Effect of Endophytic Fungi Pirifomospora indica on Flowering and Root Growth Parameters of Strawberry in Hydroponic Culture

Document Type : Research Article

Authors

• Hamidreza Rahmani
• Ebrahim Mohammadi Goltapeh

Tarbiat Modares University

https://doi.org/10.22067/jhorts4.v32i2.56832

Abstract

Introduction: Strawberry as an herbaceous perennial plant, belongs to the Rosaceae family, which is considered as an important plant, due to having various types of vitamins such as C, A, B6, E. Nowadays, the excessive use of chemical fertilizers instrawberry productionin order to increase yields, has resulted in environmental pollution and dangers on the health of consumers. Microbial endophytes are considered as the most important soil microorganisms with genetic, physiological and ecological impacts in their host plants, increasing the yield. Pirifomosporaindica is a member of Basidiomycetes in order Sebacinales.The fungus is easily cultivable, lacks host specificity and colonizes roots of many different plants, mostly in an endophytic fashion. It interacts with a wide range of hosts, including bryophytes, pteridophytes, gymnosperms and a large number of mono- and dicot plants. The fungus grows inter- and intracellularly, forms pearshaped, auto fluorescent chlamydospores within the cortex of the colonized roots and in the rhizosphere zone, but it does not invade the endodermis and the aerial parts of the plants. The fungus promotes nutrient uptake, allows plants to survive under water, temperature and salt stresses, and confers systemic resistance to toxins, heavy metal ions, insects and pathogenic organisms. In this study,the effectson the flowering and root growth parameters of strawberry in hydroponic culture was examined in a completely randomized design with 28 replicationsundergreenhouse condition of Faculty of Agriculture,TarbiatModarres University.
Materials and Methods: This research was conducted in the greenhouse of faculty of agriculture TarbiatModarres University.Fungi used in this study was prepared of fungi collection of the Department of Pathology, University of TarbiatModarres. Endophytic fungus roots was cultured in solid medium Kafer.For this study, 140 strawberry runners were prepared and then put them in a pots with diameter of 25 and height of 30 cm was cultivated in perlite and cocopeat.Two weeks afterestablishment roots, concentrations, 0 (control), 80, 160, 250 and 330 spores/ml of endophytic fungus P. indica was inoculated by injecting around roots of strawberry plants. Temperature and humidity conditions needed for fungal growth were provided in the strawberry’s greenhouse and were irrigated with a nutrient solution three times per day. Eight month after fungal inoculation flowering content was measured for all pots. One week after the last harvest length, Fresh and dry weight roots were measured. Data is transferred to excel software and then analyzed using SAS 9.1 software and comparison of means using Duncan test was conducted.
Results and Discussion: Analysis of variance showed that among treatments there is significant difference on growth parameters of strawberryplants (P < 0.01),soby increasing concentration of fungi increased growth parameters and this indicate the positive impact of the endophytic fungus onthe growth parameters of strawberry plant is inoculated with the fungus than the control plants. Results showed that the maximum and minimum effects of fungal on growth parameters related to 330 sp/ml and control treatments, respectively. flowering content showed 37 and 18.53 percent increase respectively under 330 and 250 spores/ml compared to control which can be related to absorb more nutrient elements, especially phosphorus and biomass of strawberry plants. Root dry (76.71 and 52 percent) and fresh (75.52 and 40 percent) weights were increased under 330 and 250 spores/ml treatment compared to control and were significantly different with other treatments (P < 0.05), while there was no significant difference among control, 80 and 160 spores/ml treatments. Regarding to root length, 330, 250 and 160 spores/ml treatments resulted in 72, 37 and 14.33 percent increase respectively compared to control and showed a significant difference with other treatments. In this respect, it can be stated that P. indica at high concentrations due to the increase production of auxin that increased the root length, root dry and fresh weight is inoculated plants compared to control that increase root growth parameters which cause absorb more nutrient elements from soil.
Conclusions: It can be concluded that high concentrations of the fungus P. indica can increase physiological characteristics (the flowering, root length and dry weight and fresh weight) of strawberry plants. and thus it has a positive effect on plant growth and yield.

