PROTECTIVE ROLE OF 2-BORNEOL IN THE EMERGENCE OF Allium cepa SEEDS EXPOSED TO NaCl
Palavras-chave:
Oxidative stress, salinity, phytotoxicity, borneol, A. cepaResumo
It has been proposed that borneol acts as a compound responsible for inducing tolerance to salt stress in the Allium cepa model organism. This study investigated the effect of borneol variation (100, 300 and 500 µg/mL) on the phytotoxic potential in seed emergence, growth of seedlings, roots and leaves in A. cepa under field conditions, normal and induced by NaCl (150 mM). Changes in and lipid peroxidation (LPO) levels was evaluated as markers of oxidative stress, and the antioxidant activity of borneol was evaluated by DPPH test. The exposure of A. cepa to 150 mM of NaCl significantly decreased the emergence capacity of the seeds. Nevertheless, borneol at concentrations of 100 and 300 µg/mL significantly reduced the salt stress and improved the emergence rate and the number of roots. Borneol significantly reduced lipid peroxidation (LPO) caused by NaCl, but, did not have any effect on the total iron content. Borneol exhibited DPPH radical scavenging activity similar to that of ascorbic acid used as standard antioxidant. The nutrients with the highest accumulation in the soil were P> S> Ca> N> K> Mg. Moreover, the pH was ideal for the cultivation of the species. The results of this study suggest that borneol can be used as a potential tolerance regulator to improve resistance to salt stress in Allium cepa.
Referências
[1] KUSVURAN, A. The effects of salt stress on the germination and antioxidative enzyme activity of Hungarian vetch (Vicia pannonica Crantz.) varieties. Legume Research-An Inter. J. n. 38, p. 51-59, 2015.
[2] HERNANDEZ, L.; ALEGRE, L.; MUNNE-BOSCH, S. Drought-induced changes in flavonoids and other low molecular weight antioxidants in Cistus clusii grown under Mediterranean field conditions, Tree Physiol. n. 24, p. 1303–1311, 2004.
[3] ALSAEEDI, A. et al. Exogenous nanosilica improves germination and growth of cucumber by maintaining K+/ Na+ ratio under elevated Na+ stress. Plant Physiol. Biochem. n. 125, p. 64–171, 2018.
[4] MISRA, N.; DWIVEDI, U. N. Genotypic difference in salinity tolerance of green gram cultivars. Plant Science, v. 166, n. 5, p. 1135-1142, 2004.
[5] ALMANSOURI, M.; KINET, J.-M.; LUTTS, Stanley. Effect of salt and osmotic stresses on germination in durum wheat (Triticum durum Desf.). Plant and soil, v. 231, n. 2, p. 243-254, 2001.
[6] KHALIQ, A. et al. Salinity tolerance in wheat cultivars is related to enhanced activities of enzymatic antioxidants and reduced lipid peroxidation. CLEAN–Soil, Air, Water, v. 43, n. 8, p. 1248-1258, 2015.
[7] BARNAWAL, D. et al. Plant growth‐promoting rhizobacteria enhance wheat salt and drought stress tolerance by altering endogenous phytohormone levels and TaCTR1/TaDREB2 expression. Physiologia plantarum, v. 161, n. 4, p. 502-514, 2017.
[8] IVANOVA, K. et al. Influence of Salt Stress on Stomatal, Biochemical and Morphological Factors Limiting Photosynthetic Gas Exchange in Paulownia Elongata× Fortunei. Comptes rendus de l’Académie bulgare des Sciences. v. 68, n. 2, 2015.
[9] MUNNS, R.; TESTER, M. Mechanisms of salinity tolerance. Annu. Rev. Plant Biol., v. 59, p. 651-681, 2008.
[10] FOOLAD, M. R. Recent advances in genetics of salt tolerance in tomato. Plant Cell, tissue and organ culture, v. 76, n. 2, p. 101-119, 2004.
[11] GUPTA, R. K.; ABROL, I. P. Salt-affected soils: their reclamation and management for crop production. In: Advances in soil science. Springer, New York, NY, 1990. p. 223-288.
[12] MUNNS, R. Comparative physiology of salt and water stress. Plant, cell & environment, v. 25, n. 2, p. 239-250, 2002.
[13] BARROS, M. de F. C. et al. Recuperação de solos afetados por sais pela aplicação de gesso de jazida e calcário no Nordeste do Brasil. Revista Brasileira de Engenharia Agrícola e Ambiental, v. 8, n. 1, p. 59-64, 2004.
[14] QADIR, M. et al. Phytoremediation of sodic and saline‐sodic soils. Advances in agronomy, v. 96, p. 197-247, 2007.
[15] SILVA, P. O. et al. Germination of salt-stressed seeds as related to the ethylene biosynthesis ability in three Stylosanthes species. Journal of plant physiology, v. 171, n. 1, p. 14-22, 2014.
[16] WEIDENHAMER, J. D. et al. Just how insoluble are monoterpenes? Journal of Chemical Ecology, v. 19, n. 8, p. 1799-1807, 1993.
[17] SINGH, H. P. et al. Comparative phytotoxicity of four monoterpenes against Cassia occidentalis. Annals of Applied Biology, v. 141, n. 2, p. 111-116, 2002.
[18] SINGH, H. Pal et al. Phytotoxicity of the volatile monoterpene citronellal against some weeds. Zeitschrift für Naturforschung C, v. 61, n. 5-6, p. 334-340, 2006.
[19] ZUNINO, M. P.; ZYGADLO, J. A. Effect of monoterpenes on lipid oxidation in maize. Planta, v. 219, n. 2, p. 303-309, 2004.
[20] NISHIDA, N. et al. Allelopathic effects of volatile monoterpenoids produced by Salvia leucophylla: inhibition of cell proliferation and DNA synthesis in the root apical meristem of Brassica campestris seedlings. Journal of chemical ecology, v. 31, n. 5, p. 1187-1203, 2005.
[21] LANGENHEIM, J. H. Higher plant terpenoids: a phytocentric overview of their ecological roles. Journal of chemical ecology, v. 20, n. 6, p. 1223-1280, 1994.
[22] ISMAN, M. B. Plant essential oils for pest and disease management. Crop protection, v. 19, n. 8-10, p. 603-608, 2000.
