Abstract
Endophytes of medicinal plants are valuable resources for plant growth promotion and lead drug discovery. Lemon verbena, Lippia citriodora Kunth. (Verbenaceae), is an ethnomedicinal shrub. Here, the endophytic bacterium Sphingomonas paucimobilis and the endophytic fungus Aspergillus sp. isolated from L. citriodora were used for plant interaction studies. Foliar spraying and soil drenching methods of endophyte’s inocula application were used for in planta assays. The results showed that both fungal and bacterial endophytes increased the growth parameters of L. citriodora including plant height, leaf number, fresh weight and dry weight of shoot, root and leaf. Indeed, soil drenching of S. paucimobilis increased the root weight, but its foliar spray increased the plant height. Also, soil drenching of Aspergillus sp. increased the leaves dry weight, while its foliar spray increased the number of branches, leaves, and the leaves fresh weight. Soil drenching of either of both endophytes increased the antioxidant activity of L. citriodora’s foliage, but foliar sprays yielded lower increases. Endophytes had no apparent effects on the phenolics and flavonoids at the time of sampling, i.e. 30 days post-inoculation. Our findings indicate the enhancing effects of endophyte application on the growth and antioxidant property of L. citriodora.
Similar content being viewed by others
References
Abderrahim, F., Estrella, S., Susin, C., Arribas, S. M., Gonzalez, M. C., & Condezo-Hoyos, L. (2011). The antioxidant activity and thermal stability of lemon verbena (Aloysia triphylla) infusion. Journal of Medicinal Food, 14, 517–527.
Agarwhal, S., & Shende, S. T. (1987). Tetrazolium reducing microorganisms inside the root of Brassica species. Current Science, 56, 187–188.
Argyropoulou, C., Daferera, D., Tarantilis, P. A., Fasseas, C., & Polissiou, M. (2007). Chemical composition of the essential oil from leaves of Lippia citriodora H.B.K. (Verbenaceae) at two developmental stages. Biochemical Systematics and Ecology, 35, 831–837.
Aswathy, A. J., Jasim, B., Jyothis, M., & Radhakrishnan, E. K. (2013). Identification of two strains of Paenibacillus sp. as indole 3 acetic acid-producing rhizome-associated endophytic bacteria from Curcuma longa. Biotech, 3, 219–224.
Bacon, C. W., & White, J. F. (2000). Microbial endophytes (pp. 341–388). New York: Marcel Dekker.
Bagheri, A. A., Saadatmand, N. V., Nejadsatari, T., & Babaeizad, V. (2013). Effect of endophytic fungus, Piriformospora S. indica, on growth and activity of antioxidant enzymes of rice (Oryza sativa L.) under salinity stress. International Journal of Advanced Biological and Biomedical Research, 1, 1337–1350.
Baltruschat, H., Fodor, J., Harrach, B. D., Niemczyk, E., Barna, B., Gullner, G., et al. (2008). Salt tolerance of barley induced by the root endophyte Piriformospora indica is associated with a strong increase in antioxidants. The New Phytologist, 180, 501–510.
Bangou, M. J., Méda, N. T. R., Thiombiano, A. M. E., Kiendrebéogo, M., & Zeba, B. (2012). Antioxidant and antibacterial activities of five Verbenaceae species from Burkina Faso. Current Research Journal of Biological Sciences, 4, 665–672.
Brader, G., Compant, S., Mitter, B., Trognitz, F., & Sessitsch, A. (2014). Metabolic potential of endophytic bacteria. Current Opinion in Biotechnology, 27, 30–37.
Chang, C., Yang, M., Wen, H., & Chern, J. (2002). Estimation of total flavonoid content in propolis by two complementary colorimetric methods. Journal of Food and Drug Analysis, 10, 178–182.
