Arbuscular mycorrhizal fungi in drought tolerance: response in the antioxidant metabolism of Ocimum basilicum L.
DOI:
https://doi.org/10.33448/rsd-v9i12.11016Keywords:
Medicinal plants; Metabolic changes; Antioxidants.Abstract
Basil shows great importance due to the high content of bioactive substances present in the leaves, widely used in traditional medicine and the pharmaceutical industry. However, as in most plants, physiological and biochemical changes occur in drought-prone basil plants. Arbuscular mycorrhizal fungi (AMFs) have been used to minimize these changes. This study aimed to evaluate the growth and antioxidant response of basil plants under water deficit and inoculated with AMFs Clarideoglomus etunicatum. The study was carried out in a growth chamber on basil plants inoculated with AMFs and subjected to drought after 30 days after transplantation. Seedlings inoculated with AMF showed a colonization rate of 28.66 and 32.79%. Plants without AMFs inoculation and subjected to drought showed a significant reduction in stem diameter, shoot and root length, and shoot and root biomass accumulation. However, inoculation showed improved plant physiological response under water stress, increasing chlorophyll, and relative water content. Large amounts of proline have accumulated in the leaves of inoculated AMFs plants and under stress, which shows the beneficial role of these osmolites in basil subjected to drought. The antioxidant enzymes CAT and APX showed high activity in plants exposed to drought and inoculated with AMFs, which reduced the plasma membrane's damage. AMFs in basil regulated the synthesis of osmolites and antioxidant metabolism positively, promoting drought tolerance.
References
Ahanger, M. A., & Agarwal, R. M. (2017). Salinity stress induced alterations in antioxidant metabolism and nitrogen assimilation in wheat (Triticum aestivum L.) as influenced by potassium supplementation. Plant Physiology and Biochemistry, 115, 449–460.
Ait-El-Mokhtar, M., Baslam, M., Ben-Laouane, R., Anli, M., Boutasknit, A,Mitsui, T., Wahbi, S., & Meddich, A. (2020). Alleviation of detrimental effects of salt stress on date palm (Phoenix dactylifera L.) by the application of arbuscular mycorrhizal fungi and/or compost. Frontiers in Sustainable Food Systems, 4(131), 1-19.
Allen, M. F. (2006). Water dynamics of mycorrhizas in arid soils. In: Gadd G.M. (Ed.), Fungi in Biogeochemical Cycles. Cambridge University Press; Cambridge, UK.
Ali, S., Liu, Y., Ishaq, M., Shah, T., Ilyas, A. & Din, I. (2017). Climate change and its impact on the yield of major food crops: evidence from Pakistan. Foods, 6(6), 39-58.
Al-Arjani, A. F., Hashem, A., & Abd-Allah, E. F. (2020). Arbuscular mycorrhizal fungi modulates dynamics tolerance expression to mitigate drought stress in Ephedra foliata Boiss. Saudi Journal of Biological Sciences, 27(1), 380-394.
Amiri, R., Nikbakht, A., Rahimmalek, M., & Hosseini, H. (2017). Variation in the essential oil composition, antioxidant capacity, and physiological characteristics of Pelargonium graveolens L. inoculated with two species of mycorrhizal fungi under water deficit conditions. Journal of Plant Growth Regulation, 36, 502-515.
Anderson, T. H. (2003). Microbial eco-physiological indicators to assess soil quality. Agriculture, Ecosystems & Environment, 98(1-3), 285–293.
Anderson, M. D., Prasad, T. K., & Stewart, C. R. (1995). Changes in isozyme profiles of catalase, peroxidase, and glutathione reductase during acclimation to chilling in mesocotyls of maize seedlings. Plant Physiology, 109(4), 1247-1257.
Barcelos, R. C., Jham, G. N., Dhingra, O. D., Mendonça, F. A., & Valente, V. M. (2013). Identification and quantification of the major fungitoxic components of the Brazilian basil (Ocimum basilicum L.) essential oil. Journal of Food Research, 2(5), 124-131.
Bates, L., Waldren, R. P., & Teare, I. D. (1973). Rapid determination of free proline for water-stress studies. Plant and Soil, 39, 205-207.
Brookes, P. C., Powlson, D. S., & Jenkinson, D. S. (1982). Measurement of microbial biomass phosphorus in soil. Soil Biology and Biochemistry, 14(4), 319-329.
