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Industrial Crops and Products 31 (2010) 153–157

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Industrial Crops and Products

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iological efficiency of polyphenolic extracts from pecan nuts shell (Caryallinoensis), pomegranate husk (Punica granatum) and creosote bush leavesLarrea tridentata Cov.) against plant pathogenic fungi

duardo Osorioa, Mariano Floresa, Daniel Hernándeza, Janeth Venturab,aúl Rodríguezb, Cristóbal N. Aguilarb,∗

Department of Agricultural Parasitology, Universidad Autónoma Agraria Antonio Narro, Buenavista, 25315, Saltillo, Coahuila, MexicoDepartment of Food Research, School of Chemistry, Universidad Autónoma de Coahuila, 25000, Saltillo, Coahuila, Mexico

r t i c l e i n f o

rticle history:eceived 24 March 2009eceived in revised form9 September 2009ccepted 25 September 2009

a b s t r a c t

Bioactive compounds extracted from plants or agro-industrial residues have great potential as novelfungicide sources for controlling pathogenic fungi. In this study antifungal activity of polyphenolicextracts from Larrea tridentata leaves, Carya illinoensis shells and Punica granatum husk were evaluatedin vitro against eight different plant pathogenic fungi and ten isolates of Fusarium oxysporum. Phenolicsolutions of gallic and ellagic acids were also tested at different concentrations. The polyphenolic extractstested have a high efficiency to inhibit the mycelial growth of Pythium sp., Colletotrichum truncatum, Col-

eywords:arrea tridentata Cov.arya illinoensisunica granatumlant pathogenic fungintifungal activity

letotrichum coccodes, Alternaria alternata, Fusarium verticillioides, Fusarium solani, Fusarium sambucinum,and Rhizoctonia solani. L. tridentata polyphenolic extracts also efficiently inhibited the mycelial growth ofeight out of ten F. oxysporum isolates. These results showed that the polyphenolic extracts tested possessantifungal activities against a broad spectrum of plant pathogenic fungi and could be used as potentialantifungal agents for the control of fungal plant diseases.

© 2009 Elsevier B.V. All rights reserved.

llagic acidallic acid

. Introduction

Phytopathogenic organisms cause a wide spectrum of dis-ases in plants and include fungi, nematodes, bacteria, and virusesMontesinos, 2003). Plant pathogenic fungi cause losses in numer-us economically important crops (Fletcher et al., 2006). Husseint al. (2002) found that most of grains in maize fields were infectedith Fusarium species, and soil can be considered as one of theost important inoculum sources for these species. Pythium sp.,

nd Alternaria alternata are two fungi of worldwide distribution.ankaran et al. (2005) reported that fungus like Ganoderma causesdecrease of production and death of various plants, such as cash

rops and trees in India. Several fungi have been found to induceost-harvest spoilage of fruits and vegetables, which is associatedith decrease in nutritive elements (Ray and Ravi, 2005). Diseases

aused by fungi are also a serious problem in forest management.amping-off of seedlings caused by Rhizoctonia solani were fre-uently observed on many woody perennial plants (Chang, 1997).olletotrichum gloeosporioides causes anthracnose disease of trees

∗ Corresponding author. Tel.: +52 844 416 1238; fax: +52 844 415 9534.E-mail address: cristobal.aguilar@mail.uadec.mx (C.N. Aguilar).

926-6690/$ – see front matter © 2009 Elsevier B.V. All rights reserved.oi:10.1016/j.indcrop.2009.09.017

and results in leaf spots and defoliation (Chang et al., 1997). Treesinfected with Fusarium solani showed root crown rot, dieback andwilt (Fu and Chang, 1999; Demirci and Maden, 2006).

Chemical treatments of infested soils are one of the mainsolutions for plant pathogenic disease control (Montesinos, 2003;Nunes et al., 2001). Synthetic fungicides are helpful to sustain-ing crop production by protecting plants from fungal diseases.However this agronomic practice faces new demands by the con-sumers, particularly for organic and chemically untreated products.In addition, producers and farmers are worried by the resistance ofphytopathogenic microorganisms to fungicides due this is one ofthe critical causes of poor disease control in agriculture (Aguin etal., 2006; Ishii, 2006). There are, therefore, needs to develop alter-native agents for the control of pathogenic fungal diseases in plants(Prabavathy et al., 2006; Chang et al., 2008).

