Polyphenol–Aluminum Complex Formation: Implications for Aluminum

Mar 29, 2016 - Natural polyphenols may play an important role in aluminum detoxification in some plants. We examined the interaction between Al3+ and ...
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Polyphenol−Aluminum Complex Formation: Implications for Aluminum Tolerance in Plants Liangliang Zhang,† Ruiqiang Liu,‡,§ Benjamin W. Gung,‡ Steven Tindall,‡ Javier M. Gonzalez,∥ Jonathan J. Halvorson,⊥ and Ann E. Hagerman*,‡ †

Institute of Chemical Industry of Forest Products, Chinese Academy of Forestry, Nanjing 210042, China Department of Chemistry and Biochemistry, Miami University, Oxford, Ohio 45056, United States ∥ National Soil Erosion Research Laboratory, USDA-ARS, West Lafayette, Indiana 47907, United States ⊥ Northern Great Plains Research Laboratory, USDA-ARS, Mandan, North Dakota 58554, United States ‡

S Supporting Information *

ABSTRACT: Natural polyphenols may play an important role in aluminum detoxification in some plants. We examined the interaction between Al3+ and the purified high molecular weight polyphenols pentagalloyl glucose (940 Da) and oenothein B (1568 Da), and the related compound methyl gallate (184 Da) at pH 4 and 6. We used spectrophotometric titration and chemometric modeling to determine stability constants and stoichiometries for the aluminum−phenol (AlL) complexes. The structures and spectral features of aluminum−methyl gallate complexes were evaluated with quantum chemical calculations. The high molecular weight polyphenols formed Al3L2 complexes with conditional stability constants (β) ∼ 1 × 1023 at pH 6 and AlL complexes with β ∼ 1 × 105 at pH 4. Methyl gallate formed AlL complexes with β = 1 × 106 at pH 6 but did not complex aluminum at pH 4. At intermediate metal-to-polyphenol ratios, high molecular weight polyphenols formed insoluble Al complexes but methyl gallate complexes were soluble. The high molecular weight polyphenols have high affinities and solubility features that are favorable for a role in aluminum detoxification in the environment. KEYWORDS: polyphenols, pentagalloyl glucose, oenothein B, methyl gallate, aluminum detoxification, Gaussian

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INTRODUCTION Aluminum in solution can be detrimental to crop yields because the metal inhibits root growth and function.1 As much as 40− 50% of potentially arable land in the world is acidic, with acidity particularly common in tropical regions.2 While a few food and commodity crops such as tea (Camellia sinensis), cassava (Manihot esculenta), and rubber (Hevea brasilensis) are successfully grown on acid soils, most grain and legume crops cannot be cultivated on acid soils in part because of aluminum toxicity.3 Aluminum-resistant plants employ exclusion and/or tolerance mechanisms that are centralized in the aluminumsensitive root tip region.1,4 Exclusion is the secretion of chelating agents to prevent aluminum uptake. For example, the organic carboxylic acids citrate, malate, and oxalate are secreted by the roots of aluminum-resistant cultivars of wheat (Triticum spp.), corn (Zea mays), and other crops.3 Tolerance is the production of chelating agents to fix aluminum in the cell wall, or to complex the metal in a nonreactive form in the symplast or vacuole. Tolerance has been reported for some aluminumresistant cultivars of rice (Oryza spp.), and aluminumaccumulating plants such as Hydrangea.1 Polyphenols have long been identified as potential aluminum-chelating agents based on their high affinity for aluminum and their widespread occurrence in plants.5 For example, flavonoids that are secreted into the rhizosphere may serve as chelating agents in exclusion mechanisms.6 Catechin and rutin are found in the root exudates of Rumex acetosa, an aluminum-resistant plant.7 There is also some evidence for polyphenol contribution to tolerance mechanisms. For © XXXX American Chemical Society