Keywords

• Endomycorrhiza
• Greenhouse Strawberry
• Soilless culture

20.1001.1.20084730.1397.32.2.5.6

References

1- Arzani A., Mobheli M., and Nahchiri A. 2007. Hydroponic Culture. Isfahan University of Technology Press, 210 pp, Iran.

2- Barazani O., Benderoth M., Groten K., Kuhlemeier C., and Baldwin I.T. 2005. Piriformospora indica and Sebacina vermifera increase growth performance at the expense of herbivore resistance in Nicotiana attenuata. Oecologia, 146: 234–243.

3- Bohme M. 1993. Effects of hydroponics on the development of cucumber growing in ecologically suitable substrates. International Symposium on New Cultivation Systems in Greenhouse, 361: 133-140.

4- Bonfante P. and Perotto S. 1995. Strategies of arbuscular mycorrhizal fungi when infecting host plants. New phytology, 130: 3-21.

5- Butehorn B., Rhody D., and Franken, P. 2000. Isolation and characterisation of Pitef1 encoding the translation elongation factor EF-1α of the root Endophyte Piriformospora indica. Plant Biology, 2:687–692.

6- Bould C. 1964. Leaf analysis as a guide to the nutrition of fruit crops. sand culture N, P, K, Mg experiments with strawberry (Fragaria spp.). Journal of the Science of Food and Agriculture, 15: 474-487.

7- Carrasco B., Garces M., Rojas P., Saud G., Herrera R., Retamales J.B., and Caligari P.D. 2007. The Chilean strawberry [Fragaria chiloensis (L.) Duch.]: genetic diversity and structure. Journal of the American Society for Horticultural Science, 132(4): 501-506.

8- Das A., Kamal S., Shakil Najam A., Sherameti I., Oelmuller R., Dua M., Tuteja N., Johri Atul K., and 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 & Behavior, 7: 1–10.

9- Das A., Tripathi S., and Varma A. 2014. In vitro plant development and root colonization of Coleus forskohlii by Piriformospora indica. World Journal of Microbiology and Biotechnology, 30(3): 1075-1084.

10- Dolatabadi H.K., Goltapeh E.M., Moieni A., and Varma A. 2010. Effect of different concentrations of auxin and Piriformospora indica and Sebacina vermifera on Mentha piperita and Thymus vulgaris in vitro and in vivo experiments. Journal of Medicinal Plants, 2 (9): 14-22.

11- Dolatabadi H.K., Goltapeh E.M., Moieni A., Jaimand K., Sardrood B.P., and Varma A. 2011. Effect of Piriformospora indica and Sebacina vermifera on plant growth and essential oil yield in Thymus vulgaris in vitro and in vivo experiments. Symbiosis, 53:29–35.

12- Dolatabadi H., and Goltapeh E.M. 2013. Effect of inoculation with piriformospora indica and sebacina vermifera on growth of selected brassicaceae plants under greenhouse conditions. Journal of Horticultural Research, 21(2): 115-124.

13- Druge U., Baltruschat H., and Franken P. 2007. Piriformospora indica promotes adventitious root formation in cuttings. Science Horticulture, 112: 422–426.

14- Fakhro A., Andrade-Linares D.R., Bargen S., Bandte M., Buttner C., Grosch R., Schwarz D., and Franlen P. 2010. Impact of Piriformospora indica on tomato growth and on interaction with fungal and viral pathogens. Mycorrhiza, 20: 191–200.

15- FAO F. 2011.Agricultural Organization. FAOSTAT (http://faostat. fao. org/site/567/DesktopDefault. aspx.

16- Franken P., Requena N., Butehorn B., Krajinski F., Kuhn G., Lapopin L., and Stommel M. 2000. Molecular analysis of the arbuscular mycorrhiza symbiosis. Archives of Agronomy and Soil Science, 45(4): 271-286.

17- Franken P. 2012. The plant strengthening root endophyte Piriformospora indica: potential application and the biology behind. Applied Microbiology & Biotechnology, 96:1455-1464.

