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Abscisic acid and the antioxidant system are involved in germination of Butia capitata seeds

ABSTRACT

Seed germination is an important step for plants without vegetative propagation and is a physiological process that begins with specific environmental cues resulting in biochemical responses. Breaking-dormancy is necessary to study germination in dormant seeds with asynchronous germination. We investigated the processes of breaking dormancy and germination of Butia capitata (Arecaceae) seeds, in which germination is slow and asynchronous, by operculum removal. This treatment increased germination of B. capitata to 90 %. Embryos of dry, imbibed, 24-hours post-operculum removal and early-germinated seeds were collected for biochemical analysis of the following: quantification of abscisic acid (ABA) and hydrogen peroxide (H2O2), activities of antioxidant enzymes (catalase - CAT, superoxide dismutase - SOD, glutathione reductase - GR) and histolocalization of superoxide anion (O2 -). Decreases in H2O2 and ABA were recorded 24 hours post-operculum removal. Increased GR and SOD activities during imbibition, and CAT upon germination, indicate a role in controlling reactive oxygen species. Interestingly, the accumulation of O2 - on the haustorium upon imbibition seems to be involved in germination, instead of H2O2. For B. capitata seeds, signaling from the removal of the operculum probably resulted in ABA catabolism mediated by O2 -, which thus promoted seed germination.

Keywords:
breaking-dormancy; haustorium; hormones; palm seeds; operculum; physiological dormancy; reactive oxygen species

Seed germination is one of the most important processes in the life cycle of a plant, and its success depends on environmental conditions and appropriate physiological and biochemical responses (Bewley et al. 2013Bewley JD, Bradford KJ, Hilhorst HWM, Nonogaki H. 2013. Seeds: physiology of development, germination and dormancy. New York, Springer.). Reactive oxygen species (ROS) are continuously produced in metabolically active cells of seeds (Gomes & Garcia 2013Gomes MP, Garcia QS. 2013. Reactive oxygen species and seed germination. Biologia 68: 351-357.). During metabolic recovery following imbibition, ROS production increases as germination progresses (Bailly 2004Bailly C. 2004. Active oxygen species and antioxidants in seed biology. Seed Science Research 14: 93-107.). The production of ROS stimulates the antioxidant system to scavenge toxic levels of those same chemicals as they interact with phytohormones and germination signaling pathways (Diaz-Vivancos et al. 2013Diaz-Vivancos P, Barba-Espín G, Hernández JA. 2013. Elucidating hormonal/ROS networks during seed germination: insights and perspectives. Plant Cell Reports 32: 1491-502.). Reactive oxygen species, especially hydrogen peroxide (H2O2), are known to be involved in gibberellin (GA) biosynthesis and abscisic acid (ABA) catabolism during germination (Liu et al. 2010Liu Y, Ye N, Liu R, Chen M, Zhang J. 2010. H2O2 mediates the regulation of ABA catabolism and GA biosynthesis in Arabidopsis seed dormancy and germination. Journal of Experimental Botany 61: 2979-2990.; Gomes & Garcia 2013Gomes MP, Garcia QS. 2013. Reactive oxygen species and seed germination. Biologia 68: 351-357.). The balance between these two phytohormones induces germination or the maintenance of dormancy (Bicalho et al. 2015Bicalho 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 Biology 17: 990-996.; Vieira et al. 2017Vieira BC, Bicalho EM, Munné-Bosch S, Garcia QS. 2017. Abscisic acid regulates seed germination of Vellozia species in response to temperature. Plant Biology 19: 211-2016.).

