In collaboration with Scientific Association of Iranian Medicinal Plants

Document Type : Research Paper

Authors

Seed and Plant Certification and Registration Research Institute, Agricultural Research, Education and Extension Organization (AREEO), Karaj, Iran

Abstract

This study was aimed at investigating the effects of biopriming with a number of native isolates of Trichoderma harzianum on the germination and seed vigor indices of a native cumin (Cuminum cyminum L.) population. Also, the effects of extracellular enzymes produced by these isolates as elicitors on the production and accumulation of secondary metabolites in the seedlings obtained from bioprimed seeds were studied. Based on the results, all the
T. harzianum isolates were able to produce the enzymes amylase, protease, cellulase, xylanase, chitinase, and lipase. The results also showed that the cumin seed biopriming significantly affected the germination and seed vigor indices and improved the quality and health of seeds and seedlings. In this study, the essential oil of seedlings obtained from the bioprimed seeds was extracted by water distillation and its chemical compounds were identified by GC and GC/MS. The results showed that the main compounds identified included β-pinene, ρ-cymene, limonene, γ-terpinene, terpinen-4-ol, α-terpineol, cuminaldehyde, and β-farnesene. Also, T. harzianum and the enzymes secreted by it as elicitors increased the expression of genes associated with the production and accumulation of secondary metabolites in cumin. This is the first report on the effects of seed biopriming with the native isolates of T. harzianum on the essential oil compounds of cumin seedlings. The findings of this research showed that the amount of extracellular enzymes secreted by the T. harzianum isolates is different and affects the production and accumulation of secondary metabolites in cumin.

Keywords

Main Subjects

- Aali, E., Mahmoudi, R., Kazeminia, M., Hazrati, R. and Azarpey, F., 2017. Essential oils as natural medicinal substances: review article. Tehran University Medical Journal, 75: 480-489.
- Abdel-Razik, A.A., 1970. The parasitism of white Sclerotium cepivorum Berk. the incitant of white rot of onion. Ph.D. thesis, Faculty of Agriculture, Assiut University, Assiut, Egypt.
- Adams, R.P., 2007. Identification of Essential Oils Components by Gas Chromatography/Mass Spectroscopy. Allured Publishing Corporation: Carol Stream, Illinois, USA, 804p.
- Aneja, M., Gianfagna, T.J. and Hebbar, P.K., 2005. Trichoderma harzianum produces nonanoic acid, an inhibitor of spore germination and mycelial growth of two cacao pathogens. Physiological and Molecular Plant Pathology, 67(6): 304-307.
- Ansari, O., Choghazardi, H.R., Sharif Zadeh, F. and Nazarli, H., 2012. Seed reserve utilization and seedling growth of treated seeds of mountainray (Seecale montanum) as affected bydrought stress. Cercetări Agronomice în Moldova, 2: 43-48.
- Bailey, M.J., Biely, P. and Poutanen, K., 1992. Interlaboratory testing of methods for assay of xylanase activity. Journal of Biotechnology, 23(3): 257-270.
- Bansal, R. and Mukherjee, P.K., 2016. Identification of novel gene clusters for secondary metabolism in Trichoderma genomes. Microbiology, 85: 185-190.
- Behera, S., Nagarajan, S. and Rao, L.J.M., 2004. Microwave heating and conventional roasting of cumin seeds (Cuminum cyminum L.) and effect on chemical composition of volatiles. Food Chemistry, 87: 25-29.
- Beis, S.H., Azcan, T.N., Ozek, I.T., Kara, I.M. and Baser, K.H.C., 2000. Production of essential oil from cumin seeds. Chemistry of Natural Compounds, 36(3): 265-268.
- Bennett, A.J. and Whipps, J.M., 2008. Dual application of beneficial microorganisms to seed during drum priming. Applied Soil Ecology, 38: 83-89.
- Boughendjioua, H., 2019. Characterization of aroma active compounds of cumin (Cuminum cyminum L.) seed essential oil. Modern Applications of Bioequivalence & Bioavailability, 4(2): ID555634.
- Brooks, G.F., Carroll, K.C., Butel, J.S. and Morse, S.A., 2007. Medical Microbiology. New York: McGraw-Hill, 818p.