Several studies on the fungi-toxic activities of plant secondarymetabolites have been reported (Muller-Riebau et al., 1995; Ojalaet al., 2000; Kordali et al., 2003; Nunez et al., 2006; Field et al.,

2006; Lee, 2007). Tannin-rich plants of the semiarid regions ofMexico have in most cases a pool of unknown and well-definedphytochemicals with antimicrobial potential to be used againstplant pathogenic fungi. Lira-Saldivar et al. (2003) reported that theextract of Larrea tridentata Cov. was effective against Pythium sp.

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54 E. Osorio et al. / Industrial Cro

entura-Sobrevilla et al. (2006) reported that extracts of Fluorensiaernua, Jatropha dioica, Turnera diffusa and Euphorbia antisyphiliticaere effective against some important fungi including Penicillium

urpurogenum, Fusarium spp., A. alternata, R. solani and Aspergillusavus. The chemical composition of L. tridentata and F. cernua and itsannin composition have been previously reported by our researchroup (Belmares et al., 2009). Also, we have put special atten-ion on the chemical structure and diversity of the tannins andheir biodegradation trying to develop bioprocesses that permit theiotransformation of the tannins present in some plants of semi-rid region of Mexico and produce important phenolic bioactivitiesAguilera-Carbo et al., 2009). In this study we report the antifungalctivity of polyphenolic extracts from creosote bush leaf (L. triden-ata Cov.), pecan nuts shell (Carya Illinoensis) and pomegranate huskPunica granatum) against plant pathogenic fungi.

. Methods

.1. Plant materials

L. tridentata Cov. leaves were collected in the Experimentaltation of The Universidad Autonoma Agraria “Antonio Narro”,uenavista, Saltillo, Coahuila, Mexico during August 2007. Theipening pomegranate fruits used in this study were acquired fromn orchard located in the region of Sabinas, Coahuila, Mexico duringeptember 2007. Pecan nut shells were collected during October007 in a farm located in the region of Parras, Coahuila, Mexico.hells were collected (endocarp) when fruit was ripening and readyo be used as food. Both nut shells and pomegranate husks are con-idered a by-pass product. It its known that polyphenols contentay varies according plant age, season, storage, harvest time andany other factors more. The three vegetal materials were dehy-

rated to 60 ◦C for 48 h. Samples were pulverized to a 30 mesharticle size in an industrial homogenizer (5 l; model LP12 Series00-182, JR Maquinaria para mercado S.A. de C.V., Mexico).

.2. Plant pathogenic fungi

Eight plant pathogenic fungi were selected to be used in theresent study and obtained from International Centre of Phytosan-

tary Services (CISIF) Collection (Saltillo Coahuila, Mexico). Pythiump. (1), Colletotrichum truncatum (2), Colletotrichum coccodes (3),. alternata (4), Fusarium verticillioides (5), F. solani (6), Fusariumambucinum (7) and R. solani (8) which are usual damping-offathogens of plants, causing many leaf and root diseases were used

n this study. Each fungal strain was cultured in potato dextrosegar (PDA, Difco Company) medium. Fusarium strains were iso-ated from samples of infected chili peppers (Capsicum annum L.)arvested in Fresnillo, Zacatecas, Mexico. All fungal strains wereurified by single-spore cultures on potato dextrose agar medium.

.3. Extraction of polyphenols

Extraction of polyphenolic fraction from L. tridentata was fol-owing the method reported previously by Ventura et al. (2008): a

ass of 100 g of dried powder was placed in an Erlenmeyer flaskith 400 mL of 70% acetone. The flask was covered with aluminum

oil to avoid light exposure. This mixture was refluxed at 60 ◦C for2 h. After this process, the sample was filtered using Whatmanlter paper no. 41 and centrifuged at 3500 rpm for 15 min. The sol-ent was removed using a rotary evaporator (Yamato, RE540) using

temperature below 60 ◦C and by avoiding light exposure. Polyphe-olic extract of P. granatum was obtained as follows: a mass of 150 gried powder was placed in an Erlenmeyer flask with 750 mL ofater. The flask was covered with aluminum foil to avoid light

xposure. This mixture was refluxed at 60 ◦C for 12 h. After this

Products 31 (2010) 153–157

process, the sample was filtered using Whatman filter paper no.41 and centrifuged at 3500 rpm for 15 min. For pecan nut shells,the polyphenolic fraction was obtained following the same proto-col reported for L. tridentata leaves changing the solvent by 70%methanol.

