Acyl-homoserine Lactone from Saccharum Ã officinarum with

Article pubs.acs.org/jnp

Acyl-homoserine Lactone from Saccharum × of ficinarum with Stereochemistry-Dependent Growth Regulatory Activity Vanessa G. A. Olher,†,‡ Nagela P. Ferreira,† Alan G. Souza,† Lucas U. R. Chiavelli,† Aline F. Teixeira,§ Wanderley D. Santos,§ Silvana M. O. Santin,† Osvaldo Ferrarese Filho,§ Cleuza C. Silva,† and Armando M. Pomini*,† †

Departamento de Química and §Departamento de Bioquímica, Universidade Estadual de Maringá, Avenida Colombo 5790, 87020-900, Maringá-PR, Brazil ‡ Instituto Federal do Paraná, Campus Paranavaí, Rua José Felipe Tequinha 1400, 87703-536, Paranavaí-PR, Brazil S Supporting Information *

ABSTRACT: Acyl-homoserine lactones (AHLs) are a class of compounds produced by Gram-negative bacteria that are used in a process of chemical communication called quorum sensing. Much is known about how bacteria use these chemical compounds to control the expression of important factors; however, there have been few reports about the presence and effects of AHLs in plants. In this study, the phytochemical study of leaves and culms of sugar cane (Saccharum × of f icinarum) led to the identification of N-(3-oxo-octanoyl)homoserine lactone. Since the absolute configuration of the natural product could not be determined, both R and S enantiomers of N-(3-oxo-octanoyl)homoserine lactone were synthesized and tested in sugar cane culms. The enantiomers caused changes in the mass and length of buds and roots when used at micromolar concentrations. Using the sugar cane RB96-6928 variety, the S enantiomer increased sprouting of roots more effectively than the R enantiomer. Furthermore, scanning electron microscopy showed that both the R and S enantiomers led to more stretched root cells compared with the control.

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In recent years, a growing body of evidence shows that AHLs can be detected by the host and cause significant changes in host physiology. One of the most well-studied case is the detection of AHLs produced by Pseudomonas aeruginosa by diverse protein receptors, with many immunological consequences in human physiology.13 The interkingdom chemical interactions may also be observed, for example, in certain cases of vegetable species.14−16 The physiological effects of AHLs have been mainly investigated in the model species Arabidopsis thaliana, whose genome has been completely sequenced.17 It has been shown that AHLs can cause significant effects on the growth of primary roots, modulating plant development.18 In plants, genes related to cell growth and growth hormone regulation displayed altered expression in the presence of N-hexanoylHL.14 Similar phenomena were observed in Medicago truncatula, which also exhibited changes in protein expression in the presence of AHL, including proteins related to growth and hormone production.19 It was shown that in A. thaliana the AHL response can be associated with its hydrolysis metabolite homoserine, produced by a common plant enzyme, fatty acid amide hydrolase

uorum sensing is a chemical communication mechanism employed by different species of bacteria used to adapt and survive in their environment.1 Acyl-homoserine lactones (AHLs) are the best known semiochemical compounds from Gram-negative bacteria.2 These compounds are produced by LuxI homologous enzymes using acyl-coenzyme A and Sadenosyl methionine as precursors.3 AHLs have a conserved lactone moiety, and their structural diversity is conferred by an acyl side chain that may be saturated or unsaturated or have different numbers of carbon atoms that can be oxygenated, especially at C-3.2 Once produced, AHLs are released to the extracellular medium through active pumping or diffusion.4 The extracellular concentration of these metabolites increases as the bacteria multiply, until a critical concentration is reached. At this point, the established chemical equilibrium allows interactions of these compounds with LuxR homologous enzymes, which are responsible for AHL detection.5 These interactions cause a conformational change in the receptor protein, and the resulting complex has the capacity to regulate the expression of various genes. Typically, this mechanism is responsible for controlling the expression of metabolites such as antibiotics,6 enzymes,7 and exopolysaccharides8,9 and controlling the production of factors associated with biological nitrogen fixation in plants.10,11 Overall, quorum sensing plays a key role in bacterial survival, including interactions with hosts.12 © XXXX American Chemical Society and American Society of Pharmacognosy

Received: December 4, 2015

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DOI: 10.1021/acs.jnatprod.5b01075 J. Nat. Prod. XXXX, XXX, XXX−XXX

Journal of Natural Products

Article

Figure 1. (S)-N-(3-Oxo-octanoyl)homoserine lactone and its R enantiomer.