- Brunner, K., Zeilinger, S., Ciliento, R., Woo, S.L., Lorito, M., Kubicek, C.P. and Mach, R.L., 2005. Improvement of the fungal biocontrol agent Trichoderma atroviride to enhance both antagonism and induction of plant systemic disease resistance. Applied and Environmental Microbiology, 71: 3959-3965.
- Cakir, A., Kordali, S., Zengin, H., Izumi, S. and Hirata, T., 2004. Composition and antifungal activity of essential oils isolated from Hypericum hyssopifolium and Hypericum heterophyllum. Flavour and Fragrance Journal, 19: 62-68.
- Da Silva Delabona, P., Lima, D.J., Robl, D., Rabelo, S.C., Farinas, C.S. and Da Cruz Pradella, J.G., 2016. Enhanced cellulase production by Trichoderma harzianum by cultivation on glycerol followed by induction on cellulosic substrates. Journal of Industrial Microbiology and Biotechnology, 43: 617-626.
- Derakhshan, S., Sattari, M. and Bigdeli, M., 2010. Effect of cumin (Cuminum cyminum) seed essential oil on biofilm formation and plasmid integrity of Klebsiella pneumoniae. Pharmacognosy Magazine, 6: 57-61.
- Dicke, M., Van Loon, J.J.A. and Soler, R., 2009. Chemical complexity of volatiles from plants induced by multiple attack. Nature Chemical Biology, 5: 317-324.
- EL-Manylawi, M.A. and Hanaa, F.M.A., 2009. Gas chromatography-mass spectroscopy analysis and evaluate cumin seeds and their essential oil as growth promoters of New Zeland white rabbits. International Journal of Agricultural Research, 4: 107-115.
- Entesari, M., Sharifzadeh, F., Dashtaki, M. and Ahmadzadeh, M., 2013. Effects of biopriming on the germination traits, physiological characteristics, antioxidant enzymes and control of Rhizoctonia solani of a Bean cultivar (Phaseolus vulgaris L.)‎. Iranian Journal of Field Crop Science, 44: 35-45.
- Esmaeili, F., 2015. Composition of essential oil of Cuminum cyminum. Journal of Essential Oil Bearing Plants, 18: 507-509.
- Esmaeilzadeh Bahabadi, S. and Sharifi, M., 2013. Increasing the production of plant secondary metabolites using biotic elicitors. Journal of Cell & Tissue, 4: 119-128.
- Favela-Torres, E., Aguilar, C., Contreras-Esquivel, J.C. and Viniegra-Gonzalez, G., 2005. Pectinases: 273-296. In: Pandey, A., Webb, C., Soccol, C.R. and Larroche, C., (Eds.), Enzyme Technology. vol. 14, Asiatech publisher, New Delhi, 742p.
- Fiers, M., Lognay, G., Fauconnier, M.L. and Jijakli, M.H., 2013. Volatile compound-mediated interactions between barley and pathogenic fungi in the soil. PLoS ONE, 8: e66805.
- Garcia-Careno, F., Hernandez-Cortes, M.P. and Haard, N.F., 1994. Enzymes with peptidase and proteinase activity from the digestive systems of a freshwater and a marine decapods. Journal of Agricultural and Food Chemistry, 42: 1456-1461.
- Gershenzon, J. and Dudareva, N., 2007. The function of terpene natural products in the natural world. Nature Chemical Biology, 3: 408-414.
- Gholami, A.A., 2017. Production of secondary metabolites through genetic engineering and plant tissue culture. Journal of Biosafety, 10: 17-36.
- Gravel, V., Antoun, H. and Tweddell, R.J., 2007. Growth stimulation and fruit yield improvement of greenhouse tomato plants by inoculation with Pseudomonas putida or Trichoderma atroviride: possible role of indole acetic acid (IAA). Soil Biology and Biochemistry, 39: 1968-1977.
- Gupta, A., Roy, I., Patel, R.K., Singh, S.P., Khare, S.K. and Gupta, M.N., 2005. One step purification and characterization of an alkaline protease from haloalkalophilic Bacillus sp. Journal of Chromatography A, 1075: 103-108.
- Gutowska, M., Drazen, J. and Robison, B., 2004. Digestive chitinolytic activity in marine fishes of Monterey Bay, California. Comparative Biochemistry and Physiology B, 139: 351-358.
