GERMINATION AND INITIAL GROWTH OF Sesbania punicea (Cav.)Benth.: INFLUENCE OF SALINITY, FLOODING AND LIGHT1

GERMINAÇÃO E CRESCIMENTO INICIAL DE Sesbania punicea Benth: INFLUÊNCIA DA SALINIDADE, ALAGAMENTO E LUZ.

Bianca de Borba Barreto Sonia Marisa Hefler Emanuela Garbin Martinazzo Ioni Gonçalves Colares About the authors

ABSTRACT

Sesbania punicea (Cav.) Benth. has been recommended for the recovery of degraded areas. This study aimed at verifying the effect of salinity in the germination of S. punicea seeds in different hydric and luminosity conditions and assessing the influence of salinity and flooding on the growth and concentration of photosynthetic pigments. After the morphometric measurements of the fruits and seeds, we performed germination tests in different salt concentrations (0,5, 10 and 15gL-1 NaCl), keeping the seeds in a humid substrate (normoxy) or submerged (flooding), in the presence or absence of luminosity. There was a decrease in the percentage of germination and germination speed index (GSI) of seeds that were kept submerged in the dark. The average germination time (AGT) decreased up to the concentration of 10gL-1NaCl when the seeds were submitted to submersion in the presence of light. The growth and the production of leaves of seedlings exposed to flooding decreased as the salt concentration increased. The concentrations of photosynthetic pigments of seedlings of S. punicea did not differ among the treatments. Therefore, the colonization and occupation of new degraded areas by S. punicea may be limited by the presence of salts concentrations in the soil.

Keywords:
Seeds; Seedlings; Degraded areas

RESUMO

Sesbania punicea

tem sido indicada para a recuperação de áreas degradadas. Este estudo teve como objetivo verificar o efeito da salinidade na germinação de sementes de S. punicea em diferentes condições hídricas e de luminosidade, bem como avaliar a influência da salinidade e alagamento no crescimento e concentração de pigmentos fotossintéticos. Após a realização das medidas morfométricas dos frutos e sementes, realizamos testes de germinação em diferentes concentrações de sal (0, 5, 10 e 15gL-1NaCl), mantendo as sementes em um substrato úmido (normoxia) ou submersas (alagamento), na presença ou ausência de luminosidade. Houve uma diminuição na porcentagem de germinação e índice de velocidade de germinação (IVG) de sementes que foram mantidas submersas no escuro. O tempo médio de germinação (TMG) diminuiu até a concentração de 10gL-1NaCl quando as sementes foram submetidas à submersão na presença de luz. O crescimento e a produção de folhas de plântulas expostas ao alagamento diminuíram à medida que a concentração de sal aumentou. As concentrações de pigmentos fotossintéticos de plântulas de S. punicea não diferiram entre os tratamentos. Concluímos que, a colonização e ocupação de novas áreas degradadas por S. punicea pode ser limitada pela concentração de sais no solo.

Palavras-Chave:
Áreas degradadas; Plântulas; Sementes

1. INTRODUCTION

The germination process is a critical stage for plant establishment, where reactivation of metabolic activity with increased vacuolization and reserve mobilization of endosperm cell are the first signs that a seed has transitioned to germination (Penfield, 2017Penfield S. Seed dormancy and germination. Current Biology. 2017;27:853-909.). The sequence of physiological and biochemical events during the germination of seeds is influenced by several abiotic factors, such as light, temperature and hydric saturation of the soils which can restrain or inhibit germination (Oliveira et al., 2015Oliveira AKM, Souza AS, Souza JS, Carvalho JMB. Temperature and substrate influences on seed germination and seedling formation in Callisthene fasciculata Mart. (Vochysiaceae) in the laboratory. Revista Árvore. 2015;39(3):487-95.; Oliveira and Gualtieri, 2016Oliveira AKM, Gualtieri SCJ. Gas exchange in young plants of Tabebuia aurea (Bignoniaceae Juss.) subjected to flooding stress. Revista Árvore. 2016;40(1):39-49.).