Palms (Arecaceae) are restricted to the tropics (Tomlinson 2006Tomlinson PB. 2006. The uniqueness of palms. Botanical Journal of the Linnean Society 151: 5-14.), but can be found in varying environments (Svenning 2001Svenning JC. 2001. On the role of microenvironmental heterogeneity in the ecology and diversification of neotropical rain-forest palms (Arecaceae). The Botanical Review 67: 1-53.) with many species producing seeds with primary dormancy and very slow seedling recruitment over time (Pérez et al. 2008Pérez HE, Shiels AB, Zaleski HM, Drake DR. 2008. Germination after simulated rat damage in seeds of two endemic Hawaiian palm species. Journal of Tropical Ecology 24: 555-558.; Baskin & Baskin 2013Baskin JM, Baskin CC. 2013. What kind of seed dormancy might palms have? Seed Science Research 24: 17-22.; Bicalho et al. 2015Bicalho 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 Biology 17: 990-996.). In the cerrado (Brazilian savanna), there are interesting and useful palm species that contribute to the survival and development of local communities. One such palm is Butia capitata (Mart.) Becc., popularly known as coquinho-azedo, which naturally occurs in environments with seasonal water deficit and whose fruits are used as food. The germination of B. capitata seeds is considered slow and asynchronous due to the physiological, or morphophysiological (see Baskin & Baskin 2014Baskin CC, Baskin JM. 2014. Seeds: ecology, biogeography, and evolution of dormancy and germination. San Diego, Academic Press.), dormancy of this species, which is related to the difficulty the embryo has in overcoming restrictions imposed by adjacent tissues (Oliveira et al. 2013Oliveira NCC, Lopes PSN, Ribeiro LM, Mercandante-Simões MO, Oliveira LAA, Silvério FO. 2013. Seed structure, germination, and reserve mobilization in Butia capitata (Arecaceae). Trees 27: 1633-1645.). Overexploitation and slow natural regeneration by seeds call for conservation efforts regarding the species. However, the physiological changes, as well as the underlying signaling, involved in the process of seed germination of B. capitata are not well understood.

We thus performed an experiment to better understand the relationship between abscisic acid (ABA), ROS and the antioxidant system of B. capitata embryos during germination. To facilitate the experiment and to optimize the synchrony of germination, we employed operculum removal for overcoming dormancy since this method is known to significantly increase germination of palm species (Spera et al. 2001Spera MRN, Cunha R, Teixeira JB. 2001. Quebra de dormência, viabilidade e conservação de sementes de buriti (Mauritia flexuosa). Pesquisa Agropecuária Brasileira 36: 1567-1572.; Fior et al. 2011Fior CS, Rodrigues LR, Leonhardt C, Schwarz SF. 2011. Overcoming dormancy in seeds of Butia capitata. Ciência Rural 41: 1150-1153.; Oliveira et al. 2013Oliveira NCC, Lopes PSN, Ribeiro LM, Mercandante-Simões MO, Oliveira LAA, Silvério FO. 2013. Seed structure, germination, and reserve mobilization in Butia capitata (Arecaceae). Trees 27: 1633-1645.; Bicalho et al. 2016Bicalho EM, Motoike SY, Borges EEL, Ataíde GM, Guimarães VM. 2016. Enzyme activity and reserve mobilization during macaw palm (Acrocomia aculeata) seed germination. Acta Botanica Brasilica 30: 437-444.). The operculum comprises the region with micropilar endosperm and the tegument that is pushed by the embryo during natural germination. However, the natural removal of the operculum by the embryo (visible germination) in B. capitata (and other palm species, see Segovia et al. 2003Segovia AO, Batis AI, Arechiga MR, Mendoza A. 2003. Seed biology of palms: a review. Palms 47: 79-94., and Bicalho et al. 2015) is very slow and asynchronous (Oliveira et al. 2013Oliveira NCC, Lopes PSN, Ribeiro LM, Mercandante-Simões MO, Oliveira LAA, Silvério FO. 2013. Seed structure, germination, and reserve mobilization in Butia capitata (Arecaceae). Trees 27: 1633-1645.), which would make the present experiment impracticable. Artificial removal of the operculum exposes the embryo to the environment, which may trigger some kind of signaling, but information regarding this is scarce. Thus, our main objective was to better understand the dynamics of ABA and ROS following operculum removal that leads to germination.

