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Screening of Nasturtium officinale Extracts for


Biological Activities: Implications for Plant Pathogens
a a ab ac
Özlem Darcansoy Iseri , Didem Aksoy Körpe , Feride Iffet Sahin & Mehmet Haberal
a
Institute of Transplantation and Gene Sciences, Baskent University, 06980, Ankara-Turkey
b
Department of Medical Genetics, Faculty of Medicine, Baskent University, 06570, Ankara-
Turkey
c
Department of Surgery, Faculty of Medicine, Baskent University, 06490, Ankara-Turkey
Published online: 04 Mar 2014.

To cite this article: Özlem Darcansoy Iseri, Didem Aksoy Körpe, Feride Iffet Sahin & Mehmet Haberal (2014) Screening
of Nasturtium officinale Extracts for Biological Activities: Implications for Plant Pathogens, Journal of Biologically Active
Products from Nature, 4:1, 19-28, DOI: 10.1080/22311866.2014.886962

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TBAP 4 (1) 2014 pp 19 - 28 19
ISSN Print: 2231-1866
ISSN Online: 2231-1874

Screening of Nasturtium officinale Extracts for


Biological Activities: Implications for Plant Pathogens

Özlem Darcansoy Iseri 1, Didem Aksoy Körpe 1, Feride Iffet Sahin 1,2, Mehmet Haberal 1,3

1
Institute of Transplantation and Gene Sciences, Baskent University, 06980, Ankara-Turkey
Downloaded by [University of Southern Queensland] at 02:18 09 October 2014

2
Department of Medical Genetics, Faculty of Medicine, Baskent University, 06570, Ankara-Turkey
3
Department of Surgery, Faculty of Medicine, Baskent University, 06490, Ankara-Turkey
Received 08 November 2013; accepted in revised form 12 December 2013

Abstract: Nasturtium officinale (Brassicaceae) is a succulent, rhizomatous perennial aquatic weed,


and naturally found in Turkey. The aim of the present study was to screen biological activity of leaf (L), root
(R), and seed extracts (S). Extracts were prepared using methanol (MetOH) and water (dw). Total phenol
contents were; Ldw>LMetOH>SMetOH>RMetOH>Sdw>Rdw. DPPH· scavenging activities were;
Ldw>LMetOH>SMetOH>Rdw>RMetOH>Sdw. Extracts were tested on 11 food-borne and 5 plant-borne strains
for antibacterial activity which were; LMetOH(15/16)>RMetOH(3/16)>L-Rdw (2/16)>SMetOH-dw (1/16).
All strains tested were susceptible to LMetOH (7.6<IZ<12.3 mm) except for the Pseudomonas aeruginosa.
Highest activity was against Klebsiella pneumoniae and Shigella spp. (MIC: 1024 μg.mL-1). Listeria
monocytogenes was also susceptible to RMetOH and Rdw (MIC: 2048 μg.mL-1). LMetOH, RMetOH, and
Rdw had high antibacterial activity against Xanthomonas vesicatoria, with MIC of 256 and 512 μg.mL-1,
respectively. LMetOH was also effective against Pseudomonas tomato and Erwinia caratovora (MIC: 1024
μg.mL-1). Considering eco-safety and effectiveness, antibacterial activities of plant extracts would be important
in phytopathogen control.

Key words: Watercress, food-borne pathogens, phytopathogens, free radical scavenging, phenol
content.

Introduction locally in Black Sea Region especially in salads.


Nasturtium R. Br. (Brassicaceae), a genus of The entire plant is used in home remedies for the
five plant species in the family Brassicaceae treatment of diabetes, bronchitis, asthma,
(cabbage family). Members of the Brassicaceae influenza, used as disinfectant, diuretic, expecto-
are horticultural important crop plants, and highly rant, hypoglycemic, odontalgic, and for digestive
consumed vegetables 1, 2. Brassicaceae is best aids, and is externally applied as a hot compress
known for the edible Nasturtium microphyllum for wound healing 3-6.
and Nasturtium officinale (watercress). Plant-derived compounds comprise diverse
Nasturtium officinale is a succulent, rhizomatous biological activities with different mechanisms
perennial aquatic weed, and naturally found in of actions. Some studied biological activities of
Turkey (1000-2000 m above sea level). In Europe different parts of N. officinale has anti-mitotic,
and USA, it is consumed as a vegetable in salads, anticancer, and antiestrogenic effects 7. Gill et
soups, and other recipes. In Turkey, it is consumed al. 8 reported that watercress supplementation in

*Corresponding author (Özlem Darcansoy Iseri)