example, in woody plants, small phenolics including quercetin, catechin, and chlorogenic acid are not found in root exudates but remain in the roots as potential aluminum-detoxifying agents.8 Although most studies have focused on lower molecular weight phenols and polyphenols, a few studies have explored the higher molecular weight polyphenols known as tannins. For example the flavan-3-ol derivatives known as proanthocyanidins (condensed tannins) have been identified as aluminumdetoxifying agents in plants such as camphor tree (Cinnamomum camphora)9 or Lotus pedunculatus.10 Exogenously added tannic acid protected wheat seedlings from aluminum toxicity.11 It was recently noted that while some Eucalyptus species use aliphatic organic acids as chelators to achieve aluminum resistance,12 Eucalyptus camaldulensis uses oenothein B, a high molecular weight gallate-derived polyphenol, to sequester and precipitate aluminum in the vacuole.13 This is a novel example of a physiological function for an ellagitannin that is particularly interesting because it opens new opportunities to understand and perhaps manipulate aluminum resistance in plants. Our study was designed to add new information about the chemical characteristics of oenothein B and its aluminum complexes. Oenothein B (OeB) is a product of gallic acid metabolism that is derived from the core metabolite PGG.14,15 It is not clear Received: January 21, 2016 Revised: March 22, 2016 Accepted: March 29, 2016

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Figure 1. Structural formulas for the compounds used in this study: (a) methyl gallate (MeG) (with numbering used for the computational methods), (b) quinone form of MeG, (c) the optimal Al−MeG complex based on the computational methods, (d) pentagalloyl glucose (PGG), and (e) oenothein B (OeB). room temperature (22 °C). The stock polyphenol was diluted to 10 μM with dilute hydrochloric acid solution in a 1 cm quartz cuvette and titrated with 5 μL increments of 10 mM of NaOH solution. The UV− visible spectrum from 220 to 500 nm (±0.5 nm) was recorded after each addition with an Agilent 8453 UV−visible spectrophotometer controlled by ChemStation Software (ChemStation Rev. A. 08.03). The pH was recorded with a MettlerToledo pH meter after each step of the titration, which was carried out until the mixture reached pH 11. Titrations with Al3+. The pH of each titration was controlled at pH 4 or pH 6 with 50 mM acetate buffer, which has limited tendency to form aluminum complexes in acidic aqueous solution.19 The stock solution of polyphenol was diluted to 10 μM with buffer in the cuvette, and the baseline UV−visible spectrum was recorded as described above. The sample was titrated with 2 μL additions of the 1 mM AlCl3 solution, mixing by inversion and waiting 2 min for complex formation after each addition. Preliminary experiments established that the products formed within less than 1 min and were stable for at least 30 min. The polyphenols were titrated to a final metal concentration of 30 μM for most experiments, but in some experiments the titration was carried out to 12-fold molar excess aluminum. The pH value at the end of each reaction was checked to ensure that buffering was sufficient to resist pH changes due to deprotonation of the polyphenol and hydrolysis of the metal. All titrations were performed at least three times and data were averaged. RSD for all points was 10 (Table 1, Supplemental Figure 1b). The macroscopic pKa values established by potentiometric titration were 10.3 for PGG and 10.5 for OeB. Oxidative browning associated with quinone formation was not observed for PGG or OeB with titration to pH 11 (Supplemental Figure 1a,b). C

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Figure 3. Spectra of phenols titrated with Al3+ at pH 6. (a) Methyl gallate (MeG) spectra at the indicated Al:MeG ratios. (b) Experimental spectrum obtained with 2-fold excess of Al3+ (blue) and the computed energies of transition for the Gaussian model of the Al:MeG complex (black lines). (c) Pentagalloyl glucose (PGG) spectra obtained with up to 1.5-fold molar excess of Al3+. (d) PGG spectra for Al:PGG molar ratios >1.5. (e) Oenothein B (OeB) spectra at the indicated Al:OeB ratios.

