Piriformospora indica inoculants enhance flowering, yield, and physiological characteristics of tomato (Lycopersicon esculentum) in different growth phases

Iranian Journal of Plant Physiology

دوره 12، شماره 3، مهر 2022، صفحه 4183-4194   

نوع مقاله: Original Article

شناسه دیجیتال (DOI): 10.30495/ijpp.2021.1923991.1302

نویسندگان

Esmaeel Kaboosi¹؛ Mehdi Ghabooli^{* 1}؛ Rouhollah Karimi²

¹Department of Plant Production and Genetics, Faculty of Agriculture, Malayer University, Malayer, Iran

²Department of Landscape Engineering, Faculty of Agriculture, Malayer University, Iran.

چکیده

Piriformospora indica is an endophytic fungus with plant-promoting properties in a wide range of host plants. This study aimed to assess and compare the effects of different P. indica inoculants through morphological and physiological analysis at different times (4, 8, and 12 weeks) after inoculation. The study was conducted in a completely randomized design with three levels of fungus inoculation (non-inoculated, inoculated with P. indica spore and mycelium). The results showed that both P. indica inoculants have a positive effect on measured traits at different times after inoculation. Root and shoot dry weight were increased significantly at 4, 8, and 12 weeks after inoculation. P. indica improved the reproductive phase of tomato resulting in increased dry weight of fruits by up to 51%. Most importantly, the endophyte enhanced tomato fruit yield by up to 73%. Based on experiment data, P. indica increased total chlorophyll (25%), protein (143%), and carbohydrate (44%) content in inoculated plants compared to non-inoculated plants. Besides, P. indica promoted the antioxidant capacity of inoculated plants by increasing CAT and APX activity. In our study, plant inoculation with P. indica also remarkably led to an increase in K (172%) and P (41%) content. Our data showed that both P. indica spore and mycelium have a long-term effect on tomato growth. The application of fungus inoculants promotes plant growth and yield. Hence, P. indica represents a suitable plant-stimulating biofertilizer for tomato in sustainable agriculture.

کلیدواژه‌ها

Biofertilizer؛ Biomass؛ Fruit yield؛ Growth performance؛ Phosphorus

مراجع

   

Abdel‐Shafy, H. I., W. Hegemann and A. Teiner, 1994. Accumulation of metals by vascular plants. Environmental Management and Health. 5, (2) 1-4.

Abdelaziz, M. E., M. Abdelsattar, E. A. Abdeldaym, M. A. Atia, A. W. M. Mahmoud, M. M. Saad and H. Hirt, 2019. Piriformospora indica alters Na+/K+ homeostasis, antioxidant enzymes and LeNHX1 expression of greenhouse tomato grown under salt stress. Scientia Horticulturae. 256, 108532.

Anith, K., A. Sreekumar and J. Sreekumar, 2015. The growth of tomato seedlings inoculated with co-cultivated Piriformospora indica and Bacillus pumilus. Symbiosis. 65, (1) 9-16.

Arnon, D. I., 1949. Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant physiology. 24, (1) 1.

Bajaj, R., W. Hu, Y. Huang, S. Chen, R. Prasad, A. Varma and K. E. Bushley, 2015. The beneficial root endophyte Piriformospora indica reduces egg density of the soybean cyst nematode. Biological control. 90, 193-199.

Baltruschat, H., J. Fodor, B. D. Harrach, E. Niemczyk, B. Barna, G. Gullner, A. Janeczko, K. H. Kogel, P. Schäfer and I. Schwarczinger, 2008. Salt tolerance of barley induced by the root endophyte Piriformospora indica is associated with a strong increase in antioxidants. New Phytologist. 180, (2) 501-510.

Barrs, H. and P. Weatherley, 1962. A re-examination of the relative turgidity technique for estimating water deficits in leaves. Australian journal of biological sciences. 15, (3) 413-428.

Beauchamp, C. and I. Fridovich, 1971. Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Analytical biochemistry. 44, (1) 276-287.

Burd, G. I., D. G. Dixon and B. R. Glick, 2000. Plant growth-promoting bacteria that decrease heavy metal toxicity in plants. Canadian journal of microbiology. 46, (3) 237-245.

Chance, B. and A. Maehly, 1955. [136] Assay of catalases and peroxidases.

