., & Varma, A. (2012). Evaluation of different densities of auxin and endophytic fungi (Piriformospora indica and Sebacina vermifera) on Mentha piperita and Thymus vulgaris growth. African Journal of Biotechnology, 11(7), 1644-1650. https://doi.org/10.5897/AJB10.1336
Drüge, U., Baltruschat, H., & Franken, P. (2007). Piriformospora indica promotes adventitious root formation in cuttings. Scientia Horticulturae, 112, 422-426. https://doi.org/ 10.1016/j.scienta.2007.01.018
Fakhro, A. D., Andrade-Linares, R., Von Bargen, S., Bandte, M., Buttner, C., Grosch, R., Schwarz, D., & Franken, P. (2010). Impact of Piriformospora indica on tomato growth and on interaction with fungal and viral pathogens. Mycorrhiza, 20, 191-200. https://doi.org/ 10.1007/s00572-009-0279-5
Gan, R. Y., Xu, X. R., Song, F. L., Kuang, L., & Li, H. (2010). Antioxidant activity and total phenolic content of medicinal plants associated with prevention and treatment of cardiovascular and cerebrovascular disease. Journal of Medicinal Plants Research, 4, 2438-2444. https://doi.org/10.5897/JMPR10.581
Ghasemnajad, A., & Babaeizadeh, V. (2012). The influence of piri fungus (Priformospora indica) on vegetative growth and the content of caffeic acid of leaves of artichoke (Cynara scolymus L.) plant. Journal of Plant Production Research, 18(1), 133-140. (In Persian)
Ghasemnajad, A., & Bagheri fard, A. (2014). Studying the quality of the Prunus persica (L.) Batch incubated with Piriformospora indica. Journal of Iranian Plant Ecophysiological Research, 35(3), 43-52. (In Persian)
Gholami, A., & Kochaki, A. (2001). Mycorrhiza in Sustainable Agriculture. Shahrood University Press. 212 pp. (In Persian)
Ghorbani, A., Razavi, S. M., Ghassemi Omran, V., Pirdashti, H., & Ramezani, M. (2016). Effect of endophyte fungal symbiosis of Piriformospora indica on morphological character and photosynthesis pigments in tomato (Solanum lycopersicum L.). New Cellular and Molecular Biotechnology Journal, 6(24), 57-64. (In Persian)
Gupta, M. L., Prasad, A., Ram, M., & kumar, S. (2002). Effect of the vesicular arbuscular mycorrhizal (VAM) fungus Glomus fasiculatum on the essential oil yield related characters and nutrient acquisition in the crops of different cultivars of menthol mint (Mentha arvensis) under field conditions. Bioresource Technology, 81, 77-79. https://doi.org/10.1016/S0960-8524(01)00109-2
He, Y., Oyaizu, H., & Suzuki, S. (2002). Indole-3-acetic acid production in Pseudomonas fluorescens HP72 and its association with suppression of creeping bentgrass brown patch. Current Microbiology, 74, 138-143. https://doi.org/10.1007/s00284-002-3968-2
Hiscox, J. D., & Israelstam, G. F. (1979). A method for the extraction of chlorophyll from leaf tissue without maceration. Canadian. Journal of Botany, 57, 1332-1334.  https://doi.org/10.1139/b79-163
Jenschke, G., Brandes, B., Kuhn, A. J., Schoder, W. H., Becker, J. S., & Godlbd, D. L. (2000). The mycorrhizal fungus Paxillus in volutes magnesium to Norway spruce seedlings. Evidence from stable isotope labeling. Plant and Soil, 220, 243-246.  https://doi.org/10.1023/A:1004727331860
Kapoor, R., Gir, B., & Mukerji, K. G. (2002). Effect of the vesicular arbuscular mycorrhizal (VAM) fungus Glomus fascilucatum on the essential oil yield related characters and nutrient acquisition in the crops of different cultivars of menthol mint (Mentha arvensis) under field conditions. Bioresource Technology, 81, 77–79. https://doi.org/10.1016/s0960-8524(01)00109-2
Krishna, H., Singh, S. K., Sharma, R. R., Khawale, R. N., Grover, M., & Patel ,V. B. (2005). Biochemical changes in micropropagated grape (Vitis vinifera L.) plantlets due to Arbuscular mycorrhizal fungi (AMF) inoculated during ex vitro acclimatization. Scientia Horticulture, 106, 554-567. https://doi.org/10.1016/j.scienta.2005.05.009
Kumar, M., Yadav, V., Tuteja, N., & Johri. A. K. (2009). Antioxidant enzyme activities in maize plants colonized with Piriformospora indica. Microbiology, 155, 780-790. https://doi.org/10.1099/mic.0.019869-0.
Kumari, R., Kishan, H., Bhoon, Y. K. &, Varma, A. (2003). Colonization of cruciferous plants by Piriformospora indica. Current Science, 85, 1672-1674.