- Habibi, R., Rahnama, K. and Taghinasb, M., 2015. Evaluating the effectiveness of native Trichoderma species in production of extracellular enzymes during interaction with plant pathogenic fungus Fusarium oxysporum. Journal of Applied Research Plant Protection, 4: 73-85.
- Habibi, R., Rahnama, K. and taghinasab, M., 2018. Investigation on the effect of different levels of temperature and pH of some Trichoderma isolates for biological control of tomato wilt disease under laboratory and greenhouse conditions. Journal of Plant Protection, 32: 195-199.
- Haggag, W.M. and Abo-sedera, S.A., 2005. Characteristics of three Trichoderma species in peanut haulms compost involved in biocontrol of cumin wilt disease. International Journal Agriculture Biology, 7: 222-229.
- Hampton, J.G., Boelt, B., Rolston, M.P. and Chastain, T.G., 2013. Effects of elevated CO2 and temperature on seed quality. Journal of Agricultural Science, 151: 154-162.
- Harighi, M.J., Motallebi, M. and Zamani, M.R., 2006. Purification of chitinase 42 from Trichoderma atroviride PTCC5220. Iranian Journal OF Biology, 19: 203-214.
- Harman, G.E., Björkman, T., Ondik, K. and Shoresh, M., 2008. Changing paradigms on the mode of action and uses of Trichoderma spp. for biocontrol. Outlooks on Pest Management, 19: 24-29.
- Harman, G.E. 2006. Overview of mechanisms and uses of Trichoderma spp. Phytopathology, 96: 190-194.
- Harvey, A.L., Edrada-Ebel, R. and Quinn, R.J., 2015. The re-emergence of natural products for drug discovery in the genomics era. Nature Reviews Drug Discovery, 14: 111-112.
- Held, M., Hou, H., Miri, M., Huynh, C., Ross, L., Hossain, M.S., Sato, S., Tabata, S., Perry, J., Wang, T.L. and Szczyglowski, K., 2014. Lotus Japonicus cytokinin receptors work partially redundantly to mediate nodule formation. Plant Cell, 26: 678-694.
- Horta, M.A.C., Filho, J.A.F., Murad, N.F., Santos, E.D.O., dos Santos, C.A., Mendes, J.S., Brandão, M.M., Azzoni, S.F. and de Souza, A.P., 2018. Network of proteins, enzymes and genes linked to biomass degradation shared by Trichoderma species. Scientific Reports, 8(1341): 1-11.
- ISTA, 2010. International rules for seed testing. International Seed Testing Association (ISTA), Zurich, Switzerland.
- Jun, H., Kieselbach, T. and Jönsson, L., 2011. Enzyme production by filamentous fungi: analysis of the secretome of Trichoderma reesei grown on unconventional carbon source. Microbial Cell Factories, 10(68): 1-10.
- Kaymak, H.C., Guvenc, I., Yarali, F. and Donmez, M.F., 2009. The effects of bio-priming with PGPR on germination of radish (Raphanus sativus L.) seeds under saline conditions. Turkish Journal of Agriculture and Forestry, 33: 173-179.
- Kazemizadeh, Z., Moradi, A. and Yousefi, M., 2011. Volatile constituentes from leaf and flower of Achillea nobilis L. subsp. neireichii from North of Iran. Journal of Medicinal Plants, 10: 156-162.
- Keswani, C., Mishra, S., Sarma, B.K., Singh, S.P. and Singh, H.B., 2014. Unraveling the efficient applications of secondary metabolites of various Trichoderma spp. Applied Microbiology and Biotechnology, 98: 533-544.
- Khaledi, N. and Taheri, P., 2016. Biocontrol mechanisms of Trichoderma harzianum against soybean charcoal rot caused by Macrophomina phaseolina. Journal of Plant Protection Research, 56: 21-31.
- Kikot, G.E., Hours, R.A. and Alconada, T.M., 2009. Contribution of cell wall degrading enzymes to pathogenesis of Fusarium graminearum: A review. Journal of Basic Microbiology, 49: 231-241.
- Leeder, A.C., Palma-Guerrero, J. and Glass, N.L., 2011. The social network: deciphering fungal language. Nature Reviews Microbiology, 9: 440-451.
