Abstract
Accelerated ageing is an accurate test indicator of seed vigor and storability that helps to understand the mechanisms of cellular and biochemical deterioration that occur during seed ageing. This study was carried out to elucidate the mechanisms of ageing in macaw palm embryos. Seeds were artificially aged during 4, 8 and 12 days at 45 °C and 100% relative humidity. After ageing, seeds were tested for viability (tetrazolium), electrical conductivity, lipid peroxidation (MDA) and hydrogen peroxide (H2O2) content. Part of the aged seeds was imbibed for 8 days and then determined the hydrogen peroxide content and the activity of antioxidant system enzymes (superoxide dismutase, catalase and glutathione reductase). Ageing reduced the embryo viability from 8 days of treatment and increased malondialdehyde content (MDA) and solute leakage. Hence, membrane permeability correlated with both loss of viability and lipid peroxidation. Imbibition after ageing significantly increased H2O2 content along with superoxide dismutase activity. Catalase activity was significantly higher than control in embryos aged from 8 days and imbibed, and glutathione reductase activity did not change. Our results suggest that macaw palm seed deterioration during accelerated ageing is closely related to lipid peroxidation, and that enzymatic antioxidant system is not completely efficient in reducing reactive oxygen species after imbibition, a critical phase to germination. Moreover, accelerated ageing test can be used as a reliable model to understand the mechanisms involved in palm seeds deterioration.
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References
Aebi H (1984) Oxygen radicals in biological systems. Method Enzymol 105:121–126
Ahmad P, Sarwat M, Sharma S (2008) Reactive oxygen species, antioxidants and signaling in plants. J Plant Biol 51:167–173
Al-Maskri AY, Khan MM, Al-Habsi K (2003) Effect of accelerated ageing on viability, vigor (rgr), lipid peroxidation and leakage in carrot (Daucus carota L.) seeds. Int J Agric Biol 5:580–584
Arc E, Ogé L, Grappin P, Rajjou L (2011) Plant seed: a relevant model to study aging processes. In: Olgun A (ed) The field of biological aging: past, present and future. Transworld Research Network, India, pp 87–102
Azevedo Filho J, Colombo C, Berton L (2012) Macaúba: palmeira nativa como opção bioenergética. Pesqui Tecnol 9:1–10
Bailly C (2004) Active oxygen species and antioxidants in seed biology. Seed Sci Res 14:93–107
Bailly C, Benamar A, Corbineau F, Come D (1996) Changes in malondialdehyde content and in superoxide dismutase, catalase and glutathione reductase activities in sunflower seeds as related to deterioration during accelerated aging. Physiol Plant 97:104–110
Bailly C, Benamar A, Corbineau F, Côme D (1998) Free radical scavenging as affected by accelerated ageing and subsequent priming in sunflower seeds. Physiol Plant 104:646–652
Bailly C, Bogatek-Leszczynska R, Côme D, Corbineau F (2002) Changes in activities of antioxidant enzymes and lipoxygenase during growth of sunflower seedlings from seeds of different vigour. Seed Sci Res 12:47–55
Bailly C, El-Maarouf-Bouteau H, Corbineau F (2008) From intracellular signaling networks to cell death: the dual role of reactive oxygen species in seed physiology. C R Biol 331:806–814
Barreto LC, Garcia QS, Morales M, Müller M, Munné-Bosch S (2014) Vitamin E and defense-related phytohormones are reliable markers of embryo growth in macaw palm fruits exposed to various storage conditions. Plant Cell Tissue Organ 118:203–213
Barreto LC, Magalhães ALL, Takahashi JA, Garcia QS (2016) Dynamic of reserve compounds of mesocarp and seeds of macaw palm (Acrocomia aculeata) submitted to different storage conditions. Trees. doi:10.1007/s00468-016-1423-4
Belletti P, Lanteri S, Lotito S (1991) The influence of temperature and moisture on seed ageing in Iceland poppy (Papaver nudicaule L.). Sci Hortic 48:153–158
Beyer WF, Fridovich I (1987) Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Anal Biochem 161:559–566
Bhattachrjee S (2005) Reactive oxygen species and oxidative burst: roles in stress, senescence and signal transduction in plant. Curr Sci 89:1113–1121