Complexation Reaction with Aluminum at pH 6. Titration with AlCl3 in pH 6 buffered solution yielded characteristic spectral changes for each polyphenol. The products were red-shifted relative to the parent compound, but the shifts were smaller for the aluminum complexes than for the deprotonated forms of the polyphenols (Table 1). For MeG, the transition to the aluminum complex was defined by a single isosbestic point at 285 nm (Figure 3a). We examined the predicted spectra of various aluminum−MeG complexes (Supplemental Table S1) and found that only one of the possible complexes corresponded well to the experimental spectrum (Figure 3b). The optimal structure chelated the metal with the deprotonated hydroxyl groups on C6 and C7 of methyl gallate, and with the remaining groups on the octahedral aluminum filled by water and chloride (Figure 1e).

For PGG, titration with aluminum proceeded through two isosbestic points, one at 298 nm for low aluminum to polyphenol ratios (Figure 3c) and a second one at 292 nm when the Al:PGG ratio exceeded 1.5 (Figure 3d). The aluminum complexes were spectrally distinct, with the species formed at low levels of aluminum red-shifted more than the complex formed at higher levels of aluminum (Table 1, Figure 3c,d). For OeB, titration was accompanied by spectral changes proceeding through a single isosbestic point (287 nm) (Figure 3e) and the product was red-shifted relative to the parent compound (Table 1, Figure 3e). Titration with as much as 12fold molar excess aluminum did not yield new spectra, indicating that the species formed at 3-fold excess aluminum were the fully saturated complexes. The stoichiometric ratios (AlnLm where L is the polyphenolic ligand) were calculated using Job’s method of continuous D

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Figure 4. Data from Job’s method, in which the total concentration of metal plus ligand was maintained at 20 μM at pH 6. The points are the average values from 3 determinations, the blue lines are empirical fits to the equation shown above the plots, and the red line indicates the ratio corresponding to the largest absorbance change. (a) Methyl gallate (MeG) and Al3+. (b) Oenothein B (OeB) and Al3+.

stability constants calculated by chemometric modeling from the data obtained at pH 4 were much smaller than those established at pH 6 (Table 2). Solubility of Complexes. Tahara et al.13 noted that OeB forms insoluble complexes with aluminum at vacuolar pH 4, and speculated that OeB may detoxify aluminum by precipitation in the vacuole. We compared the tendency of MeG, PGG, and OeB to form insoluble complexes with aluminum at pH 4 (Table 3) and found that all three

variation for all conditions except PGG at pH 6, since mixtures containing more than one complex with overlapping spectra cannot be analyzed with simple Job plots.31 The plots indicated that MeG formed a 1:1 complex with Al at pH 6 while OeB formed Al3L2 complexes under these conditions (Figure 4a,b). The spectrophotometric titration data were fit using chemometric methods to elucidate reaction products and estimate conditional stability constants (β) (Table 2). The Table 2. Conditional Stability Constants for Al−Polyphenol Complexes (AlnLm) at pH 6 and pH 4

Table 3. Solubility of Aluminum−Polyphenol Complexesa

log βa methyl gallate

visual precipitation

pentagalloyl glucose

oenothein B

23.01 (0.09)

20.87 (0.02)

Al:L (mole:mole)

methyl gallate

pentagalloyl glucose

oenothein B

0 0.5 1 2 4

no no no no no

no yes yes yes no

no no yes yes no

pH 6 Al + L = AlL 3Al + 2L = Al3L2 2Al + L = Al2L

6.01 (0.03)b

11.22 (0.07)

a

Unbuffered aqueous solutions of the polyphenol (0.5 mM) and metal were mixed to achieve the indicated aluminum to polyphenol (Al:L) ratios, and the pH was adjusted to 4.0 by addition of small amounts of NaOH solution.

pH 4 Al + L = AlL

5.25 (0.01)

4.75 (0.02)

