Actividad Antifungica de Aceite Eseencial de Limoncillo Contra Patogenos en Poscosecha

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Antifungal activity of lemongrass ( Cympopogon citratus L.) essential oilagainst key postharvest pathogens

Nikos G. Tzortzakis , Costas D. Economakis Department of Hydroponics and Aromatic plants, Institute of Olive Tree and Subtropical Plants, National Agricultural Research Foundation (N.AG.RE.F.),

Agrokipion, 73100, Chania, Greece

Received 24 September 2006; accepted 5 January 2007

Abstract

Lemongrass ( Cympopogon citratus L.) oil (ranging between 25 and 500 ppm) was tested for antifungal activity against Colletotrichumcoccodes , Botrytis cinerea , Cladosporium herbarum , Rhizopus stolonifer and Aspergillus niger in vitro. Oil-enrichment resulted in significant ( P b 0.05) reduction on subsequent colony development for the examined pathogens. Fungal spore production inhibited up to 70% at 25 ppm of lemongrass oil concentration when compared with equivalent plates stored in ambient air. In the highest oil concentration (500 ppm) employed,fungal sporulation was completely retarded. Lemongrass oil reduced spore germination and germ tube length in C. coccodes , B. cinerea ,C. herbarum and R. stolonifer with the effects dependent on oil concentration. However, lemongrass oil (up to 100 ppm) accelerated sporegermination for A. niger . Work is currently focussing on the mechanisms underlying the impacts of essential oil volatiles on disease development with a major contribution to limiting the spread of the pathogen by lowering the spore load in the storage/transit atmospheres as well as the use of essential oil as an alternative food preservative. 2007 Elsevier Ltd. All rights reserved.

Keywords: Antifungal activity; Essential oils; Fungal growth; Lemongrass

Industrial relevance: The present study suggests that the use of pure lemongrass essential oil is an innovative and useful tool as alternative to the use of syntheticfungicides or other sanitation techniques in storage/packaging. Oil enrichment may reduce disease development with a major contribution to limiting the spread of the pathogen by lowering the spore load (spore production) in the storage/transit atmospheres as well as the use of essential oil as an alternative food preservative.The effectiveness (oil concentration) of the oil depends on the target pathogen. The effects of natural compounds on individual microorganisms (fungi and bacteria), both responsible for spoilage and food-borne pathogens, as well as the minimum concentration to gain effectiveness without affecting fresh produce quality andstorage deserve further research.

1. Introduction

The widespread use of pesticides has significant drawbacksincluding increased cost, handling hazards, concern about pesticide residues on food, and threat to human health andenvironment ( Paster & Bullerman, 1988 ). Public awareness of these risks has increased interest in finding safer alternatives protectants to replace synthetic chemical pesticides. One suchalternative is the use of natural plant protectants with pesticidal

activity, as well as they tend to have low mammalian toxicity,less environmental effects and wide public acceptance ( Don-

Pedro, 1996; Hamilton-Kemp et al., 2000; Liu & Ho, 1999;Paranagama, Abeysekera, Abeywickrama, & Nugaliyadd,2003; Paster, Menasherov, Ravid, & Juven, 1995 ).

Essential oils are complex volatile compounds produced indifferent plant parts, which are known to have various functionsin plants including conferring pest and disease resistance(Goubran & Holmes, 1993 ). The complexity in essential oils isdue to terpene hydrocarbons as well as their oxygenatedderivatives, such as alcohols, aldehydes, ketones, acids andesters (Wijesekara, Ratnatunga, & Durbeck, 1997 ).

Lemongrass ( Cympopogon citratus L.) is a plant in the grassfamily that contains 1 to 2% essential oil on a dry basis with

Innovative Food Science and Emerging Technologies 8 (2007) 253 258www.elsevier.com/locate/ifset

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E-mail addresses: [email protected] ,[email protected] (N.G. Tzortzakis).