Lenin, M., Selvakumar, G., Thamiziniyan, P., & Rajendiran, R. (2010). Growth and biochemical changes of vegetable seedlings induced by Arbuscular mycorrhizal fungus. Journal of Environmental Studies and Sciences, 1, 27-31.
Lugtenberg, B., & Kamilova, F. (2009). Plant growth promoting rhizobacteria. Annual Review of Microbiology, 63, 541-556. https://doi.org/10.1146/annurev.micro.62.081307.162918
Maccready, R. M., Goggolz, J., Silviera, V., & Owenc, H. S. (1950). Determination of starch and amylase in vegetables. Analytical Chemistry, 22, 1156- 1158. https://doi.org/10.1021/ac60045a016
Mahmoudzadeh, M., Rasouli-Sadaghiani, M. H., Hassani, A., & Barin, M. (2015). The role of mycorrhizal inoculation on growth and essential oil of peppermint (Mentha piperita). Journal of Horticulture Science, 29(3), 342-348. (In Persian)
Martin, C. A., & Stutz, J. C. (2004). Interactive effects of temperature and Arbuscular mycorrhizal fungi on growth, P uptake and root respiration of Capsicum annuum L. Mycorrhiza, 4, 241-244. https://doi.org/10.1007/s00572-003-0261-6
Mathur, N., & Vyas, A. (1995). Changes in isozyme patterns of peroxidase and polyphenol oxidase by VAM fungi in roots of Ziziphus species. Plant Physiology, 4, 498-500. https://doi.org/10.1016/S0176-1617(11)81777-3
Meixtner, C., Ludwig-muller, J., Miersch, O., Gressoff, P., Staehelin, C., & Vierheilig, H. (2005). Lake of mycorrhizal autoregulation and phytohormonal changes in the supernodulating soybean mutant nts 1007. Planta, 222, 709-715. https://doi.org/10.1021/ac60045a016
Miller, G. L. (1959). Use of dinitrosalisylic acid reagent for determination of reducing sugars. Analytical Chemistry, 32, 426-428. https://doi.org/10.1021/ac60147a030
Naupaka, B., Zimmerman, P., & Vitousek, M. (2012). Fungal endophyte communities reflect environmental structuring across a Hawaiian landscape. PNAS, 109(32), 13022-13027. https://doi.org/10.1073/pnas.1209872109
Otroshy, M., Vafadar Esfehan, F., & Amooaghaie, R. (2015). Effect of mycorrhiza and plant growth promoting rhizobacteria on plant growth rate, flowering time and stevioside accumulation pattern in Stevia rebaudiana Bert. Iranian Journal of Medicinal and Aromatic Plants, 31(2), 220-234.
Parvizi, K. H., Dashti, F., Esna-ashari, M., & Rejali Bojar, M. (2014). Evaluation the effect of mycorrhizal inoculums on plant growth regulator levels and quality of minituber production in potato plantlets. Plant Production Technology, 13(1), 109-117.
Porras-Soriano, A., & Soriano-Martín, M. L. (2009). Arbuscular mycorrhizal fungi increased growth, nutrient uptake and tolerance to salinity in olive trees under nursery conditions. Journal of Plant Physiology, 166, 1350-1359. https://doi.org/10.1016/j.jplph.2009.02.010
Poupin, M. J., Greve, M., Carmona, V., & Pinedo, L. (2016). A complex molecular interplay of auxin and ethylene signaling pathways is involved in Arabidopsis growth promotion by Burkholderia phytofirmans PsJN. Frontaris in Plant Science, 7, 1-16.  https://doi.org/10.3389/fpls.2016.00492
Ragazzi, E., & Veronese, G. (1973). Quantitative analysis of phenolic compounds after thin-layer chromatographic separation. Journal of Chromatography, 77, 369-375. https://doi.org/10.1016/S0021-9673(00)92204-0
Rahimi Tanha, S., Ghasemnajad, A., Babaeizadeh, V., & Alaeddin, M. Z. (2017). Piriformospora indica mutualistic effect on Cynara scolymus (L.) under water and saline stress. Journal of Plant Production Research, 23(4), 37-57.
Rahmatzadeh, S., Khara, J., & Kazemi Tabar, S. K. (2014), Evaluation of the effect of Glomus etunicatum mycorrhizal fungus on photosynthetic photosensitization and antioxidant properties of seedlings (Catharanthus roseus L.) regenerated during adaptation conditions. Iranain of Journal Plant Ecophysiological Research, 8(4), 12-20. https://doi.org/10.3923/pjbs.2007.2363.2367
Ramesh, K., Singh, V., & Megeji, N. W. (2006). Cultivation of Stevia [Stevia rebaudiana (Bert.) Bertoni]: A comprehensive review. Advances in Agronomy, 89, 137-177. https://doi.org/10.1016/S0065-2113(05)89003-0
Saleh, M., & Al-Garni, S. (2006). Increased heavy metal tolerance of cowpea plant by dual inoculation of an arbuscular mycorrhizal fungi and nitrogen-fixer Rhizobium bacterium. African Journal of Biotechnol, 5(2), 133-42.