Carneiro, M. M. L. C., Deuner, S., Oliveira, P. V., Teixeira, S. B., Sousa, C. P., Bacarin, M. A., & Moraes, D. M. (2011). Atividade antioxidante e viabilidade de sementes de girassol após estresse hídrico e salino. Revista Brasileira de Sementes, 33(4), 752-761.
Caverzan, A., Casassola, A., & Brammer, S. P. (2016). Antioxidant responses of wheat plants under stress. Genetics and Molecular Biology, 39(1), 1-6.
Chai, Q., Gan, Y., Zhao, C., Xu, H. L., Waskom, R. M., Niu, Y., & Siddique, K. H. M. (2015). Regulated deficit irrigation for crop production under drought stress. A review. Agronomy for Sustainable Development, 36(3), 1-21.
Cornic, G., & Fresneau, C. (2002). Photosynthetic carbon reduction and carbon oxidation cycles are the main electron sinks for photosystem II activity during a mild drought. Annals of Botany, 89(7), 887–894.
Duc, N. H., Csintalan, Z., & Posta, K. (2018). Arbuscular mycorrhizal fungi mitigate negative effects of combined drought and heat stress on tomato plants. Plant Physiology and Biochemistry, 132, 1-30.
El-Esawi, M. A., Elansary, H. O., Elshanhory, N., Abdel-Hamid, A. M. E., & Elshikh, M. S. (2017). Salicylic acid-regulated antioxidante mechanisms and gene expression enhance Rosemary performance under saline conditions. Frontiers in Physiology, 8(716), 1-14.
Garcia, C. L., Dattamudi, S., Chanda, S., & Jayachandran, K. (2019). Effect of salinity stress and microbial inoculations on glomalin production and plant growth parameters of snap bean (Phaseolus vulgaris). Agronomy, 9(9), 545-566.
Gerdemann, J. W., & Nicolson, T. H. (1963). Spores of mycorrhizal endogene species extracted from soil by wet sieving and decanting. Transactions of the British Mycological Society, 46, 235-244.
Gholinezhad, E., Darvishzadeh, R., Moghaddam, S. S., & Popović-Djordjević, J. (2020). Effect of mycorrhizal inoculation in reducing water stress in sesame (Sesamum indicum L.): The assessment of agrobiochemical traits and enzymatic antioxidant activity. Agricultural Water Management, 238, 1-11.
Giannopolitis, C. N., & Ries, S. K. (1977). Superoxide dismutases: Occurrence in higher plants. Plant Physiology, 59(2), 309-314.
Giovanetti, M., & Mosse, B. (1980). An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytologist, 84(3), 489-500.
Golubkina, N., Logvinenko, L., Novitsky, M., Zamana, S., Sokolov, S., Molchanova, A., Shevchuk, O., Sekara, A., Tallarita, A., & Caruso, G. (2020). Yield, essential oil and quality performances of Artemisia dracunculus, Hyssopus officinalis and Lavandula angustifolia as affected by arbuscular mycorrhizal fungi under organic management. Plants, 9(3), 375-391.
Gomes, M. M. A., Lagôa, A. M. M. A., Medina, C. L., Machado, E. C., & Machado, M. A. (2004). Interactions between leaf water potential, stomatal conductance and abscisic acid content of orange trees submitted to drought stress. Brazilian Journal of Plant Physiology, 16, 155-161.
González-González, M. F., Ocampo-Alvarez, H., Santacruz-Ruvalcaba, F., Sánchez-Hernández, C. V., Cassarubias-Castillo, K., Becerril-Espinosa, A., Castañeda-Nava, J. J., & Hernández-Herrera, R. M. (2020). Physiological, ecological, and biochemical implications in tomato plants of two plant biostimulants: arbuscular mycorrhizal fungi and seaweed extract. Frontiers in Plant Science, 11(999), 1-18.
Havir, E. A., & McHale, N. A. (1987). Biochemical and developmental characterization of multiple forms of catalase in tobacco leaves. Plant Physiology, 84(2), 450-455.
Hamurcu, M., Khan, M. K., Pandey, A., Ozdemir, C., Avsaroglu, Z. Z., Elbasan, F., Omay, A. H., & Gezgin, S. (2020). Nitric oxide regulates watermelon (Citrullus lanatus) responses to drought stress. Biotechnology, 10(494), 1-14.
Hazzoumi, Z., Moustakime, Y., Elharchli, E. H., & Khalid, A. (2015). Effect of arbuscular mycorrhizal fungi (AMF) and water stress on growth, phenolic compounds, glandular hairs, and yield of essential oil in basil (Ocimum gratissimum L). Chemical and Biological Technologies in Agriculture, 2(1), 1-11.