[23] LEE, B.-H. et al. Fumigant toxicity of essential oils from the Myrtaceae family and 1, 8-cineole against 3 major stored-grain insects. Journal of Stored Products Research, v. 40, n. 5, p. 553-564, 2004.
[24] KORDALI, S. et al. Antifungal, phytotoxic and insecticidal properties of essential oil isolated from Turkish Origanum acutidens and its three components, carvacrol, thymol and p-cymene. Bioresource Technology, v. 99, n. 18, p. 8788-8795, 2008.
[25] HORVÁTHOVÁ, E. et al. Effects of borneol on the level of DNA damage induced in primary rat hepatocytes and testicular cells by hydrogen peroxide. Food and Chemical Toxicology, v. 47, n. 6, p. 1318-1323, 2009.
[26] BHATIA, S. P.; LETIZIA, C. S.; API, A. M. Fragrance material review on borneol. Food and chemical toxicology, v. 46, n. 11, p. S77-S80, 2008.
[27] WU, H.-Y. et al. The synergetic effect of edaravone and borneol in the rat model of ischemic stroke. European Journal of Pharmacology, v. 740, p. 522-531, 2014.
[28] ASPLUND, R. Owen. Some quantitative aspects of the phytotoxicity of monoterpenes. Weed Science, v. 17, n. 4, p. 454-455, 1969.
[29] IQBAL, M. et al. Bioassays based on higher plants as excellent dosimeters for ecotoxicity monitoring: a review.vChemistry International, v. 5, n. 1, p. 1-80, 2019.
[30] LEME, D. M.; MARIN-MORALES, M. A. Allium cepa test in environmental monitoring: a review on its application. Mutation Research/Reviews in Mutation Research, v. 682, n. 1, p. 71-81, 2009.
[31] PATNAIK, A. R.; ACHARY, V. M. M.; PANDA, B. B. Chromium (VI)-induced hormesis and genotoxicity are mediated through oxidative stress in root cells of Allium cepa L. Plant growth regulation, v. 71, n. 2, p. 157-170, 2013.
[32] KUMARI, M. et al. Cytogenetic and genotoxic effects of zinc oxide nanoparticles on root cells of Allium cepa. Journal of hazardous materials, v. 190, n. 1-3, p. 613-621, 2011.
[33] MODLITBOVÁ, P. et al. Short-term assessment of cadmium toxicity and uptake from different types of Cd-based Quantum Dots in the model plant Allium cepa L. Ecotoxicology and environmental safety, v. 153, p. 23-31, 2018.
[34] FOUAD, A. S.; HAFEZ, R. M. The effects of silver ions and silver nanoparticles on cell division and expression of cdc2 gene in Allium cepa root tips. Biologia Plantarum, v. 62, n. 1, p. 166-172, 2018.
[35] RAJPUT, V. D. et al. Effects of copper nanoparticles (CuO NPs) on crop plants: a mini review. BioNanoScience, v. 8, n. 1, p. 36-42, 2018.
[36] FATMA, F. et al. Phytotoxicity of pesticides mancozeb and chlorpyrifos: correlation with the antioxidative defence system in Allium cepa. Physiology and molecular biology of plants, v. 24, n. 1, p. 115-123, 2018.
[37] LUO, Y. et al. Seed germination test for toxicity evaluation of compost: Its roles, problems and prospects. Waste Management, v. 71, p. 109-114, 2018.
[38] BEWLEY J. D.; BLACK M. Seeds: Physiology of Development and Germination, 2nd (edn), Plenum Press, New York, London, USA. 1994
[39] DA SILVA, L. C. et al. Influence of temperature on the germination and root size of Acmella oleracea (L.) RK Jansen. Revista Agro@ mbiente On-line, v. 14, 2020.
[40] LABOURIAU, L. G. On the frequency of isothermal germination in seeds of Dolichos biflorus L. Plant and Cell Physiology, v. 19, n. 3, p. 507-512, 1978.
[41] ORZOLEK, M. D. Establishment of vegetables in the field. HortTechnology, v. 1, n. 1, p. 78-81, 1991.
[42] GRASSBAUGH, E. M.; BENNETT, M. A. Factors affecting vegetable stand establishment. Scientia Agricola, v. 55, n. SPE, p. 116-120, 1998.
[43] HACKBART, V. C. dos S.; CORDAZZO, C. V. Ecologia das sementes e estabelecimento das plântulas de Hydrocotyle bonariensis Lam. 2003.
[44] LEAL, C. C. P. et al. Water stress on germination and vigor of ‘mofumbo’(Combretum leprosum Mart.) seeds at different temperatures. Revista Ciência Agronômica, v. 51, n. 1, 2020.
[45] MARTINS, C. C.; NAKAGAWA, J.; BOVI, M. L. A. Efeito da posição da semente no substrato e no crescimento inicial das plântulas de palmito-vermelho (Euterpe espiritosantensis Fernandes–Palmae). Revista Brasileira de Sementes, v. 21, n. 1, p. 164-173, 1999.
[46] FOTOPOULOS, V. et al. Involvement of AsA/DHA and GSH/GSSG ratios in gene and protein expression and in the activation of defence mechanisms under abiotic stress conditions. In: Ascorbate-glutathione pathway and stress tolerance in plants. Springer, Dordrecht, 2010. p. 265-302.
[47] GUNES, A. et al. Salicylic acid induced changes on some physiological parameters symptomatic for oxidative stress and mineral nutrition in maize (Zea mays L.) grown under salinity. Journal of Plant Physiology, v. 164, n. 6, p. 728-736, 2007.
[48] DHANYALAKSHMI, K. H.; VIJAYALAKSHMI, C.; BOOMINATHAN, R. Evaluation of physiological and biochemical responses of rice (Oryza sativa L.) varieties to salt stress. Indian Journal of Agricultural Research, v. 47, n. 2, p. 91-99, 2013.
[49] MISHRA, A.; CHOUDHURI, M. A. Effects of salicylic acid on heavy metal-induced membrane deterioration mediated by lipoxygenase in rice. Biologia Plantarum, v. 42, n. 3, p. 409-415, 1999.