Sandhya, V., Ali, S. K. Z., Grover, M., Reddy, G., & Venkateswaralu, B. (2010). Effect of plant growth promoting Pseudomonas spp. on compatible solutes antioxidant status and plant growth of maize under drought stress. Plant Growth Regulation, 62, 21-30. https://doi.org/10.1007/s10725-010-9479-4
Schulz, B., Wanke, S., Draeger, S., & Aust, H. J. (1993). Endophytes from herbaceous plants and shrubs: effectiveness of surface sterilization methods. Mycological Research, 97, 1447-1450.  https://doi.org/10.1016/S0953-7562(09)80215-3
Sharma, M., Schmid, M., Rothballer, M., Hause, G., Zuccaro, A., Imani, J., Kampfer, P., Domann, E., Schafer, P., Hartmann, A., & Kogel, K. H. (2015). Detection and identification of bacteria intimately associated with fungi of the order Sebacinales. Cell Microbiology, 10, 2235-2246.  https://doi.org/10.1111/j.1462-5822.2008.01202.x
Shoresh, M., Harman, G. E., & Mastouri, F. (2010). Induced systemic resistance and plant responses to fungal biocontrol agents. Annual Review of Phytopathology, 48, 21-43. https://doi.org/10.1146/annurev-phyto-073009-114450
Sikora, R. A., Schafer, K., & Dababat, A. (2007). Modes of action associated with microbially induced in planta suppression of plant-parasitic nematodes. Australasian Plant Pathology, 36, 124-134. https://doi.org/10.1071/AP07008
Singh, A., Sharma, J., Rexer, K. H., & Varma, A. (2000). Plant productivity determinants beyond Minerals, water and light. Piriformospora indica: a revolutionary plant growth promoting fungus. Current Science, 79, 101-106.
Srivastava, G. C., & Sairam, R. K. (2002). Changes in antioxidant activity in sub-cellular fractions of tolerant and susceptible wheat genotypes in response to long term salt stress. Plant Science, 162(6), 897-904.  https://doi.org/10.1016/S0168-9452(02)00037-7
Tanwar, A., Aggarwal, A., Yadav, A., & Kadian, N. (2011). Enhanced growth and yield of Capsicum annum L. with two endomycorrhizal fungi and other bio-inuculants. Indian Botanical Society, 90(4), 351-359.
Toussaint, J. P., St-Arnaud, M., & Charest, C. (2004). Nitrogen transfer and assimilation between the arbuscular mycorrhizal fungus Glomus intraradices Schenck and Smith and Ri T-DNA roots of Daucus carota L. in an in vitro compartmented system. Canadian Journal of Microbiology, 50, 251-260. https://doi.org/10.1139/w04-009
Vamerali, T. M., Saccomani, S., Bona, G., Mosca, M., Guarise, A.,  & Ganis, A. (2003). Comparison of root characteristics in relation to nutrient and water stress in tow maize hybrids. Plant Soil, 255, 157-67. https://doi.org/10.1023/A:1026123129575
Vierheilig, H., Coughlan, A. P., Wyss, U., & Piche, Y. (1998). Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Applied and Environmental Microbiology, 64, 5004-5007.
Waller, F., Achatz, B., Baltruschat, H., Fodor, J., Becker, K., Fischer, M., Heier, T., Hckelhoven, R., Neumann, C., Von Wettstein, D., Franken, P., & Kogel, K. (2005). The endophytic fungus Piriformospora indica reprograms barley to salt-stresstolerance, disease resistance, and higher yield. Proceedings of the National Academy of Sciences, 102, 38, 13386-13391. https://doi.org/10.1073/pnas.0504423102
Wu, Q. S., & Xia, R. 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.  https://doi.org/10.1016/j.jplph.2005.04.024
Zamioudis, C., Mastranesti, P., Dhonukshe, P., Blilou, I., & Pieterse, C. M. (2013). Unraveling root developmental programs in itiated by beneficial Pseudomonas spp. bacteria. Plant Physiology, 162, 304-318. https://doi.org/10.1104/pp.112.212597
Zaiyou, J., Li, M., & Xiqiao, H. (2017). An endophytic fungus efficiently producing paclitaxel isolated from Taxus wallichiana var. mairei. Medicine (Baltimore), 96(27), e7406. https://doi.org/10.1097/MD.0000000000007406
Zare Hoseini, R., Mohammadi Goltapeh, E., Kalatejari, S., & Dehghani Mashkani, M. (2015). Effect of vermicompost and fungi inoculation on growth characteristics and steviosid content of Stevia rebaudiana Bert. Journal of Medicinal Plants, 4(56), 179-188. (In Persian)