Hoagland, D. R., & Arnon, D. I. (1950). The water culture method for growing plants without soils. California Agricultural Experiment Station.
Jenkinson, D. S., & Powlson, D. S. (1976). The effects of biocidal treatments on metabolism in soil-I. Fumigation with chloroform. Soil Biology and Biochemistry, 8(3), 167-177.
Kaschuk, G., Alberton, O., & Hungria, M. (2010). Three decades of soil microbial biomass studies in Brazilian ecosystems: Lessons learned about soil quality and indications for improving sustainability. Soil Biology and Biochemistry, 42(1), 1-13.
Kavoosi, G., & Amirghofran, Z. (2017). Chemical composition, radical scavenging and anti-oxidant capacity of Ocimum basilicum essential oil. Journal of Essential Oil Research, 29(2), 189–199.
Kavi Kishor, P. B., & Sreenivasulu, N. (2014). Is proline accumulation per se correlated with stress tolerance or is proline homeostasisa more critical issue? Plant, Cell and Environment, 37(2), 300-311.
Latef, A. A. H. A., Hashem, A., Rasool, S., Abd-Allah, E. F., Alqarawi, A. A., Egamberdieva, D., Jan, S., Anjum, N. A., & Ahmad, P. (2016). Arbuscular mycorrhizal symbiosis and abiotic stress in plants: a review. Journal of Plant Biology, 59, 407-426.
Lei, P., Xu, Z., Liang, J., Luo, X., Zhang, Y., Feng, X., & Xu, H. (2016). Poly (γ-glutamic acid) enhanced tolerance to salt stress by promoting proline accumulation in Brassica napus L. Plant and Growth Regulation, 78, 233–241.
Li, J., Meng, B., Chai, H., Yang, X., Song, W., Li, S., Lu, A., Zhang, T., & Sun, W. (2019). Arbuscular mycorrhizal fungi alleviate drought stress in C3 (Leymus chinensis) and C4 (Hemarthria altissima) grasses via altering antioxidant enzyme activities and photosynthesis. Frontiers in Plant Science, 10(499), 1-12.
Mahdavikia, H., Rezaei-Chiyaneh, E., Rahimi, A., & Mohammadkhani, N. (2019). Effects of fertilizer treatments on antioxidant activities and physiological traits of basil (Ocimum basilicum L.) under water limitation conditions. Journal of Medicinal Plants and By-products, 2, 143-151.
Mancosu, N., Snyder, R. L., Kyriakakis, G., & Spano, D. (2015). Water scarcity and future challenges for food production. Water, 7(3), 975–992.
Mathur, S., Tomar, R. S., & Jajoo, A. (2019). Arbuscular mycorrhizal fungi (AMF) protects photosynthetic apparatus of wheat under drought stress. Photosynthesis Research, 139(3), 227-238.
Maya, M. A., & Matsubara, Y. I. (2013). Influence of arbuscular mycorrhiza on the growth and antioxidative activity in cyclamen under heat stress. Mycorrhiza, 23, 381-390.
Miller, G., Suzuki, N., Ciftci-Yilmaz, S., & Mittler, R. (2010). Reactive oxygen species homeostasis and signaling during drought and salinity stresses. Plant, Cell & Environment, 33, 453–467.
Moreira, F. M. S., & Siqueira, J. O. (2006). Microbiologia e bioquímica do solo. Lavras: UFLA.
Mota, I., Sánchez-Sánchez, J., Pedro, L. G., & Sousa, M. J. (2020). Composition variation of the essential oil from Ocimum basilicum L. cv. Genovese Gigante in response to Glomus intraradices and mild water stress at different stages of growth. Biochemical Systematics and Ecology, 90, 1-14.
Moustaka, J., Tanou, G., & Adamakis, I. D. (2015). Leaf age-dependent photoprotective and antioxidative response mechanisms to paraquat-induced oxidative stress in Arabidopsis thaliana. International Journal of Molecular Sciences, 16(6), 1-18.
Nakano, Y., & Asada, K. (1981). Hydrogen peroxide is scavenged by ascorbate specific peroxidase in spinach chloroplasts. Plant and Cell Physiology, 22(5), 867-880.