E-mail: < odiseri@baskent.edu.tr, oiseri@gmail.com > © 2013, Har Krishan Bhalla & Sons
Özlem Darcansoy Iseri et al., / TBAP 4 (1) 2014 19 - 28 20
diet was shown to reduce lymphocyte DNA Germany), and incubated for 24 h at room
damage and to alter blood antioxidant status in temperature (dark) with continuous shaking. For
healthy adults. In addition, fresh watercress was aqueous extraction, 10 g of dried material was
shown to modulate the SOD and GPX enzymes mixed with 100 mL of distilled water (dw), and
in blood cells in vitro and in vivo 9. Induction of incubated for 1 h at 70°C water bath (dark) with
some detoxification enzymes in hepatocellular continuous shaking. Solutions were filtered
carcinoma cells have also been reported 10. (Whatman No. 40), and the filtrates were
Screening of plants which are used as lyophilized by using a freeze-dryer at -50°C,
traditional remedies increase the chance of 0.50hPa (LyoPro 3000, Thermo Scientific Heto,
finding new bioactive formulations. Ethno- Allerod, Denmark). Dry material was recovered
pharmacological and ethnobotanical studies have in dimethyl sulfoxide (DMSO; Sigma-Aldrich,
suggested that the medicinal plants can have St. Louis, MO, USA) and dw for MetOH and
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considerable antibacterial effect 11, 12, 13. According aqueous extracts, respectively. Extracts were
to the World Health Organization, a medicinal stored at -20°C.
plant is plant which, in one or more of its organs,
contains substance that can be used for Analysis of total phenols (TP) in the extracts
therapeutic purposes, or which are precursors for The Folin-Ciocalteu method was used to assay
chemo-pharmaceutical semi-synthesis. Plant total phenols 15, 16. Two microliters of sample (0.05
species that are currently use for medicinal g.mL-1), 50 μL Folin’s Reagent (Sigma-Aldrich),
purposes are about 20,000. So it is important to and 300 μL 10 % (w/v) sodium carbonate (Sigma-
screen antibacterial potential of different plant Aldrich) were sequentially added to 1 mL assay
species and organs, either in the form of crude mixture, and the mixture was incubated at 40°C
extracts or as components isolated from them. water bath for 30 min. The absorbance was
We have previously, identified high measured at 765 nm, and the amount of total
antibacterial activity of Urtica spp. seed extracts phenols were represented as mg gallic acid
on both food and plant pathogenic bacteria 14. In (Sigma-Aldrich) equivalents (GAE) per g extract
the light of our previous findings, we investigated using gallic acid calibration curve (R2>0.9).
antibacterial effects of leaf (L), root (R) and seed Assays were performed as triplicate experiments.
extracts (S) of Nasturtium officinale in the present
study with particular implications for plant patho- DPPH radical scavenging assay (DRSA)
genic bacteria. Aqueous and methanol extracts Electron donation ability of extracts was
were also evaluated for their total phenol content measured according to decoloration of purple
and free radical scavenging activity. colored free radical solution of DPPH 17. Three
milliliters of serial extract dilutions (3.125-1600
Materials and methods mg.mL-1) were mixed with 1 mL 200 mM MetOH
Plant material and extraction solution of DPPH· (Sigma), vortexed and
Nasturtium officinale was collected from Rize, incubated at room temperature (dark) for 30 min.
Turkey in between July and September (2010). The absorbance was measured at 517 nm.
Voucher specimens were identified by Assoc. Inhibition of DPPH· was calculated as Eq.1:
Prof. Dr. Evren Cabi (Department of Biology,
Namik Kemal University, Tekirdag, Turkey), and DPPH radical scavenging activity (DRSA, %) =
stored as herbarium materials. Plants were also [(Acontrol-Asample) / Acontrol)] × 100 Eq.1
cultured from seeds in the Greenhouse of Institute
of Transplantation and Gene Sciences, Baskent where Acontrol is the absorbance of the control
University (Kazan-Ankara, Turkey). Dry leaves, and Asample is the absorbance of the samples
roots, and seeds were powdered by using a coffee containing extracts and standards. Inhibitory
blender. Powder (10 g) was mixed with 100 mL concentration 50 (IC 50 ) of extracts were
of pure methanol (MetOH; Merck, Darmstadt, calculated from trend lines of DRSA versus
Özlem Darcansoy Iseri et al., / TBAP 4 (1) 2014 19 - 28 21
sample concentration plots (R2>0.9). Butylated Disc-diffusion assay
hydroxytoluene (BHT; Sigma-Aldrich), L- The stock solutions of extracts were diluted to
ascorbic acid (AscA; Sigma-Aldrich), and α- a final concentration of 22.5 mg.mL -1 with
tocopherol (α-Toc; Sigma-Aldrich) were used as distilled water, and filter sterilized by 0.45 μm
controls in the assays. Assays were performed as Millipore filters. Disc-diffusion method 19 was
triplicate experiments. followed by spreading 100 μL of 0.5 McFarland
standard turbid cell suspensions on MH agar. The
Antibacterial activities discs of 6 mm in diameter were impregnated with
Test strains 20 μL of 22.5 mg.mL-1 extract solutions (450 μg
Standard and isolated strains of bacteria used per disc). The DMSO concentrations in the 22.5
to test antibacterial activities of the extracts are mg.mL-1 diluted extract solutions were 18 % (v/
given in Table 1. Bacteria were obtained from v) at most, and below 10 % (v/v) for most of the
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the stock cultures of Department of Medical extracts. So, 20 % (v/v) DMSO was tested as
Microbiology, Faculty of Medicine, Baskent solvent control. Ampicillin (Amp; 10 μg per disc),
University (Ankara, Turkey) and Department of tetracycline (Tet; 30 μg per disc), gentamicin
Plant Protection, Çukurova University (Adana, (Gent; 10 μg per disc), and sulbactam + cefopera-
Turkey). The bacterial stock cultures were zone (Sul+Cef; 50+50 mg per disc) were used as
maintained on Mueller Hinton (MH) (Oxoid CM positive reference standards. The plates were
337, Basingstoke, Hampshire, UK) agar at 4°C. incubated at 37°C for 24 h for food-borne
Before the assay, food-borne and plant-borne bacterial strains, at 27°C for 48 h for plant-borne
strains were grown overnight at 37°C and 48 h at isolates. Antibacterial activity was evaluated by
27°C, respectively in MH broth. measuring the zone of inhibition (IZ) in mm for
Table 1. Bacterial strains tested