18- Ghimire S. R., Charlton N.D., and Craven K.D. 2009. The Mycorrhizal Fungus, Sebacina vermifera, Enhances Seed Germination and Biomass Production in Switchgrass (Panicum virgatum L). Bioenergy Research, 2:51–58.

19- Gosal S.K., Karlupia A., Gosal S.S., Chhibba I.M., and Varma A. 2010. Biotization with Piriformospora indica and Pseudomonas fluorescens improves survival rate, nutrient acquisition, field performance and saponin content of micropropagated Chlorophytum sp. Indian Journal of Biotechnology, 9: 289–297.

20- Gerdmann J.W., and Nicolson T.H. 1963. Spore of mycorrhizal Engogone species extracted from soil by wet sieving and decanting. Transactions of the British Mycological Society, 46: 235-244.

21- Haynes R.J., and Goh K.M. 1987. Effects of nitrogen and potassium applications on strawberry growth, yield and quality. Communications in Soil Science and Plant Analysis, 18: 457-471.

22- Hill T.W., and Kafer E. 2001. Improwed protocols for aspergillus medium: trace elements and minimum medium salt stock solutions. Fungal Genetic News Letter, 48: 20-21.

23- Husaini A.M., Abdin M.Z., Khan S., Xu Y.W., Aquil S., and Anis M. 2012. Modifying strawberry for better adaptability to adverse impact of climate change. Current Science, 102:1660–1673.

24- Kafer E. 1977. Meiotic and mitotic recombination in Aspergillus and its chromosomal aberrations. Advances in Genetic, 19: 33-131.

25- Kapoor R., Giri B., and Mukerji K.G. 2004. Improved growth and essential oil yield and quality in foeniculum vulgare Mill on mycorrhizal inoculation supplemented with P-fertilizer. BioresourceTechnology, 93: 307- 311.

26- Kirch H.H., Vera-Estrella R., Golldack D., Quigley F., Michalowski C.B., Barkla B.J., and Bohnert H.J. 2000. Expression of water channel proteins in Mesembryanthemum rystallinum. Plant Physiology, 123: 111- 124.

27- Kumari R., Kishan H., Bhoon Y.K., and Varma A. 2003. Colonization of cruciferous plants by Piriformospora indica. Current Science, 85:1672–1674.

28- Malla R., Prasad R., Kumari R., Giang P. H., Pokharel U., Oelmüller R., and Varma A. 2004. Phosphorus solubilizing symbiotic fungus: Piriformospora indica. Journal of Endocytobiosis and Cell Research, 15:579-600.

29- Murphy B.R., Doohan F.M., and Hodkinson T.R. 2014. Yield increase induced by the fungal root endophyte Piriformospora indica in barley grown at low temperature is nutrient limited. Symbiosis, 62(1): 29-39.

30- Neocleous D., and Vasilakakis M. 2010. Effects of cultivars and substrates on soilless strawberry production in Cyprus p. 435-440. In 28th International Horticultural Congress on Science and Horticulture for People (IHC2010): International Symposium on 926, Lisbon, Portugal.

31- Oelmuller R., Shahollari B., Peskan-Berghofer T., Trebicka A., Giong P.H., Sherameti I., Oudhoff M., Venus Y., Altschmied L., and Varma A. 2004. Molecular analyses of the interaction between Arabidopsis roots and the growth-promoting fungus Piriformospora indica. Journal of Endocytobiosis and Cell Research, 15: 504-17.

32- Peskan-Berghofer T., Shahollari B., Giong P.H., Hehl S., Markert C., and Blanke V. 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 endoplasmatic reticulum and at the plasma membrane. Plant Physiology, 122:465–77.

33- Prajapati K., Yami K.D., and Singh A. 2008. Plant growth promotional effect of Azotobacter chroococcum, Piriformospora indica and vermicompost on rice plant. Nepal Journal of Science and Technology, 9: 85-90.

34- Pham H.G., Kumari R., Singh A., Malla R., Prasad R., Sachdev M., Kaldorf M., Buscot F., Oelmueller R., Hampp, R., Saxena A.K., Rexer K.H., Kost G., and Varma A. 2004. Axenic culture of symbiotic fungus Piriformospora indica. p. 593-613. In: Plant surface microbiology (Varma, A., Abbott, L.K., Werner, D., Hampp, R., eds) Springer –Heidelberg, Berlin.