Fruits of B. capitata were collected in the municipality of Mirabela, state of Minas Gerais. The region is tropical with hot summers and very dry winters; the mean annual precipitation is approximately 900 mm with a seasonal water deficit, and the mean annual temperature is 22 °C with a thermal range of approximately 15 °C (Cwa by the Köppen system) (Köppen 1900Köppen W. 1900. Versuch einer Klassifikation der Klimate, vorzugsweise nach ihren Beziehungen zur Pflanzenwelt. Geographische Zeitschrift 6: 593-611.; Alvares et al. 2013Alvares CA, Stape JL, Sentelhas PC, Gonçalves JLM, Sparovek G. 2013. Köppen’s climate classification map for Brazil. Meteorologische Zeitschrift 22: 711-728.).

Approximately 4000 B. capitata fruits were collected from at least 100 trees. Four replicates of 15 seeds were sowed in distilled water and used to determine imbibition time by weighing the seeds daily until they reached a constant weight. Four replicates of 25 seeds were used for preliminary germination experiments. These seeds were surface sterilized with 5 % NaClO for 15 minutes and then rinsed three times with distilled water. The seeds were then held in distilled water for three days and subsequently transferred to transparent germination boxes lined with a double layer of filter paper moistened with distilled water, which were kept in a germination chamber at 30 °C for 30 days under a 12 h - photoperiod (Phillips, 40 µmol photons m-2 s-1).

The opercula of the seeds were removed three days after immersion in distilled water (when imbibition stabilized). After this dormancy-breaking treatment, the germination experiment was carried out in the germination chambers as previously described with germination percentages being evaluated daily. The criterion used for visible germination was the protrusion of the cotyledonary petiole.

Embryos were extracted from seeds at different phases of the germination process: pre-imbibition (D, dry), post-imbibition (I), 24 hours after operculum removal (24 h), and early germination (G, visible germination). The sampled embryos were used for the following biochemical analyses: quantification of ABA and H2O2; enzymatic activity of catalase (CAT), superoxide dismutase (SOD), glutathione reductase (GR); and localization of superoxide anion O2 -. Germination phases were independently sampled with the samples consisting of four replicates of 200 embryos.

Abscisic acid extraction was performed following Weiler (1980Weiler EW. 1980. Radioimmunoassays for the differential and direct analysis of free and conjugated abscisic acid in plant extracts. Planta 148: 262-272.), with some modifications. Four replicates of 100 mg of embryos were powdered using a mortar and pestle with liquid nitrogen and then homogenized in 80% methanol with 0.5 mg mL-1 ascorbic acid and 10 mg L-1 BHT. The samples were then added to pH 7.0 TBS buffer with the resulting solution reaching less than 10% organic solvents. Quantification of ABA (controls, standard curve, samples and calculations) was performed strictly following the recommendations of Phytodetek® ABA Test Kits (Agdia Incorporated, Indiana, USA). Since water content increased throughout imbibition, the values of ABA quantification obtained for I, 24 h and G phases were corrected based on D phase moisture content.

Quantification of H2O2 was performed following Velikova et al. (2000Velikova V, Yordanov I, Edreva A. 2000. Oxidative stress and some antioxidant systems in acid rain-treated bean plants: Protective role of exogenous polyamines. Plant Science 151: 59-66.). Four replicates of 100 mg of embryos were powdered using a mortar and pestle with liquid nitrogen, homogenized with 0.1 % trichloroacetic acid (TCA), and centrifuged at 12000 g for 15 minutes. The extract was reacted with 10 mM of pH 7.0 phosphate buffer and 1 M KI. The absorbance was recorded at 390 nm and the H2O2 content subsequently calculated from the standard curve. The values of H2O2 were also corrected as for ABA quantification.

Antioxidant enzyme extract was prepared following Gomes et al. (2013Gomes MP, Carneiro MMLC, Nogueira COG, Soares AM, Garcia QS. 2013. The system modulating ROS content in germinating seeds of two Brazilian savanna tree species exposed to As and Zn. Acta Physiologiae Plantarum 35: 1011-1022.). Four replicates of 100 mg of embryos were pulverized in liquid nitrogen and homogenized in 100 mM of pH 7.8 phosphate buffer with 100 mM EDTA and 5 % PVP. The extract was then centrifuged at 12000 g (4 °C) and subsequently used to evaluate enzymatic activity and protein content, the latter using Bradford's method (Bradford 1976Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72: 248-254.).

