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Herbicidal and Plant-growth Stimulating Effects of Phenolic Compounds Isolated from Lichens.

1. INTRODUCTION

The current demand for large-scale food production has greatly increased the agricultural use of synthetic pesticides, but considerable efforts have been made to reduce their use, both to diminish their levels in foods and to decrease the environmental impact of agriculture [1].

The search for natural pesticides has gained impetus following the observation of undesirable effects of synthetic herbicides on ecosystems. Plants have chemical defense mechanisms that involve phytotoxins, or allelochemicals--secondarymetabolism compounds that provide protection against other plants, phytophagous insects, and herbivorous predators. This phenomenon is known as allelopathy [2].

Allelopathic agents reported from higher plants include coumarins, flavonoids, alkaloids, tannins, certain quinones, hydroxamic acids, sesquiterpene lactones, and various mono-, sesqui-, di-, and triterpenes, among other compounds, synthesized from either the acetate or the shikimate pathways [3]. Many secondary compounds from plants, microorganisms, and lichens are toxic to insects, microbes, and other organisms. Through the acetate-polymalonate pathway, lichens produce phenolic substances that appear to play anti-herbivory roles [4]. Secondary metabolites of lichens are most likely involved in defense mechanisms against insects and herbivores, parasitism by other fungi, and competition from bryophytes, vascular seedlings, and other lichens [5].

Barbatic, evernic, diffractaic, and 4-Odemethylbarbatic acids are known to inhibit growth in Lactuca sativa seedlings. Acting as PSII-inhibiting herbicides, these compounds interrupt photosynthetic electron transport in isolated chloroplasts. Of these depsides, 4-0-demethylbarbatic acid exhibits the highest activity [6]. Emodin and its analogues are highly active against grasses, causing malformations and bleaching in early seedlings. Analogues of rhodocladonic acid cause root malformations in both dicotyledon and monocotyledon seedlings. (-)Usnic acid indirectly inhibits carotenoid biosynthesis by inhibiting 4-hydroxyphenylpyruvate dioxygenase (HPPD), and the in vitro activity of this acid is superior to that of other synthetic inhibitors of this enzyme currently in use as herbicides [5, 7]. Phenolic compounds deriving from depsides have also been tested as potential herbicides. Orsellinic and p-methyl orsellinic acids and 4-O-methyl derivatives have been shown to inhibit growth in L. sativa seedlings [8]. Other phenolic compounds include those present in the herbicide Letharal[R]--a mixture of 12 phenolic substances, most of them phenol-substituted [9]. The homologous series from methyl to pentyl orsellinate and compounds with ramified chains--namely, isopropyl, sec-butyl, and tert-butyl orsellinates--have been assayed in the germination of L. sativa and A. cepa. None of the orsellinates tested significantly affected the germination of L. sativa, whereas ethyl, n-propyl, n-butyl, iso-propyl, and n-butyl orsellinates significantly influenced A. cepa germination. Also, A. cepa proved more sensitive to these compounds at concentrations of [10.sup.-3], [10.sup.-5], [10.sup.-7], and [10.sup.-9] M [8]. Protocetraric and fumaprotocetraric acids showed herbicide and allelopathic effects on L. sativa seeds [10].

In continuation of our research, this article reports the isolation of diffractaic (1), hypostictic (2), protocetraric (3), salazinic (4), secalonic (5), and usnic (6) acids and atranorin (7) (Figure 1), along with the results of their allelopathic bioassays. Each compound was tested at concentrations of [10.sup.-3], [10.sup.-5], [10.sup.-7], and [10.sup.-9] M on A. cepa cv. Baia periforme.

2. MATERIAL AND METHODS

General procedures

Si-gel (Merck 230-400 mesh) was used for the chromatography column. Nuclear magnetic resonance (NMR) spectroscopy was performed on a Bruker DPX-300 spectrometer using the solvent as an internal reference. Melting points were determined on a Uniscience Melting Point apparatus without corrections. Optical rotation measurements were recorded on a Perkin Elmer 341 polarimeter at 589 nm. Thin-layer chromatography (TLC) was performed on plates pre-coated with silica gel 60 F254 (Merck), and the spots visualized by spraying the plates with a 10% H2SO4 methanol solution, followed by heating. The solvents were purified by distillation.