The log β values were established using chemometric modeling of spectrophotometric titration data. bNumbers in parentheses are standard deviations calculated by the modeling software based on the least-squares fit of the spectrophotometric data for at least 15 titration points at 1 nm intervals between 220 and 500 nm. a

compounds were fully soluble at 0.5 mM in aqueous solution at pH 4. MeG was not precipitated by aluminum at any of the tested concentrations, consistent with its tendency not to form complexes at low pH. PGG precipitated when aluminum was added at molar ratios from 0.5 to 2.0. OeB−aluminum complexes were slightly more soluble, forming precipitates at molar ratios ranging from 1.0 to 2.0. Neither polyphenol was precipitated when aluminum was in large excess to the polyphenol (molar ratio ≥4), and the polyphenol−metal complexes were completely soluble at pH values below 4.

results from the Job plots were confirmed with the chemometric software, which gave converged on the 1:1 and 3:2 complexes for MeG and OeB, respectively. The chemometric software was used to establish that PGG formed an Al2L complex at lower metal concentrations and Al3L2 at higher metal concentrations. The chemometric modeling yielded predicted spectra that were consistent with the experimental data (Supplemental Figure 2). Complexation Reaction with Aluminum at pH 4. The spectral changes with addition of Al at pH 4 were very small (Table 1, Supplemental Figure 3a−c). For MeG, complexes with spectrally unique features did not form at pH 4, and the chemometric modeling did not converge on a complex. For PGG and OeB, 1:1 complexes formed based on spectral changes (Table 1, Supplemental Figure 3b,c), Job plots (data not shown), and the chemometric modeling. Conditional

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DISCUSSION We found that the monomeric phenolic compound MeG had an affinity for aluminum similar to other simple o-diphenols.32 The conditional log β values for aluminum−catechol and aluminum−gallic acid complexes at pH 7 are 7.7 and 8.7, respectively.32 Not surprisingly, these values are slightly larger than the log β (pH 6) that we obtained for MeG; because the deprotonated form of the phenol chelates the metal, condiE

DOI: 10.1021/acs.jafc.6b00331 J. Agric. Food Chem. XXXX, XXX, XXX−XXX

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Journal of Agricultural and Food Chemistry tional log β increases with pH until the pH approaches the pKa of the phenolic moiety.33 Quantitative data describing metal− high molecular weight polyphenol complexes have not previously been published. We found that the log β values at pH 6 for the aluminum−high molecular weight polyphenol complexes (PGG and OeB) are much larger than the value for MeG. Conditional log β values and pKa values like those found in Table 2 can be used to estimate log β.34 We estimate log β ∼ 14 for MeG and log β ∼ 50 for the Al3L2 complexes of PGG or OeB. The value for MeG is consistent with values for propyl gallate (log β = 17) and gallic acid (log β = 14).35,36 The values for the high molecular weight polyphenols are quite large and are comparable to the affinities of various oxygen-based siderophores for metals such as Fe3+ or Al3+.37 Thus, our data support a role for chelation by phenols, especially high molecular weight polyphenols, in the environment. We performed molecular modeling of MeG using the TDDFT method to elucidate its acid−base and aluminumcomplexing properties. The same approach has been used to explore interactions between the phenolic compound esculetin and metals including aluminum.21 Comparison of the predicted and actual spectra of fully protonated and various possible deprotonated MeG structures established that the C6 and C7 phenolic groups are deprotonated successively, with oxidation to the quinone causing browning after the second deprotonation. The models of aluminum complexes with MeG showed that the C6 and C7 oxygens serve as the metal ligands in the aluminum complex (Figure 1c). The best spectral predictions were found with the remaining sites on the aluminum filled with water and chloride. Neither Gaussian modeling nor the spectral data gave any evidence for complexes with stoichiometries other than 1:1 for MeG at pH 6. Speciation of aluminum complexes is pH-dependent with a general trend toward formation of multiligand species (AlL2, AlL3) with increasing pH.35 However, for MeG, it has been suggested that 1:1 complexes predominate through pH 7,38 consistent with our observations. The higher molecular weight polyphenols did not converge on a single structure at the B3LYP/6-31G(d) level of theory. Our chemometric modeling at low Al:PGG ratios predicted Al2L complexes, which correspond to the stoichiometry reported for the aluminum complex of quercetin.39 In the quercetin complex there are two types of chelating groups, the diphenol on the flavonoid B ring and a second, weaker site comprising the carbonyl group and 3-hydroxyl of the C ring. For PGG, all of the chelating sites are ortho-diphenolic groups distributed around a roughly spherical PGG molecule,40 consistent with a structure in which aluminum ions reside on opposite sides of the PGG. The Al3L2 species predominated with OeB and with PGG at higher metal levels. To achieve this stoichiometry the aluminum ions must form bridges between the polyphenols similar to the bridged Al2L3 species that was previously identified in a study of aluminum complexes of the simple phenol gallic acid.36 High molecular weight polyphenols have many more potential chelating sites than simple phenols, so more complex stoichiometries are not surprising. We did our experiments at pH 4 and pH 6, which represent the pH range of the cell vacuole12,41 and acidic soils including aluminum-rich soils.42 The aliphatic carboxylic acids that are commonly invoked as aluminum detoxicants, such as citrate and malate, have low pKa values that favor deprotonation and