(FAAH).20 Additionally, this study found that long-chain AHLs were more easily hydrolyzed by FAAH and therefore led to an increase in the growth of primary roots of A. thaliana. Furthermore, it was found that (S)-N-(3-oxo-dodecanoyl)-HL was more active than its R enantiomer. The presence of the S enantiomer inhibited root growth at high concentrations (100 μM) and activated their growth at low concentrations (0.1 μM).20 Saccharum × of ficinarum is a grass belonging to the Poaceae family and is popularly known as sugar cane. This plant is distributed in tropical and subtropical climates and is an important agricultural product in Brazil, India, the Caribbean, and the United States.21 It is historically one of the main agricultural products of Brazil, used for the production of both sugar and ethanol, which may represent a less polluting alternative energy resource.22 Due to significant interest in this product and the need for producing food and renewable fuels to meet the growth and development of the world population, the discovery of new compounds capable of improving the yield of the crops of this culture is essential. Several studies have shown that sugar cane contains a wide variety of endophytic bacteria that colonize its tissues in symbiosis with the plant. Among these microorganisms, Gluconacetobacter, Azospirilum, Acetobacter, and Herbaspirillum spp. are the main nitrogen-fixing symbiotic agents in sugar cane and may influence the growth and development of the plant.23−26 In addition to the nitrogen-fixing species, other genera such as Enterobacter, Pantoea, Kluyvera, Citrobacter, Klebsiella, Pseudomonas, and Burkholderia may also influence plant growth and development.27,28 Among these bacteria, many are known to produce AHLs, especially Azospirilum.29 In this respect, it is essential to pay attention to the species Gluconacetobacter diazotrophicus, which was isolated as endophytic in sugar cane. A chemical study of the cultivation media from this bacteria showed the presence of various AHLs, including saturated N-hexanoyl-HL, N-octanoyl-HL, N-decanoyl-HL, and the derived β-carbonylated N-(3-oxo-decanoyl)-HL and N-(3-oxo-dodecanoyl)-HL.30 However, the authors did not verify if these metabolites were present in sugar cane extracts. Some research groups have attempted to characterize the presence of AHLs in plant tissues. Some time ago it was noted that bioreporters based on Agrobacterium tumefaciens NTL4(pZLR4) mutant cells were able to detect AHL or compounds with counterpart activities in extracts from corn leaves infected by Pantoea agglomerans, the causative agent for maize white spot disease.31 The same phenomenon has been previously observed in pea seedlings.32 Despite the knowledge gained from these studies, the biological activities of the compounds are still poorly understood for commercial plant species. Tomato was the first commercial species where the effects of exposure to AHL were studied. In this species, it was found that genes associated with ethylene production (an important plant hormone) were affected by the presence of bacterial signaling compounds.33 The activity of N-(3-oxo-octanoyl)-HL was determined in

soybean and corn, and it increased the germination rate and yield of the crop in field tests.34,35 In this paper, a study of the effects of AHL on the growing of sugar canes culms is reported. The first objective was to characterize bacterial signaling compounds that could be present in plant tissues. The phytochemical study of an extract obtained from sugar cane (stalks and leaves) led to the characterization of an AHL, which was subsequently synthesized and biologically assayed to characterize its physiological response in the plant rooting and budding processes. The importance of the absolute configuration of the compound for their biological activities was also investigated. Phytochemical Study of Sugar Cane and AHL Identification. Isolation of AHLs from plant tissues remains a challenge. AHLs are produced in low quantities by endophytic bacteria (usually at nanomolar concentrations). For this reason, the experimental design had to be optimized in many ways. In addition to a large amount of plant material in natura, EtOAc was used for extraction because it is known for efficiently extracting metabolites from this class.36 A laborious phytochemical study was performed using column chromatography with silica gel and Sephadex LH-20 to purify the target compound. Next, GC-MS analyses were performed to permit accurate identification of metabolites and comparisons of spectra with commercially available standards, since the natural product was isolated in minute amounts and NMR structural investigations were not possible.9,36 Fractions were analyzed by GC-MS by monitoring chromatographic peaks with characteristic AHL fragmentation patterns.37 One fraction gave a chromatogram containing a peak with a retention time of 13.20 min, which showed a mass spectrum with a typical fragment at m/z 143.07 resulting from McLafferty rearrangement commonly observed for the acylated side chain (Figure 1, Supporting Information).37 Another characteristic fragment was evidenced at m/z 100.02 and assigned to the homoserine lactone moiety. The MS data of the natural product were consistent with those observed for N-(3-oxo-octanoyl)homoserine lactone.31 In order to unambiguously determine the structure, the standard (±)-N-(3-oxo-octanoyl)-HL was commercially purchased (Aldrich) and analyzed by GC-MS using the same experimental conditions applied to the analysis of the natural product. A comparison of spectra led to the identification of the compound in the extract of S. × off icinarum as N-(3-oxo-octanoyl)-HL. This is one of the most commonly reported bacterial signaling compounds. This compound is produced, for example, by Agrobacterium tumefaciens to regulate the expression of genes involved in plasmid transfer.38 Although it was not possible to determine the absolute configuration, several studies demonstrated an S absolute configuration for naturally produced AHL (Figure 1).36 AHL Syntheses and Sugar Cane Rooting Biological Assays. After isolation and characterization of the natural product, the S and R enantiomers were prepared according to reported methodology.36 Furthermore, the synthesized R and S B