Chen, L., Xu, M., Zheng, Y., Men, Y., Sheng, J., & Shen, L. (2014). Growth promotion and induction of antioxidant system of tomato seedlings (Solanum lycopersicum L.) by endophyte TPs-04 under low night temperature. Scientia Horticulturae, 176, 143–150.
da Silva, T. F., Vollu, R. E., Jurelevicius, D., Alviano, D. S., Alviano, C. S., Blank, A. F., & Seldin, L. (2013). Does the essential oil of Lippia sidoides Cham. (pepper-rosmarin) affect its endophytic microbial community? BMC Microbiology, 13, 29.
de Siqueira, V., Conti, R., Magali de Araújo, J., & Souza-Motta, C. M. (2011). Endophytic fungi from the medicinal plant Lippia sidoides Cham. And their antimicrobial activity. Symbiosis, 53, 89–95.
Duarte, M. C. T., Figueira G. M., Sartoratto A., et al. (2005). Anti-Candida activity of Brazilian medicinal plants. Journal of Ethnopharmacology, 97, 305–311.
Ernst, M., Mendgen, K. W., & Wirsel, S. G. R. (2003). Endophytic fungal mutualists: Seed-borne spp. enhance reed biomass production in axenic microcosms. Molecular Plant-Microbe Interactions, 16, 580–587.
Funes, L., Fernández-Arroyo, S., Laporta, O., Pons, A., Roche, E., & Segura-Carretero, A. (2009). Correlation between plasma antioxidant capacity and verbascoside levels. Food Chemistry, 117, 589–598.
Gagné, S., Richard, C., Rouseau, H., & Antoun, H. (1987). Xylem-residing bacteria in alfalfa roots. Canadian Journal of Microbiology, 33, 996–1000.
Glick, B. R. (2015). Beneficial plant-bacterial interactions. Heidelberg: Springer.
Hallmann, J., Quadt-Hallmann, A., Mahaffee, W. F., & Kloepper, J. W. (1997). Bacterial endophytes in agricultural crops. Canadian Journal of Microbiology, 43, 895–914.
Hardoim, P. R., van Overbeek, L. S., Berg, G., Pirttilä, A. M., Compant, S., Campisano, A., Doring, M., & Sessitsch, A. (2015). The hidden world within plants: Ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiology and Molecular Biology Reviews, 79, 293–320.
Hoffman, M. T., Gunatilaka, M., Wijeratne, E. M. K., Gunatilaka, A. A. L., & Arnold, A. E. (2013). Endohyphal bacterium enhances production of indole-3-acetic acid by a foliar fungal endophyte. PLoS One, 8, e73132.
Hol, W. H. G., de la Peña, E., Moens, M., & Cook, R. (2007). Interaction between a fungal endophyte and root herbivores of Ammophila arenaria. Basic and Applied Ecology, 8, 500–509.
Hosseyni Moghaddam, M. S., & Soltani, J. (2014a). Bioactivity of endophytic Trichoderma fungal species from the plant family Cupressaceae. Annales de Microbiologie, 64, 753–761.
Hosseyni Moghaddam, M. S., & Soltani, J. (2014b). Psychrophilic endophytic fungi with bioactivity inhabit Cupressaceae plant family. Symbiosis, 63, 79–86.
Hosseyni Moghaddam, M. S., Soltani, J., Babalhavaeji, F., Hamzei, J., Nazeri, S., & Mirzaei, S. (2013). Bioactivities of endophytic Penicillia from Cupressaceae. Journal of Crop Protection, 2, 421–433.
James, E. K., Gyaneshwar, P., Mathan, N., Barraquio, Q. L., Reddy, P. M., Iannetta, P. P. M., Olivares, F. L., & Ladha, J. K. (2002). Infection and colonization of rice seedlings by the plant growth-promoting bacterium Herbaspirillum seropedicae Z67. Molecular Plant-Microbe Interactions, 15, 894–906.
Janarthine, S. R., & Eganathan, P. (2012). Plant growth promoting of endophytic Sporosarcina aquimarina SjAM16103 isolated from the pneumatophores of Avicennia marina L. International Journal of Microbiology, 1–10.