Neto, L. P., Souza, L. M., Morais, M. B., Arruda, E., Figueiredo, R. C. B. Q., Albuquerque, C. C., & Ulisses, C. (2020). Morphophysiological and biochemical responses of Lippia grata Schauer (Verbenaceae) to water defcit. Journal of Plant Growth Regulation, 39, 26-40.
Novello, P. F. A. M., Bonacina, C., Stracieri, J., Campos, C. F. de A. A., Gonçalves, J. E., Gazim, Z. C., & Souza, S. G. H. de. (2020). Water deficit induces changes in grown, oxidative metabolism and phenylpropanoids biosynthesis in Ocimum basilicum L. Research, Society and Development, 9(11), e74591110590.
Pellegrino, E., Di Bene, C., Tozzini, C., & Bonari, E. (2011). Impact on soil quality of a 10-year-old short-rotation coppice poplar stand compared with intensive agricultural and uncultivated systems in a Mediterranean area. Agriculture, Ecosystems & Environmental, 140(2), 245-54.
Poonkodi, K. (2016). Chemical composition of essential oil of Ocimum basilicum L. (basil) and its biological activities-an overview. Journal of Critical Reviews, 3(3), 56–62.
Porcel, R., & Ruiz-Lozano, J. M. (2004). Arbuscular mycorrhizal influence on leaf water potential, solute accumulation, and oxidative stress in soybean plants subjected to drought stress. Journal of Experimental Botany, 55(403), 1743–1750.
Portes, M. T., Alves, T. H., & Souza, G. M. (2006). Water deficit affects photosynthetic induction in Bauhinia forficata Link (Fabaceae) and Esenbeckia leiocarpa Engl. (Rutaceae) growing in understorey and gap conditions. Brazilian Journal of Plant Physiology, 18(4), 491-502.
Rouached, A., Slama, I., Zorrig, W., Jdey, A., Cukier, C., Rabhi, O. T., Limami, A. M., & Abdelly, C. (2013). Differential performance of two forage species: Medicago truncatula and Sulla carnosa under water deficit stress and recovery. Crop & Pasture Science, 64(3), 254-264.
Rubab, S., Hussain, I., Khan, B. A., Unar, A. A., Abbas, K. A., Khichi, Z. W., Khan, M., Khanum, S., Rehman, K. U., & Khan, H. (2017). Biomedical description of Ocimum basilicum L. Journal of Islamic International Medical College, 12(1), 59-67.
Rufino, M. S. M., Alves, R. E., Brito, E. S., Morais, S. M., Sampaio, C. G., Pérez-Jiménez, J., & Saura-Calixto, F. D. (2007). Metodologia científica: determinação da atividade antioxidante total em frutas pela captura do radical livre DPPH. Comunicado Técnico nº 127. Fortaleza: EMBRAPA.
Salam, E. A., Alatar, A., & El-Sheikh, M. A. (2017). Inoculation with arbuscular mycorrhizal fungi alleviates harmful effects of drought stress on damask rose. Saudi Journal of Biological Science, 25(8), 1772–1780.
Sambatti, J. A., Junior, I. G. S., Costa, A. C. S., & Tormena, C. A. (2003). Estimativa da acidez potencial pelo método do pH SMP em solos da formação Caiuá - noroeste do estado do Paraná. Revista Brasileira de Ciência do Solo, 27(2), 257-264.
Santander, C., Aroca, R., Ruiz-Lozano, J. M., Olave, J., Cartes, P., Borie, F., & Cornejo, P. (2017). Arbuscular mycorrhiza effects on plant performance under osmotic stress. Mycorrhiza, 27, 639-657.
Schonfeld, M. A., Johnson, R. C., Carwer, B. F., & Mornhinweg, D. W. (1988). Water relations in winter wheat as drought resistance indicators. Crop Science, 28, 526-531.
Selvaraj, T., Nisha, M. C., & Rajeshkumar, S. (2009). Effect of indigenous arbuscular mycorrhizal fungi on some growth parameters and phytochemical constituents of Pogostemon patchouli Pellet. Maejo Internacional Journal of Science and Technology, 3(1), 222-234.
Sharma, S., Villamor, J. G., & Verslues, P. E. (2011). Essential role of tissue‐specific proline synthesis and catabolism in growth and redox balance at low water potential. Plant Physiology, 157(1), 292– 304.
Shirazi, M., Gholami, H., Kavoosi, G., Rowshan, V., & Tafsiry, A. (2014). Chemical composition, antioxidant, antimicrobial and cytotoxic activities of Tagets minuta and Ocimum basilicum essential oils. Food Science & Nutrition, 2(2), 146–155.