[50] TEIXEIRA, P. C.; DONAGEMMA, G. K.; FONTANA, A.; TEIXEIRA, W. G. (Ed.). Manual de métodos de análise de solo. 3. ed. rev. e ampl. Brasília, DF: Embrapa, pt. 1, cap. 4, p. 34-46, 2017
[51] PÕLDMA, P. et al. Selenium treatment under field conditions affects mineral nutrition, yield and antioxidant properties of bulb onion (Allium cepa L.). Acta Sci. Pol., Hortorum Cultus, v. 12, n. 6, p. 167-181, 2013.
[52] FISKESJÖ, G. The Allium test as a standard in environmental monitoring. Hereditas, v. 102, n. 1, p. 99-112, 1985.
[53] KAMDEM, J. P. et al. Antioxidant activity, genotoxicity and cytotoxicity evaluation of lemon balm (Melissa officinalis L.) ethanolic extract: Its potential role in neuroprotection. Industrial Crops and Products, v. 51, p. 26-34, 2013.
[54] KLIMACZEWSKI, C. V. et al. Antioxidant activity of Peumus boldus extract and alkaloid boldine against damage induced by Fe (II)–citrate in rat liver mitochondria in vitro. Industrial Crops and Products, v. 54, p. 240-247, 2014.
[55] BARBOSA FILHO, V. M. et al. Phytochemical constituents, antioxidant activity, cytotoxicity and osmotic fragility effects of Caju (Anacardium microcarpum). Industrial Crops and Products, v. 55, p. 280-288, 2014.
[56] DUARTE, A. E. et al. Antimicrobial activity and Modulatory effect of essential oil from the leaf of Rhaphiodon echinus (Nees & Mart) Schauer on some antimicrobial drugs. Molecules, v. 21, n. 6, p. 743, 2016.
[57] AFTAB, S. et al. Impact of potassium on the growth and yield contributing attributes of onion (Allium cepa L.). Asian Research Journal of Agriculture, p. 1-4, 2017.
[58] MOLLAVALI, M. et al. Nitrogen form and mycorrhizal inoculation amount and timing affect flavonol biosynthesis in onion (Allium cepa L.). Mycorrhiza, v. 28, n. 1, p. 59-70, 2018.
[59] MENDES, A. M. S. et al. Nutrição mineral e adubação da cultura da cebola no Submédio do Vale do São Francisco. Embrapa Semiárido-Circular Técnica (INFOTECA-E), 2008.
[60] MEKONNEN, D. A.; MIHRETU, F. G.; WOLDETSADIK, K. Farmyard manure and intra-row spacing on yield and yield components of Adama Red onion (Allium cepa L.) cultivar under irrigation in Gewane District, Afar Region, Ethiopia. Journal of Horticulture and Forestry, v. 9, n. 5, p. 40-48, 2017.
[61] RESENDE, GM de; COSTA, N. D.; SOUZA, RJ de. Cultivo da cebola no Nordeste. Petrolina: Embrapa Semi-Árido, 2007. Sistemas de Produção, 3. 2012.
[62] BÜNEMANN, E. K. et al. Soil quality–A critical review. Soil Biology and Biochemistry, v. 120, p. 105-125, 2018.
[63] DAKER, A. Irrigação e drenagem: A água na agricultura. Freitas Bastos, 1988.
[64] RICHARDS, L. A. Diagnosis and improvement of saline and alkali soils. Handbook No. 60. US Department of Agriculture, Washington, DC, 1954.
[65] FASSBENDER, H. W.; BORNEMISZA, Elemer. Química de suelos con énfasis en suelos de América Latina. Iica, 1987.
[66] ROLSTON, D. E.; BIGGAR, J. W.; NIELSEN, D. R. Effect of salt on soils. California Agriculture 38:11-13. 1984.
[67] Saffaryazdi, A.; Lahouti, M.; Ganjeali, A. The effect of different concentrations of selenium on morphophysiological characteristics of spinach (Spinacia oleracea L.), J. Hort. Sci. 26, 292-300. 2012.
[68] MARSCHNER, H. Marschner's mineral nutrition of higher plants. Academic press, 2011.
[69] NUNES, R. T. C. et al. Desempenho germinativo de sementes de girassol submetidas ao estresse salino. Cultura Agronômica: Revista de Ciências Agronômicas, v. 25, n. 1, p. 79-92, 2016.
[70] PINHEIRO, D. T. et al. Germination and antioxidant action in melon seeds exposed to salt stress. Pesquisa Agropecuária Tropical, v. 46, n. 3, p. 336-342, 2016.
[71] SCANDALIOS, J. G. Oxidative stress: molecular perception and transduction of signals triggering antioxidant gene defenses. Brazilian journal of medical and biological research, v. 38, n. 7, p. 995-1014, 2005.
[72] HALLIWELL, B. Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant physiology, v. 141, n. 2, p. 312-322, 2006.
[73] MILLER, G. A. D. et al. Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant, cell & environment, v. 33, n. 4, p. 453-467, 2010.
[74] YACOUBI, R. et al. Proteomic analysis of the enhancement of seed vigour in osmoprimed alfalfa seeds germinated under salinity stress. Seed Science Research, v. 23, n. 2, p. 99-110, 2013.
[75] ANSARI, N. A.; KHALEGHI, S.-S. Germination and emergence response of some onion cultivars of southern Iran to salinity stress. Seed Science and Biotechnology, v. 3, n. 1, p. 21-23, 2009.
[76] BYBORDI, A.; SAADAT, S.; ZARGARIPOUR, P. The effect of zeolite, selenium and silicon on qualitative and quantitative traits of onion grown under salinity conditions. Archives of Agronomy and Soil Science, v. 64, n. 4, p. 520-530, 2018.
[77] DE GÓIS, V. A.; TORRES, S. B.; PEREIRA, R. A. Germinação de sementes de maxixe submetidas a estresse salino. Revista Caatinga, v. 21, n. 4, 2008.
[78] LACERDA, C. F. et al. Morpho-physiological responses of cowpea leaves to salt stress. Brazilian Journal of Plant Physiology, v. 18, n. 4, p. 455-465, 2006.
[79] GAMIELY, S. et al. Onion plant growth, bulb quality, and water uptake following ammonium and nitrate nutrition. HortScience, v. 26, n. 8, p. 1061-1063, 1991.
[80] BREWSTER, J. L. The classification, origins, distribution and economic importance of the major vegetable crops. Onions and Other Vegetable Alliums. Wallingford: CAB International, p. 1-18, 1994.