Catalase activity was determined following Aebi (1984Aebi H. 1984. [13] Catalase in vitro. In: Packer L. (ed.) Methods in enzymology. San Diego, San Diego Academic Press. p. 121-126.) in 67 mM phosphate buffer (pH 7.0) with 10 mM H2O2 and adequate amounts of the enzyme extract. Consumption of H2O2 was recorded at 240 nm for 2 minutes (Ɛ = 0.0394 mM−1 cm−1). Superoxide dismutase activity was determined in a reaction buffer containing 50 mM phosphate buffer (pH 7.8), 13 mM L-methionine, 0.1 mM EDTA, 0.002 mM riboflavin, and 0.075 mM nitroblue tetrazolium (NBT) (Giannopolitis & Ries 1977Giannopolitis CN, Ries SK. 1977. Superoxide dismutases: I. Occurrence in higher plants. Plant Physiology 59: 309-314.). Blue formazan concentrations were read at 575 nm, and one unit of SOD was considered as the amount of enzyme necessary to reduce 50 % of the O2 -. Glutathione reductase activity was determined in media containing 100 mM phosphate buffer (pH 7.8), 50 mM oxidized glutathione, 5 mM NADPH, and adequate amounts of the enzymatic extract, with NADPH oxidation being monitored at 340 nm (Ɛ = 6.2 mM-1 cm-1) (Foyer & Halliwell 1976Foyer CH, Halliwell B. 1976. The presence of glutathione and glutathione reductase in chloroplasts: A proposed role in ascorbic acid metabolism. Planta 133: 21-25.).

Histolocalization of superoxide anion (O2 -) was performed strictly following Oracz et al. (2012Oracz K, Voegele A, Tarkowská D, et al. 2012. Myrigalone A inhibits Lepidium sativum seed germination by interference with gibberellin metabolism and apoplastic superoxide production required for embryo extension growth and endosperm rupture. Plant and Cell Physiology 53: 81-95.). Twenty embryos of each phase were immersed in 10 mM of TRIS buffer (pH 7.0) with 1 mM of a nitroblue tetrazolium (NBT) solution for 10 minutes. The embryos were then washed three times in 10 mM TRIS buffer (pH 7.0) and photographed.

The data for ABA, H2O2 and antioxidant enzyme activities were tested for normality and homoscedasticity using Cochran and Levene´s test, respectively. Normal and homoscedastic or transformed data (arcsine root square) were analyzed by ANOVA followed by the Tukey test for comparisons of all means at 5 % level of probability, using Statistica 7 StatSoft® software.

The germination of B. capitata seeds was 88 % at 72h post-operculum removal (Fig. 1A) with great concentrations of ABA prior to imbibition (Fig. 1B). Biosynthesis of ABA has been shown to be a response to water deficit (Bray 1997Bray EA. 1997. Plant responses to water deficit. Trends in Plant Science 2: 48-54.), a common condition in plants growing in localities with well-defined dry seasons (Liu et al. 2005Liu F, Jensen CR, Andersen MN. 2005. A review of drought adaptation in crop plants: changes in vegetative and reproductive physiology induced by ABA-based chemical signals. Australian Journal of Agricultural Research 56: 1245-1252.), as is the case for B. capitata. The initially high levels of ABA observed for B. capitata embryos reduced during imbibition (Fig. 1B). Reductions in ABA levels during imbibition were also observed by Bicalho et al. (2015Bicalho 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 Biology 17: 990-996.) for macaw palm embryos, and by Dias et al. (2017Dias DS, Ribeiro LM, Lopes PSN, Munné-Bosch S, Garcia QS. 2017. Hormonal profile and the role of cell expansion in the germination control of Cerrado biome palm seeds. Plant Physiology and Biochemistry 118: 168-177.) in the cotyledonary petiole of B. capitata seeds, both of which were related to leakage. In this work the reduction in H2O2 levels was found only 24 h after operculum removal (Fig. 1C) and the presence of H2O2 has been shown to induce ABA catabolism in pea seeds, thereby allowing germination (Barba-Espin et al. 2010Barba-Espin G, Diaz-Vivancos P, Clemente-Moreno MJ, et al. 2010. Interaction between hydrogen peroxide and plant hormones during germination and the early growth of pea seedlings. Plant, Cell & Environment 33: 981-994.). It is interesting to point out that in the present work ABA levels decreased continuously from I to early-germination phase (Fig. 1B). Concentrations of H2O2 were also observed to be maintained in the early-germination phase relative to 24h post-operculum removal (Fig. 1C).