Lichens

The lichens Parmotrema dilatatum (Vain.) Hale (CGMS 49840), Usnea subcavata Motika (CGMS 49843), Parmotrema cetratum (Ach.) Hale, and Pseudoparmelia sphaerospora (Nyl.) Hale (CGMS 49837) were collected near Piraputanga village, Aquidauana county, Mato Grosso do Sul state, Brazil (20[degrees]27'21.2"S, 55[degrees]29'00.9"W, approx. 200 m in altitude; P. cetratum on rock, P. dilatatum, U. subcavata and P. sphaerospora on corticicolous substrate in open woods). The species were identified by Dr. Mariana Fleig, of the Universidade Federal do Rio Grande do Sul, and Dr. Marcelo P. Marcelli, of the Instituto de Botanica de Sao Paulo and the vouchers were deposited at the Campo Grande Herbarium of the Universidade Federal de Mato Grosso do Sul (CGMS 49840, for P. dilatatum; CGMS 49843, for U. subcavata; CGMS 37950, for P. cetratum; and CGMS 49837, for P. sphaerospora).

Extraction and isolation of compounds

Extraction of atranorin and protocetraric acid (from P. dilatatum), usnic and diffractaic acids (from U. subcavata), secalonic and hypostictic acids (from P. sphaerospora), and salazinic acid (from P. cetratum) were conducted according to Honda et al. [11]. The talli (20.0-40.0 g) were powdered and exhaustively extracted with hexane, followed by acetone, at room temperature. The extracts were concentrated in vacuo. Each hexane extract was fractionated in a silica gel column and eluted with hexane and hexane-ethyl acetate mixtures of increasing polarity to yield atranorin (P. dilatatum and P. cetratum) and usnic and diffractaic acids (U. subcavata) and secalonic acid (P. sphaerospora). From the acetone extracts of P. dilatatum, P. sphaerospora, and P. cetratum, protocetraric, hypostictic, and salazinic acids were isolated, respectively. These compounds were purified with a small volume of acetone in an ice bath, followed by centrifugation. The procedure was repeated until obtaining compounds of >95% purity, as determined by TLC and NMR. The resultant structures were confirmed by analyzing their NMR spectra ([sup.1]H, [sup.13]C, and DEPT 135[degrees]) and comparing these with published data [12-19]. Supplementary Material available: NMR data ([1.sup]H and [sup.13]C) of compounds 1-7.

Bioassays

Commercially available seeds of A. cepa cv. Baia periforme were employed. The germination and growth bioassays were conducted in Petri dishes (6 cm), each containing 50 seeds distributed in a randomized design on a sheet of Whatman paper moistened with 1.0 mL of test solution and Tween 80 (100 pg/mL, 1.5 mL). The plates were placed in a growth chamber and kept at 15 [degrees]C. Four replicates were performed for each concentration [20]. The test solutions at [10.sup.-3] M were prepared using acetone, while those at [10.sup.-5], [10.sup.-7], and [10.sup.-9] M were obtained by dilution. The control tests were conducted under the same conditions, in the absence of compounds. To evaluate seed emergence, readings were taken daily, in accordance with Leather and Einhellig [21]. The experiment was concluded when the germination pattern repeated for three consecutive days. Radicle and coleoptile lengths were measured (10 seeds per dish) three days after germination.

Statistical treatment

Germination and growth assay values were subjected to ANOVA to detect significant differences. Dunnett's test was applied for multiple comparisons of mean length values at the various concentrations in relation to controls. A significance level of 5% was adopted for all statistical tests.

3. RESULTS AND DISCUSSION

Allium cepa cv. Baia periforme (onion, Monocotyledoneae) was selected as the target species for its rapid growth and visible response in bioassays. The results obtained are presented in Table 1.

The compounds exhibited either stimulant or inhibitory effects on germination and on radicle and coleoptile growth, depending on the formulation tested. Seed germination was promoted by diffractaic (1) ([10.sup.-3] and [10.sup.-9] M), hypostictic (2) ([10.sup.-3] M), secalonic (5) ([10.sup.-3] and [10.sup.-5] M), and usnic (6) ([10.sup.-3] and [10.sup.-5] M) acids, but inhibited by protocetraric (3) and salazinic (4) acids and atranorin (7) (Figure 2). Diffractaic (1), hypostictic (2), and secalonic (5) acids significantly promoted radicle growth, depending on concentration.