2.4. Monomeric phenolics and polyphenolic extractsconcentrations

Aqueous solutions of gallic and ellagic acids (Sigma reagent)were prepared at four concentrations (125, 250, 500 and 1000 ppm)and maintained in black bottles at 4 ◦C until their use in the antifun-gal activity assay. Polyphenolic solutions of extract of L. tridentata,P. granatum and C. illinoensis were prepared at concentrations of0.02, 0.05, 0.10 and 0.20 ppm.

2.5. Conditions of antifungal assay

All micro-assays were evaluated in conventional microplates ofpolystyrene, which were sterilized by autoclaving at 10 pounds per20 min. Each well of the microplate was filled with 200 �L of ster-ile Sabouraud dextrose agar and inoculated with 20 �L of sporessuspension (at a concentration of 2 × 107 fungal spores per mL).After, 20 �L of polyphenolic extracts or monomeric phenolics solu-tion were added. A control treatment (sterile water) was includedin the test. Inoculated microplates were incubated at 30 ◦C dur-ing 24–48 h. Fungal growth was stereoscopically monitored withobservations each 6 h, using a stereoscope Zeiss Olympus SZ30.

2.6. Experimental design and data analysis

A nonparametric one way ANOVA design was used to evalu-ate the effect of each of the factors (the polyphenolic solutions,their concentrations and the fungal strains) on antifungal activ-ity. Five replicates were evaluated in each assay. Experimental unitper replication were 10 plate wells. Fungal growth inhibition wasevaluated as qualitative trait (presence and absence). If the fungusgrew on all plate wells, it was considered 0% of inhibition and soon. Data were ranked as 1 = 0% growth inhibition, 11 = 100% growthinhibition; each group of data was analyzed individually by PROCNPAR1WAY using the software SAS version 6.03. The significancevalue that was used to reject the null hypothesis was p = <0.05.Fungal species were grouped according their sensibility to plantextracts and monophenols (Wilcoxon test). Extracts and monophe-nols were arbitrarily grouping according to their fungicide capacity.

3. Results and discussion

In this study, the antifungal activity of polyphenolic andmonomeric phenolic extracts were tested against well-known phy-topathogenic fungi. Results of biological activity of these extractsagainst eight fungal strains showed that L. tridentata polyphenolicextracts had a strong fungicide effect on the growth of Phytiumsp., C. coccodes, C. truncatum, A. alternata, F. solani and R. solani(Table 1). F. verticilloides was only affected by the fungistatic activityof the extracts. Fungicide activity was considered when no fun-gal growth was observed in the plates and fungistatic activity wasconsidered when fungal growth was delayed. These results areaccording with those reported by Lira-Saldivar et al. (2003), theseauthors mentioned the fungicide activity of extracts of L. tridentataagainst Phytium species. Our results show clearly the L. tridentata

extracts exhibit a biological activity against some Oomycetes andDeuteromycetes.

Pecan nut shell polyphenolic extracts inhibited the growth ofPhytium sp., C. coccodes, C. truncatum, F. sambucinum and R. solani,while a fungistatic effect was evidenced against A. alternata, F. solani

E. Osorio et al. / Industrial Crops and Products 31 (2010) 153–157 155

Table 1Percentages of fungal growth inhibition using different poly- and monomeric phenolic extracts.

Fungal strain Creosote bush(0.70 mg L−1)

Pecan nut shell(0.20 mg L−1)

Pomegranate(0.21 mg L−1)

Gallic acid(1000 mg L−1)

Ellagic acid(1000 mg L−1)

Pythium sp 100a 100 75 50 100Colletotrichum truncatum 100 100 100 100 25Colletotrichum coccodes 100 100 100 50 100Alternaria alternata 100 50 0 0 0Fusarium verticillioides 75 50 25 0 0Fusarium solani 100 75 0 25 75

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Fusarium sambucinum 100 100Rhizoctonia solani 100 100

a % fungal growth inhibition.

nd F. verticilloides (Table 1). There is no reported information abouthe use of pecan nut shell extracts as inhibitor of microbial growth.his study reveals the great biological potential of this residue duets high concentration of polyphenols, mainly of hydrolysable andondensed tannins (Medina, 2007).