[81] BERNSTEIN, Leon; FRANCOIS, L. E.; CLARK, R. A. Interactive effects of salinity and fertility on yields of grains and vegetables 1. Agronomy Journal, v. 66, n. 3, p. 412-421, 1974.
[82] SHANNON, M. C.; GRIEVE, C. M. Tolerance of vegetable crops to salinity. Scientia horticulturae, v. 78, n. 1-4, p. 5-38, 1998.
[83] MAIA, J. M. et al. Salt-induced changes in antioxidative enzyme activities in root tissues do not account for the differential salt tolerance of two cowpea cultivars. Brazilian Journal of Plant Physiology, v. 22, n. 2, p. 113-122, 2010.
[84] ASHRAF, M. P. J. C.; HARRIS, P. J. C. Potential biochemical indicators of salinity tolerance in plants. Plant science, v. 166, n. 1, p. 3-16, 2004.
[85] HAJIBAGHERI, M. A. et al. Salinity resistance in Zea mays: fluxes of potassium, sodium and chloride, cytoplasmic concentrations and microsomal membrane lipids. Plant, Cell & Environment, v. 12, n. 7, p. 753-757, 1989.
[86] POTTERS, G. et al. Stress-induced morphogenic responses: growing out of trouble?. Trends in plant science, v. 12, n. 3, p. 98-105, 2007.
[87] SUN, F. et al. Salt modulates gravity signaling pathway to regulate growth direction of primary roots in Arabidopsis. Plant physiology, v. 146, n. 1, p. 178-188, 2008.
[88] BERNSTEIN, N.; ESHEL, A.; BEECKMAN, T. Effects of salinity on root growth. Plant roots: the hidden half, p. 1-784, 2013.
[89] JULKOWSKA, M. M. et al. Capturing Arabidopsis root architecture dynamics with ROOT-FIT reveals diversity in responses to salinity. Plant Physiology, v. 166, n. 3, p. 1387-1402, 2014.
[90] OKUSANYA, O. T. The effect of sea water and temperature on the germination behaviour of Crithmum maritimum. Physiologia Plantarum, v. 41, n. 4, p. 265-267, 1977.
[91] CREELMAN, R. A. et al. Water deficit and abscisic acid cause differential inhibition of shoot versus root growth in soybean seedlings: analysis of growth, sugar accumulation, and gene expression. Plant Physiology, v. 92, n. 1, p. 205-214, 1990.
[92] SAAB, I. N. et al. Increased endogenous abscisic acid maintains primary root growth and inhibits shoot growth of maize seedlings at low water potentials. Plant physiology, v. 93, n. 4, p. 1329-1336, 1990.
[93] WAHID, A. et al. Short term incubation of sorghum caryopses in sodium chloride levels: changes in some pre-and post-germination physiological parameters. Plant Science, v. 139, n. 2, p. 223-232, 1998.
[94] DASH, M.; PANDA, S. K. Salt stress induced changes in growth and enzyme activities in germinating Phaseolus mungo seeds. Biologia plantarum, v. 44, n. 4, p. 587-589, 2001.
[95] PINHEIRO, H. A. et al. Leaf gas exchange, chloroplastic pigments and dry matter accumulation in castor bean (Ricinus communis L) seedlings subjected to salt stress conditions. Industrial Crops and Products, v. 27, n. 3, p. 385-392, 2008.
[96] FERREIRA-SILVA, S. L. et al. Changes in physiological indicators associated with salt tolerance in two contrasting cashew rootstocks. Brazilian Journal of Plant Physiology, v. 20, n. 1, p. 51-59, 2008.
[97] DA SILVA, E. N.et al. Ion uptake and growth of pinhão-manso under different salinity levels. Revista Ciência Agronômica, v. 40, n. 2, p. 240, 2009.
[98] MARTINO, L. De et al. The antigerminative activity of twenty-seven monoterpenes. Molecules, v. 15, n. 9, p. 6630-6637, 2010.
[99] MEAGHER, E. A.; FITZGERALD, G. A. Indices of lipid peroxidation in vivo: strengths and limitations. Free Radical Biology and Medicine, v. 28, n. 12, p. 1745-1750, 2000.
[100] MITTLER, R. Oxidative stress, antioxidants and stress tolerance. Trends in plant science, v. 7, n. 9, p. 405-410, 2002.
[101] TANOU, G. et al. Proteomics reveals the overlapping roles of hydrogen peroxide and nitric oxide in the acclimation of citrus plants to salinity. The Plant Journal, v. 60, n. 5, p. 795-804, 2009.
[102] WANG, P. et al. Hydrogen peroxide–mediated activation of MAP kinase 6 modulates nitric oxide biosynthesis and signal transduction in Arabidopsis. The Plant Cell, v. 22, n. 9, p. 2981-2998, 2010.
[103] FILIPPOU, P.; ANTONIOU, C.; FOTOPOULOS, V. Effect of drought and rewatering on the cellular status and antioxidant response of Medicago truncatula plants. Plant Signaling & Behavior, v. 6, n. 2, p. 270-277, 2011.
[104] ABOGADALLAH, G. M. Insights into the significance of antioxidative defense under salt stress. Plant signaling & behavior, v. 5, n. 4, p. 369-374, 2010.
[105] BARTOLI, C. G. et al. Interactions between hormone and redox signalling pathways in the control of growth and cross tolerance to stress. Environmental and Experimental Botany, v. 94, p. 73-88, 2013.
[106] MATYSIK, J. et al. Molecular mechanisms of quenching of reactive oxygen species by proline under stress in plants. Current Science, p. 525-532, 2002.
[107] MUNNÉ-BOSCH, S.; QUEVAL, G.; FOYER, C. H. The impact of global change factors on redox signaling underpinning stress tolerance. Plant Physiology, v. 161, n. 1, p. 5-19, 2013.
[108] DUAN, J. et al. Exogenous spermidine affects polyamine metabolism in salinity-stressed Cucumis sativus roots and enhances short-term salinity tolerance. Journal of plant physiology, v. 165, n. 15, p. 1620-1635, 2008.
[109] YAZICI, I. et al. Salinity tolerance of purslane (Portulaca oleracea L.) is achieved by enhanced antioxidative system, lower level of lipid peroxidation and proline accumulation. Environmental and Experimental Botany, v. 61, n. 1, p. 49-57, 2007.