35- Phillip J. M., and Hayman D.S. 1970. Improved procedures for clearing roots and staining parasitic and VAM fungi for rapid assessment of infection. Transactions of the British Mycological Society, 55: 158–161.

36- Qiang X., Weiss M., Kogel K.H. and Schafer P. 2012. Piriformospora indica—a mutualistic basidiomycete with an exceptionally large plant host range. Molecular plant Pathology, 13(5): 508-518.

37- Rashmi K., Latha J.N.L., Sowjanya T.N., Kirannayi P., Rao M.V., Menon C., and Mohan P.M. 2003. Colonization of cruciferous plants by Piriformospora indica. Current Science, 85(12): 1672.

38- Rai M., Acharya D., Singh, A., and Varma A. 2001. Positive growth responses of the medicinal plants Spilanthes calva and Withania somnifera to inoculation by Piriformospora indica in a field trial. Mycorrhiza, 11(3): 123-128.

39- Rai M., and Varma, A. 2005. Arbuscular mycorrhiza-like biotechnological potential of Piriformospora indica, which promotes the growth of Adhatoda vasica Nees. Electronic Journal of Biotechnology, 8(1): 1-6.

40- Satheesan J., Narayanan A. K. and Sakunthala M. 2012. Induction of root colonization by Piriformospora indica leads to enhanced asiaticoside production in Centella asiatica. Mycorrhiza, 22:195–202.

41- Sahay N.S., and Varma A. 1999. Piriformospora indica: a new biological hardening tool for micropropagated plants. FEMS Microbiology Letters, 181: 297–302.

42- Schafer P., Pfiffi S., Voll L.M., Zajic D., Chandler P.M., Waller F., Scholz U., Pons-Kuhnemann J., Sonnewald S., Sonnewald, U., and Kogel K.H. 2009. Manipulation of plant innate immunity and gibberellin as factor of compatibility in the mutualistic association of barley roots with Piriformospora indica. Plant Journal, 59:461–474.

43- Serfling A., Wirsel S.G., Lind V., and Deising H.B. 2007. Performance of the biocontrol fungus Piriformospora indica on wheat under greenhouse and field conditions. Phytopathology, 97: 523-531.

44- Shahollari B., Varma A., and Oelmuller R. 2005. Expression of a receptor kinase in Arabidopsis roots is stimulated by the basidiomycete Piriformospora indica and the protein accumulates in Triton X-100 insoluble plasma membrane microdomains. Journal of Plant Physiology, 162: 945-958.

45- Singh A., and Varma A. 2005. Functional and immune-characterization of Sebacinales fungi with a broad mycorrhizal potentials. Scientific World, 3(3): 53-61.

46- Sun C.A., Johnson J., Cai D.G., Sherameti I., Oelmuller R., and Lou B.G. 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. Journal Plant Physiology, 167:1009–1017.

47- Verma S., Varma A., Rexer K.H., Hassel A., Kost G., Sarbhoy A., Bisen P., Butehorn B., Varma A., Sahay N.S., Butehorn B., & Franken P. 1998. Piriformospora indica a cultivable plant growth-promoting root endophyte. Applied and Environmental Microbiology, 65: 2741–2744.

48- Varma A., Verma S., Sudah S.N., and Franken P. 1999. Piriformospora indica, a cultivable plant growth-promoting root endophyte. Applied and Environmental Microbiology, 65:2741–2744.

49- Varma A., Bakshi M., Lou B., Hartmann A., and Oelmueller R. 2012. Piriformospora indica: A novel plant growth-promoting mycorrhizal fungus. Agricultural Research, 1:117-131.

50- Waller F., Mukherjee K., Deshmukh S.D., Achatz B., Sharma M., Schaefer P., and Kogel K.H. 2008. Systemic and local modulation of plant responses by Piriformospora indica and related Sebacinales species. Journal Plant Physiology, 165:60–70.