Coleoptile growth was stimulated by diffractaic (1) and hypostictic (2) acids, but inhibited by protocetraric (3), salazinic (4), secalonic (5), and usnic (6) acids and atranorin (7). Usnic acid (6) at 103M concentration promoted stronger inhibition of two processes investigated, which inhibited radicle and coleoptile growth by 54% and 43%, respectively. This effect may be consequent to the spatial arrangement of its molecule, which possibly influenced its biological activity, and to the high concentration employed, which may have affected secondary molecular sites [22]. According to Lasceve & Gaugain [23], usnic acid induces morphological changes in radicles.

These changes may have resulted from an ability of usnic acid to interfere with a range of physiological processes, among them the permeability of algal membranes to organic substances, without significant modification of ionic permeability [24]. At low concentration (5 x [10.sup.-5] M), usnic acid has been reported to induce stomatal closure, reducing water loss. In field experiments performed in arid environments to test its antitranspiration activity in sunflowers, usnic acid decreased water loss without affecting C[O.sub.2] uptake--a noteworthy effect that suggests the possibility of using this acid on trees to prevent excessive drying [25].

In the present study, allelopathic effects were more evident on growth than on germination, particularly for protocetraric (3) and salazinic (4) acids and atranorin (7). Ferreira & Aquila [26] pointed out that although germination is less sensitive than plantlet growth to the action of allelochemicals, changes in germination and growth patterns may result from effects on membrane permeability, DNA transcription and transduction, action of secondary messengers, respiration, and conformation of enzymes and receptors.

No patterns have been detected for the effects of compounds pertaining to any given chemical class, particularly in the case of protocetraric (3) and salazinic (4) acids. In fact, isolated functional groups in a molecule are not always sufficient to impart it with significant biological activity. Rather, the entire molecular structure may have to be taken into account to explain its higher potential for biological activity [27].

Exposed to protocetraric acid (3), L. sativa seedlings were reported to develop greater leaf areas at all concentrations tested, in addition to demonstrating hypocotyl and root stimulus [10]. Lichen compounds have exhibited different effects, depending on the target species, with usnic acid (6) having more marked effects on onion, while not inhibiting growth in lettuce plantlets, even at high concentrations. Diffractaic acid (1), however, stimulated radicle growth and inhibited hypocotyl length in lettuce, while also promoting development of onion plantlets [6].

The lichen substances assayed can manifest their allelopathic potential on diverse communities, given the evidence that they can be disseminated by lixiviation into the environment, where they accumulate by resisting microbiological activity, penetrating the cell walls of seeds and acting as allelochemicals [8].

The results obtained reveal that these compounds exert allelopathic activities when applied to monocotyledon species, making them good candidates for use as herbicides for weed control.

4. CONCLUSION

Diffractaic (1) and hypostictic (2) acids were found to stimulate plant growth, protocetraric (3) and salazinic (4) acids and atranorin (7) exhibited a herbicidal effect, inhibiting germination of onion seeds and slowing radicle and coleoptile growth--features that suggest their utility as natural herbicides. Usnic acid (6) promoted seed germination and slowed both radicle growth (by 54%) and coleoptile growth (by 43%) when tested at [10.sup.-3] M. These findings invite further studies to elucidate the mode of action of the compounds investigated, including their synthesis in amounts sufficient for field experiments.

5. ACKNOWLEDMENTS

The authors thank Dr. Mariana Fleig and Dr. Marcelo P. Marcelli for identifying the lichen species. Thanks are also given to CNPq, Fundect, and the Universidade Federal de Mato Grosso do Sul for their financial support.

6. REFERENCES AND NOTES

[1] Fomsgaard, I. S. J. Agric. Food Chem. 2006, 54, 987. [CrossRef]

[2] Pinto, A. C.; Silva, D. H. S.; Bolzani, V. S.; Lopes, N. P.; Epifanio, R. A. Quim. Nova 2002, 25, 45. [CrossRef]

[3] Einhellig, F. A. In: Allelopathy - Organisms, Processes and Applications. Iderjit, K.M.M.; Dakshini, F.A. E., eds. ACS Symposium Series, 1993, 582, 1-22.

[4] Nash III, T. H. In: Lichen Biology, 1st. ed. Nash III, T. H., ed. Cambridge: Cambridge University Press, 1996, chapter 1.