Article

Figure 2. Effect of (S)-N-(3-oxo-octanoyl)homoserine lactone and its R enantiomer (0.5 mg/L) on culms of sugar cane, variety RB96-6928. (A) Roots’ dry weight. (B) Roots’ length. (C) Buds’ dry weight. (D) Buds’ length. Means significantly higher than the control (Dunnett’s test, p ≤ 0.05) are marked *.

enantiomers were characterized by GC-MS, 1D and 2D 1H and 13 C NMR, and specific rotation data. In this study a bioassay was developed to show the effects of the synthesized AHL in sugar cane roots and buds. Growing experiments were performed from stem sections of two varieties of sugar cane (culms). The RB96-6928 variety (RB) is used commercially in large sugar cane plantations, while the SP80-3280 variety (SP) is widely used in experimental assays because it is the variety used in Brazil for the sugar cane genome sequencing program.39 The effects of AHL were determined by measuring the dry mass and length of roots and buds. It was observed that the natural AHL was found in sugar cane in very low concentration (approximately 0.02 mg/kg of fresh plant material), and the bioassays with the synthetic compounds were carried out using a similar concentration. In the experiment conducted with the RB variety, it was found that both enantiomers (0.5 mg/L each) led to an increase in root dry mass [S, 113.2%; R, 20.8%] and total root length [S, 68.6%; R, 11.9%], but the S enantiomer was more active and caused a statistically significant effect in comparison with the control (Figure 2). In the buds, the biological response to the enantiomers was distinct. The S enantiomer stimulated growth as measured by an increase in bud length (20.5%) and dry matter weight (42.5%), while the R enantiomer led to a decrease in dry matter weight (−39.9%) and bud length (−28.1%), compared with the control (Figure 2). To better understand the effect of the R enantiomer, the rootlets of treated culms were analyzed by SEM (Figure 3). The results showed that cells were elongated for both the R and S enantiomers compared with the control. This result showed that both enantiomers induced phenotypic changes in the roots of the plant.

Figure 3. Scanning electron microscopy (50 μm) of sugar cane roots (variety RB96-6928) cultivated in the presence of control solution (A), (S)-N-(3-oxo-octanoyl)homoserine lactone (0.5 mg/L, B), and its R enantiomer (0.5 mg/L, C).

There are a limited number of studies on the effect of the R enantiomer of AHL in plants. The results in Figure 3C suggest that this enantiomer has also physiological effects in sugar cane, similar to the S enantiomer, in spite of the nonsignificant statistical differences (Dunnett’s test) observed in root dry weight (Figure 2A) and root length (Figure 2B) of sugar cane C



Article

Figure 4. Effect of (R)-N-(3-oxo-octanoyl)homoserine lactone at different concentrations on sugar cane (variety RB96-6928) root growth. (A) Root dry weight. (B) Root length. Means significantly higher than the control (Dunnett’s test, p ≤ 0.05) are marked *.