Khani, A., Basavand, F., & Rakhshani, E. (2012). Chemical composition and insecticide activity of lemon verbena essential oil. Journal of Crop Protection, 1, 313–320.
Kim, S., Lowman, S., Hou, G., Nowak, J., Flinn, B., & Mei, C. (2012). Growth promotion and colonization of switchgrass Panicum virgatum cv. Alamo by bacterial endophyte Burkholderia phytofirmans strain PsJN. Biotechnology for Biofuels, 5, 37.
Luo, S., Xu, T., Chen, L., Chen, J., Rao, C., Xiao, X., Wan, Y., Zeng, G., Long, F., Liu, C., & Liu, Y. (2012). Endophyte-assisted promotion of biomass production and metal-uptake of energy crop sweet sorghum by plant-growth-promoting endophyte Bacillus sp. SLS18. Applied Microbiology and Biotechnology, 93, 1745–1753.
Marks, S., & Clay, K. (1990). Effects of CO2 enrichment, nutrient addition and fungal endophyte infection on the growth of two grasses. Oecologia, 84, 207–214.
Mcdonald, S., Prenzler, P. D., Autolovich, M., & Robards, K. (2001). Phenolic content and antioxidant activity of olive extracts. Food Chemistry, 73, 73–84.
Mucciarelli, M., Scannerini, S., Bertea, C., & Maffei, M. (2003). In vitro and in vivo peppermint (Mentha piperita) growth promotion by nonmycorrhizal fungal colonization. The New Phytologist, 158, 579–591.
Nemat Shahi, M. M., Elhami Rad, A. H., Pedram, N. A., & Nemat, S. N. (2014). Study of antioxidant activity and free radical scavenging ability of lemon Verbena (Lippia Citriodora). Advances in Natural and Applied Science, 8, 59–63.
Owen, N. L., & Hundley, N. (2004). Endophytes the chemical synthesizers inside plants. Science Progress, 87, 79–99.
Pakvaz, S., & Soltani, J. (2016). Endohyphal bacteria from fungal endophytes of the Mediterranean cypress (Cupressus sempervirens) exhibit in vitro bioactivity. Forest Pathology, 46, 569–581.
Pascual, M. E., Slowing, K., Carretero, E., Sanchez, M. D., & Villar, A. (2001). Lippia: Traditional uses, chemistry and pharmacology: A review. Journal of Ethnopharmacology, 76, 201–214.
Redman, R. S., Dunigan, D. D., & Rodriguez, R. J. (2001). Fungal symbiosis: From mutualism to parasitism, who controls the outcome, host or invader? The New Phytologist, 151, 705–716.
Rodriguez, R. J., Redman, R. S., & Henson, J. M. (2004). The role of fungal symbioses in the adaptation of plants to high stress environments. Mitigation and Adaptation Strategies for Global Change, 9, 261–272.
Roos, I. M. M., & Hattingh, M. J. (1983). Scanning electron microscopy of Pseudomonas syringae pv. morspronorum on sweet cherry leaves. Phytopathology, 108, 18–25.
Rouhier, N., Koh, C. S., Gelhaye, E., Corbier, C., Favier, F., Didierjean, C., et al. (2008). Redox based anti-oxidant systems in plants: Biochemical and structural analyses. Biochimica et Biophysica Acta, 1780, 1249–1260.
Scott, R. I., Chard, J. M., Hocart, M. J., Lennard, J. H., & Graham, D. C. (1996). Penetration of potato tuber lenticels by bacteria in relation to biological control of blackleg disease. Potato Research, 39, 333–344.
Soltani, J., & Hosseyni Moghaddam, M. S. (2014). Diverse and bioactive endophytic aspergilli inhabit Cupressaceae plant family. Archives of Microbiology, 196, 635–644.