Silva, S. R. S., Demuner, A. J., Barbosa, L. C. A., Casali, V. W. D., Nascimento, E. A., & Pinheiro, A. L. (2002). Efeito do estresse hídrico sobre características de crescimento e a produção de óleo essencial de Melaleuca alternifolia Cheel. Acta Scientiarum, 24, 1363-1368.
Silva, F. C. (2009). Manual de análises químicas de solos, plantas e fertilizantes. Brasília: Embrapa informação tecnológica.
Silveira, J. A. G., Melo, A. R. B., Viégas, R. A., & Oliveira, J. T. A. (2001). Salt-induced effects on the nitrogen assimilation related to growth in cowpea plants. Environmental and Experimental Botany, 46(2), 171-179.
Smith, S. E., & Read, D. J. (2008). Mycorrhizal symbiosis. Academic Press, Amsterdam, NL.
STATSOFT, Inc. (2017). Statistica data analysis software system version 13.1. Disponível em: < http://www.statsoft.com>
Taiz, L., & Zeiger, E. (2017). Fisiologia vegetal. Porto Alegre: Artemed.
Tate, K. R., Ross, D. J., & Feltham, C. W. (1988). A direct extraction method to estimate soil microbial C: Effects of experimental variables and some different calibration procedures. Soil Biology and Biochemistry, 20(3), 329-335.
Tisarum, R., Theerawitaya, C., Samphumphuang, T., Phisalaphong, M., Singh, H. P., & Cha-um, S. (2019). Promoting water deficit tolerance and anthocyanin fortification in pigmented rice cultivar (Oryza sativa L. subsp. indica) using arbuscular mycorrhizal fungi inoculation. Physiology and Molecular Biology of Plants, 25, 821-835.
Tyagi, S., Sharma, S., Taneja, M., Shumayla, Kumar, R., Sembi, J. K., & Upadhyay, S. K. (2017). Superoxide dismutases in bread wheat (Triticum aestivum L.): Comprehensive characterization and expression analysis during development and, biotic and abiotic stresses. Agri Gene, 6, 1-13.
Umoh, R. A., Johnny, I. I., Udoh, A. E., Elijah, A. A., Umoh, O. T., & Essiet, L. E. (2020). Comparative evaluation of the larvicidal properties of methanol extracts and fractions of Ocimum gratissimum L. and Ocimum basilicum L. leaves (Lamiaceae) on the fourth instar larvae of Culex quinquefasciatus L. and control of filariasis. Journal of Complementary and Alternative Medical Research, 11(3), 24-31.
Vanani, F. R., Shabani, L., SAbzalian, M. R., Dehghanian, F., & Winner, L. (2020). Comparative physiological and proteomic analysis indicates lower shock response to drought stress conditions in a self-pollinating perennial ryegrass. Plos One, 15(6): e0234317.
Vance, E. D., Brookes, P. C., & Jenkinson, D. S. (1987). An extraction method for measuring soil microbial biomass. Soil Biology and Biochemistry, 19(6), 703-707.
Witt, C., Gaunt, J. L., Galicia, C. C., Ottow, J. C. G., & Neue, H. U. (2000). A rapid chloroform-fumigation extraction method for measuring soil microbial biomass carbon and nitrogen in flooded rice soils. Biology and fertility of Soils, 30(5), 510-519.
Yooyongwech, S., Theerawitaya, C., Samphumphuang, T., & Cha-Um, S. (2013). Water-deficit tolerant identification in sweet potato genotypes (Ipomoea batatas (L.) Lam.) in vegetative developmental stage using multivariate physiological índices. Scientia Horticulturae, 162(23), 242-251.
Zangaro, W., Alves, R. A., Lescano, L. E., & Ansanelo, A. P. (2012). Investment in fine roots and arbuscular mycorrhizal fungi decrease during succession in three Brazilian ecosystems. Biotropica, 44(2), 141- 150.
Zhang, Z., Zhang, J., Xu, G., Zhou, L. & Li, Y. (2019). Arbuscular mycorrhizal fungi improve the growth and drought tolerance of Zenia insignis seedlings under drought stress. New Forests, 50(4), 593-604.
Zhu, X. C., Song, F. B., Liu, S. Q., Liu, T. D., & Zhou, X. (2012). Arbuscular mycorrhizae improves photosynthesis and water status of Zea mays L. under drought stress. Plant, Soil and Environment, 58(4), 186–191
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