(RB variety) treated with the R enantiomer. Thus, to better understand the effects of the R enantiomer on plant roots, different concentrations of the R enantiomer (0.1, 0.5, 1.0, and 5.0 mg/L, Figure 4) were tested with the SP80-3280 sugar cane variety. In this experiment, it was observed that at low concentrations (0.1 and 0.5 mg/L) the R enantiomer stimulated root growth as measured by an increase in both dry mass (47.2% and 97.6%, respectively, Figure 4A) and length (44.6% and 66.5%, respectively, Figure 4B). However, higher concentrations of the R enantiomer (5.0 mg/L) suppressed plant development, with a reduction in the mass (−43.6%) and length (−38.9%) of roots compared with the control. The hoods of rootlets from both treatments were analyzed by scanning electron microscopy (SEM), and at a concentration of 5.0 mg/L, plant tissues and cells showed annatto-morphological abnormalities (Figure 5D) compared with the experiment at 0.1 mg/L (Figure 5B), where the cells showed only elongation compared with the control (Figure 5A). The results for the R enantiomer in sugar cane roots were consistent with those reported for the S enantiomer in A. thaliana reported in the literature, which showed stimulatory activity of root growth at low concentrations and inhibition at high concentrations.20 These results, together with SEM analyses (Figure 3C), showed that both enantiomers stimulated cell elongation. This led to the conclusion that both enantiomers were able to modulate the growth of roots in sugar cane. Furthermore, the fact that the R and S enantiomers have different biological effects at the same concentration suggests that differences may be due to different affinities of the enantiomers for enzymes related to plant development, in particular the FAAH-catalyzed hydrolysis reaction and the detection of the products by regulatory proteins. Although the mechanism of action is connected to the hydrolysis of homoserine, the acyl side chain may play an important role in the transport of these molecules through cell membranes. The transport mechanism involving AHL in plant cells is largely unknown. Herein, it was shown that natural product research coupled to organic synthesis and bioassays may be an important tool to understand the presence and action of AHL in plants. The results may have several applications. One of the major objectives is to accelerate plant growth and increase nutrient levels, both in the planting/rooting/budding phase and during normal development. The development of compounds with the capacity to modulate plant growth, especially during early

Figure 5. Scanning electron microscopy (50 μm) of the hoods of rootlets (variety SP80-3280) cultivated in the presence of control solution (A) and 0.1 (B), 0.5 (C), and 5.0 mg/L (D) of (R)-N-(3-oxooctanoyl)homoserine lactone.

meristem development, is important to optimize crop yields. It may be especially important for modulating time for rooting and sprouting, increasing crop uniformity, increasing viable roots, and reducing susceptibility of planting buds to pathogens. AHLs are emerging as compounds that may help to achieve these goals, and it is believed that they will have commercial applications in the future. However, more studies are needed to better understand the mechanism of action of AHLs in plants, including the effects of these compounds on long-term plant development and sucrose production.

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EXPERIMENTAL SECTION

General Experimental Procedures. The optical rotations were measured in EtOAc on a PerkinElmer polarimeter 343 model at 20 °C and 589 nm, with an optical path cell of 10 mm. NMR spectra were acquired on Bruker spectrometers, models Avance III HD 300 and 500, operating at 300.06 and 500.00 MHz for 1H and 75.50 and 125.50 MHz for 13C. Chemical shifts are reported in ppm with reference to internal TMS (δ = 0.0 ppm). CDCl3 and methanol-d4 were used (Aldrich) in the NMR analyses. Gas chromatography coupled to mass D