Soltani, J., & Hosseyni Moghaddam, M. S. (2015). Fungal endophyte diversity and bioactivity in the Mediterranean cypress Cupressus sempervirens. Current Microbiology, 70, 580–586.
Soltani, J., Zaheri-Shoja, M., Hamzei, J., Hosseyni-Moghaddam, M. S., & Pakvaz, S. (2016). Diversity and bioactivity of endophytic bacterial community of Cupressaceae. Forest Pathology, 46, 353–361.
Sørensen, J., Sessitsch, A. (2015) Plant-associated bacteria lifestyle and molecular interactions. In Van Elsas, J.D., et al. (Eds.), Modern soil microbiology. 2nd edn. CRC Press, 2006, (pp. 211–236).
Sprent, J. I., & de Faria, S. M. (1998). Mechanisms of infection of plants by nitrogen fixing organisms. Plant and Soil, 110, 157–165.
Stojichevich, S. S., Stanisavljevich, I. V., Velichkovich, D. T., Veljkovich, V. B., & Lazich, M. L. (2008). Comparative of the antioxidant and antimicrobial activities of Sempervium marmoreum L. extracts obtained by various extraction techniques. Journal of the Serbian Chemical Society, 73, 597–607.
Strobel, G., & Daisy, B. (2003). Bioprospecting for microbial endophytes and their natural products. Microbiology and Molecular Biology Reviews, 67, 491–502.
Sun, Y., Cheng, Z., & Glick, B. R. (2009). The presence of a 1-aminocyclopropane-1-carboxylate (ACC) deaminase deletion mutation alters the physiology of the endophytic plant growth-promoting bacterium Burkholderia phytofirmans PsJN. FEMS Microbiology Letters, 296, 131–136.
Sun, C., Johnson, J. M., Cai, D., Sherameti, I., Oelmüller, 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-localized CAS protein. Journal of Plant Physiology, 167, 1009–1017.
Tiwari, R., Awasthi, A., Mall, M., Shukla, A. K., Satya Srinivas, K. V. N., Syamasundar, K. V., & Kalra, A. (2013). Bacterial endophyte-mediated enhancement of in planta content of key terpenoidindole alkaloids and growth parameters of Catharanthus roseus. Industrial Crops and Products, 43, 306–310.
van Peer, R., & Schippers, B. (1989). Plant growth responses to bacterization with selected Pseudomonas spp. strains and rhizosphere microbial development in hydroponic cultures. Canadian Journal of Microbiology, 35, 456–463.
Varma, A., Verma, S., Sudha Sahay, N., Butehorn, B., & Franken, P. (1999). Piriformospora indica, a cultivable plant-growth-promoting root endophyte. Applied and Environmental Microbiology, 65, 2741–2744.
White, J. F., & Torres, M. S. (2010). Is plant endophyte-mediated defensive mutualism the result of oxidative stress protection? Physiologia Plantarum, 138, 440–446.
White, D. C., Sutton, S. D., & Ringelberg, D. B. (1996). The genus Sphingomonas: Physiology and ecology. Current Opinion in Biotechnology, 7, 301–306.
Waller, F., Achatz, B., Baltruschat, H., Fodor, J., Becker, K., et al. (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, 13386–13391.
Acknowledgments
Dr. Soheila Mirzaei, PhD, is appreciated for her assistance in microscopy studies for fungi identification. This work was financially supported by a grant from Bu-Ali Sina University (BASU) to A. Azizi. J. Soltani dedicates this work to Setia Soltani.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
Authors declare no conflict of interest.
Electronic supplementary material
Supplementary Table 1
(DOCX 16 kb)
Rights and permissions
About this article
Cite this article
Golparyan, F., Azizi, A. & Soltani, J. Endophytes of Lippia citriodora (Syn. Aloysia triphylla) enhance its growth and antioxidant activity. Eur J Plant Pathol 152, 759–768 (2018). https://doi.org/10.1007/s10658-018-1520-x
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10658-018-1520-x