Figure 1
Germination percentage and biochemical parameters for embryos of Butia capitata during phases of germination. Graphics show germination percentage from the dormancy-breaking process (A); levels of ABA (B) and H2O2 (C); and CAT (D), SOD (E) and GR (F) activities during germination phases. Dots or bars are means ± standard error of four replicates. Means followed by the same letters do not differ according to Tukey test at 5% of probability. ABA, abscisic acid; H2O2, hydrogen peroxide; CAT, catalase; SOD, superoxide dismutase; GR, glutathione reductase (y-axis); D, dry; I, imbibed; 24h, 24 hours after operculum removal; G, early-germinated (x-axis).

As shown by purple coloration indicating a positive reaction with NBT, O2 - was intensely produced in the haustorium region of B. capitata embryos since imbibition (Fig. 2). Interestingly, the presence of O2 - was indicated only in haustorium region, which is rich in reserves for early seedling growth. These results suggest that the haustorium has actions that go beyond reserve mobilization beginning with the first events of imbibition (see the increasing color intensity from D to G embryos of B. capitata; Fig. 2). The haustorium can also be assumed to play a role as a source of signaling mediated by O2 - formation. An interesting relationship was observed here between ABA and ROS: reductions of both ABA and H2O2 levels following operculum removal (Fig. 1B), with an increase in O2 - formation (Fig. 2). These results indicate that the dynamics of ROS and ABA are related to operculum removal. This leads to the suggestion that the exposure of the embryo to O2 due to operculum removal (dormancy-breaking process) induced metabolic changes in hormonal and oxidant components. Reductions in H2O2 levels and increasing O2 - formation in embryos of after operculum removal have also been observed in other palm species (TRS Santos unpubl. res.). The formation of ROS during germination is a natural process due to the reactivation of metabolism and increased respiration (Diaz-Vivancos et al. 2013Diaz-Vivancos P, Barba-Espín G, Hernández JA. 2013. Elucidating hormonal/ROS networks during seed germination: insights and perspectives. Plant Cell Reports 32: 1491-502.), and can serve as a window of signaling, or the cause of damage if overproduced (El-Maarouf-Bouteau & Bailly 2008El-Maarouf-Bouteau H, Bailly C. 2008. Oxidative signaling in seed germination and dormancy. Plant Signaling & Behavior 3: 175-182.). Therefore, the activity of antioxidant enzymes during germination of B. capitata seeds was investigated.

Figure 2
Histolocalization of superoxide anions (O2 -) in embryos of Butia capitata seeds during germination. The dark blue/purple indicates the presence of the anion. D, dry; I, imbibed; 24h, 24 hours after operculum removal; G, early-germinated.

Among the enzymes investigated here, SOD and GR were observed to have increased activity relative to D seeds as soon as imbibition occurred (Fig. 1E, F), while CAT activity was higher in the early-germination phase than in phases I and 24h post-operculum removal (P < 0.05; Fig. 1D). The SOD and GR results indicate that imbibition in B. capitata seeds seems to induce or stimulate the activity of antioxidant enzymes. Indeed, that imbibition leads to increased respiration metabolism, which generates ROS and stimulates antioxidant pathways to keep redox homeostasis under control, has been widely discussed (Foyer & Noctor 2005Foyer CH, Noctor G. 2005. Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. The Plant Cell 17: 1866-1875.; El-Maarouf-Bouteau & Bailly 2008El-Maarouf-Bouteau H, Bailly C. 2008. Oxidative signaling in seed germination and dormancy. Plant Signaling & Behavior 3: 175-182.; Diaz-Vivancos et al. 2013Diaz-Vivancos P, Barba-Espín G, Hernández JA. 2013. Elucidating hormonal/ROS networks during seed germination: insights and perspectives. Plant Cell Reports 32: 1491-502.; Gomes & Garcia 2013Gomes MP, Garcia QS. 2013. Reactive oxygen species and seed germination. Biologia 68: 351-357.). It is important to point out that CAT activity was at least 10-fold higher than that of SOD (Fig. 1D, E), suggesting that H2O2 was maintained at non-toxic levels in germinating seeds (higher CAT activity). Another interesting observation is that the increased SOD activity upon imbibition did not eliminate O2 -, which leads to the conclusion that the presence of this molecule is essential for the process of seed germination. Moreover, since O2 - is present only in the haustorium, it participates in germination itself and not only in reserve mobilization (a post-germinative event). Altogether, as germination of B. capitata seeds progresses successfully, the activities of CAT, SOD and GR can be assured and are essential for keeping ROS under control during the recovery of metabolism, and thus allowing germination to occur.