[110] SU, J. et al. Composition and biological activities of the essential oil extracted from a novel plant of Cinnamomum camphora Chvar. Borneol. Journal of Medicinal Plants Research, v. 6, n. 18, p. 3487-3494, 2012.
[2] HERNANDEZ, L.; ALEGRE, L.; MUNNE-BOSCH, S. Drought-induced changes in flavonoids and other low molecular weight antioxidants in Cistus clusii grown under Mediterranean field conditions, Tree Physiol. n. 24, p. 1303–1311, 2004.
[3] ALSAEEDI, A. et al. Exogenous nanosilica improves germination and growth of cucumber by maintaining K+/ Na+ ratio under elevated Na+ stress. Plant Physiol. Biochem. n. 125, p. 64–171, 2018.
[4] MISRA, N.; DWIVEDI, U. N. Genotypic difference in salinity tolerance of green gram cultivars. Plant Science, v. 166, n. 5, p. 1135-1142, 2004.
[5] ALMANSOURI, M.; KINET, J.-M.; LUTTS, Stanley. Effect of salt and osmotic stresses on germination in durum wheat (Triticum durum Desf.). Plant and soil, v. 231, n. 2, p. 243-254, 2001.
[6] KHALIQ, A. et al. Salinity tolerance in wheat cultivars is related to enhanced activities of enzymatic antioxidants and reduced lipid peroxidation. CLEAN–Soil, Air, Water, v. 43, n. 8, p. 1248-1258, 2015.
[7] BARNAWAL, D. et al. Plant growth‐promoting rhizobacteria enhance wheat salt and drought stress tolerance by altering endogenous phytohormone levels and TaCTR1/TaDREB2 expression. Physiologia plantarum, v. 161, n. 4, p. 502-514, 2017.
[8] IVANOVA, K. et al. Influence of Salt Stress on Stomatal, Biochemical and Morphological Factors Limiting Photosynthetic Gas Exchange in Paulownia Elongata× Fortunei. Comptes rendus de l’Académie bulgare des Sciences. v. 68, n. 2, 2015.
[9] MUNNS, R.; TESTER, M. Mechanisms of salinity tolerance. Annu. Rev. Plant Biol., v. 59, p. 651-681, 2008.
[10] FOOLAD, M. R. Recent advances in genetics of salt tolerance in tomato. Plant Cell, tissue and organ culture, v. 76, n. 2, p. 101-119, 2004.
[11] GUPTA, R. K.; ABROL, I. P. Salt-affected soils: their reclamation and management for crop production. In: Advances in soil science. Springer, New York, NY, 1990. p. 223-288.
[12] MUNNS, R. Comparative physiology of salt and water stress. Plant, cell & environment, v. 25, n. 2, p. 239-250, 2002.
[13] BARROS, M. de F. C. et al. Recuperação de solos afetados por sais pela aplicação de gesso de jazida e calcário no Nordeste do Brasil. Revista Brasileira de Engenharia Agrícola e Ambiental, v. 8, n. 1, p. 59-64, 2004.
[14] QADIR, M. et al. Phytoremediation of sodic and saline‐sodic soils. Advances in agronomy, v. 96, p. 197-247, 2007.
[15] SILVA, P. O. et al. Germination of salt-stressed seeds as related to the ethylene biosynthesis ability in three Stylosanthes species. Journal of plant physiology, v. 171, n. 1, p. 14-22, 2014.
[16] WEIDENHAMER, J. D. et al. Just how insoluble are monoterpenes? Journal of Chemical Ecology, v. 19, n. 8, p. 1799-1807, 1993.
[17] SINGH, H. P. et al. Comparative phytotoxicity of four monoterpenes against Cassia occidentalis. Annals of Applied Biology, v. 141, n. 2, p. 111-116, 2002.
[18] SINGH, H. Pal et al. Phytotoxicity of the volatile monoterpene citronellal against some weeds. Zeitschrift für Naturforschung C, v. 61, n. 5-6, p. 334-340, 2006.
[19] ZUNINO, M. P.; ZYGADLO, J. A. Effect of monoterpenes on lipid oxidation in maize. Planta, v. 219, n. 2, p. 303-309, 2004.
[20] NISHIDA, N. et al. Allelopathic effects of volatile monoterpenoids produced by Salvia leucophylla: inhibition of cell proliferation and DNA synthesis in the root apical meristem of Brassica campestris seedlings. Journal of chemical ecology, v. 31, n. 5, p. 1187-1203, 2005.
[21] LANGENHEIM, J. H. Higher plant terpenoids: a phytocentric overview of their ecological roles. Journal of chemical ecology, v. 20, n. 6, p. 1223-1280, 1994.
[22] ISMAN, M. B. Plant essential oils for pest and disease management. Crop protection, v. 19, n. 8-10, p. 603-608, 2000.
[23] LEE, B.-H. et al. Fumigant toxicity of essential oils from the Myrtaceae family and 1, 8-cineole against 3 major stored-grain insects. Journal of Stored Products Research, v. 40, n. 5, p. 553-564, 2004.
[24] KORDALI, S. et al. Antifungal, phytotoxic and insecticidal properties of essential oil isolated from Turkish Origanum acutidens and its three components, carvacrol, thymol and p-cymene. Bioresource Technology, v. 99, n. 18, p. 8788-8795, 2008.
[25] HORVÁTHOVÁ, E. et al. Effects of borneol on the level of DNA damage induced in primary rat hepatocytes and testicular cells by hydrogen peroxide. Food and Chemical Toxicology, v. 47, n. 6, p. 1318-1323, 2009.
[26] BHATIA, S. P.; LETIZIA, C. S.; API, A. M. Fragrance material review on borneol. Food and chemical toxicology, v. 46, n. 11, p. S77-S80, 2008.
[27] WU, H.-Y. et al. The synergetic effect of edaravone and borneol in the rat model of ischemic stroke. European Journal of Pharmacology, v. 740, p. 522-531, 2014.
[28] ASPLUND, R. Owen. Some quantitative aspects of the phytotoxicity of monoterpenes. Weed Science, v. 17, n. 4, p. 454-455, 1969.