Pomegranate husk extracts showed a strong inhibitory effectgainst C. truncatum, C. coccodes and R. solani, but this effect wasot similar on A. alternata and F. solani (Table 1). Also, there is noublished information reporting the fungal activity of the residuesf pomegranate fruits.

In the present study, it was shown that gallic acid inhibited therowth of C. truncatum and acted as fungistatic against A. alter-ata, F. verticilloides and F. sambucinum (Table 1). On the otherand, ellagic acid inhibited the growth of Phytium sp., C. coccodesnd showed a fungistatic activity against F. solani, C. truncatum, F.ambucinum and R. solani.

The analysis of fungal inhibition growth trait (Table 2) with theonparametric one way ANOVA design yield a chi-square value of7.506 with seven degree of freedom (corresponding to a signifi-ance value lower than p = 0.05), therefore it was determined thatnhibition of fungal growth was different among the eight phy-opathogenic fungal species evaluated. In studies like this, it haseen mentioned that differences in fungal growth are influenced byhe fungal specie, concentration and type of bioactive compounds.equida et al. (2002) reported the fungicide activity of several plantxtracts, emphasizing the use of extracts from P. parviflora, D. dis-olor, B. glutinosa and L. tridentata against A. flavus, A. niger, F. poaend F. verticillioides.

To determine the effect of polyphenols and monomeric phe-olics on the fungal growth inhibition, it was needed to run aonparametric one way analysis, which yield a chi-square valuef 34.409 with 4 degree of freedom and a significance value lower

han p = 0.05 (Table 2), showing that the type of extract affect in aifferent way the growth of the different fungal species. In addi-ion, for the determination of the growth inhibition degree due tooncentration of polyphenolic and monomeric phenolic extracts, ahi-square value of 37.130 with 4 degree of freedom and a signif-

able 2ilcoxon test results for parameters considered in the Kruskal–Wallis test for the evalu

henolic extracts.

Fungal strain Mean value Poly- and monomeric phenolic extract

Phytium sp. 79.8 Larrea tridentataC. truncatum 71.6 Carya illinoensisC. coccodes 78.4 Punica granatumA. alternata 124.1 Gallic acidF. verticilloides 149.8 Ellagic acidF. solani 123.9F. sambucinum 116.5R. solani 59.9

ChisQ 57.5 34.41df 7 4Prob > chisQ 0.0001 0.0001

25 0 75100 25 75

icance value lower than p = 0.05 (Table 2) was estimated, showingthat extract concentration affect in a different way the fungalgrowth.

According with the obtained results in the Wilcoxon mean ranks(Table 2) for inhibition of fungal growth, it was possible to group thefungal strains in 4 groups according to their sensibility to growthinhibition: group 1 (highly sensible) was integrated only by R.solani; group 2 (sensible) integrated by Phytium sp., C. truncatumand C. coccodes; group 3 (moderately sensible) integrated by A.alternata, F. solani and F. sambucinum; and the group 4 (slightlysensible) was integrated by F. verticilloides. Table 2 also presentsthe effect provoked by the several polyphenolic and monomericphenolic extracts. In this case, three groups can be integrated,group 1 (strong fungicide) creosote bush, group 2 (potent fungicide)pecan nut shell and ellagic acid, and group 3 (regular fungicide)pomegranate husk and gallic acid.

The chemical composition and the polyphenolic profile of cre-osote bush, the strongest fungicide of this study were reportedpreviously by Trevino-Cueto et al. (2007). This study was carriedout under a very low concentration of polyphenolic and monomericphenolic extracts, for this reason the great potential of biologicalactivity of these plants can be estimated.