Hydric saturation of the soil restrains the amount of oxygen and, within short time, may generate a hypoxic environment or even an anoxic one. Metabolic changes in the germinative process can occur as a function of oxygen depletion in the medium. Conditions of anoxia may accelerate the rate of anaerobic fermentation and result in the depletion of reserve carbohydrates, and consequently interfere with the germination of the seeds (Ferreira et al., 2009Ferreira CS, Piedade MTF, Tiné MAS, Rossatto DR, Parolin P, Buckeridge MS. The role of carbohydrates in seed germination and seedling establishment of Himatanthus sucuuba, an Amazonian tree with populations adapted to flooded and non-flooded conditions. Annals of Botany. 2009;104(6):1111-9.). Salinity is another important factor that interferes in the germination of seeds, growth and reproduction of the plants (Parida and Das, 2005Parida AK, Das AB. Salt tolerance and salinity effects on plants: a review. Ecotoxicology and Environmental Safety. 2005;60:324-49.). In saline soils, the germination and survival of the seedlings are conditioned by the capacity to accumulate salts in the cell juice, as a mechanism to compensate for the low osmotic potential and ensure water absorption (Willadino and Camara, 2010Willadino LE, Camara TR. Tolerância das plantas à salinidade: aspectos fisiológicos e bioquímicos. Enciclopédia Biosfera. 2010;6(11):1-23.).

Optimal conditions for the development of species, viability and seed germination rate can be used to predict the impact that some species may cause in the ecosystems. Therefore, succession, natural regeneration and rehabilitation studies of degraded areas have germination and the establishment of seedlings as their guiding principles (Gomes and Fernandes, 2002Gomes V, Fernandes GW. Germinação de aquênios de Baccharis dracunculifolia D. C. (Asteraceae). Acta Botanica Brasilica. 2002;16:421-7.).

Sesbania punicea (Cav.) Benth. (Fabaceae), a species originally from South America, is distributed throughout the phytogeographic domains of Atlantic Forest, Pampa and Pantanal (Bergmann, 2014Bergmann K. Sesbania punicea (Cav.) Benth. 2014. [accessed in: Aug. 20, 2018]. Available in: https://botany.cz/en/sesbania-punicea/.
https://botany.cz/en/sesbania-punicea/...
; Queiroz, 2018Queiroz RT. Sesbania in Flora do Brasil 2020 em construção. Jardim Botânico do Rio de Janeiro. [access in: Aug. 20, 2018] Available in: http://reflora.jbrj.gov.br/reflora/floradobrasil/FB101171..
http://reflora.jbrj.gov.br/reflora/flora...
). It is considered an invasive exotic species in some places of North America, Europe, South Africa and Australia, to where it was taken as an ornamental plant and then quickly spread (Woodward and Quinn, 2011Woodward SL, Quinn JA. Encyclopedia of invasive species: from africanized honey bees to zebra mussels. Greenwood Press; 2011. 764p.; WIDEpac, 2012WIDEPac. A guide for integrated management of weeds in cotton. Australia Government. Cotton Research and Development Corporation. 2012. 225p.).The species has been cultivated as an ornamental plant, showing excessive success in its naturalization, with propagation often facilitated by natural perturbations such as fires, storms, change in the use of land and excessive building in formerly forested land, where the plant settles and spreads in clearings (Ulibarri et al., 2002Ulibarri EA, Sosa EVG, Cialdella AM, Fortunato RE, Bazzano D. Leguminosas; Nativas y exóticas. 2002. 320p. (Colección Biota Rioplatense, v.7)). As it tolerates poor soil very well and can easily adapt to any climate, this species can infest humid or flooded areas, including irrigated rice cultures (Kissmann and Groth, 1992Kissmann KG, Groth D. Plantas infestantes e nocivas. São Paulo: BASF; 1992.).

Because of their high survival rates in perturbed environments, some species of the genus Sesbania have been recommended for recovering degraded areas in Brazil (Chaves et al., 2003Chaves LLB, Carneiro JGA, Barroso DG, Leles, PSS . Efeitos da inoculação com rizóbio e da adubação nitrogenada na produção de mudas de Sesbania em substrato constituído de resíduos agroindustriais. Revista Árvore. 2003; 27(4):443-9.). For instance, S. virgata has been indicated for recovering riparian forests (Silva et al., 2011Silva PEM, Santiago EF, Daloso DM, Silva EM, Silva JO. Quebra de dormência em sementes de Sesbania virgata (Cav.) Pers. Idesia. 2011;29(2):39-45.). However, the use of species of this genus in environmental recovery projects should be analyzed cautiously because of the easy spread and infesting characteristics for the species (WIDEpac, 2012WIDEPac. A guide for integrated management of weeds in cotton. Australia Government. Cotton Research and Development Corporation. 2012. 225p.).