- Li, R. and Jiang, Z., 2004. Chemical composition of the essential oil of Cuminum cyminum L. from China. Flavour and Fragrance Journal, 19: 311-313.
- Lorito, M., Woo, S.L., Harman, G.E. and Monte, E., 2010. Translational research on Trichoderma: from ’omics to the field. Annual Review of Phytopathology, 48: 395-417.
- Malmierca, M.G., Mccormick, S.P., Cardoza, R.E., Alexander, N.J., Monte, E. and Gutiérrez S., 2015. Production of trichodiene by Trichoderma harzianum alters the perception of this biocontrol strain by plants and antagonized fungi. Environmental Microbiology, 17(8): 2628-2646.
- Mazid, M., Khan, T. and Mohammad, F., 2011. Role of secondary metabolites in defense mechanisms of plants. Biochemical Medicine, 3: 232-249.
- Miller, G.L., 1959. Use of dinitrosalicylic acid reagent for determination of reducing sugar. Analytical Chemistry, 31: 426-428.
- Moore, B.D., Andrew, R.L., Kulheim, C. and Foley, W.J., 2014. Explaining intraspecific diversity in plant secondary metabolites in an ecological context. New Phytologist, 201: 733-750.
- Mukherjee, P.K., Horwitz, B.A. and Kenerley, C.M., 2012. Secondary metabolism in Trichoderma - A genomic perspective. Microbiology, 158: 35-45.
- Namdeo, A.G., 2007. Plant cell elicitation for production of secondary metabolites. Pharmacognosy Reviews, 1: 69-79.
- Nautiyal, P.C., 2009. Seed and seedling vigor traits in groundnut (Arachis hypogaea L.). Seed Science and Technology, 37: 721-735.
- Ortega, L.M., Kikot, G.E., Astoreca, A.L. and Alconada, T.M., 2013. Screening of Fusarium graminearum isolates for enzymes extracellular and deoxynivalenol production. Journal of Mycology, 358140: 1-7.
- Paiva, N.L., 2000. An introduction to the biosynthesis of chemicals used in plant microbe interactions. Journal of Plant Growth Regulation, 19: 131-143.
- Peter, K.V., 2003. Handbook of Herbs and Spices: Vol. 1. Cambridge, UK: Woodhead Publishing Ltd, 319p.
- Piri, R., Moradi, A., Balouchi, H. and Salehi, A., 2019. Improvement of cumin (Cuminum cyminum) seed performance under drought stress by seed coating and biopriming. Scientia Horticulturae, 257: 1-8.
- Pu, G.B., Dong-Ming, M., Chen, J.L., Ma, L.Q., Wang, H. and Li, G.F., 2009. Salicylic acid activates artemisinin biosynthesis in Artemisia annua L. Plant Cell Report, 28: 1127-1135.
- Rana, V.S., 2014. Chemical composition of the essential oil of Cuminum cyminum L. seeds from Western India. Journal of Medicinal Plants and By-products, 3: 207-210.
- Reino, J.L., Guerrero, R.F., Hernandez-Galan, R. and Collado, I.G., 2008. Secondary metabolites from species of the biocontrol agent Trichoderma. Phytochemistry, 7: 89-123.
- Rezalou, Z., Shahbazi, S. and Askari, H., 2020. Effect of biopriming with Trichoderma on germination and vegetative characteristics of sweet corn, sugar. Iranian Journal of Seed Science and Technology, 8: 199-210.
- Sahana, K., Nagarajan, S. and Rao, L.J.M., 2011. Cumin (Cuminum cyminum L.) seed volatile oil: Chemistry and role in health and disease prevention: 417-427. In: Preedy, V.R., Watson, R.R., Patel, V.B., (Eds.). Nuts & Seeds in Health and Disease Prevention. New York, Elsevier, 1226p.
- Sangwan, N.S., Farooqi, A.H., Shabih, F. and Sangwan, R.S., 2001. Regulation of essential oil production in plants. Journal of Plant Growth Regulation, 34: 21-34.
- Seyed Asli, N., Harighi, M.J., Zamani, M.R. and Motalebi, M., 2004. Study of chitinolytic enzyme production in Trichoderma isolates. Iranian Journal of Biology, 17: 227-246.