In this study, the antifungal effect of these extracts also wastested against 10 different single-spore isolates of Fusarium oxyspo-rum (Table 3). Creosote bush extracts inhibited 8 out of 10 Fusariumevaluated strains, probably due to genetic differences among thefungal isolates (Ventura-Sobrevilla et al., 2006). Pecan nut shellextracts inhibited the 50% of Fusarium strains, and the rest wasaffected by the fungistatic activity. Pomegranate husk extracts onlyexhibited a fungistatic activity against the 10 Fusarium evaluatedstrains. This study demonstrated the selective fungicide activity ofgallic acid against F. oxysporum, because this compound was not

previously tested by its antifungal activity. This selective fungicideactivity of gallic acid was stronger than that showed by ellagic acidsolutions.

The nonparametric one way analysis with four degree offreedom yield significant chi-square values (corresponding to a

ation of the growth inhibition of eight fungal strains using poly- and monomeric

s Mean value Extract concentrations Mean value

73.1 1 80.079.4 2 83.7

116.0 3 96.2135.8 4 95.7

98.2 5 (reference blank) 146.9

037.140.0001

156 E. Osorio et al. / Industrial Crops and Products 31 (2010) 153–157

Table 3Percentages of growth inhibition of ten F. oxysporum strains using different poly- and monomeric phenolic extracts.

Fungal strain Creosote bush(0.70 mg kg−1)

Pecan nut Shell(0.20 mg kg−1)

Pomegranate(0.21 mg kg−1)

Gallic acid(1000 mg kg−1)

Ellagic acid(1000 mg kg−1)

1 100a 100 0 0 502 0 50 0 25 503 100 75 0 0 754 100 100 25 0 05 100 75 50 0 06 100 75 25 0 757 100 100 25 0 758 100 100 25 0 09 100 100 0 0 0

10 75 75 25 0 0

a % fungal growth.

Table 4Wilcoxon test results for parameters considered in the Kruskal–Wallis test for the growth inhibition of ten F. oxysporum strains using poly- and monomeric phenolic extracts.

F. oxysporum strain Mean value Poly- and monomeric phenolic extracts Mean value Extract concentrations Mean value

1 123.4 Creosote bush 86.6 1 97.42 125.7 Pecan nut shell 74.6 2 107.23 113.7 Pomegranate husk 162.5 3 124.04 132.1 Gallic acid 171.7 4 141.45 122.1 Ellagic acid 132.2 5 (reference blank) 157.56 134.17 104.28 118.69 134.410 146.7

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ChisQ 7.6 88.8df 9 4Prob > chisQ 0.0001 0.0001

ignificance value lower than p = 0.05) showed that fungicide activ-ty was seriously affected by the type (chi-square value = 88.8)nd concentration (chi-square value = 27.3) of the extracts testedTable 4). This table shows the mean ranks of Wilcoxon of thenalysis of the fungicide activity against 10 Fusarium strains,emonstrating that pecan nut shells, creosote bush extracts andallic acid solutions are good option in the control of differenttrains of F. oxysporum.

Antifungal activities against plant pathogenic fungi have beenxplored in different sources of phytochemicals with high bioactivectivity, including essential oils and some constituents of Caocedrusacrolepis var, formosana (Chang et al., 2008), lemon, mandarin,

rapefruit and orange (Viuda-Martos et al., 2008), propolis (Koct al., 2007), Aloe vera (Jasso de Rodriguez et al., 2005), and Lar-ea dibaricata, Zuccagnia punctata and Larrea cuneifolia (Quiroga etl., 2001). Extracts of these plants are being characterized to iden-ify the main bioactive compounds with antifungal activity (Cowan,999). Particularly, poly and monomeric phenols exhibit a strongntifungal activity based on the capacity of these compounds toorm complexes with polysaccharides and proteins of external lay-rs of the fungal cells destabilizing the functions of cell walls andembranes, provoking the death of microorganisms (Aguilar et al.,

007).In this work we describe the use of agro-industrial residues as

otential sources of this kind of bioactive compounds, which rep-esent an attractive alternative to produce extracts with an amplepectrum of antifungal activity.

. Conclusions

This study demonstrates the high antifungal capacity of poly-nd monomeric phenolic extracts, particularly of those preparedrom agro-industrial residues (pomegranate husk and pecan nuthell) and creosote bush leaves. Low concentration extracts are

27.940.0001

capable to inhibit a great variety of fungal species. Particularly,pecan nut shell extracts inhibited 80% of the tested F. oxysporumstrains.

Acknowledgement

Authors want to thank the financial support of programCONACYT-CONAFOR-2004-13.

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