Sesbania punicea is a shrub or small tree and can grow up to five meters high. It has paripinnate leaves, each with 7-16(18) pairs of oppositely arranged leaflets, sometimes with thorny stipules and small stipules, and slender stems. Blooming occurs in spring and summer with big, showy, red-orange flowers, producing fruit in autumn. The fruit is a straight, pendulous, tetragonal and dehiscent legume, which produces 3-9(10) seeds (Ulibarri et al., 2002Ulibarri EA, Sosa EVG, Cialdella AM, Fortunato RE, Bazzano D. Leguminosas; Nativas y exóticas. 2002. 320p. (Colección Biota Rioplatense, v.7); Bergmann, 2014Bergmann K. Sesbania punicea (Cav.) Benth. 2014. [accessed in: Aug. 20, 2018]. Available in: https://botany.cz/en/sesbania-punicea/.
https://botany.cz/en/sesbania-punicea/...
). This is a fast-growing species that produces a large amount of seeds that can spread to long distances through water currents (Hunter and Platenkamp, 2003Hunter J, Platenkamp GAJ. The hunt for red Sesbania: biology, spread and prospects for control. Cal EPPC Newsletter. 2003;11(2):4-6.; Woodward and Quinn, 2011Woodward SL, Quinn JA. Encyclopedia of invasive species: from africanized honey bees to zebra mussels. Greenwood Press; 2011. 764p.). The species reproduces only through seeds, whose viability, in a seed bank, is no longer than 2-3 years (Hoffmann and Moran, 1998Hoffmann JH, Moran VC. The population dynamics of an introduced tree, Sesbania punicea, in South Africa, in response to long-term damage caused by different combinations of three species of biological control agents. Oecologia. 1998;114:343-8.).

Although the occurrence of S. punicea is facilitated by environmental perturbations, making it an infesting species, studies that approach the requirements for the germination of its seeds and its adaptability to stressful environmental conditions is necessary for understanding the development and establishment of this species. Such information helps environmental managers make decisions about the necessity of intervention for species control or the use of the species in vegetal restoration projects. Two limiting factors for the establishments of many species in the coastal region of southern Brazil can be cited: the variations in hydrological conditions and the presence of salinity in the soil. Therefore, this study aims to investigate the effect of salinity during the germination of Sesbania punicea seeds in different hydric and luminosity conditions and assess the influence of salinity and flooding on the growth.

2. MATERIALS AND METHODS

2.1. Place and collection of seeds

We obtained seeds of S. punicea from fruits of 20 different matrices present in the Environmental Protection Area (APA) of Verde Lagoon, located in the city of Rio Grande, RS, Brazil (32º06’ and 32º09’S to 52º10’ and 52º11’W). Samples of the plants were collected, mounted herbarium specimens and deposited in the Herbarium HURG of the University Federal of Rio Grande - FURG, asvoucher specimens under voucher number HURG 2662.

Fruits in similar ripeness status were collected in April 2012 and taken to the Laboratory of Vegetal Physiology of the Federal University of Rio Grande - FURG, where we carried out the experiments. After collecting the fruits, we mixed them and manually opened them for the seeds. The seeds that were dark-colored stained or had holes were discarded, and those that were intact and light-colored were packed in kraft paper envelopes and stored in a dry and airy place until the beginning of the experiments, a week later. In order to assess the reproductive investment of the species, an aliquot of 200 fruits was taken from the total number of fruits collected. We performed morphometry measurements of fruits and seeds, taking into consideration: length and width of the fruit (cm), number of seeds per fruit, size (cm) and mass (g) of the seeds. We weighed the seeds using an analytical balance accurate to 0.1mg, and we took the measurements with calipers.