Food-borne pathogens Strain

Escherichia coli ATCC 25922


Enterococcus gallinarum CDC-NJ-4
Enterococcus faecalis ATCC 29212
Streptococcus pyogenes ATCC 19615
Staphylococcus aureus ATCC 33591
Listeria monocytogenes ATCC 7644
Pseudomonas aeruginosa ATCC 27853
Klebsiella pneumoniae Clinical isolate, Baskent University Hospitals
Proteus vulgaris Clinical isolate, Baskent University Hospitals
Shigella spp. Clinical isolate, Refik Saydam Hygiene Institute
Bacillus pumilus Zea mays isolate M118
Plant-borne pathogens
Clavibacter michiganensis Erd-Cmm; L. esculentum isolate; Erdemli, Mersin;
subsp. michiganensis Çukurova University, Department of Plant Protection
Pseudomonas tomato Erd-Pst; L. esculentum isolate; Erdemli, Mersin; Çukurova
University, Department of Plant Protection
Xanthomonas vesicotoria Krs-Xav; C. annum isolate; Karaisali, Adana; Çukurova
University, Department of Plant Protection
Erwinia caratovora Khs-Ecc; L. esculentum isolate; Kocahasanli, Mersin;
Çukurova University, Department of Plant Protection
Erwinia amylovara Poz-Ea; P. communis L. isolate Pozantý, Adana; Çukurova
University, Department of Plant Protection
Özlem Darcansoy Iseri et al., / TBAP 4 (1) 2014 19 - 28 22
each strain. All assays were performed in DPPH in methanol solution in the presence of a
quadrates. hydrogen donating antioxidant due to the
formation of the nonradical form DPPH-H which
Micro-well dilution assay is measured spectrophotometrically. LMetOH,
The minimal inhibition concentrations (MIC) Ldw and SMetOH extracts had higher DRSA with
were studied for the extracts and strains which lower IC50 in comparison to other extracts (Table
had 7 mm< IZ according to disc-diffusion assays. 2). IC50 (DRSA) of standards; AscA, BHT, and
Two hundred microliters of 2048 μg.mL-1 extracts α-Toc were 5.9 μg.mL -1 ± 0.3 μg.mL -1, 12.6
in MH broth were dispensed into the 3rd column μg.mL-1 ± 0.5 μg.mL-1, and 5.3 μg.mL-1 ± 0.5
of 96-well plates, and serial 100 μL 2-fold μg.mL-1, respectively.
dilutions were performed to 4 μg.mL-1. First two
columns served as medium and cell controls. Antibacterial activities
Plates were inoculated with 100 μL of cell
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Table 3 demonstrates the disc-diffusion results.