The present study showed the involvement of ROS and antioxidant enzymes other than ABA during the germination process of the palm species Butia capitata. The involvement of H2O2 and O2 - during the entire process was evident. Interestingly, it seems that superoxide anion is more related to germination signaling in B. capitata seeds than the expected H2O2, by interacting with ABA after operculum removal and allowing germination itself to proceed. The activity of GR and SOD had important roles in ROS scavenging during the entire process, while CAT activity must be related to the initial development of seedlings due to its increased activity in early-germination seeds, as shown here. Taking all the enzymes together, their role in ROS scavenging seems to be secondary to their role in seed germination signalling. The marked presence of O2 - was essential for demonstrating that the haustorium is important for palm seed germination from the beginning of the germination process. Actually, the role of the haustorium during palm seed germination itself has been neglected in previous works and needs to be investigated more deeply in B. capitata and in other palm species.

Acknowledgements

We thank to Prof. LV Modolo for equipment using and to Prof. MP Gomes for critical reading the manuscript. Financial support was provided by CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico, 446346/2014-4) and FAPEMIG (Fundação de Amparo à Pesquisa do Estado de Minas Gerais, PPM-00163-16). EM Bicalho received a postdoctoral scholarship from CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior); TRS Santos was granted a scholarship from CNPq; QS Garcia received a research productivity scholarship from CNPq.