2.2. Germination Tests

Taking into account that the seeds of the genus Sesbania show different levels of tegument dormancy (Ferreira et al., 2005Ferreira C, Piedade MTF, Parolin P, Barbosa KM. Tolerância de Himatanthus sucuuba Wood. (Apocynaceae) ao alagamento na Amazonia Central. Acta Botanica Brasilica. 2005;19:425-9.), the seeds were scarified with number-eight wood sandpaper, according to the recommendation of Fowler and Bianchetti (2000)Fowler JAP, Bianchetti A. Dormência em sementes florestais. Colombo: Embrapa Florestas; 2000.. Germination tests were performed on eight samples of 25 seeds, for each of the four treatments: normoxy/ light and normoxy/dark; flooded/light and flooded/ dark. The conditions of each treatment were: (a) sowing the seeds in “gerbox” type boxes, on a sheet of blotting paper moistened with 25 mL of saline solution with concentrations of 0,5,10 and 15gL-1NaCl, and transferred to a germination chamber (SL-224 Solab) at 25ºC, with a photoperiod of 12h light/12h dark (NR-L, normoxy/ light treatment) or 24h dark (NR-D, normoxy/dark treatment); (b) sowing the seeds in Falcon pipes (50 mL) filled with 25 mL of saline solution with concentrations of 0, 5, 10 and 15gL-1NaCl, and transferred to a germination chamber (SL-224 Solab) at 25ºC, with a photoperiod of 12h light/12h dark (FL-L, flooded/ light treatment) or 24h dark (FL-D, flooded/dark treatment).

We observed germination daily for 30 days, and the seeds that showed a minimal root protrusion of 2mm were considered germinated (Rehman, 1996Rehman S, Harris PJC, Bourne WF, Wilkin J. The effects of sodium chloride on germination and the potassium and calcium contents of Acacia seeds. Seed Science and Technology. 1996;25:45-57.). The treatments whose germination occurred in the dark were counted with safety green light (Amaral-Baroli and Takaki, 2001Amaral-Baroli A, Takaki M. Phytochrome controls achene germination in Bidens pilosa L. (Asteraceae) by very low fluence response. Brazilian Archives of Biology and Technology. 2001;44:121-4.). In order to check the possibility of dormancy induced by low osmotic potential, the seeds that did not germinate after 30 days of incubation in salinities higher than zero were submitted to the procedure of salt stress relief (Khan and Gul, 2006Khan MA, Gul B. Halophyte seed germination. In: Khan MA, Weber DJ, editors. Eco-physiology of high salinity tolerant plants. Dordrecht: Springer Publications; 2006. p.11-30.). For this, the seeds were washed with distilled water and placed in distilled water for germination, under the same conditions described above, for 15 more days.

Germination was analyzed by the following parameters: percentage of germination (G); germination speed index (GSI), given by the equation GSI=ΣG1/T1++Gi/Ti, where G1 to Gi represents the number of seeds germinated each day and T1 to Ti is the time in days (Oliveira et al., 2009Oliveira ACS, Martins GN, Silva RF, Vieira HD. Testes de vigor em sementes baseados no desempenho de plântulas. Inter Science Place. 2009;2(4):1-21.); average time of germination (AGT) according to the equation ATG=Σnxd/N, where n is the number of seeds germinated within a time interval, d is the period of incubation, in days, at the moment of germination, and N is the total number of germinated seeds in the treatment (Brenchley and Probert, 1998Brenchley JL, Probert RJ. Seed germination responses to some environmental factors in the seagrass Zostera capricorni from eastern Australia. Aquatic Botany. 1998;62:177-88.).

2.3. Growth responses of the seedlings

In order to analyze the initial growth of the seedlings of S. punicea in different hydric and saline concentrations, after scarification the seeds were placed in a clear polystyrene vase. This vase contained 0.5Kg of soil collected in the Environmental Protection Area (APA) of Verde Lagoon, previously dried at 200ºC for two hours (Lima Junior, 2010Lima Junior MJV. Manual de procedimentos para análise de sementes florestais. Manaus: UFAM; 2010. [accessed in: Aug 16, 2018]. Available in: https://www.researchgate.net/publication/ 232768692.
https://www.researchgate.net/publication...
). After sowing the seeds, we used the following treatments: normoxy/light treatment with daily irrigation with 25mL of salt solution with 0, 5, 10 and 15 gL-1NaCl, and flooded/light treatment, keeping 1cm layer of water over the substratum, under the same salt concentrations (0, 5, 10 and 15gL-1NaCl). The seedlings were kept under these conditions for 60 days, and after that, we analyzed the total number of leaves and the height of the plants.