suspension per well containing 5 μL of 0.5 Leaf methanol extract had activity against all
McFarland standard turbid fresh bacterial food-borne pathogens tested except for the P.
cultures. Plates were incubated at previously aeruginosa. Similarly it was effective against 4
mentioned conditions, and optical density was plant-borne pathogens out of 5 strains tested
measured at 600 nm with an ELISA reader (except for the C. michiganensis). Highest
(Biotek Instrument ELx800, VT, USA). The MIC activity was obtained against K. pneumoniae in
was defined as the lowest concentration to inhibit all strains tested. Aqueous leaf extract was effec-
90 % of bacterial growth. MIC was confirmed tive against E. feacalis and S. pyogenes among
by inoculating 5 μL samples from clear wells on all strains tested. Aqueous and methanol extracts
MH agar. of the leaves were effective only against C. michi-
ganensis among all strains tested. L. mono-
Results cytogenes and X. vesicatoria was susceptible to
Total phenol content of the extracts methanol extracts of leaf and root, and aqueous
Total phenols content of the extracts are given extract of root.
in Table 2 in terms of mg gallic acid equivalents DMSO had no effect on the strains tested at its
per g extract. Total phenolic content of extracts solvent concentration. Lowest MICs determined
were Ldw>LMetOH>SMetOH>RMetOH> were 1024 μg.mL -1 for K. pneumoniae and
Sdw>Rdw. Shigella spp. among food-borne pathogens tested
(Table 4). MIC of methanol extracts of leaf and
DPPH radical scavenging activity (DRSA) root, and aqueous extract of root for X. vesivatoria
Free radical scavenging activity (FRSA) of the growth were 256 and 512 μg.mL -1. MICs of
plant extracts have been performed using DPPH methanol leaf extract were 1024 μg.mL-1 for P.
radical. Method is based on the reduction of tomato and E. caratovora.

Table 2. Total phenols (TP) and IC50 of free radical


scavenging activity (DRSA) of the extracts

Extracts Solvent TP(mg GAE/g extract) μg/mL)


IC50 DRSA(μ

Leaf MetOH 51.9 ± 2.3 34.0 ± 0.6


dw 60.9 ± 5.5 27.3 ± 1.2
Seed MetOH 43.7 ± 6.2 62.9 ± 6.0
dw 14.8 ± 1.1 769.0 ± 15.0
Root MetOH 20.2 ± 1.5 628.6 ± 21.9
dw 12.3 ± 1.2 510.3 ± 8.9
Özlem Darcansoy Iseri et al., / TBAP 4 (1) 2014 19 - 28 23
Table 3. Results of disc diffusion assay

N. officinale (IZ; mm) Antibiotics (IZ; mm)


Leaf Seed Root
Food-borne Met dw Met dw dw Met Amp Tet Gent Sul+Cef
(10 μg) (30 μg) (10 μg) (50+50 μg)

E. coli 7.7 - - - - - 18.3 27.5 25.8 34.5


E. gallinarum 8 - - - - - 26.5 11.3 23.5 23.0
E. faecalis 8.3 9.3 - - - - 28.0 17.0 19.3 18.3
S. pyogenes 9.3 7.8 - - - - 25.0 11.5 22.0 21.8
S. aureus 7.8 - - - - - 23.8 13.8 9.5 32.0
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L. monocytogenes 10.5 - - - 10.5 10.5 27.8 31.0 30.0 31.0


P. aeruginosa - - - - - - 18.5 33.5 26.8 28.8
K. pneumoniae 12.3 - - - - - - 17.5 25.8 29.0
P. vulgaris 7.6 - - - - - - 19.0 25.8 31.3
Shigella 9.8 - - - - - 30.0 32.5 29.8 30.8
B. pumilus 9.8 - - - - - 33.0 32.5 32.0 31.5
Plant-borne
C. michiganensis - - 7 7 - - - 65.5 34.9 58.8
P. tomato 10.5 - - - - - - 47.3 38.3 38.0
X. vesicotoria 10.9 - - - 9.5 9.7 9.3 50.5 34.3 43.0
E. caratovora 11.0 - - - - - - 44.3 31.5 30.5
E. amylovara 7.6 - - - - 9.3 15.0 40.3 25.3 40.5

Table 4. Results of micro-well dilution assay

N. officinale (MIC; μg/mL)


Leaf Seed Root Antibiotic
Food-borne Met dw Met dw dw Met (MIC; μg/mL)