[29] IQBAL, M. et al. Bioassays based on higher plants as excellent dosimeters for ecotoxicity monitoring: a review.vChemistry International, v. 5, n. 1, p. 1-80, 2019.
[30] LEME, D. M.; MARIN-MORALES, M. A. Allium cepa test in environmental monitoring: a review on its application. Mutation Research/Reviews in Mutation Research, v. 682, n. 1, p. 71-81, 2009.
[31] PATNAIK, A. R.; ACHARY, V. M. M.; PANDA, B. B. Chromium (VI)-induced hormesis and genotoxicity are mediated through oxidative stress in root cells of Allium cepa L. Plant growth regulation, v. 71, n. 2, p. 157-170, 2013.
[32] KUMARI, M. et al. Cytogenetic and genotoxic effects of zinc oxide nanoparticles on root cells of Allium cepa. Journal of hazardous materials, v. 190, n. 1-3, p. 613-621, 2011.
[33] MODLITBOVÁ, P. et al. Short-term assessment of cadmium toxicity and uptake from different types of Cd-based Quantum Dots in the model plant Allium cepa L. Ecotoxicology and environmental safety, v. 153, p. 23-31, 2018.
[34] FOUAD, A. S.; HAFEZ, R. M. The effects of silver ions and silver nanoparticles on cell division and expression of cdc2 gene in Allium cepa root tips. Biologia Plantarum, v. 62, n. 1, p. 166-172, 2018.
[35] RAJPUT, V. D. et al. Effects of copper nanoparticles (CuO NPs) on crop plants: a mini review. BioNanoScience, v. 8, n. 1, p. 36-42, 2018.
[36] FATMA, F. et al. Phytotoxicity of pesticides mancozeb and chlorpyrifos: correlation with the antioxidative defence system in Allium cepa. Physiology and molecular biology of plants, v. 24, n. 1, p. 115-123, 2018.
[37] LUO, Y. et al. Seed germination test for toxicity evaluation of compost: Its roles, problems and prospects. Waste Management, v. 71, p. 109-114, 2018.
[38] BEWLEY J. D.; BLACK M. Seeds: Physiology of Development and Germination, 2nd (edn), Plenum Press, New York, London, USA. 1994
[39] DA SILVA, L. C. et al. Influence of temperature on the germination and root size of Acmella oleracea (L.) RK Jansen. Revista Agro@ mbiente On-line, v. 14, 2020.
[40] LABOURIAU, L. G. On the frequency of isothermal germination in seeds of Dolichos biflorus L. Plant and Cell Physiology, v. 19, n. 3, p. 507-512, 1978.
[41] ORZOLEK, M. D. Establishment of vegetables in the field. HortTechnology, v. 1, n. 1, p. 78-81, 1991.
[42] GRASSBAUGH, E. M.; BENNETT, M. A. Factors affecting vegetable stand establishment. Scientia Agricola, v. 55, n. SPE, p. 116-120, 1998.
[43] HACKBART, V. C. dos S.; CORDAZZO, C. V. Ecologia das sementes e estabelecimento das plântulas de Hydrocotyle bonariensis Lam. 2003.
[44] LEAL, C. C. P. et al. Water stress on germination and vigor of ‘mofumbo’(Combretum leprosum Mart.) seeds at different temperatures. Revista Ciência Agronômica, v. 51, n. 1, 2020.
[45] MARTINS, C. C.; NAKAGAWA, J.; BOVI, M. L. A. Efeito da posição da semente no substrato e no crescimento inicial das plântulas de palmito-vermelho (Euterpe espiritosantensis Fernandes–Palmae). Revista Brasileira de Sementes, v. 21, n. 1, p. 164-173, 1999.
[46] FOTOPOULOS, V. et al. Involvement of AsA/DHA and GSH/GSSG ratios in gene and protein expression and in the activation of defence mechanisms under abiotic stress conditions. In: Ascorbate-glutathione pathway and stress tolerance in plants. Springer, Dordrecht, 2010. p. 265-302.
[47] GUNES, A. et al. Salicylic acid induced changes on some physiological parameters symptomatic for oxidative stress and mineral nutrition in maize (Zea mays L.) grown under salinity. Journal of Plant Physiology, v. 164, n. 6, p. 728-736, 2007.
[48] DHANYALAKSHMI, K. H.; VIJAYALAKSHMI, C.; BOOMINATHAN, R. Evaluation of physiological and biochemical responses of rice (Oryza sativa L.) varieties to salt stress. Indian Journal of Agricultural Research, v. 47, n. 2, p. 91-99, 2013.
[49] MISHRA, A.; CHOUDHURI, M. A. Effects of salicylic acid on heavy metal-induced membrane deterioration mediated by lipoxygenase in rice. Biologia Plantarum, v. 42, n. 3, p. 409-415, 1999.
[50] TEIXEIRA, P. C.; DONAGEMMA, G. K.; FONTANA, A.; TEIXEIRA, W. G. (Ed.). Manual de métodos de análise de solo. 3. ed. rev. e ampl. Brasília, DF: Embrapa, pt. 1, cap. 4, p. 34-46, 2017
[51] PÕLDMA, P. et al. Selenium treatment under field conditions affects mineral nutrition, yield and antioxidant properties of bulb onion (Allium cepa L.). Acta Sci. Pol., Hortorum Cultus, v. 12, n. 6, p. 167-181, 2013.
[52] FISKESJÖ, G. The Allium test as a standard in environmental monitoring. Hereditas, v. 102, n. 1, p. 99-112, 1985.
[53] KAMDEM, J. P. et al. Antioxidant activity, genotoxicity and cytotoxicity evaluation of lemon balm (Melissa officinalis L.) ethanolic extract: Its potential role in neuroprotection. Industrial Crops and Products, v. 51, p. 26-34, 2013.
[54] KLIMACZEWSKI, C. V. et al. Antioxidant activity of Peumus boldus extract and alkaloid boldine against damage induced by Fe (II)–citrate in rat liver mitochondria in vitro. Industrial Crops and Products, v. 54, p. 240-247, 2014.
[55] BARBOSA FILHO, V. M. et al. Phytochemical constituents, antioxidant activity, cytotoxicity and osmotic fragility effects of Caju (Anacardium microcarpum). Industrial Crops and Products, v. 55, p. 280-288, 2014.