2.4. Extraction and quantification of photosynthetic pigments

At the end of the growth experiment, seedlings with 60 days of growth were used for the extraction and quantification of photosynthetic pigments (chlorophyll a, chlorophyll b, total chlorophyll and carotenoids). For this, only seedlings originating from the normoxy / light treatment, submitted to different concentrations of NaCl, were used. Due to low production of leaves by plants growing in flooding conditions, we have not performed the extraction and quantification of photosynthetic pigments for this treatment.

After gauging the fresh mass, we macerated the samples with acetone 80%. The macerate obtained was filtered and the volume of acetone was filled up to 100mL.After that, a Biospetro SP-22 spectrophotometer was used at wavelengths of 663nm, 645nm and 470nm. The concentrations of the pigments were determined according to per the formulae of Arnon (1945)Arnon DJ. Cooper enzimes in isolated chloroplast: Polyphenoloxidade in Beta vulgaris. Plant Physiology. 1945;24:1-15. for chlorophylls and Lichtenthaler (1987)Lichtenthaler HK. Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods in Enzymology. 1987;148:350-82. for carotenoids.

2.5. Data analysis

This study used a completely randomized experimental design.Afterverifyingthenormalization of the data, the germination percentages were transformed by using the expression arcsen v %, and the growth values were transformed in v x for their normalization. However, the data presented here are not transformed. For the analysis of the germination and growth data, a regression analysis was applied for to verify the differences between the averages in the treatments. When there was significance at 5%, the germination data were adjusted by orthogonal polynomials. The data of concentration of pigments were submitted to variance analysis by F test and the means were compared by Tukey’s test, with an error probability of 5%. The quantitative characteristics were submitted to descriptive analysis for obtaining their respective means.

3. RESULTS

We collected 1500 fruits of S. punicea from 20 matrices present in the study area, totaling approximately 7600 seeds,whose weightwas 0.532Kg. Fifty-five percent of the seeds collected were intact and 45% were predated, with holes in the endocarp caused by driller insects. Table 1 shows the descriptive analysis of the morphometric measurements of the fruits and seeds.

Table 1
Morph metric measurements of fruits and seeds of Sesbania punicea collected in the Environmental Protection Area (APA) of Verde Lagoon (N = 200).
Tabela 1
Medidas morfométricas de frutos e sementes de Sesbania punicea coletados na Área de Proteção Ambiental (APA) da Lagoa Verde (N = 200).

Figure 1 shows the germinative behavior of the seeds of S. punicea in relation to the salt concentration. The germination of seeds that had been kept submerged (flooded) and in the dark adjusted to the linear model and showed a tendency to decrease as the salt concentration increased. There was a 73% decrease in the germination of seeds kept under these conditions for the concentration of 15gL-1NaCl when compared to the control (0gL-1 NaCl).

Seeds that had been kept under normoxy conditions in the dark showed quadratic adjustment for the variable germination, with a high coefficient of determination (R2 = 0.87). The point of minimal response for seeds under these conditions was 24%. On the other hand, seeds kept submerged and in the presence of light, like those kept submerged in the dark, showed a decrease in germination up to the highest salt concentration. There was a decrease of approximately 25% in the germination of seeds under the concentration of 15gL-1NaCl, in comparison with those under concentration of 0gL1NaCl (Figure 1A).There was no significant difference (P>0.05) in the average germination time (AGT) of seeds and in the germination speed index (GSI) under the influence of normoxy/light treatments (Figures 1A and 1B).

For other treatments, GSI data adjusted to the quadratic model (Figure 1B).There was a tendency for decreasing germination speed index in seeds kept submerged in the dark up to the concentration of 15gL1NaCl. Seeds kept submerged with light showed their point of maximum response in concentration of 6.5gL1NaCl with a subsequent tendency to decrease up to the highest salt concentration. However, seeds kept in normoxy in the dark showed a tendency for decreasing germination speed index up to the point of minimum response (2.6gL-1NaCl), with a subsequent tendency to increase up to the highest salt concentration(15gL-1NaCl).

Seeds under light submersion conditions presented significant differences (R2 = 0.94), in the average germination time (AGT) with increasing NaCl concentration (Figure 1C). The seeds under these conditions showed a decrease in the average germination time up to the concentration of 10gL-1NaCl with a subsequent increase up to the highest concentration. There was no significant difference (P>0.05) in the average germination time of seeds under the influence of normoxy/dark and flooded/dark treatments. There were no answers in germination in seeds submitted to salt stress relief and germinated for 15 days using distilled water in conditions of flooded or normoxy dark/light treatments.