References

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  • Alvares CA, Stape JL, Sentelhas PC, Gonçalves JLM, Sparovek G. 2013. Köppen’s climate classification map for Brazil. Meteorologische Zeitschrift 22: 711-728.
  • Bailly C. 2004. Active oxygen species and antioxidants in seed biology. Seed Science Research 14: 93-107.
  • Barba-Espin G, Diaz-Vivancos P, Clemente-Moreno MJ, et al 2010. Interaction between hydrogen peroxide and plant hormones during germination and the early growth of pea seedlings. Plant, Cell & Environment 33: 981-994.
  • Baskin CC, Baskin JM. 2014. Seeds: ecology, biogeography, and evolution of dormancy and germination. San Diego, Academic Press.
  • Baskin JM, Baskin CC. 2013. What kind of seed dormancy might palms have? Seed Science Research 24: 17-22.
  • Bewley JD, Bradford KJ, Hilhorst HWM, Nonogaki H. 2013. Seeds: physiology of development, germination and dormancy. New York, Springer.
  • Bicalho EM, Motoike SY, Borges EEL, Ataíde GM, Guimarães VM. 2016. Enzyme activity and reserve mobilization during macaw palm (Acrocomia aculeata) seed germination. Acta Botanica Brasilica 30: 437-444.
  • 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 Biology 17: 990-996.
  • Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72: 248-254.
  • Bray EA. 1997. Plant responses to water deficit. Trends in Plant Science 2: 48-54.
  • Dias DS, Ribeiro LM, Lopes PSN, Munné-Bosch S, Garcia QS. 2017. Hormonal profile and the role of cell expansion in the germination control of Cerrado biome palm seeds. Plant Physiology and Biochemistry 118: 168-177.
  • Diaz-Vivancos P, Barba-Espín G, Hernández JA. 2013. Elucidating hormonal/ROS networks during seed germination: insights and perspectives. Plant Cell Reports 32: 1491-502.
  • El-Maarouf-Bouteau H, Bailly C. 2008. Oxidative signaling in seed germination and dormancy. Plant Signaling & Behavior 3: 175-182.
  • Fior CS, Rodrigues LR, Leonhardt C, Schwarz SF. 2011. Overcoming dormancy in seeds of Butia capitata Ciência Rural 41: 1150-1153.
  • 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.
  • Foyer CH, Noctor G. 2005. Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. The Plant Cell 17: 1866-1875.
  • Giannopolitis CN, Ries SK. 1977. Superoxide dismutases: I. Occurrence in higher plants. Plant Physiology 59: 309-314.
  • Gomes MP, Carneiro MMLC, Nogueira COG, Soares AM, Garcia QS. 2013. The system modulating ROS content in germinating seeds of two Brazilian savanna tree species exposed to As and Zn. Acta Physiologiae Plantarum 35: 1011-1022.
  • Gomes MP, Garcia QS. 2013. Reactive oxygen species and seed germination. Biologia 68: 351-357.
  • Köppen W. 1900. Versuch einer Klassifikation der Klimate, vorzugsweise nach ihren Beziehungen zur Pflanzenwelt. Geographische Zeitschrift 6: 593-611.
  • Liu F, Jensen CR, Andersen MN. 2005. A review of drought adaptation in crop plants: changes in vegetative and reproductive physiology induced by ABA-based chemical signals. Australian Journal of Agricultural Research 56: 1245-1252.
  • Liu Y, Ye N, Liu R, Chen M, Zhang J. 2010. H2O2 mediates the regulation of ABA catabolism and GA biosynthesis in Arabidopsis seed dormancy and germination. Journal of Experimental Botany 61: 2979-2990.
  • Oliveira NCC, Lopes PSN, Ribeiro LM, Mercandante-Simões MO, Oliveira LAA, Silvério FO. 2013. Seed structure, germination, and reserve mobilization in Butia capitata (Arecaceae). Trees 27: 1633-1645.
  • Oracz K, Voegele A, Tarkowská D, et al 2012. Myrigalone A inhibits Lepidium sativum seed germination by interference with gibberellin metabolism and apoplastic superoxide production required for embryo extension growth and endosperm rupture. Plant and Cell Physiology 53: 81-95.
  • Pérez HE, Shiels AB, Zaleski HM, Drake DR. 2008. Germination after simulated rat damage in seeds of two endemic Hawaiian palm species. Journal of Tropical Ecology 24: 555-558.
  • Segovia AO, Batis AI, Arechiga MR, Mendoza A. 2003. Seed biology of palms: a review. Palms 47: 79-94.
  • Spera MRN, Cunha R, Teixeira JB. 2001. Quebra de dormência, viabilidade e conservação de sementes de buriti (Mauritia flexuosa). Pesquisa Agropecuária Brasileira 36: 1567-1572.
  • Svenning JC. 2001. On the role of microenvironmental heterogeneity in the ecology and diversification of neotropical rain-forest palms (Arecaceae). The Botanical Review 67: 1-53.
  • Tomlinson PB. 2006. The uniqueness of palms. Botanical Journal of the Linnean Society 151: 5-14.
  • Velikova V, Yordanov I, Edreva A. 2000. Oxidative stress and some antioxidant systems in acid rain-treated bean plants: Protective role of exogenous polyamines. Plant Science 151: 59-66.
  • Vieira BC, Bicalho EM, Munné-Bosch S, Garcia QS. 2017. Abscisic acid regulates seed germination of Vellozia species in response to temperature. Plant Biology 19: 211-2016.
  • Weiler EW. 1980. Radioimmunoassays for the differential and direct analysis of free and conjugated abscisic acid in plant extracts. Planta 148: 262-272.

Publication Dates

  • Publication in this collection
    21 Sept 2018
  • Date of issue
    Jan-Mar 2019

History

  • Received
    29 May 2018
  • Accepted
    16 Aug 2018
Sociedade Botânica do Brasil SCLN 307 - Bloco B - Sala 218 - Ed. Constrol Center Asa Norte CEP: 70746-520 Brasília/DF. - Alta Floresta - MT - Brazil
E-mail: acta@botanica.org.br