Bicalho EM, Pintó-Marijuan M, Morales M, Müller M, Munné-Bosch S, Garcia QS (2015) Control of macaw palm seed germination by the gibberellin/abscisic acid balance. Plant Biol 17:990–996
Blokhina O (2003) Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann Bot 91:179–194
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Cakmak I, Horst WJ (1991) Effect of aluminium on lipid peroxidation, superoxide dismutase, catalase, and peroxidase activities in root tips of soybean (Glycine max). Physiol Plant 83:463–468
Corbineau F, Picard MA, Fougereux JA, Ladonne F, Côme D (2000) Effects of dehydration conditions on desiccation tolerance of developing pea seeds as related to oligosaccharide content and cell membrane properties. Seed Sci Res 10:329–339
Ellis R, Hong T (1991) Seed storage behaviour in Elaeis guineensis. Seed Sci Res 1:99–104
Foyer CH, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133:21–25
Galleschi L, Capocchi A, Ghiringhelli S, Saviozzi F, Calucci L, Pinzino C, Zandomeneghi M (2002) Antioxidants, free radicals, storage proteins, and proteolytic activities in wheat (Triticum durum) seeds during accelerated aging. J Agric Food Chem 50:5450–5457
Giannopolitis CN, Ries SK (1977) Superoxide dismutases. Plant Physiol 59:309–314
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930
Goel A, Goel AK, Sheoran IS (2003) Changes in oxidative stress enzymes during artificial ageing in cotton (Gossypium hirsutum L.) seeds. J Plant Physiol 160:1093–1100
Gomes MP, Garcia QS (2013) Reactive oxygen species and seed germination. Biologia 68:351–357
Gordin CRB, Scalon SDPQ, Masetto TE (2015) Accelerated aging test in niger seeds. J Seed Sci 37:234–240
Hay FR, Merritt DJ, Soanes JA, Dixon KW (2010) Comparative longevity of Australian orchid (Orchidaceae) seeds under experimental and low temperature storage conditions. Bot J Linn Soc 164:26–41
Hendry GAF (1993) Oxygen, free radical processes and seed longevity. Seed Sci Res 3:141–153
Hiane PA, Ramos MM, Ramos MIL, Macedo MLR (2005) Óleo da polpa e amêndoa de bocaiúva, Acrocomia aculeata (Jacq.) Lodd. Caracterização e composição em ácidos graxos. Braz J Food Tech 8:256–259
Hodges DM, DeLong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207:604–611
Hossain MA, Bhattacharjee S, Armin SM, Qian P, Xin W, Li HY, Burritt DJ, Fujita M, Tran LSP (2015) Hydrogen peroxide priming modulates abiotic oxidative stress tolerance: insights from ROS detoxification and scavenging. Front Plant Sci 6:1–19
Kibinza S, Vinel D, Côme D, Bailly C, Corbineau F (2006) Sunflower seed deterioration as related to moisture content during ageing, energy metabolism and active oxygen species scavenging. Physiol Plant 128:496–506
Krainart C, Siri B, Vichitphan K (2015) Effects of accelerated aging and subsequent priming on seed quality and biochemical change of hybrid cucumber (Cucumis sativa Linn.) seeds. J Agric Technol 11:165–179
Kumar JSP, Prasad RS, Banerjee R, Thammineni C (2015) Seed birth to death: dual functions of reactive oxygen species in seed physiology. Ann Bot 116:663–668
Lehner A, Mamadou N, Poels P, Côme D, Bailly C, Corbineau F (2008) Changes in soluble carbohydrates, lipid peroxidation and antioxidant enzyme activities in the embryo during ageing in wheat grains. J Cereal Sci 47:555–565
Leprince O, Hendry GAF, McKersie BD (1993) The mechanisms of desiccation tolerance in developing seeds. Seed Sci Res 3:231–246
Liu R, Lai T, Xu Y, Tian S (2013) Changes in physiology and quality of Laiyang pear in long time storage. Sci Hortic 150:31–36
McDonald MB (1999) Seed deterioration: physiology, repair and assessment. Seed Sci Technol 27:177–237
Merritt DJ, Senaratna T, Touchell DH, Dixon KW, Sivasithamparam K (2003) Seed ageing of four Western Australian species in relation to storage. Seed Sci Res 13:155–165
Meyer AJ (2008) The integration of glutathione homeostasis and redox signaling. J Plant Physiol 165:1390–1403
Mira S, Estrelles E, González-Benito ME, Corbineau F (2011) Biochemical changes induced in seeds of Brassicaceae wild species during ageing. Acta Physiol Plant 33:1803–1809
Moura E, Ventrella M, Motoike S (2010) Anatomy, histochemistry and ultrastructure of seed and somatic embryo of Acrocomia aculeata (Arecaceae). Sci Agric 67:399–407