E. coli 2048< - - - - - 16 (Amp)


E. gallinarum 2048< - - - - - 32 (Amp)
E. faecalis 2048< 2048< - - - - 16 (Amp)
S. pyogenes 2048< 2048< - - - - 8 (Amp)
S. aureus 2048 - - - - - 16 (Amp)
L. monocytogenes 2048 - - - 2048 2048 <0.125 (Amp)
P. aeruginosa - - - - - - 16 (Sul+Cef)
K. pneumoniae 1024 - - - - - 0.5 (Sul+Cef)
P. vulgaris 2048< - - - - - 0.5 (Sul+Cef)
Shigella spp 1024 - - - - - 0.5 (Amp)
B. pumilus 2048< - - - - - 0.25 (Amp)
Plant-borne
C. michiganensis - - 2048< 2048< - - 2 (Sul+Cef)
P. tomato 1024 - - - - - 8 (Sul+Cef)
X. vesicotoria 256 - - - 512 512 1 (Sul+Cef)
E. caratovora 1024 - - - - - 8 (Sul+Cef)
E. amylovara 2048< - - - - 2048 32 (Sul+Cef)
Özlem Darcansoy Iseri et al., / TBAP 4 (1) 2014 19 - 28 24
Discussion well correlated to DPPH• scavenging activity (R2
Plants are potential sources of natural bioactive = 0.86). DPPH• scavenging activity of the leaf
compounds such as secondary metabolites and extracts were comparable to activity of natural
antioxidants. Bioactive compounds are diverse and synthetic antioxidants, and considerably
in chemical structure. Bioactivity of several higher than the root extracts and aqueous seed
edible plant parts such as fruits, vegetables, extract. The DPPH• scavenging activity of the
flowers, leaves, and roots have been identified plant extracts appears to be depending on the
so far. The secondary metabolites from plants concentration of phenols, and their electron
have been reported to be potent free radical transfer/hydrogen donating ability. To our
scavengers. The formation of free radicals may knowledge, antioxidant activity of the roots and
be inhibited by reducing hydroperoxides and seeds has not been studied so far.
hydrogen peroxide, and by sequestering metal Watercress is an excellent source for
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ions through complexation/chelation reactions. glucosinolates 27. The hydrolysis products of