Article

8′), 1.29 (4H, m, H-6′ and H-7′), 1.59 (2H, m, H-5′), 2.24 (1H, m, H4a), 2.72 (1H, m, H-4b), 2.53 (2H, t, J 6.0 Hz, H-4′), 3.47 (2H, s, H2′), 4.47 (1H, ddd, J 10.8, 9.3, 6.6 Hz, H-5), 4.28 (1H, ddd, J 9.0 and 1.8 Hz, H-5), 4.60 (1H, dd, J 9.3 and 10.8 Hz, H-3); 13C NMR (75.4 MHz, CDCl3) δ 206.4 (C-3′), 177.2 (C-2), 169.4 (C-1′), 67.2 (C-5), 49.2 (C-3), 48.2 (C-2′), 43.6 (C-4′), 32.3 (C-6′), 29.6 (C-4), 24.1 (C7′), 23.2 (C-5′), 14.3 (C-8′); EIMS (70 eV) m/z 224.1 (36), 143.1 (32), 100 (12), 56 (100). (R)-N-(3-Oxo-octanoyl)homoserine lactone: [α]20D +14 (c 1.0, EtOAc); 1H NMR (CDCl3, 300.06 MHz) δ 0.88 (3H, t, J 6.0 Hz, H8′), 1.28 (4H, m, H-6′ and H-7′), 1.57 (2H, m, H-5′), 2.25 (1H, m, H4a), 2.72 (1H, m, H-4b), 2.52 (2H, t, J 6.0 Hz, H-4′), 3.46 (2H, s, H2′), 4.46 (1H, ddd, J 10.8, 9.3, 6.6 Hz, H-5), 4.28 (1H, ddd, J 9.0 and 1.8 Hz, H-5), 4.61 (1H, dd, J 9.3 and 10.8 Hz, H-3); 13C NMR (75.4 MHz, CDCl3) δ 206.7 (C-3′), 175.2 (C-2), 166.4 (C-1′), 66.1 (C-5), 49.2 (C-3), 48.5 (C-2′), 43.9 (C-4′), 31.3 (C-6′), 29.8 (C-4), 22.5 (C7′), 23.2 (C-5′), 14.1 (C-8′); EIMS (70 eV) m/z 224.1 (16), 143.1 (14), 99 (19), 42 (100). Sugar Cane Growth Regulatory Activity Bioassay. The bioassay to measure the growth regulatory activity of the synthesized AHL was done with sugar cane SP80-3280 variety (obtained from the State University of Maringá) and RB96-6928 variety (courtesy of the Santa Terezinha Sugar Cane Mill located in the city of Maringá, Brazil). For the SP80-3280 variety, the R enantiomer was evaluated at concentrations of 0.1, 0.5, 1.0, and 5.0 mg/L. Both the S and R enantiomers were tested at a concentration of 0.5 mg/L for variety RB96-6928. Sugar cane culms (n = 6) approximately 3.0 cm diameter and 5.0 cm in length were sterilized with 70% EtOH and submerged for 30 min in control solution (100 μL of DMSO/1000 mL of H2O) or control solution containing AHL at different concentrations. The culms were incubated in vermiculite and maintained in a growth chamber at 30 °C for 8 days with a photoperiod cycle of 12:12 h light/dark. Culms were irrigated every other day with control solution or the solution containing AHL. After the incubation period, the lengths and masses of the buds and roots were estimated after drying in an oven at 80 °C. All calculated parameters (masses and lengths) were divided by the diameter of the culms. The one-way variance analysis to test the significance of the observed differences was carried out with the Prism package (version 3.0, GraphPad Software) using Dunnett’s test, and p values ≤ 0.05 were considered statistically significant. Scanning Electron Microscopy of Roots. Small sections of roots (5 mm) were fixed in Eppendorf tubes with Karnovsky solution (2.5% glutaraldehyde and 2.0% paraformaldehyde in 0.05 M cacodylate buffer, pH 7.2). The samples were dehydrated using propanone (70%, 90%, and 100%) to the critical point temperature of 9 °C and 55 bar of CO2. After drying, the samples were metalized using high-purity gold and then analyzed in a scanning electron microscope.