[5] Dayan, F. E.; Romagni, J. G. Pesticide Outlook 2001, 12, 229. [CrossRef]

[6] Nishitoba, Y.; Nishimura, H.; Nishiyama, T.; Mizutani, J. Phytochemistry 1987, 26, 318. [CrossRef]

[7] Romagni, J. G.; Meazza, G.; Dhammika, N. N. P.; Dayan, F. E. FEBS Letters 2000, 480, 301. [CrossRef]

[8] Marante, F. J. T.; Castellano, A. G.; Rosas, F. E.; Aguiar, J. Q.; Barrera, J. B. J. Chem. Ecol. 2003, 29, 2049. [CrossRef]

[9] Peres, M. T. L. P.; Mapeli, A. M.; Faccenda, O; Gomes, A. T.; Honda, N. K. Braz. Arch. Biol. Technol. 2009, 52, 1019. [CrossRef]

[10] Tigre, R. C.; Silva, N. H.; Santos, M. G.; Honda, N. K.; Falcao, E. P. S.; Pereira, E. C. Ecotox. Environ. Safe. 2012, 84, 125. [CrossRef]

[11] Honda, N. K.; Pavan, F.R.; Coelho, R. G.; Leite, A. S. R.; Micheletti, A. C.; Lopes, T. I. B.; Misutsu, M. Y.; Beatriz, A.; Brum, R. L.; Leite, C. O. F. Phytomedicine 2010, 17, 328. [CrossRef]

[12] Bayir, Y.; Odabasoglu, F.; Cakir, A.; Aslan, A.; Suleyman, H.; Halici, M.; Kazaz, C. Phytomedicine 2006, 13, 584. [CrossRef]

[13] Carvalho, A. E.; Barison, A.; Honda, N. K.; Ferreira, A. G. ; Maia, G. J. Electroanal. Chem. 2004, 572, 1. [CrossRef]

[14] Sundholm, E. G.; Huneck, S. Chem. Scripta 1981, 18, 233.

[15] Huneck, S.; Yoshimura, I. Identification of Lichen Substances, Berlin, Springer, 1996.

[16] Eifler-Lima, V. L.; Sperry, A.; Simbandhit, S.; Boustie, J.; Tomasi, S.; Shenkel, E. Magn. Res. Chem. 2000, 38, 472. [CrossRef]

[17] Yosioka, I.; Yamauchi, H.; Murata, K.; Kitagawa, I. Chem. Pharm. Bull. 1972, 20, 1082. [CrossRef]

[18] Honda, N. K. Liquens de Mato Grosso do Sul - Estudo Quimico e Avaliacao da Atividade Biologica. [Doctoral dissertation]. Araraquara, Brazil: Departamento de Quimica Organica, Instituto de Quimica, Universidade Estadual Paulista - UNESP, 1997. [link]

[19] Konig, G. M.; Wright, A. D. Phytochem. Anal. 1999, 10, 279. [CrossRef]

[20] Brasil. Ministerio da agricultura. Regras para a analise de sementes. 1992, 365 p.

[21] Leather, G. R.; Einhellig, F. A. In: The Science of Allelopathy. Putnam, A.R.; Tang, C.S., eds. New York, John Wiley and Sons, 1986, p 133-146.

[22] Duke, S. O.; Romagni, J. G.; Dayan, F. E. Crop Protection 2000, 19, 583. [CrossRef]

[23] Lasceve, G.; Gaugain, F. J. Plant Physiol. 1990, 136, 723. [CrossRef]

[24] Vainshtein, E. A. Fiziol. Rast. (Moscow) 1985, 32, 1153.

[25] Carbonnier, J. In: Recherches et applications dans le domaine des antitranspirants stomatiques. Carbonnier, J.; Laffray, D., eds. Paris: ,Agence de Cooperation Culturelle et Technique, 1986, p 147-171.

[26] Ferreira, A. G.; Aquila, M. E. A.. Rev. Bras. Fisiol. Veg. 2000, 12, 175.

[27] Barbosa, L. C. A.; Maltha, C. R. A.; Borges, E. E. L. Quim. Nova 2002, 25, 203. [CrossRef]

Marize T. L. Pereira Peres (a), Ana M. Mapeli (b), Odival Faccenda (c), Neli K. Honda (d) *

(a) Laboratory of Natural Pesticides, Universidade Federal de Mato Grosso do Sul, Caixa postal 549, Campo Grande, MS 79070-900, Brazil.

(b) Center for Biological and Health Sciences, Universidade Federal do Oeste da Bahia, Barreiras, BA 47808-021, Brazil.

(c) Department of Computing and Information Sciences, Universidade Estadual de Mato Grosso do Sul, Caixa Postal 351, Dourados, MS 79084-970, Brazil.