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widely variation of the chemical composition as a function of genetic diversity, habitat and agronomic treatment of the culture(Carlson, Machado, Spricigo, Periera, & Bolzan, 2001 ). Lemon-

grass essential oil is characterized by a high content of citral(composed of neral and geranial isomers (c. 69%)), which is usedas a rawmaterial for the production of ionone, vitaminA andbeta-carotene ( Paviani, Pergher, & Dariva, 2006 ). Several studiesreported antimicrobial activities (even for human pathogenicfungi) by lemongrass oil ( Appendini & Hotchkiss, 2002;Daferera, Ziogas, & Polissiou, 2003; Hammer, Carson, & Riley,1999; Plotto, Roberts, & Roberts, 2003; Saikia, Khanuja, Kahol,Gurta, & Kumar, 2001; Serrano, Martinez-Romero, Castillo,Guillen, & Valero, 2005 ). Indeed, the lemongrass oil exhibited a broad spectrum of fungitoxicity by inhibiting completely growthof 35, 45, and 47 fungal species at 500, 1000, and 1500 ppm,respectively, and its fungitoxic potency remained unaltered for 210 days of storage, after which it started to decline, withconsiderable interests in the application of lemongrass oil for the preservation of stored food crops ( Mishra & Dubey, 1994 ).Moreover, the essential oil of C. citratus was superior to syntheticfungicides like Agrosan GN, Dithane M-43 and copper oxychloride ( Mishra & Dubey, 1994; Adegoke & Odesola,1996 ). Lemongrass as well as oregano and bay oil inhibited allmicroorganisms examined at 2% (v/v) (Adegoke & Odesola,1996; Hammer et al., 1999 ). Moreover, lemongrass oil wasnonphytotoxic in nature, since it did not exhibit any adverseeffects on germination and seedling growth of wheat and rice(Mishra & Dubey 1994 ). Interestingly, lemongrass oil showed

higher activity than pure isolate (citral) as reported by Saikia et al.(2001) .The aim of this study was to determine the efficacy of

lemongrass oil against postharvest pathogens with emphasis for the possible future use of the essential oil as alternative antimouldcompounds.

2. Material and methods

2.1. Plants and oils constituents

Essential oil derived from lemongrass ( C. citratus L.) wasobtained from the Natural Product Division (Neal's YardRemedies, Manchester, UK). Essential oil extracted by hydro-

distillation and its quality andstabilitywas certified by suppliers.The analysis of the essential oil was performed using a Hewlett Packard 6890 GC, equipped with a HP-5MS (crosslinked 5%PH ME Siloxane) capillary column (30 m, 0.25 mm i.d.,0.25 mm film thickness) and a mass spectrometer 5973 asdetector (Tzortzakis, unpublished data). The carrier gas washelium, by a rate of 1 ml/min. Column temperature was initiallykept for 3 min at 50 C, then gradually increased to 300 C at a4 C/min rate and then held to 300 C for 20 C/min. For GC MS detection an electron ionization system was used withionization energy of 70 eV. Injector and detector (MS transfer line) temperatures were set at 230 C and 310 C, respectively.Diluted samples of 0.1 ml were injected manually and splitless.The relative percentage-concentration of compounds wasobtained by integrating the peak area of the chromatograms(see Table 1 ).

2.2. Inocula

Colletotrichum coccodes , Cladosporium herbarum and Aspergillus niger isolated from tomato fruit ( Lycopersiconesculentum L.) were supplied by DSMZ (Deutsche Sammlungvon Mikroorganismen und Zellekulturen GmbH, Mascheroder Weg, Braunschweig, Germany). Botrytis cinerea and Rhizopus stolonifer isolated from tomato were supplied by CABI (CabiBioscience UK Centre, Bakeham Lane, Egham, England).Isolates were aseptically sub-cultured on standard triple-ventedPetri dishes containing 20 ml of Potato Dextrose Agar (PDA,Oxoid Ltd, Hampshire, UK). Plates were incubated in the dark at 25 C for 1 week and cultures were stored at 4 C for long-term use.