[56] DUARTE, A. E. et al. Antimicrobial activity and Modulatory effect of essential oil from the leaf of Rhaphiodon echinus (Nees & Mart) Schauer on some antimicrobial drugs. Molecules, v. 21, n. 6, p. 743, 2016.
[57] AFTAB, S. et al. Impact of potassium on the growth and yield contributing attributes of onion (Allium cepa L.). Asian Research Journal of Agriculture, p. 1-4, 2017.
[58] MOLLAVALI, M. et al. Nitrogen form and mycorrhizal inoculation amount and timing affect flavonol biosynthesis in onion (Allium cepa L.). Mycorrhiza, v. 28, n. 1, p. 59-70, 2018.
[59] MENDES, A. M. S. et al. Nutrição mineral e adubação da cultura da cebola no Submédio do Vale do São Francisco. Embrapa Semiárido-Circular Técnica (INFOTECA-E), 2008.
[60] MEKONNEN, D. A.; MIHRETU, F. G.; WOLDETSADIK, K. Farmyard manure and intra-row spacing on yield and yield components of Adama Red onion (Allium cepa L.) cultivar under irrigation in Gewane District, Afar Region, Ethiopia. Journal of Horticulture and Forestry, v. 9, n. 5, p. 40-48, 2017.
[61] RESENDE, GM de; COSTA, N. D.; SOUZA, RJ de. Cultivo da cebola no Nordeste. Petrolina: Embrapa Semi-Árido, 2007. Sistemas de Produção, 3. 2012.
[62] BÜNEMANN, E. K. et al. Soil quality–A critical review. Soil Biology and Biochemistry, v. 120, p. 105-125, 2018.
[63] DAKER, A. Irrigação e drenagem: A água na agricultura. Freitas Bastos, 1988.
[64] RICHARDS, L. A. Diagnosis and improvement of saline and alkali soils. Handbook No. 60. US Department of Agriculture, Washington, DC, 1954.
[65] FASSBENDER, H. W.; BORNEMISZA, Elemer. Química de suelos con énfasis en suelos de América Latina. Iica, 1987.
[66] ROLSTON, D. E.; BIGGAR, J. W.; NIELSEN, D. R. Effect of salt on soils. California Agriculture 38:11-13. 1984.
[67] Saffaryazdi, A.; Lahouti, M.; Ganjeali, A. The effect of different concentrations of selenium on morphophysiological characteristics of spinach (Spinacia oleracea L.), J. Hort. Sci. 26, 292-300. 2012.
[68] MARSCHNER, H. Marschner's mineral nutrition of higher plants. Academic press, 2011.
[69] NUNES, R. T. C. et al. Desempenho germinativo de sementes de girassol submetidas ao estresse salino. Cultura Agronômica: Revista de Ciências Agronômicas, v. 25, n. 1, p. 79-92, 2016.
[70] PINHEIRO, D. T. et al. Germination and antioxidant action in melon seeds exposed to salt stress. Pesquisa Agropecuária Tropical, v. 46, n. 3, p. 336-342, 2016.
[71] SCANDALIOS, J. G. Oxidative stress: molecular perception and transduction of signals triggering antioxidant gene defenses. Brazilian journal of medical and biological research, v. 38, n. 7, p. 995-1014, 2005.
[72] HALLIWELL, B. Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant physiology, v. 141, n. 2, p. 312-322, 2006.
[73] MILLER, G. A. D. et al. Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant, cell & environment, v. 33, n. 4, p. 453-467, 2010.
[74] YACOUBI, R. et al. Proteomic analysis of the enhancement of seed vigour in osmoprimed alfalfa seeds germinated under salinity stress. Seed Science Research, v. 23, n. 2, p. 99-110, 2013.
[75] ANSARI, N. A.; KHALEGHI, S.-S. Germination and emergence response of some onion cultivars of southern Iran to salinity stress. Seed Science and Biotechnology, v. 3, n. 1, p. 21-23, 2009.
[76] BYBORDI, A.; SAADAT, S.; ZARGARIPOUR, P. The effect of zeolite, selenium and silicon on qualitative and quantitative traits of onion grown under salinity conditions. Archives of Agronomy and Soil Science, v. 64, n. 4, p. 520-530, 2018.
[77] DE GÓIS, V. A.; TORRES, S. B.; PEREIRA, R. A. Germinação de sementes de maxixe submetidas a estresse salino. Revista Caatinga, v. 21, n. 4, 2008.
[78] LACERDA, C. F. et al. Morpho-physiological responses of cowpea leaves to salt stress. Brazilian Journal of Plant Physiology, v. 18, n. 4, p. 455-465, 2006.
[79] GAMIELY, S. et al. Onion plant growth, bulb quality, and water uptake following ammonium and nitrate nutrition. HortScience, v. 26, n. 8, p. 1061-1063, 1991.
[80] BREWSTER, J. L. The classification, origins, distribution and economic importance of the major vegetable crops. Onions and Other Vegetable Alliums. Wallingford: CAB International, p. 1-18, 1994.
[81] BERNSTEIN, Leon; FRANCOIS, L. E.; CLARK, R. A. Interactive effects of salinity and fertility on yields of grains and vegetables 1. Agronomy Journal, v. 66, n. 3, p. 412-421, 1974.
[82] SHANNON, M. C.; GRIEVE, C. M. Tolerance of vegetable crops to salinity. Scientia horticulturae, v. 78, n. 1-4, p. 5-38, 1998.
[83] MAIA, J. M. et al. Salt-induced changes in antioxidative enzyme activities in root tissues do not account for the differential salt tolerance of two cowpea cultivars. Brazilian Journal of Plant Physiology, v. 22, n. 2, p. 113-122, 2010.
[84] ASHRAF, M. P. J. C.; HARRIS, P. J. C. Potential biochemical indicators of salinity tolerance in plants. Plant science, v. 166, n. 1, p. 3-16, 2004.
[85] HAJIBAGHERI, M. A. et al. Salinity resistance in Zea mays: fluxes of potassium, sodium and chloride, cytoplasmic concentrations and microsomal membrane lipids. Plant, Cell & Environment, v. 12, n. 7, p. 753-757, 1989.
[86] POTTERS, G. et al. Stress-induced morphogenic responses: growing out of trouble?. Trends in plant science, v. 12, n. 3, p. 98-105, 2007.