(d) Institute of Chemistry, Universidade Federal de Mato Grosso do Sul, Caixa postal 549, Campo Grande, MS 79070-900, Brazil.

Article history: Received: 02 July 2015; revised: 12 August 2015; accepted: 20 August 2015. Available online: 24 September 2015. DOI: http://dx.doi.org/10.17807/orbital.v7i3.756

* Corresponding author. E-mail: nelihonda8@gmail.com

Caption: Figure 1. Structures of the lichen compounds tested on Allium cepa cv. Baia periforme (onion, Monocotyledoneae).

Caption: Figure 2. Effects of the lichen compounds investigated (1-7) on germination of Allium cepa. (*) 1 x [10.sup.-3] M; (*) 1 x [10.sup.-5] M; (*) 1 x [10.sup.-7] M; (*) 1 x [10.sup.-9] M.

Caption: Figure 3. Effects of the lichen compounds investigated (1-7) on growth of Allium cepa seedlings. (*) 1 x [10.sup.-3] M; (*) 1 x [10.sup.-5] M; (*) 1 x [10.sup.-7] M; (*) 1 x [10.sup.-9] M.
Table 1. Germination and growth of Allium cepa seeds treated with
lichen compounds (1-7), compared with untreated controls.

                          Germination (%; mean [+ or -] SD)

                        Control              [10.sup.-3] M

1 Diffractaic     46.3 [+ or -] 0.203   48.3 (*) [+ or -] 0.259
  acid
2 Hypostictic     46.3 [+ or -] 0.203   47.8 (ns) [+ or -] 0.187
  acid
3 Protocetraric   46.8 [+ or -] 0.259   40.3 (*) [+ or -] 0.387
  acid
4 Salazinic       46.8 [+ or -] 0.259   39.3 (*) [+ or -] 0.316
  acid
5 Secalonic       46.3 [+ or -] 0.203   49.0 (*) [+ or -] 0.354
  acid
6 Usnic acid      46.3 [+ or -] 0.203   48.5 (*) [+ or -] 0.338
7 Atranorin       46.8 [+ or -] 0.259   45.8 (ns) [+ or -] 0.287

                           Germination (%; mean [+ or -] SD)

                       [10.sup.-5] M              [10.sup.-7] M

1 Diffractaic     48.0 (ns) [+ or -] 0.172   48.0 (*) [+ or -] 0.295
  acid
2 Hypostictic     46.3 (ns) [+ or -] 0.381   47.0 (ns) [+ or -] 0.323
  acid
3 Protocetraric   43.5 (ns) [+ or -] 0.120   44.3 (ns) [+ or -] 0.502
  acid
4 Salazinic       44.0 (ns) [+ or -] 0.283   44.3 (ns) [+ or -] 0.366
  acid
5 Secalonic       48.8 (*) [+ or -] 0.127    46.8 (ns) [+ or -] 0.131
  acid
6 Usnic acid      49.3 (*) [+ or -] 0.197    47.5 (*) [+ or -] 0.170
7 Atranorin       45.3 (ns) [+ or -] 0.326   44.3 (ns) [+ or -] 0.195

                        Germination               Root length
                   (%; mean [+ or -] SD)     (mm; mean [+ or -] SD)

                       [10.sup.-9] M                Control

1 Diffractaic     48.3 (*) [+ or -] 0.149     6.30 [+ or -] 0.216
  acid
2 Hypostictic     46.8 (ns) [+ or -] 0.209    6.30 [+ or -] 0.216
  acid
3 Protocetraric   44.0 (ns) [+ or -] 0.207    6.20 [+ or -] 0.141
  acid
4 Salazinic       43.3 (ns) [+ or -] 0.199    6.20 [+ or -] 0.141
  acid
5 Secalonic       47.3 (ns) [+ or -] 0.226    6.30 [+ or -] 0.216
  acid
6 Usnic acid      48.0 (ns) [+ or -] 0.124    6.30 [+ or -] 0.216
7 Atranorin       43.5 (ns) [+ or -] 0.175    6.20 [+ or -] 0.141

                          Root length (mm; mean [+ or -] SD)