Radical scavenging action is dependent on both glucosinolates include isothiocyanates, nitriles,
reactivity and concentration of the antioxidant 20. epithionitriles and thiocyanates. The types of
Flavonoids and phenolic acids are the most compounds produced are specific to the
important groups of secondary metabolites and respective glucosinolates present in the tissue 28,
bioactive compounds in plants 21. Phenols are 29
. Glucosinolate hydrolysis products, in parti-
found in all parts of plants such as leaves, fruits, cular, isothiocyanates are effective inhibitors the
seeds, roots and bark 22. Plant polyphenols, a Gram-negative and Gram-positive pathogenic
diverse group of phenolic compounds (such as bacterial growth 30. Antimicrobial activity of
flavonols, anthocyanins, phenol acids) possess an isothiocynates has been related to the inactivation
ideal structural chemistry for free radical of extracellular enzymes through oxidative
scavenging activity. Antioxidative properties of cleavage of disulfide bonds, and the formation
polyphenols arise from their high reactivity as of the reactive thiocyanate radical was proposed
hydrogen or electron donors from the ability of to mediate the antimicrobial effect 31. In addition,
the polyphenol derived radical to stabilize and high antimicrobial effect of phenol compounds
delocalize the unpaired electron (chain-breaking has also been discussed in terms their ability to
function) and from their potential to chelate metal alter microbial cell permeability, membrane
ions (termination of the Fenton reaction) 23. Many function, and interaction with membrane proteins,
studies have shown good positive correlation causing deformation in structure and function-
between antioxidant capacity and total phenol ality, although the exact mechanism of action is
content of spices, medicinal herbs, and other not clear yet 32.
dietary plants 24. Previously, fresh N. officinale Antibacterial activity of extracts were LMetOH
leaves were determined as good sources of (15/16)>RMetOH (3/16)>L and Rdw (2/16)>S
antioxidants, with high content of polyphenol, MetOH and dw (1/16) (Table 3). Higher
derivatives of quercetin and kaempferol, and antibacterial activity of leaf extracts may depend
vitamin C 25. A hundred gram of fresh watercress primarily on the variations in composition of
leaves contained 43 mg of vitamin C, 4700 IU of bioactive molecules of leaves, including phenol
vitamin A, and 34 mg of α-tocopherol 24. The compounds and glucosinolate compounds.
main compounds of the oil of leaves were Higher antibacterial activity of the leaf methanol
myristicin (57.6 %), α-terpinolene (8.9 %), and extract in comparison to aqueous extract, on the
limonene (6.7 %) 26. Water and ethanol extracts other hand, primarily depends on the difference
of watercress leaves were also determined as of bioactive molecules extracted by polar/non-
antioxidants against lipid peroxidation in linoleic polar solvents.
acid, liver, brain and kidney homogenate model Food-borne diseases are one of the major
systems 6. worldwide problems, and prevention of food
In our study, phenol content of the extracts were spoilage, caused by many bacteria such as E. coli,
Özlem Darcansoy Iseri et al., / TBAP 4 (1) 2014 19 - 28 25
Enterobacter spp. Bacillus spp., S. aureus, K. antibacterial activity against these bacteria with
pneumonia, and L. monocytogenes have industrial MIC = 1024 mg.mL-1. Antibacterial activity of
importance 33. Recently, considerable interest has these extracts on plant pathogens are classified
been given to plant extracts for controlling as strong inhibition (X. vesicotoria) and moderate
pathogens, and toxin producing bacteria in foods. inhibition (P. tomato and E. caratovora) based
According to MIC values, Aligiannis et al. 34 have on the classification of Aligiannis et al. 34. Plant
reported a classification of plant extracts; strong originated antibacterial compounds, due to their
inhibition: MIC<500 μg.mL-1, moderate inhi- non-toxic eco-friendly nature, can be an alter-
bition: 600 μg.mL-1<MIC<1500 μg.mL-1, and low native approach to plant disease management.
inhibition: 1600 μg.mL-1<MIC. Potential use of the plant derived extracts may
Concordantly, results obtained with K. be as seed protectants and disinfectants,
pneumonia, Shigella spp., and even L. mono- particularly for the seed-borne and transmitted
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cytogenes seem to be promising, and to our bacterial diseases. According to a study of Kotan
knowledge no such data exist considering N. et al. 40, Satureja spicigera essential oil, carvacrol
officinale and these species so far. Nonetheless, and thymol were more effective than strepto-
n-hexane, ethanol and aqueous leaf extracts of mycin sulfate according to seed disinfection
N. officinale, was shown to exert antibacterial assays conducted with P. tomato, X. vesicotoria
activity against S. aureus, B. subtilis, and P. and C. michiganensis infected tomato and pepper
aeruginosa 35. Interestingly, leaf extract of N. seeds. Interestingly, Balestra et al. 41 performed
officinale was also shown to exhibit anti- in vivo antibacterial tests of A. sativum and F.
mycobacterial activity against the sensitive and carica extracts with P. tomato, X. vesicotoria and
resistant M. tuberculosis (MIC = 100 μg.mL-1) C. michiganensis inoculated tomato plants, and
36
, and seed extracts against M. bovis (MIC = 500 observed disease control at 15 days post-
μg.mL-1) 37. inoculation. In both studies MIC for the extracts
The control of bacterial diseases of crops is a and assay concentrations seem to be higher when
considerable agricultural problem due to the compared to our results. To our knowledge, this
limited availability of bactericidal agents. Use of is the first report demonstrating the antibacterial
antibiotic and copper compounds is very activity of watercress on phytopathogenic
restricted in many countries, for either human and bacteria, and considering low MIC results
animal health or the environment 38. Secondly, obtained with the extracts have potential for
phytopathogenic bacteria spread at long distances further research and application on seed
by contaminated and infected seeds. In addition, disinfection.
resistant populations of E. amylovora, Pseudo- The results presented here enable comparative
monas spp., and Xanthomonas campestris have evaluation of total phenol content, DPPH•
been determined 39. scavenging and antibacterial activity of methanol
X. vesicatoria is the causal agent of bacterial and aqueous N. officinale extracts of leaves, roots
spot disease, and has a wide range of hosts and seeds. Though, studies of chemical content
especially of Solanaceaous plants including analysis are required; this study gives a
tomato and pepper. Disease causes considerable preliminary but comprehensive insight to
crop loss, and persistent on seeds. In our study, bioactive potential of N. officinale. Considering
methanolic leaf extract exerted high antimicrobial limited availability of bactericidal agents in plant
activity against X. vesicatoria with a MIC of 256 disease control, antibacterial activities of plant
μg.mL-1. In addition, both methanol and aqueous extracts are important for development of bio-
extracts of the root had antimicrobial activity organic agriculture practices.
(MIC = 512 μg.mL-1). Other pthytopathogens, P.
tomato and E. caratovora, are the causative Acknowledgements
agents of bacterial soft rot and bacterial speck Authors acknowledge Department of Medical
disease in tomato leaves. Methanol extract had Biochemistry, Faculty of Medicine, Baskent
Özlem Darcansoy Iseri et al., / TBAP 4 (1) 2014 19 - 28 26
University for lyophilization process. Assoc. Prof. Faculty of Medicine, Baskent University. Dr.
Dr. Evren Cabi is greatly acknowledged for Mehlika Benli is also greatly acknowledged for
identification of voucher specimens. Phyto- her contributions. This study was approved by
pathogen strains were generous gift of Prof. Dr. Baskent University Institutional Review Board
Yesim Aysan, and food-borne strains were (Project no: DA10/17), and supported by Baskent
donated by Department of Medical Microbiology, University Research Fund.

References
1. Cartea, M.E., Francisco, M., Soengas, P., Velasco, P. (2011). Phenolic compounds in Brassica
vegetables. Molecules, 16: 251-280.
2. Monteiro, A., Lunn, T. (1999). Trends and perspectives of vegetable brassica breeding world-
wide. World Conference of Horticultural Research, 495: 273-279.
Downloaded by [University of Southern Queensland] at 02:18 09 October 2014