Murugesan P, Mathur RK, Pillai RSN, Babu MK (2005) Effect of accelerated aging on seed germination of oil palm (Elaeis guineensis Jacq. var. dura Becc.). Seed Technol 27:108–112
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880
Negreiros GF, Perez SCJG (2004) Resposta fisiológica de sementes de palmeiras ao envelhecimento acelerado. Pesqui Agropecu Bras 39:391–396
Noctor G, Mhamdi A, Chaouch S, Han Y, Neukerman J, Marquez-Garcia B, Queval G, Foyer CH (2012) Glutathione in plants: an integrated overview. Plant Cell Environ 35:454–484
Nonogaki H, Bassel GW, Bewley JD (2010) Germination—still a mystery. Plant Sci 179:574–581
Priestley DA, Leopold AC (1979) Absence of lipid oxidation during accelerated aging of soybean seeds. Plant Physiol 63:726–729
Ratajczak E, Pukacka S (2005) Decrease in beech (Fagus sylvatica) seed viability caused by temperature and humidity conditions as related to membrane damage and lipid composition. Acta Physiol Plant 27:3–12
Ratajczak E, Małecka A, Bagniewska-Zadworna A, Kalemba EM (2015) The production, localization and spreading of reactive oxygen species contributes to the low vitality of long-term stored common beech (Fagus sylvatica L.) seeds. J Plant Physiol 174:147–156
Ribeiro LM, Garcia QS, Oliveira DMT, Neves SC (2010) Critérios para o teste de tetrazólio na estimativa do potencial germinativo em macaúba. Pesqui Agropecu Bras 45:361–368
Ribeiro LM, Neves SC, Silva PO, Andrade IG (2011) Germinação de embriões zigóticos e desenvolvimento in vitro de coquinho-azedo. Revista Ceres 58:133–139
Roberts EH, Ellis RH (1989) Water and seed survival. Ann Bot 63:39
Rubio Neto A, Silva FG, Sales JF, Pires LL, Freitas BSM, Souza AL (2015) Effects of drying temperature on viability of macaw palm (Acrocomia aculeata) zygotic embryos. Afr J Biotechnol 14:319–326
Silva PO, Ribeiro LM, Simões MOM, Lopes SN, Farias TM, Garcia QS (2013) Fruit maturation and in vitro germination of macaw palm embryos. Afr J Biotechnol 12:446–452
Stewart RR, Bewley JD (1980) Lipid peroxidation associated with accelerated aging of soybean axes. Plant Physiol 65:245–248
Sung JM, Jeng TL (1994) Lipid peroxidation and peroxide-scavenging enzymes associated with accelerated aging of peanut seed. Physiol Plant 91:51–55
Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants. Plant Sci 151:59–66
Walters C (1998) Understanding the mechanisms and kinetics of seed aging. Seed Sci Res 8:223–244
Walters C, Wheeler LM, Grotenhuis JM (2005) Longevity of seeds stored in a genebank: species characteristics. Seed Sci Res 15:1–20
Wang F, Wang R, Jing W, Zhang W (2011) Quantitative dissection of lipid degradation in rice seeds during accelerated aging. Plant Growth Regul 66:49–58
Wojtyla Ł, Garnczarska M, Zalewski T, Bednarski W, Ratajczak L, Jurga S (2006) A comparative study of water distribution, free radical production and activation of antioxidative metabolism in germinating pea seeds. J Plant Physiol 163:1207–1220
Xia F, Chen L, Sun Y, Mao P (2015) Relationships between ultrastructure of embryo cells and biochemical variations during ageing of oat (Avena sativa L.) seeds with different moisture content. Acta Physiol Plant 37:1–11
Zacheo G, Cappello AR, Perrone LM, Gnoni GV (1998) Analysis of factors influencing lipid oxidation of almond seeds during accelerated ageing. Leb Wiss Technol 31:6–9
Acknowledgements
We thank Dr. Luzia Valentino Modolo for providing reagents and equipment and Elisa Monteze Bicalho for the support on enzyme analyses. Financial support for this research was received through FAPEMIG (Fundação de Amparo à Pesquisa do Estado de Minas Gerais) and CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico) L.C.B. received fellowship from FAPEMIG and Q.S.G. received research productivity scholarships from CNPq.
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Communicated by A. Gniazdowska-Piekarska.
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Barreto, L.C., Garcia, Q.S. Accelerated ageing and subsequent imbibition affect seed viability and the efficiency of antioxidant system in macaw palm seeds. Acta Physiol Plant 39, 72 (2017). https://doi.org/10.1007/s11738-017-2367-z
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DOI: https://doi.org/10.1007/s11738-017-2367-z