metal chelation even in acidic soils.3,43 In the absence of metal, phenols are fully protonated at pH 4 to 6, but the literature and our data demonstrate that metals can displace the proton from o-diphenols.35,44 For example, we detected strong complexes between aluminum and all three phenolic ligands at pH 6, and for the two high molecular weight polyphenols at pH 4. Interestingly, the first pKa values for the polyphenols were substantially higher (10.3−10.5) than the first pKa for MeG (8.8). Shifts of up to 2 pH units in pKa values due to microenvironment hydrophobicity and neighboring functional groups have been reported for ionizable functional groups in biomacromolecules.45 The polyphenols had higher pKa values than MeG but surprisingly were more effective aluminumchelating agents at pH 4. The ability of the high molecular weight compounds to bind aluminum at lower pH than the monomer may be due to geometric features (chelate effect) or polarity of the macromolecule that favors complex formation. These factors must allow the aluminum to compete effectively with the high pKa protons of the polyphenol. We hypothesized that aluminum−OeB complexes would have a higher stoichiometric ratio, a higher affinity, and a lower solubility than aluminum complexes of MeG or PGG, providing a rationale for use of the metabolically more costly polymer as an aluminum detoxicant in E. camaldulensis. Our data do show that high molecular weight polyphenols form stronger complexes than the lower molecular weight phenols, with log β values for the polyphenols 2−4 times the log β values for MeG. However, OeB and PGG have similar affinities, making them both good candidates for providing protection from aluminum toxicity, in contrast to our hypothesis. Furthermore, our data do not support the hypothesis that the polyphenols bind more aluminum per galloyl group than simple phenols. Although the molar stoichiometric ratio for polyphenols is larger (Al2L, Al3L2) than the ratio for methyl gallate (AlL), the ratio per galloyl group is much smaller for the polyphenols. For example, PGG has five galloyl groups so the Al2L complex has two aluminum ions per five galloyl groups. In comparison, MeG chelated one aluminum per galloyl group at pH 6. OeB comprises ten galloyl groups and thus has an even smaller stoichiometric ratio on a galloyl group basis. Our hypothesis regarding the solubility of aluminum−phenol complexes was partially supported. At the pH and polyphenol concentrations reported for vacuoles in E. camaldulensis root tissue,12,13 MeG formed soluble complexes, suggesting that low molecular weight phenols are not suitable for sequestering aluminum. However, both PGG and OeB formed insoluble complexes, refuting our hypothesis that OeB is preferentially used as a detoxicant based on solubility of its metal complexes. We have demonstrated that the two polyphenols PGG and OeB have similar potential to detoxify aluminum by forming high affinity complexes that are insoluble at vacuolar pH value. Although PGG binds more aluminum per galloyl group, E. camaldulensis uses the metabolically more costly PGG dimer, OeB, for detoxification. We explored other properties of the high molecular polyphenols in an effort to better understand features that might favor natural selection of one detoxicant over another, and found that polarity was a key distinguishing feature for PGG and OeB. The tolerance mechanism requires the detoxifying compound to be stored in the vacuole. Although the solubility characteristics of the aluminum complexes of PGG and OeB are similar, the compounds themselves have very different solubility profiles. PGG has very low water solubility (Kow = 50) while OeB is quite waterF