3. Zargari, A. (1987). Medicinal plants Tehran. Tehran University Press. 1: 199-204 p.


4. Bown, D. (1995). Encyclopaedia of herbs and their uses. Dorling Kindersley, London.
5. Miraldi, E., Ferri, V., Mostaghimi, S. (2001). Botanical drugs and preparations in the traditional
medicine of West Azerbaijan (Iran). Journal of Ethnopharmacology, 75: 77-87.
6. Ozen, T. (2009). Investigation of antioxidant properties of Nasturtium officinale (watercress)
leaf extracts. Acta Poloniae Pharmaceutica, 66: 187-913.
7. Verhoeven, D.T., Goldbohm, R.A., van Poppel, G., Verhagen, H., van den Brandt, P.A.
(1996). Epidemiological studies on brassica vegetables and cancer risk. Cancer Epidemiology,
Biomarkers and Prevention, 5: 733-748.
8. Gill, C.I.R., Haldar, S., Boyd, L.A., Bennett, R., Whiteford, J., Butler, M., Pearson, J.R.,
Bradbury, I., Rowland, I.R. (2007). Watercress supplementation in diet reduces lymphocyte
DNA damage and alters blood antioxidant status in healthy adults. American Journal of Clinical
Nutrition, 85: 504-510.
9. Hofmann, T., Kuhnert, A., Schubert, A., Gill, C., Rowland, I.R., Pool-Zobel, B.L., Glei, M.
(2009). Modulation of detoxification enzymes by watercress: in vitro and in vivo investigations
in human peripheral blood cells. European Journal of Nutrition, 48: 483-491.
10. Lhostea, E.F., Glouxa, K., De Waziersb, I., Garridoa, S., Lorya, S., Philippea, C., Rabota,
S., Knasmüllerc, S. (2004). The activities of several detoxication enzymes are differentially
induced by juices of garden cress, water cress and mustard in human HepG2 cells. Chemico-
Biological Interactions, 150: 211-219.
11. Coelho de Souzaa, G., Haasb, A.P.S., von Poserc, G.L., Schapovalc, E.E.S., Elisabetsky, E.
(2003). Ethnopharmacological studies of antimicrobial remedies in the south of Brazil. Journal
of Ethnopharmacology, 90: 135-143.
12. Gertsch, J., Niomawë, Gertsch-Roost, K., Sticher, O. (2004). Phyllanthus piscatorum, ethno-
pharmacological studies on a women’s medicinal plant of the Yanomam¨ý Amerindians. Journal
of Ethnopharmacol, 91: 181-188.
13. Cakilcioglu, U., Khatun, S., Turkoglu, I., Hayta, S. (2011). Ethnopharmacological survey of
medicinal plants in Maden (Elazig-Turkey). Journal of Ethnopharmacology, 137: 469-486.
14. Körpe, D.A., Iseri, Ö.D., Sahin, F.I., Cabi, E., Haberal, M. (2012). High-antibacterial activity
of Urtica spp. seed extracts on food and plant pathogenic bacteria. International Journal of Food
Science and Nutrition, 64(3): 355-362.
15. Folin, O., Ciocalteu, V. (1927). Tyrosine and tryptophane determination in proteins. Journal of
Biological Chemistry, 27: 627-650.
16. Slinkard, K., Singleton, V.L. (1977). Total phenol analyses: automation and comparison with
manual methods. American Journal of Enology and Viticulture, 28: 49-55.
17. Sharma, O.P., Bhat, T.K. (2009). DPPH antioxidant assay revisited. Food Chemistry, 113:
Özlem Darcansoy Iseri et al., / TBAP 4 (1) 2014 19 - 28 27
1202-1205.
18. Ersayýn Yasýnok, A., Sahin, F.I., Haberal, M. (2008). Isolation of endopyhtic and xylanolytic
Bacillus pumilus strains from Zea mays. AUFA Journal of Agricultural Sciences, 14: 374-380.
19. Murray, P.R., Baron, E.J., Pfaller, M.A., Tenover, F.C., Yolke, R.H. (1995). Manual of Clini-
cal Microbiology. 6th ed. Washington, DC: ASM.
20. Apak, R., Güçlü, K., Demirata, B., Özyürek, M., Çelik, S.E., Bektaþoglu, B., Berker, K.I.,
Özyurt, D. (2007). Comparative evaluation of various total antioxidant capacity assays applied
to phenolic compounds with the CUPRAC Assay. Molecules, 12: 1496-1547.
21. Kim, D., Jeond, S., Lee, C. (2003). Antioxidant capacity of phenolic phytochemicals from
various cultivars of plums. Food Chemistry, 81: 321-326.
22. Mathew, S., Abraham, T.E. (2006). Studies on the antioxidant activities of Cinnamon (Cinna-
momum verum) bark extracts through in vitro models. Food Chemistry, 94: 520-528.
Downloaded by [University of Southern Queensland] at 02:18 09 October 2014