Costa, J. M. and J. E. Loper, 1994. Characterization of siderophore production by the biological control agent Enterobacter cloacae. MPMI-Molecular Plant Microbe Interactions. 7, (4) 440-448.

Debbarma, M. and S. P. Das, 2017. Priming of seed: enhancing growth and development. Int J Curr Microbiol App Sci. 6, (12) 2390-2396.

Del Río, L. A., F. Sevilla, L. M. Sandalio and J. M. Palma, 1991. Nutritional effect and expression of SODs: induction and gene expression; diagnostics; prospective protection against oxygen toxicity. Free Radical Research Communications. 13, (1) 819-827.

Dickison, W. 2000. Integrative plant anatomy.,(Harcourt Academic Press: San Diego, CA). Calif

Fakhro, A., D. R. Andrade-Linares, S. Von Bargen, M. Bandte, C. Büttner, R. Grosch, D. Schwarz and P. Franken, 2010. Impact of Piriformospora indica on tomato growth and on interaction with fungal and viral pathogens. Mycorrhiza. 20, (3) 191-200.

Ghabooli, M., 2014. Effect of Piriformospora indica inoculation on some physiological traits of barley (Hordeum vulgare) under salt stress. Chemistry of natural compounds. 50, (6) 1082-1087.

Ghabooli, M., G. Hosseini Salekdeh and M. Sepehri, 2015. The effect of mycorrhiza-like fungus Piriformospora indica on some morphophysiological traits of rice under normal and drought stress conditions.

Ghabooli, M., E. Rezaei, Z. Movahedi and E. Mohsenifard, 2020. Effect of Piriformospora indica inoculation on some morphophysiological parameters in licorice (Glycyrrhiza glabra L.) under drought stress. Iranian Journal of Plant Physiology. 10, (4) 3379-3389.

Ghaffari, M. R., M. Ghabooli, B. Khatabi, M. R. Hajirezaei, P. Schweizer and G. H. Salekdeh, 2016. Metabolic and transcriptional response of central metabolism affected by root endophytic fungus Piriformospora indica under salinity in barley. Plant molecular biology. 90, (6) 699-717.

Giannopolitis, C. N. and S. K. Ries, 1977. Superoxide dismutases: I. Occurrence in higher plants. Plant physiology. 59, (2) 309-314.

Gill, S. S., R. Gill, D. K. Trivedi, N. A. Anjum, K. K. Sharma, M. W. Ansari, A. A. Ansari, A. K. Johri, R. Prasad and E. Pereira, 2016. Piriformospora indica: potential and significance in plant stress tolerance. Frontiers in Microbiology. 7, 332.

Guerfel, M., O. Baccouri, D. Boujnah, W. Chaïbi and M. Zarrouk, 2009. Impacts of water stress on gas exchange, water relations, chlorophyll content and leaf structure in the two main Tunisian olive (Olea europaea L.) cultivars. Scientia Horticulturae. 119, (3) 257-263.

Haas, D. and G. Défago, 2005. Biological control of soil-borne pathogens by fluorescent pseudomonads. Nature reviews microbiology. 3, (4) 307-319.

Hamilton, C. E., P. E. Gundel, M. Helander and K. Saikkonen, 2012. Endophytic mediation of reactive oxygen species and antioxidant activity in plants: a review. Fungal Diversity. 54, (1) 1-10.

Irigoyen, J., D. Einerich and M. Sánchez‐Díaz, 1992. Water stress induced changes in concentrations of proline and total soluble sugars in nodulated alfalfa (Medicago sativd) plants. Physiologia plantarum. 84, (1) 55-60.

Justice, A. H., J. E. Faust and J. L. Kerrigan, 2018. Evaluating a novel method to introduce a mycorrhizal-like fungus, Piriformospora indica, via an inoculated rooting substrate to improve adventitious root formation. Horttechnology. 28, (2) 149-153.

Khan, A. L., M. Waqas, M. Hamayun, A. Al-Harrasi, A. Al-Rawahi and I.-J. Lee, 2013. Co-synergism of endophyte Penicillium resedanum LK6 with salicylic acid helped Capsicum annuum in biomass recovery and osmotic stress mitigation. BMC microbiology. 13, (1) 1-13.

Kieber, J. J. and G. E. Schaller, 2018. Cytokinin signaling in plant development. Development. 145, (4)

Kloepper, J. W., J. Leong, M. Teintze and M. N. Schroth, 1980. Enhanced plant growth by siderophores produced by plant growth-promoting rhizobacteria. Nature. 286, (5776) 885-886.