The length of the aerial part of seedlings under normoxy conditions decreased linearly up to concentration 15gL-1NaCl, with a 48% decrease between the highest and lowest concentrations (0gL-1NaCl). Seedlings under the influence of flooding showed quadratic adjustment for the height of aerial part, with a decrease in the height of the aerial part up to the point of minimal response of 11.6 gL-1NaCl (Figure 2A). The number of leaves of plants under the influence of flooding adjusted to the quadratic model with high coefficient of determination (R2 = 0.94), with the point of minimal response in the concentration of 10.1gL1NaCl. There was no significant difference (P>0.05) in the number of leaves of plants under the influence of the normoxy treatment (Figure 2B).

The concentrations of photosynthetic pigments in seedlings of S. punicea that had been kept under normoxy conditions with light are shown in Table 2. There was no significant difference (P>0.05) between the values of chlorophylls and carotenoids in the different salt concentrations tested.

Table 2
Chlorophyll a, b and total chlorophyll, and carotenoid pigments, expressed in mg g-1 fresh mass, in leaves of Sesbania punicea submitted to normoxy and different concentrations of NaCl.
Tabela 2
Clorofila a, b e clorofila total e pigmentos carotenóides, expressos em mg g-1 de massa fresca, em folhas de Sesbania punicea submetidas a normoxia e diferentes concentrações de NaCl.

4. DISCUSSION

The fruits of Sesbania punicea, collected in the APA (Environmental Protection Area) of Verde Lagoon, showed seeds with little variation in average size (0.6 ± 0.01cm) and weight (0.07± 0.01g), with a high predation rate (45%). The average fresh mass of 100 seeds was very similar to the values found by Poletto et al. (2007)Poletto RS, Delachiave MEA, Pinho SZ. Superação da dormência de sementes de Sesbania virgata (CAV.) Poir. Revista Científica Eletrônica de Engenharia Florestal. 2007;5(9);1-18. for the species Sesbania virgata. According to Hoffmann and Moran (1998)Hoffmann JH, Moran VC. The population dynamics of an introduced tree, Sesbania punicea, in South Africa, in response to long-term damage caused by different combinations of three species of biological control agents. Oecologia. 1998;114:343-8., S. punicea presents a high fruit production as a survival strategy, since the seeds undergo strong predation pressure, besides having a short life in the seed bank.

The excess of water during germination may impose anoxic conditions to the seeds. Seeds of many terrestrial plants that display high germination rates in soil do not germinate in water, because they can quickly lose viability under such conditions (Parolin, 2001Parolin P. Seed germination and early establishment of 12 tree species from nutrient-rich and nutrient-poor Central Amazonian floodplains. Aquatic Botany. 2001;70:89-103.). According to Okamoto and Joly (2000)Okamoto JM, Joly CA. Ecophysiology and respiratory of Inga sessilis (Vell.) Mart. (Mimosaceae) seeds subjected to hypoxia and anoxia. Revista Brasileira Botânica. 2000;23(1):51-7., for the species Inga sessilis, anoxia can be lethal to the seeds. Although flood conditions have influenced the resumptionof embryogrowth, there was arelative increase in the percentage of germination of seeds stored in these conditions, when compared to those germinated in normoxy. Seeds of Tabebuia cassinoides, typical species of environments with flooding, did not germinate under conditions of total submersion and anoxic, but under normoxic conditions or partial submersion the seeds reached 100% of germination (Kolb and Joly, 2010Kolb R, Joly CA. Germination and anaerobic metabolism of seeds of Tabebuia cassinoides (Lam.) DC subjected to flooding and anoxia. Flora. 2010;205:112-7.). Seedlings of Tabebuia aurea, another species characteristic of flooded environments, survive in conditions of stress by flooding and anoxic for more than 48 hours, reducing its metabolic activity (Oliveira and Gualtieri, 2016Oliveira AKM, Gualtieri SCJ. Gas exchange in young plants of Tabebuia aurea (Bignoniaceae Juss.) subjected to flooding stress. Revista Árvore. 2016;40(1):39-49.).