- Seyis, I. and Aksoz, N., 2005. Effect of carbon and nitrogen sources on xylanase production by Trichoderma harzianum 1073 D3. International Biodeterioration and Biodegradation Journal, 55: 115-119.
- Shi, T., Shao, C., Liu, Y., Zhao, D., Cao, F., Fu, X., Yu, J., Wu, J., Zhang, Z. and Wang, C., 2020. Terpenoids from the coral-derived fungus Trichoderma harzianum (XS-20090075) induced by chemical epigenetic manipulation. Frontiers in Microbiology, 11: 1-12.
- Singh, A., Srivastava, S. and Singh, H.B., 2007. Effect of substrates on growth and shelf life of Trichoderma harzianum and its use in biocontrol of diseases. Bioresource Technology, 9: 470-473.
- Sowbhagya, H.B., Sathyendra Rao, B.V. and Krishnamurthy, N., 2008. Evaluation of size reduction and expansion on yield and quality of cumin (Cuminum cyminum) seed oil. Journal of Food Engineering, 84: 595-600.
- Tabatabaei, S.A. and Shakeri, E., 2014. Effect of seed priming on germination traits Cumin (Cuminum cyminum) under drought and salinity stresses. Arid Biome Scientific and Research Journal, 4: 66-74.
- TajickGhanbari, M.A., Mohammadkhani, H.S. and Babaeizad, V., 2014. Identification of some secondary metabolites produced by four Penicillium species. Mycologia Iranica, 1: 107-113.
- Tavakoli, H.R., Mashak, Z., Moradi, B. and Sodagari H.R., 2015. Antimicrobial activities of the combined use of Cuminum Cyminum L. essential oil, Nisin and storage temperature against Salmonella typhimurium and Staphylococcus aureus invitro. Jundishapur Journal of Microbiology, 8: 1-7.
- Ulhoa, C.J. and Peberdy, J.F., 1992. Purification and some properties of the extracellular chitinase produced by Trichoderma harzianum. Enzyme and Microbial Technology, 14: 236-240.
- Vinale, F. and Sivasithamparam, K., 2020. Beneficial effects of Trichoderma secondary metabolites on crops. Phytotherapy Research, 34(11): 1-8.
- Vinale, F., Sivasithamparam, K., Ghisalberti, E.L., Marra, R., Barbetti, M.J., Li, H., Woo, S.L. and Lorito, M., 2008. A novel role for Trichoderma secondary metabolites in the interactions with plants. Physiological and Molecular Plant Pathology, 72: 80-86.
- Vyas, R.K. and Mathur, K., 2002. Trichoderma spp. in cumin rhizosphere and their potential in suppression of wilt. Indian Phytopathology, 55: 455-457.
- Wanner, J., Bail, S., Jirovetz, L., Buchbauer, G., Schmidt, E., Gochev, V., Girova, T., Atanasova, T. and Stoyanova, A., 2010. Chemical composition and antimicrobial activity of cumin oil (Cuminum cyminum, Apiaceae). Natural Product Communications. 5: 1355-1358.
- Windham, M.T., Elad, Y. and Baker, K. 2005. A mechanism for increased plant growth inoculated by Tricoderma spp. Phytopathology, 6: 518-521.
- Wood, T.M. and Bhat, M., 1998. Methods for measuring cellulase activities. Methods in Enzymology, 160: 87-112.
- Zahir, Z.A., Arshad, M.G. and Frankenberger, W.T., 2004. Plant growth promoting Rhizobacteria application and perspectives in agriculture. Advances in Agronomy, 81: 96-168.
- Zavvari, F., Sahebani, N.A. and Etebarian, H.R., 2012. Measuring of b-1,3-glucanase activity in Trichoderma virens isolates and selection of the best isolates for biological control of cucumber root rot. Journal of Agricultural Knowledge and Sustainable Production, 22: 149-161.
- Zhao, J., Davis, L.C. and Verpoorte, R., 2005. Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnology Advances, 23: 283-333.
- Zhao, Z., Liu, H., Wang, C. and Xu, J.R., 2013. Comparative analysis of fungal genomes reveals different plant cell wall degrading capacity in fungi. BMC Genomics, 14: 274.