2.3. Impact of lemongrass oil on pathogen development in vitro

Antifungal activity on fungal colony development wasobtained by dilution method (25 ppm, 50 ppm, 100 ppm and500 ppm) of essential oil ( C. citratus ) in the appropriate culturemedia-PDA. The oils were dissolved in 5% Tween 20 and addedto the 20 ml of PDA before solidified into Petri dish. One disc(0.5 cm diameter) of mycelial plug, taken from the edge of four-to-six-day-old fungal cultures, was placed into the Petri dish.Petri dishes were placed in containerswith filter paper moistenedwith water maintaining high relative humidity (RH 90 95%)

during the inoculation period. The containers were thentransferred to storage at 13 C in a cold room and incubatedfor six days for C. coccodes , C. herbarum and A. niger , four days for B. cinerea and three days for R. stolonifer . Controlsconsisted with 5% Tween 20 mixed with PDA and were handledsimilarly with the exception of the volatile treatment. Theefficacy of treatments was evaluated by measuring fungalcolonydevelopment (in cm 2 ).

2.4. Impact of lemongrass oil on fungal spore production and spore germination

Spores from six- to ten-day-old colonies (untilspores formed) of C. coccodes , B. cinerea , C. herbarum , R. stolonifer and A. niger

Table 1Percentage composition (> 1%) of the lemongrass essential oil

Components Retention time (min) Lemongrass oil (%)

Limonene 15.789 4.39Citronellal 20.804 1.32n.i. 21.248 2.16

Borneol 21.248 2.16n.i. 21.902 1.66 Neral 24.055 31.85Geranial 25.120 40.79 Neryl acetate 28.204 2.95Z-caryophyllene 30.011 2.71Identified components (%) 96

n.i.: not identified.

254 N.G. Tzortzakis, C.D. Economakis / Innovative Food Science and Emerging Technologies 8 (2007) 253 258


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previously exposed to lemongrass oil-enrichment (25 ppm,

50 ppm, 100 ppm and 500 ppm) were collected by adding 5 mlof sterile water containing 0.1% (v/v) Tween 80 (for better sporeseparation) to each Petri dish and rubbing the surface with a sterileL-shaped spreader (3 times). The suspension was collected andthen centrifuged at room temperature at 2000 g (Sorvall RC-5BPlus, Dupont, Wilmington, USA) for 5 min. The supernatant wasdiscarded and re-centrifuged until 1 ml of highly concentratedspore solution remained. A haemocytometer slide was used tocount spore production.

Fungistatic or fungicidal effects were examined on sporeviability following oil treatments. Spores from six- to ten-day-oldcolonies of C. coccodes , B. cinerea , C. herbarum , R. stolonifer and A. niger previously exposed to lemongrass oil-enrichment (25 ppm, 50 ppm, 100 ppm and 500 ppm) were collected as

described above. Spore suspension was inoculated on fresh PDA

medium (2 3 mm thick). Plates were exposed to ambient air at 13 C for 24 h and for each of six replicates, 100 spores wereexamined and the extent of spore germination assessed bylooking for the presence of germ tubes. Results were expressedin terms of the percentage of spores germinated. Moreover, germtube length ( m) was also evaluated. All experiments wererepeated twice.

2.5. Statistical analysis

Data were first tested for normality, and then subjected toanalysis of variance (ANOVA). Significant differences betweenmean values were determined using Duncan's Multiple Rangetest ( P = 0.05) following one-way ANOVA. Statistical analyses

Fig. 1. Impacts of lemongrass ( Cympopogon citratus L.) essential oil-enrichment on colony growth (cm 2 ) of Colletotrichum coccodes , Botrytis cinerea , Cladosporiumherbarum , Rhizopus stolonifer and Aspergillus niger raised on PDA. Plates were incubated in controlled environment champers maintained at 13 C and 95% RH.Values represent means ( SE) of measurements made on six independent plates per treatment.



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were performed using SPSS (SPSS Inc., Chicago, USA) andgraph was produced using Prism v.2.0 (Graph Pad Inc., San

Diego, USA).