[87] SUN, F. et al. Salt modulates gravity signaling pathway to regulate growth direction of primary roots in Arabidopsis. Plant physiology, v. 146, n. 1, p. 178-188, 2008.
[88] BERNSTEIN, N.; ESHEL, A.; BEECKMAN, T. Effects of salinity on root growth. Plant roots: the hidden half, p. 1-784, 2013.
[89] JULKOWSKA, M. M. et al. Capturing Arabidopsis root architecture dynamics with ROOT-FIT reveals diversity in responses to salinity. Plant Physiology, v. 166, n. 3, p. 1387-1402, 2014.
[90] OKUSANYA, O. T. The effect of sea water and temperature on the germination behaviour of Crithmum maritimum. Physiologia Plantarum, v. 41, n. 4, p. 265-267, 1977.
[91] CREELMAN, R. A. et al. Water deficit and abscisic acid cause differential inhibition of shoot versus root growth in soybean seedlings: analysis of growth, sugar accumulation, and gene expression. Plant Physiology, v. 92, n. 1, p. 205-214, 1990.
[92] SAAB, I. N. et al. Increased endogenous abscisic acid maintains primary root growth and inhibits shoot growth of maize seedlings at low water potentials. Plant physiology, v. 93, n. 4, p. 1329-1336, 1990.
[93] WAHID, A. et al. Short term incubation of sorghum caryopses in sodium chloride levels: changes in some pre-and post-germination physiological parameters. Plant Science, v. 139, n. 2, p. 223-232, 1998.
[94] DASH, M.; PANDA, S. K. Salt stress induced changes in growth and enzyme activities in germinating Phaseolus mungo seeds. Biologia plantarum, v. 44, n. 4, p. 587-589, 2001.
[95] PINHEIRO, H. A. et al. Leaf gas exchange, chloroplastic pigments and dry matter accumulation in castor bean (Ricinus communis L) seedlings subjected to salt stress conditions. Industrial Crops and Products, v. 27, n. 3, p. 385-392, 2008.
[96] FERREIRA-SILVA, S. L. et al. Changes in physiological indicators associated with salt tolerance in two contrasting cashew rootstocks. Brazilian Journal of Plant Physiology, v. 20, n. 1, p. 51-59, 2008.
[97] DA SILVA, E. N.et al. Ion uptake and growth of pinhão-manso under different salinity levels. Revista Ciência Agronômica, v. 40, n. 2, p. 240, 2009.
[98] MARTINO, L. De et al. The antigerminative activity of twenty-seven monoterpenes. Molecules, v. 15, n. 9, p. 6630-6637, 2010.
[99] MEAGHER, E. A.; FITZGERALD, G. A. Indices of lipid peroxidation in vivo: strengths and limitations. Free Radical Biology and Medicine, v. 28, n. 12, p. 1745-1750, 2000.
[100] MITTLER, R. Oxidative stress, antioxidants and stress tolerance. Trends in plant science, v. 7, n. 9, p. 405-410, 2002.
[101] TANOU, G. et al. Proteomics reveals the overlapping roles of hydrogen peroxide and nitric oxide in the acclimation of citrus plants to salinity. The Plant Journal, v. 60, n. 5, p. 795-804, 2009.
[102] WANG, P. et al. Hydrogen peroxide–mediated activation of MAP kinase 6 modulates nitric oxide biosynthesis and signal transduction in Arabidopsis. The Plant Cell, v. 22, n. 9, p. 2981-2998, 2010.
[103] FILIPPOU, P.; ANTONIOU, C.; FOTOPOULOS, V. Effect of drought and rewatering on the cellular status and antioxidant response of Medicago truncatula plants. Plant Signaling & Behavior, v. 6, n. 2, p. 270-277, 2011.
[104] ABOGADALLAH, G. M. Insights into the significance of antioxidative defense under salt stress. Plant signaling & behavior, v. 5, n. 4, p. 369-374, 2010.
[105] BARTOLI, C. G. et al. Interactions between hormone and redox signalling pathways in the control of growth and cross tolerance to stress. Environmental and Experimental Botany, v. 94, p. 73-88, 2013.
[106] MATYSIK, J. et al. Molecular mechanisms of quenching of reactive oxygen species by proline under stress in plants. Current Science, p. 525-532, 2002.
[107] MUNNÉ-BOSCH, S.; QUEVAL, G.; FOYER, C. H. The impact of global change factors on redox signaling underpinning stress tolerance. Plant Physiology, v. 161, n. 1, p. 5-19, 2013.
[108] DUAN, J. et al. Exogenous spermidine affects polyamine metabolism in salinity-stressed Cucumis sativus roots and enhances short-term salinity tolerance. Journal of plant physiology, v. 165, n. 15, p. 1620-1635, 2008.
[109] YAZICI, I. et al. Salinity tolerance of purslane (Portulaca oleracea L.) is achieved by enhanced antioxidative system, lower level of lipid peroxidation and proline accumulation. Environmental and Experimental Botany, v. 61, n. 1, p. 49-57, 2007.
[110] SU, J. et al. Composition and biological activities of the essential oil extracted from a novel plant of Cinnamomum camphora Chvar. Borneol. Journal of Medicinal Plants Research, v. 6, n. 18, p. 3487-3494, 2012.
Downloads
Publicado
2022-12-31
Como Citar
Larisse Bernardino dos Santos, Jailson Renato de Lima Silva, Carlos Vinicius Barros Oliveira, Adrielle Rodrigues Costa, Maria Keliane Alves de Souza, Thalyta Julyanne Silva de Oliveira, Daniel Honorato Neves, José Wellington Macêdo Viana, Antonio Ivanildo Pinho, Pedro Silvino Pereira, Ana Cristina Diogo Gomes de Melo, Cícera Maria Rocha Sousa, Luiz Marivando Barros, Jean Paul Kamdem, & Antonia Eliene Duarte. (2022). PROTECTIVE ROLE OF 2-BORNEOL IN THE EMERGENCE OF Allium cepa SEEDS EXPOSED TO NaCl. South American Journal of Basic Education, Technical and Technological, 9(1), 164–184. Recuperado de https://periodicos.ufac.br/index.php/SAJEBTT/article/view/4353
Edição
Seção
Artigos Originais Ciências Agrárias