Kokalis–Burelle, N., C. Vavrina, E. Rosskopf and R. Shelby, 2002. Field evaluation of plant growth-promoting rhizobacteria amended transplant mixes and soil solarization for tomato and pepper production in Florida. Plant and Soil. 238, (2) 257-266.

Kord, H., B. Fakheri, M. Ghabooli, M. Solouki, A. Emamjomeh, B. Khatabi, M. Sepehri, G. H. Salekdeh and M. R. Ghaffari, 2019. Salinity-associated microRNAs and their potential roles in mediating salt tolerance in rice colonized by the endophytic root fungus Piriformospora indica. Functional & integrative genomics. 19, (4) 659-672.

Krishnaveni, N., B. Dipika, D. Ramani and C. Chakravarthy, 2014. Cultivable endophytic mycobiont Piriformospora indica in millet growth promotion. Int J Sci Eng Technol Res. 3, (7) 2033-2047.

Lahrmann, U. and A. Zuccaro, 2012. Opprimo ergo sum—evasion and suppression in the root endophytic fungus Piriformospora indica. Molecular plant-microbe interactions. 25, (6) 727-737.

Malla, R., R. Prasad, R. Kumari, P. Giang, U. Pokharel, R. Oelmüller and A. Varma, 2004. Phosphorus solubilizing symbiotic fungus: Piriformospora in-dica. Endocytobiosis Cell Res. 15, (2) 579-600.

Mane, A., T. Deshpande, V. Wagh, B. Karadge and J. Samant, 2011. A critical review on physiological changes associated with reference to salinity. International Journal of Environmental Sciences. 1, (6) 1192.

Ngwene, B., S. Boukail, L. Söllner, P. Franken and D. Andrade-Linares, 2016. Phosphate utilization by the fungal root endophyte Piriformospora indica. Plant and Soil. 405, (1) 231-241.

Nouh, F. a. A., H. H. A. Nahas and A. M. Abdel-Azeem, 2020. Piriformospora indica: Endophytic Fungus for Salt Stress Tolerance and Disease Resistance. Agriculturally Important Fungi for Sustainable Agriculture. 261-283.

Oelmüller, R., I. Sherameti, S. Tripathi and A. Varma, 2009. Piriformospora indica, a cultivable root endophyte with multiple biotechnological applications. Symbiosis. 49, (1) 1-17.

Olson, M. E. and J. A. Rosell, 2013. Vessel diameter–stem diameter scaling across woody angiosperms and the ecological causes of xylem vessel diameter variation. New phytologist. 197, (4) 1204-1213.

Pal, A. and S. Pandey, 2017. Symbiosis of arbuscular mycorrhizal fungi and Pennisetum glaucum l. improves plant growth and glomalin-related soil protein in barren soil. Int J Sci Invent Today. 6, (6) 783-792.

Pan, R., L. Xu, Q. Wei, C. Wu, W. Tang, R. Oelmüller and W. Zhang, 2017. Piriformospora indica promotes early flowering in Arabidopsis through regulation of the photoperiod and gibberellin pathways. PLoS One. 12, (12) e0189791.

Ramamoorthy, V., R. Viswanathan, T. Raguchander, V. Prakasam and R. Samiyappan, 2001. Induction of systemic resistance by plant growth promoting rhizobacteria in crop plants against pests and diseases. Crop protection. 20, (1) 1-11.

Richardson, A. E. and R. J. Simpson, 2011. Soil Microorganisms Mediating Phosphorus Availability: Phosphorus plant physiology. Plant physiology (Bethesda). 156, (3) 989-996.

Ruiz-Lozano, J. M., R. Porcel, C. Azcón and R. Aroca, 2012. Regulation by arbuscular mycorrhizae of the integrated physiological response to salinity in plants: new challenges in physiological and molecular studies. Journal of Experimental Botany. 63, (11) 4033-4044.

Russo, V. M., 2006. Biological amendment, fertilizer rate, and irrigation frequency for organic bell pepper transplant production. HortScience. 41, (6) 1402-1407.

Russo, V. M. and P. Perkins-Veazie, 2010. Yield and nutrient content of bell pepper pods from plants developed from seedlings inoculated, or not, with microorganisms. HortScience. 45, (3) 352-358.