An important restriction resulting from excess water is an inadequate supply of oxygen to submerged plant tissues. Anaerobic conditions result in a rapid change in the expression of genes, which play a vital role in the metabolism of cells partially deficient in oxygen (Jackson and Colmer, 2005Jackson MB, Colmer TD. Response and adaptation by plants to flooding stress. Annals of Botany. 2005;96(4):501-5.). The root system of the T. cassinoides plants presented high amounts of ethanol under conditions of soil water saturation, corroborated by an increase in ADH activity (Kolb and Joly, 2009Kolb RM, Joly CA. Flooding tolerance of Tabebuia cassinoides: Metabolic, morphological and growth responses. Flora. 2009;204(7)528-35.). Seeds of T. cassinoides submerged and in anoxia showed activation of glycolytic pathway after a day of soaking and ethanol was the main product formed, along with an expressive production of lactate and malate (Kolb and Joly, 2010Kolb R, Joly CA. Germination and anaerobic metabolism of seeds of Tabebuia cassinoides (Lam.) DC subjected to flooding and anoxia. Flora. 2010;205:112-7.).

The saline stress affects the germination of seeds because of the osmotic effect, ion toxicity, or both. The plant can have various mechanisms for dealing with damage caused by salt, such as modifications in development, activity of antioxidant enzymes and hormonal production (Zhang et al., 2010Zhang H, Irving LJ, Mcgill C, Matthew C, Zhou D, Kemp P. The effects of salinity and osmotic stress on barley germination rate: sodium as an osmotic regulator. Annals of Botany. 2010;106:1027-35.). The effect of NaCl on germination of seeds of Suaeda physophora, Haloxylon ammodendron and Haloxylon persicum was due to both osmotic stress and ion toxicity (Song et al., 2005Song J, Feng G, Tian C, Zhang F. Strategies for adaptation of Suaeda physophora, Haloxylon ammodendron and Haloxylon persicum to a saline environment during seed-germination stage. Annals of Botany. 2005;96:399-405.).

The presence of dissolved osmolytes in the water causes a decrease in their hydric potential, being first perceived by the root system of the plants, inducing osmotic stress and reducing water availability (Acosta-Motos etal., 2017Acosta-Motos JR, Ortuño MF, Bernal-Vicente A, Diaz-Vivancos P, Sanchez-Blanco MJ, Hernandez JA. Plant responses to salt stress: adaptive mechanisms. Agronomy. 2017;7(1):18.),which can also affectseed germination due to the low availability of water free. The decrease in the number of germinated seeds with the increase of salt concentration as well as the absence of germination in the salt stress relief tests may represent an indication of the damage caused by salt to the embryo of S. punicea. Some studies have shown how germination can be inhibited under high concentration of salt and that the seeds can germinate after saline stress conditions are removed (Khan et al., 2000Khan MA, Ungar IA, Showalter AM. Effects of salinity on growth, water relations and ion accumulation of the subtropical perennial halophyte, Atriplex griffithiivar Stocksii. Annals of Botany. 2000;85:225-32., 2001Khan MA, Gul B, Weber DJ. Influence of salinity and temperature on the germination of Kochias coparia. Wetlands Ecology and Management. 2001;9:483-9.; Song et al., 2005Song J, Feng G, Tian C, Zhang F. Strategies for adaptation of Suaeda physophora, Haloxylon ammodendron and Haloxylon persicum to a saline environment during seed-germination stage. Annals of Botany. 2005;96:399-405.). However, this kind of response has been found in halophyte species.

Among the most common effects of soil salinity, growth inhibition by ions Na+ and Cl- is considered the main cause of the decrease in the speed of physiological and biochemical processes and consequent reduction in plant growth (Flowers, 2005Flowers TJ. Improving crop salt tolerance. Journal of Experimental Botany. 2005;55(396):307-19.; Dhanapackiam and Muhammad Ilyas, 2010Dhanapackiam S, Muhammad Ilyas MH. Effect of NaCl salinity on growth, nodulation and total nitrogen in Sesbania grandiflora. Indian Journal of Science and Technology. 2010;3(1):87-9.). The growth results observed in this study show the deleterious effect of salinity on the growth of seedlings of S. punicea. After 60 days of growth, there was an evident decrease in the size of seedlings and in the number of leaves produced as the concentration of saline solution increased.