3. Results and discussion

Culture PDA media with lemongrass oil-enrichment resultedin significant ( P b 0.05) reduction on subsequent colonydevelopment of C. herbarum (up to 18%) at 100 ppm as wellas B. cinerea (up to 33%) and R. stolonifer (up to 16%) at 25 ppm (Fig. 1). Moreover, the highest oil concentrationemployed (500 ppm) revealed complete (100%) inhibition onfungal colony development for all the pathogens per se. Thisconcentration was fungicidal for C. coccodes , C. herbarum , R. stolonifer and A. niger after 10 days inoculation. However, incase of B. cinerea at 500 ppm, fungal colony development initiated after 8 days of inoculation and fungal colony growthinhibited up to 60% following 10 days inoculation (data not presented). Baratta et al. (1998) reported 91% inhibition of thegrowth of A. niger in liquid culture media, when treated with1000 ppm lemongrass oil. Lemongrass oil decreased Fusariumverticillioides growth in PDA by 90 and 100% at 500 and1000 ppm, respectively ( Mishra & Dubey, 1994 ) being inaccordance with the present study. However, Adegoke & Odesola

(1996) reported contrasting results, that F. verticillioides growthwas not affected when lemongrass oil was added in culturemedium. In vitro studies of oregano, thyme, lemongrass, andcilantro vapours (500 1000 ppm) showed complete growthinhibition of B. cinerea and Alternaria arborescens . Geotrichumcandidum was more sensitive to lemongrass oil vapours than tothyme or oregano oils ( Plotto et al., 2003 ). Lemongrass oil wasonly effective at 1000 ppm, whereas no inhibition observed for Rhizopus fungi ( Plotto et al., 2003 ). Indeed, antimicrobial activityand preservative of lemongrass oil are believed to be associatedwith phytochemical components of the lemongrass powder, likealkaloids, tannins and cardiac glycosides ( Adegoke & Odesola,1996 ).

The impact of lemongrass oil-enrichment on fungal sporu-lation in PDA revealed spore production to be significantly( P b 0.05) inhibited when compared with equivalent platesstored in ambient air, with spore production depressed by 70%for B. cinerea , 58% for C. coccodes , 41% for A. niger , 40% for

C. herbarum , and 35% for R. stolonifer at 25 ppm (Table 2 ).Moreover, spore production was completely inhibited at thehighest oil concentration (500 ppm) examined for all of the pathogens. Previous studies reported that the sporulation of Aspergillus flavous was completely inhibited by C. citrates(2800 ppm) when used as fumigant whereas aflatoxin production inhibited at 100 ppm of C. citrates treatments(Paranagama et al., 2003 ).

Table 3 shows the impact of lemongrass oil on sporegermination and germ tube length. ANOVA revealed sporegermination to be significantly ( P b 0.05) reduced by lemongrassoil in C. coccodes , B. cinerea, C. herbarum and R. stolonifer with the impacts of oil dependent on different oil concentrations.The greater inhibition on spore germination was observed in

Table 2Impacts of lemongrass ( Cympopogon citratus L.) essential oil-enrichment onspore production (number of spores10 6 ) by Colletotrichum coccodes , Botrytiscinerea , Cladosporium herbarum , Rhizopus stolonifer and Aspergillus niger raised on PDA

Treatment C. coccodes B. cinerea C. herbarum R. stolonifer A. niger

Control 12.10a

14.28a

79.35a

14.13a

169.50a

25 ppm 5.13 b 4.30 b 47.70 b 9.23 b 99.35 b

50 ppm 2.55 c 5.23 b 45.38 b 8.63 b 62.93 b

100 ppm 1.53 cd 5.75 b 39.88 b 5.00 c 63.13 b

500 ppm 0.00 d 0.00 c 0.00 c 0.00 d 0.00 c

Plates were incubated in controlled environment champers maintained at 13 Cand 95% RH. Values represent means of measurements made on six independent plates per treatment. In each column, values followed by the same letter do not differ significantly at P =0.05 according to Duncan's Range Test.

Table 3Impacts of lemongrass ( Cympopogon citratus L.) essential oil-enrichment onspore germination (%) and germ tube length (in m) in parenthesis of Colletotrichum coccodes , Botrytis cinerea , Cladosporium herbarum , Rhizopus stolonifer and Aspergillus niger raised on PDA and measured after 24 hincubation in controlled environment champers maintained at 13 C and 95%RH

Treatment C. coccodes B. cinerea C. herbarum R. stolonifer A. niger

Control 97 a (146 a ) 100a (211 a ) 60a (31a ) 100a (222 a ) 9c (15 b )25 ppm 95 a (165 a ) 99a (195 a ) 42 b (31a ) 100a (165 c ) 52 b (20ab )50 ppm 72 b (63 b ) 94 b (164 a ) 21c (34a ) 100a (215 ab ) 50 b (26a )100 ppm 73 b (61 b ) 93 b (161 a ) 19c (42a ) 98 b (179 bc ) 71a (24a )500 ppm 0 c (0c ) 0c (0 b ) 0d (0 b ) 0c (0d ) 0c (0c )

Values represent means of measurements made on six independent plates per

treatment. In each column, values followed by the same letter do not differ significantly at P =0.05 according to Duncan's Range Test.