Sahay, N. and A. Varma, 1999. Piriformospora indica: a new biological hardening tool for micropropagated plants. FEMS Microbiology letters. 181, (2) 297-302.

Santos-Sánchez, N., R. Valadez-Blanco and R. Salas-Coronado, 2013. Factors affecting the antioxidant content of fresh tomatoes and their processed products. Tomatoes: Cultivation, Varieties and Nutrition Higashide T, Nova Science Publishers, Hauppauge, NY, USA.

Shahollari, B., A. Varma and R. Oelmüller, 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, (8) 945-958.

Sharifi, M., M. Mohtashamian, H. Riyahi, A. Aghaee and S. Alavi, 2011. The Effects of Vesicular-Arbuscular Mycorrhizal (VAM) Fungus Glomus etunicatum on Growth and some Physiological Parameters of Basil. Journal of Medicinal Plants. 10, (38) 85-94.

Sherameti, I., B. Shahollari, Y. Venus, L. Altschmied, A. Varma and R. Oelmüller, 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. Journal of Biological Chemistry. 280, (28) 26241-26247.

Sirrenberg, A., C. Göbel, S. Grond, N. Czempinski, A. Ratzinger, P. Karlovsky, P. Santos, I. Feussner and K. Pawlowski, 2007. Piriformospora indica affects plant growth by auxin production. Physiologia plantarum. 131, (4) 581-589.

Sun, C., J. M. Johnson, D. Cai, I. Sherameti, R. Oelmüller and B. Lou, 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 of plant physiology. 167, (12) 1009-1017.

Terhonen, E., K. Blumenstein, A. Kovalchuk and F. O. Asiegbu, 2019. Forest tree microbiomes and associated fungal endophytes: Functional roles and impact on forest health. Forests. 10, (1) 42.

Vavrina, C. S., 1998. Transplant age in vegetable crops. HortTechnology. 8, (4) 550-555.

Verma, S., A. Varma, K.-H. Rexer, A. Hassel, G. Kost, A. Sarbhoy, P. Bisen, B. Bütehorn and P. Franken, 1998. Piriformospora indica, gen. et sp. nov., a new root-colonizing fungus. Mycologia. 90, (5) 896-903.

Vessey, J. K., 2003. Plant growth promoting rhizobacteria as biofertilizers. Plant and soil. 255, (2) 571-586.

Wakelin, S. A., R. A. Warren, P. R. Harvey and M. H. Ryder, 2004. Phosphate solubilization by Penicillium spp. closely associated with wheat roots. Biology and Fertility of Soils. 40, (1) 36-43.

Waller, F., B. Achatz, H. Baltruschat, J. Fodor, K. Becker, M. Fischer, T. Heier, R. Hückelhoven, C. Neumann and D. Von Wettstein, 2005. The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proceedings of the National Academy of Sciences. 102, (38) 13386-13391.

Wang, H., J. Zheng, X. Ren, T. Yu, A. Varma, B. Lou and X. Zheng, 2015. Effects of Piriformospora indica on the growth, fruit quality and interaction with Tomato yellow leaf curl virus in tomato cultivars susceptible and resistant to TYCLV. Plant Growth Regulation. 76, (3) 303-313.

Waqas, M., A. L. Khan, M. Kamran, M. Hamayun, S.-M. Kang, Y.-H. Kim and I.-J. Lee, 2012. Endophytic fungi produce gibberellins and indoleacetic acid and promotes host-plant growth during stress. Molecules. 17, (9) 10754-10773.

Xu, L., C. Wu, R. Oelmüller and W. Zhang, 2018. Role of phytohormones in Piriformospora indica-induced growth promotion and stress tolerance in plants: more questions than answers. Frontiers in microbiology. 9, 1646.

Yadav, V., M. Kumar, D. K. Deep, H. Kumar, R. Sharma, T. Tripathi, N. Tuteja, A. K. Saxena and A. K. Johri, 2010. A phosphate transporter from the root endophytic fungus Piriformospora indica plays a role in phosphate transport to the host plant. Journal of Biological Chemistry. 285, (34) 26532-26544.

Yun, P., L. Xu, S.-S. Wang, L. Shabala, S. Shabala and W.-Y. Zhang, 2018. Piriformospora indica improves salinity stress tolerance in Zea mays L. plants by regulating Na+ and K+ loading in root and allocating K+ in shoot. Plant growth regulation. 86, (2) 323-331.