Not all the species respond to salinity in the same manner. Tolerance varies in every culture and within the same species. The effect of salinity can be attributed to the water deficit caused by excess soluble salts in the root zone, causing a decrease in turgescence, reduction in cell expansion and consequent reductionin plant growth (Khalid and Silva, 2010Khalid A, Silva JAT. Yield, essential oil and pigment content of Calendula officinalis L. flower heads cultivated under salt stress conditions. Scientia Horticulturae. 2010;126(2):297-305.). Osmotic balance is essential for plants growing in saline medium, it can affect almost all aspects of plant development including: germination, vegetative growth and reproductive development (Shrivastava and Kumar, 2015Shrivastava P, Kumar R. Soil salinity: A serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation. Saudi Journal of Biological Sciences. 2015;22(2):123-31.). We observed a similar result in our study. In spite of the variability of the samples, there was an evident decrease in growth as the salt concentration increased.

The photosynthetic pigments of plants of S. punicea kept in different salt concentrations and in the absence of flooding were not affected by the salt concentrations. Despite the fact that the values showed a tendency to decrease as the salt concentration increased, the high coefficient of variation made it impossible for us to distinguish the means. Conversely, the concentrations of photosynthetic pigments of plants of Bruguiera parviflora cultivated in hydroponics (Parida et al., 2001Parida A, Das AB, Das P. Na Cl stress causes changes in photosynthetic pigments, proteins, and other metabolic components in the leaves of a true mangrove, Bruguiera parviflora, in hydroponic cultures. Journal of Plant Biology. 2001;45(1):28-36.), of the halophyte Plantago coronopus (Koyro, 2006Koyro HW. Effect of salinity on growth, photosynthesis, water relations and solute composition of the potential cash crop halophyte Plantago coronopus (L.). Environmental and Experimental Botany. 2006;56:136-46.), of Glaucium flavum (Cambrollé et al., 2011Cambrollé J, Redondo-Gómez S, Mateos-Naranjo E, Luque T, Figueroa ME. Physiological responses to salinity in the yellow-horned poppy, Glaucium flavum. Plant Physiology and Biochemistry, 2011;49:186-94.) and of the cowpea Vignia sinensis (Kandil et al, 2017Kandil AA, Shareif AE, Gad MA. Effect of salinity on germination and seeding parameters of forage Cowpea Seed. Research Journal of Seed Science. 2017;10(1):17-26.) were affected by salt stress.

Sesbania punicea is a species whose distribution is facilitated by perturbations in the nature, such as land clearing (Ulibarri et al., 2002Ulibarri EA, Sosa EVG, Cialdella AM, Fortunato RE, Bazzano D. Leguminosas; Nativas y exóticas. 2002. 320p. (Colección Biota Rioplatense, v.7)) and the presence of poor soils (Kissmann and Groth, 1992Kissmann KG, Groth D. Plantas infestantes e nocivas. São Paulo: BASF; 1992.). The high tolerance to salinity during the germination of the seeds may represent another facilitator for the spread of the species in environments with stressful characteristics, such as saline soils. The germination responses of S. punicea observed in this study show a competitive advantage of the species for quickly occupying perturbed environments, even in saline soils. However, characterizing and using S. punicea as a species with a great potential for recovering degraded areas might not be effective due to salinity, as the growth of the seedlings was affected by the increase in the salt concentration. This fact might limit occupation and spread of the species in new colonized areas.

6. CONCLUSION

The responses of germination and the development of the seedlings of S. punicea were affected by hydric conditions. The presence of NaCl affected negatively the germinative process in normoxic conditions. Flooding decreases the percentage of germination as salt concentrations increase. There is a decrease in the growth of the seedlings and in the production of leaves as the salt concentration increases. Therefore, thecolonization and occupation of new degraded areas by S. punicea may be limited by the presence of salt concentrations in the soil.

7.ACKNOWLEDGMENTS

We thank the Fundação de Coordenação e Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for funding this project. We are also grateful to undergraduates Thais Silva de Almeida and Luis Fernando Bilibio Westphalen for their assistance in the field and laboratory activities, and to Renan Castro Ferreira for his collaboration in the English translation of this manuscript

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Publication Dates

  • Publication in this collection
    08 Nov 2018
  • Date of issue
    2018

History

  • Received
    31 Jan 2018
  • Accepted
    30 Aug 2018
Sociedade de Investigações Florestais Universidade Federal de Viçosa, CEP: 36570-900 - Viçosa - Minas Gerais - Brazil, Tel: (55 31) 3612-3959 - Viçosa - MG - Brazil
E-mail: rarvore@sif.org.br