                       [10.sup.-3] M              [10.sup.-5] M

1 Diffractaic     7.15 (*) [+ or -] 0.208    6.43 (ns) [+ or -] 0.206
  acid
2 Hypostictic     7.08 (*) [+ or -] 0.171    6.63 (ns) [+ or -] 0.222
  acid
3 Protocetraric   5.85 (ns) [+ or -] 0.129   6.33 (ns) [+ or -] 0.171
  acid
4 Salazinic       5.98 (ns) [+ or -] 0.096   6.25 (ns) [+ or -] 0.265
  acid
5 Secalonic       7.18 (*) [+ or -] 0.171    6.88 (*) [+ or -] 0.150
  acid
6 Usnic acid      2.90 (*) [+ or -] 0.141    6.35 (ns) [+ or -] 0.238
7 Atranorin       5.78 (*) [+ or -] 0.206    6.18 (ns) [+ or -] 0.096

                           Root length (mm; mean [+ or -] SD)

                       [10.sup.-7] M              [10.sup.-9] M

1 Diffractaic     6.58 (ns) [+ or -] 0.236   6.63 (ns) [+ or -] 0.126
  acid
2 Hypostictic     6.50 (ns) [+ or -] 0.183   6.48 (ns) [+ or -] 0.126
  acid
3 Protocetraric   6.43 (ns) [+ or -] 0.287   6.55 (ns) [+ or -] 0.208
  acid
4 Salazinic       6.58 (*) [+ or -] 0.222    6.63 (*) [+ or -] 0.126
  acid
5 Secalonic       6.70 (*) [+ or -] 0.183     6.73 (*) [+ or -] 0.96
  acid
6 Usnic acid      6.38 (ns) [+ or -] 0.189   6.28 (ns) [+ or -] 0.150
7 Atranorin       6.43 (ns) [+ or -] 0.189   6.40 (ns) [+ or -] 0.082

                       Coleoptile length (mm; mean [+ or -] SD)

                        Control              [10.sup.-3] M

1 Diffractaic     9.30 [+ or -] 0.231   10.25 (*) [+ or -] 0.129
  acid
2 Hypostictic     9.30 [+ or -] 0.231   9.78 (*) [+ or -] 0.171
  acid
3 Protocetraric   9.38 [+ or -] 0.189   8.78 (*) [+ or -] 0.096
  acid
4 Salazinic       9.38 [+ or -] 0.189   8.75 (*) [+ or -] 0.173
  acid
5 Secalonic       9.30 [+ or -] 0.231   9.20 (ns) [+ or -] 0.183
  acid
6 Usnic acid      9.30 [+ or -] 0.231   5.28 (*) [+ or -] 0.126
7 Atranorin       9.38 [+ or -] 0.189   9.18 (ns) [+ or -] 0.189

                       Coleoptile length (mm; mean [+ or -] SD)

                       [10.sup.-5] M              [10.sup.-7] M

1 Diffractaic     9.28 (ns) [+ or -] 0.222   9.28 (ns) [+ or -] 0.150
  acid
2 Hypostictic     9.08 (ns) [+ or -] 0.150   9.25 (ns) [+ or -] 0.173
  acid
3 Protocetraric   8.88 (*) [+ or -] 0.222    9.28 (ns) [+ or -] 0.096
  acid
4 Salazinic       9.25 (ns) [+ or -] 0.300   9.43 (ns) [+ or -] 0.206
  acid
5 Secalonic       9.05 (ns) [+ or -] 0.191   8.78 (*) [+ or -] 0.189
  acid
6 Usnic acid      9.18 (ns) [+ or -] 0.206   9.15 (ns) [+ or -] 0.129
7 Atranorin       9.38 (ns) [+ or -] 0.189   9.25 (ns) [+ or -] 0.379

                     Coleoptile length
                   (mm; mean [+ or -] SD)

                       [10.sup.-9] M

1 Diffractaic     9.23 (ns) [+ or -] 0.126
  acid
2 Hypostictic     9.38 (ns) [+ or -] 0.096
  acid
3 Protocetraric   9.55 (ns) [+ or -] 0.129
  acid
4 Salazinic       9.53 (ns) [+ or -] 0.150
  acid
5 Secalonic       8.80 (*) [+ or -] 0.141
  acid
6 Usnic acid      8.88 (*) [+ or -] 0.126
7 Atranorin       9.50 (ns) [+ or -] 0.183

(ns) Mean value not significantly different from controls;
* mean values significantly different from controls.
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Title Annotation:Full Paper
Author:Peres, Marize T.L. Pereira; Mapeli, Ana M.; Faccenda, Odival; Honda, Neli K.
Publication:Orbital: The Electronic Journal of Chemistry
Date:Jul 1, 2015
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