Fig. 2. Illustration (400 magnification) of (A) control and (B) lemongrass(Cympopogon citratus L.) essential oil-enrichment (100 ppm) on germ tubelength of Botrytis cinerea , raised on PDA and measured after 24 h incubation incontrolled environment champers maintained at 13 C and 95% RH.



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C. herbarum (81%) and the least in R. stolonifer (2%). However,lemongrass oil (up to 100 ppm) accelerated spore germinationfor A. niger . Indeed, the greatest oil concentration (500 ppm)inhibited spore germination due to failure of spore production.Lemongrass oil-enriched PDA reduced germ tube length for C. coccodes , whereas no major differences were observed for B. cinerea , C. herbarum and R. stolonifer (see Table 3 and Fig. 2for B. cinerea ). Increased spore germination accelerated byincreased lemongrass oil concentration resulted in increasedgerm tube length for A. niger . However, oil treatments revealedno differences on fungal spore viability among the treatmentswhen five essential oils (lemongrass, cinnamon, rosemary,lavender and basil) were tested for antifungal activity against green mould ( P. digitatum ) implying that effects were fungistatic(Tzortzakis, unpublished data) being in accordance with the previous studies ( Alzoreky & Nakahara, 2003; Mishra & Dubey,1994 ). Moreover, it was reported that lemongrass oil has not demonstrated fungicidal activity against P. digitatum and

P. italicum when applied as a fumigant ( Goubran & Holmes,1997 ) contrasting the present results when examined in different pathogens probably due to variation of the treatment and/or pathogen per se.

This study indicated that essential oils may possess antifungalactivity and can be exploited as an ideal treatment for future plant disease management programs eliminating fungal spread.Recently, there has been a considerable interest in extracts andessential oils fromaromatic plants with antimicrobial activities for controlling pathogens and/or toxin producing microorganisms infoods (Reddy, Angers, Gosselin, & Arul, 1998; Soliman &Badeaa, 2002; Valero & Salmeron, 2003 ). Essential oils arenatural products extracted from vegetal materials, which becauseof their antibacterial, antifungal, antioxidant and anti-carcinogen-ic properties can be used as natural additives in many foods(Teissedre& Waterhouse, 2000 ). In general,the levels of essentialoils and their compounds necessary to inhibit microbial growthare higher in foods than in culture media. This is due tointeractions between phenolic compounds and the food matrix( Nuchas & Tassou, 2000 ) and should be considered for commercial applications. Treatment with basil oil controlledcrown rot and anthracnose prolonging storage of bananas(Anthony, Abeywickrama, & Wijeratnam, 2003 ) as well ascinnamon and eucalyptus oil-enrichment reduced fruit decay andimproved fruit quality of tomato and strawberries ( Tzortzakis, in

press). However, phytotoxicity on the fresh commodity is also to be considered while lemongrass emulsions were more damagingto the tomato tissue than thyme or oregano essential oils ( Plottoet al., 2003 ). Suppression on spore production by oil treatment could make a major contribution to limiting the spread of the pathogen by lowering the spore load in the storage atmosphereandon surfaces. The mechanism underlying theaction of essentialoil-enrichmenton the switch between vegetative and reproductive phases of fungal development remains to be understood. Theimpacts of oils on sporulation may reflect effects of the volatilesemitted by oils on surface mycelial development (and thus the platform to support spore production) and/or the perception/ transduction of signals involved in the switch from vegetative toreproductive development.

Acknowledgement

We thank Dr. Paul Donohoe and colleagues, EnvironmentalMass Spectrometry Unit, Newcastle University, UK, for their respective technical inputs on oil analysis.

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Actividad Antifungica de Aceite Eseencial de Limoncillo Contra Patogenos en Poscosecha

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