23. Rice-Evans, C., Miller, N., Paganga, G. (1997). Antioxidant properties of phenolic compounds.
Trends in Plant Science, 2: 152-159.
24. Lu, M., Yuan, B., Zeng, M., Chen, J. (2011). Antioxidant capacity and major phenolic com-
pounds of spices commonly consumed in China. Food Research International, 44: 530-536.
25. Martínez-Sánchez, A., Gil-Izquierdo, A., Gil, M.I., Ferreres, F. (2008). A comparative study
of flavonoid compounds, vitamin C, and antioxidant properties of baby leaf Brassicaceae species.
Journal of Agricultural and Food Chemistry, 56: 2330-2340.
26. Amiri, H. (2012). Volatile constituents and antioxidant activity of flowers, stems and leaves of
Nasturtium officinale R. Br. Natural Product Research, 26: 109-115.
27. Palaniswamy, U.R., McAvoy, R.J., Bible, B.B., Stuart, J.D. (2003). Ontogenic variations of
ascorbic acid and phenethyl isothiocyanate concentrations in watercress (Nasturtium officinale
R.Br.) leaves. Journal of Agricultural and Food Chemistry, 51: 5504-5509.
28. Fahey, J.W., Zalcmann, A.T., Talalay, P. (2001). The chemical diversity and distribution of
glucosinolates and isothiocyanates among plants. Phytochemistry, 56: 5-51.
29. Bones, A.M., Rossiter, J.T. (2006). The enzymic and chemically induced decomposition of
glucosinolates. Phytochemistry, 67: 1053-1067.
30. Saavedra, M.J., Borges, A., Dias, C., Aires, A., Bennett, R.N., Rosa, E.S., Simões, M. (2010).
Antimicrobial activity of phenolics and glucosinolate hydrolysis products and their synergy
with streptomycin against pathogenic bacteria. Medicinal Chemistry, 6: 174-183.
31. Delaquis, P.J., Mazza, G. (1995). Antimicrobial properties of isothiocyanates in food preser-
vation. Food Technology, 49: 73-84.
32. Tiwari, B.K., Valdramidis, V.P., O’Donnel, C.P., Muthukumarappan, K., Bourke, P., Cullen,
P.J. (2009). Application of natural antimicrobials for food preservation. Journal of Agricultural
and Food Chemistry, 57: 5987-6000.
33. Sahin, F., Güllüce, M., Dafererad, D., Sökmen, A., Sökmen, M., Polissioud, M., Agar, G.,
Özer, H. (2004). Biological activities of the essential oils and methanol extract of Origanum
vulgare ssp. vulgare in the Eastern Anatolia region of Turkey. Food Control, 15: 549-557.
34. Aligiannis, N., Kalpotzakis, E., Mitaku, S., Chinou, I.B. (2001). Composition and antimicro-
bial activity of the essential oils of two species. Journal of Agriculture and Food Chemistry, 49:
4168-4170.
35. Penecilla, G.L., Magno, C.P. (2011). Antibacterial activity of extracts of twelve common medi-
cinal plants from the Philippines. Journal of Medicinal Plants Research, 5: 3975-3981.
36. Camacho-Corona Mdel, R., Ramírez-Cabrera, M.A., Santiago, O.G., Garza-González, E.,
Palacios Ide, P., Luna-Herrera, J. (2008). Activity against drug resistant-tuberculosis strains
of plants used in Mexican traditional medicine to treat tuberculosis and other respiratory diseases.
Phytotherapy Research, 22: 82-85.
Özlem Darcansoy Iseri et al., / TBAP 4 (1) 2014 19 - 28 28
37. Abou El Seoud, K.A.E., Bibby, M.C., Shoeib, N., Wright, C.W. (2003). Evaluation of some
Egyptian plant species for in vitro antimycobacterial and cytotoxic activities. Pharmaceutical
Biology, 41: 463-465.
38. Lo Cantore, P., Iacobellis, N.S., De Marco, A., Capasso, F., Senatore, F. (2004). Antibacterial
activity of Coriandrum sativum L. and Foeniculum vulgare Miller Var. vulgare (Miller) essential
oils. Journal of the Science of Food and Agriculture, 52: 7862-7866.
39. McManus, P.S., Stockwell, V.O., Sundin, G.W., Jones AL. (2002). Antibiotic use in plant
agriculture. Annual Reviews of Phytopathology, 40: 443-465.
40. Kotan, R., Cakir, A., Dadasoglu, F., Aydin, T., Cakmakci, R., Ozer, H., Kordali, S., Mete,
E., Dikbas, N. (2010). Antibacterial activities of essential oils and extracts of Turkish Achillea,
Satureja and Thymus species against plant pathogenic bacteria. Journal of the Science of Food
and Agriculture, 90: 145-160.
Downloaded by [University of Southern Queensland] at 02:18 09 October 2014

41. Balestra, G.M., Heydari, A., Ceccarelli, D., Ovidi, E., Quattrucci, A. (2009). Antibacterial
effect of Allium sativum and Ficus carica extracts on tomato bacterial pathogens. Crop Protection,
28: 807-811.

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