spectrometry analyses were performed in a Focus GC (ThermoFinnigan) gas chromatograph coupled to a DSQ II (ThermoFinnigan) mass selective detector operating with 70 eV electron impact, fitted with a quadrupole analyzer and an FID electron impact detector. Helium (99.999%) was used as carrier gas at a column flow of 1 mL/min. The analyses were performed with the injector operating at 250 °C in splitless injection mode. The capillary column used was DB-5 (30 m × 0.25 mm × 0.25 μm) (5% phenyl, 95% methylpolysiloxane), and the oven temperature program was from 100 to 290 °C at 10 °C/min. Samples were prepared from 1 mg of each compound dissolved in 1 mL of EtOAc (HPLC grade). Column chromatography (CC) was performed using silica gel 60 (70−230 mesh) (Merck or Fluka) and Sephadex-LH 20. For thin-layer chromatography (TLC), either silica gel 60 or 60 GF254 (Merck) was employed with 0.25 mm of stationary phase. The TLC spots were visualized by spraying an HOAc/H2SO4/anisaldehyde/MeOH solution followed by plate heating. SEM analyses were performed on a Shimadzu SS-550 Super Scan microscope. All reagents and standards used in the synthesis and analyses were purchased from Sigma-Aldrich (Milwaukee, WI, USA). Dichloromethane was dried by stirring over anhydrous CaCl2. Isolation of N-(3-Oxo-octanoyl)homoserine Lactone from Sugar Cane Extract. Leaves and culms of Saccharum × of f icinarum were collected in the city of Munhoz de Mello, Paraná, Brazil, from a young (2-month-old) commercial plant, in September 2011. The plant material in natura (4.36 kg) was milled on a knife mill and subjected to exhaustive extraction with EtOAc at room temperature using 40 L of solvent. After evaporation of the solvent under reduced pressure (38 °C), 72.00 g of crude EtOAc extract was obtained. Part of the crude extract (70.00 g) was subjected to filtration on a chromatographic column of silica gel 60 (80 g, ⦶ = 5 cm) with solvents n-hexane, EtOAc, and MeOH, resulting in the n-hexane (7.64 g), EtOAc (33.75 g), and MeOH (7.72 g) fractions. Part of the EtOAc fraction (32.00 g) was subjected to silica gel CC 60 (158.00 g, ⦶ = 4.5 cm) with n-hexane, n-hexane/CH2Cl2, CH2Cl2, CH2Cl2/EtOAc, EtOAc, EtOAc/MeOH, and pure MeOH in increasing polarity. It yielded 548 fractions, which were pooled according to similarity in TLC. The subfractions eluted with CH2Cl2/EtOAc 80:20% and 75:25% were subjected to successive gel filtration using Sephadex LH20 with MeOH to remove chlorophyll and fatty acids. The samples were analyzed by GC-MS. Synthesis of (S)- and (R)-N-(3-Oxo-octanoyl)homoserine Lactone. AHLs were synthesized according to well-established reported protocols.40 N,N-Dicyclohexylcarbodiimide (2.2 mmol), 4(dimethylamino)pyridine (2.1 mmol), and Meldrum’s acid (2.0 mmol) were added to a round-bottom flask containing a CH2Cl2 solution of 2.0 mmol of hexanoic acid. The reaction mixture was sparged with N2 for 10 s, and the round-bottom flask was subsequently sealed. The reaction mixture was stirred at room temperature for 24 h and then filtered to remove the N,N-dicyclohexylurea. The organic layer was evaporated, leaving behind a yellow-colored oil. EtOAc was added, and the mixture was washed with aqueous HCl solution (2 mol/L, 3 × 20 mL) and distilled H2O (3 × 20 mL) and dried over anhydrous MgSO4. After filtration, the organic layer was evaporated under reduced pressure to yield the Meldrum acid derivative, which was utilized in the next synthetic step. Et3N (1.2 mmol) and (R)- or (S)-α-amino-γ-butyrolactone hydrochloride (0.91 mmol) were added to the solution of the Meldrum acid derivative (0.91 mmol) in CH3CN (22.5 mL, HPLC grade). The reaction mixture was kept under reflux for 5 h. The solvent was evaporated under reduced pressure, and the resulting white solid was dissolved in an EtOAc/MeOH solution (20:5 mL). This solution was washed with saturated aqueous NaHCO3 solution (3 × 20 mL), 1 M KHSO4 (3 × 20 mL), and saturated aqueous NaCl (3 × 20 mL). The organic layer was dried over MgSO4 and filtered, and the solvent was evaporated. The crude product was purified by silica gel CC with n-hexane, CH2Cl2, and EtOAc in increasing polarity, yielding the S (60% overall yield) and R (55% overall yield) enantiomers. (S)-N-(3-Oxo-octanoyl)homoserine lactone: [α]20D −10 (c 1.0, EtOAc); 1H NMR (CDCl3, 300.06 MHz) δ 0.88 (3H, t, J 6.0 Hz, H-

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ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jnatprod.5b01075. 1 H and 13C NMR spectra of synthesized compounds; GC-MS data for acyl-homoserine lactone (PDF)

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was supported by the Conselho Nacional de ́ Desenvolvimento Cientifico e Tecnológico (CNPq) and the E



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́ Superior Coordenaçaõ de Aperfeiçoamento de Pessoal de Nivel (CAPES).

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