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soluble (Kow = 0.5).46 Nonpolar phenolics like PGG are likely to reside in membranes while more polar phenolics like OeB remain soluble and available for functions such as aluminum sequestration.47 We have replaced our original hypotheses with a novel model in which E. camaldulensis accumulates OeB for aluminum detoxification because of the balance between water solubility of the parent compound and insolubility of the aluminum complex. In many plants, protection from aluminum toxicity is achieved by exclusion, with roots exuding organic acids into the rhizosphere, where they chelate Al3+ ions, forming nontoxic compounds that do not enter the root.1 One of the few welldocumented examples of exclusion mechanisms for high molecular weight polyphenols demonstrated that the complex mixture of polyphenols comprising tannic acid protected wheat seedlings from aluminum intoxication.11 Nonpolar polyphenols tend to bind to soil rapidly and very tightly compared to more polar polyphenols,46 and tend to increase cation exchange capacity of soils, presumably by binding to the soil and creating new metal ion binding sites on the soil.48 Thus, we propose that nonpolar polyphenols such as PGG are well suited to serve as exuded detoxicants that ensure that aluminum remains immobilized and soil bound. More polar polyphenols in root exudates may increase metal availability, which could be beneficial for metal nutrients.49 Diversity of polyphenol production by plants is an unexplained aspect of plant metabolism. Plants make diverse polyphenol products by complex pathways that are highly regulated at the genetic and environmental levels,50 but there is no widely accepted rationale for production of these assemblages of molecules. We propose that plants produce a diverse range of polyphenols in order to tune the molecules to specific functions. Previous studies have focused on the biological activities of polyphenols such as metal binding, protein precipitation, or antioxidant potential. We suggest extending comparisons to include polarity and thus solubility of the polyphenols as an essential driver of biological function. Compounds with very similar bioactivities but different polarities should be effective in different cellular or extracellular environments, providing plants with extended abilities to interact with the environment.51 A similar proposal was recently put forward for microbial siderophores, which may be chemically tailored to manipulate water solubility and membrane permeability to exploit different metal-containing environments.52 Our data suggest that it would be useful to more systematically test other plants and their polyphenols as potential chelators/precipitating agents for aluminum and other potentially toxic metals for application via bioengineering or soil amendment. We have done preliminary screening of PGG and several metals and have found that PGG forms strong complexes with Cu2+, Fe3+, and Sn2+. Plants to explore could include members of the Primrose family, a source of diverse ellagitannins including OeB.17 Another likely source of aluminum-chelating polyphenols is tea, which is well-known as an aluminum-accumulating plant that increases synthesis of various polyphenols in response to aluminum-rich soils.53 In these experiments, we focused on polyphenols classified as hydrolyzable tannins, but other classes of polyphenols such as condensed tannins (proanthocyanidins) deserve similar attention.

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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.jafc.6b00331. Table of transition wavelengths and oscillator strengths and UV/vis spectra (PDF)

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. Present Address §

R.L.: School of Environment & Natural Resources, The Ohio State University, Columbus, Ohio 43210. Funding

This work was partially funded by National Natural Science Foundation of China (No. 31500485) and by USDA Specific Cooperative Agreement 58-1932-6-634 to Miami University. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS Dr. Greg Reese, Research Computing Resources, Miami University, Oxford, OH, provided assistance with the analysis of the Job plot data.

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ABBREVIATIONS USED MeG, methyl gallate; OeB, oenothein B; PGG, β-1,2,3,4,6penta-O-galloyl-D-glucopyranose

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REFERENCES

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DOI: 10.1021/acs.jafc.6b00331 J. Agric. Food Chem. XXXX, XXX, XXX−XXX