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Plant-derived Antibacterial Metabolites Suppressing Tomato Bacterial Wilt Caused by Ralstonia solanacearum
Res. Plant Dis. 2017;23:89-98
Published online June 30, 2017
© 2017 The Korean Society of Plant Pathology.

Thuy Thu Vu1,2, Gyung Ja Choi1,2,*, and Jin-Cheol Kim3,*

1Department of Green Chemistry and Environmental Biotechnology, Korea University of Science and Technology, Daejeon 34113, Korea,
2Center for Eco-friendly New Materials, Korea Research Institute of Chemical Technology, Daejeon 34114, Korea,
3Department of Agricultural Chemistry, College of Agriculture and Life Sciences, Chonnam National University, Gwangju 61186, Korea
Co-corresponding authors GJ Choi Tel: +82-42-860-7434 Fax: +82-42-861-4913 E-mail: kjchoi@krict.re.kr
JC Kim Tel: +82-62-530-2132 Fax: +82-62-530-2139 E-mail: kjinc@jnu.ac.kr
Received February 13, 2017; Revised March 1, 2017; Accepted March 1, 2017.
cc This is an open access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
Abstract

Ralstonia solanacearum species complex (RSSC) causes bacterial wilt, and it is one of the most important soil-borne plant pathogenic bacteria. RSSC has a large host range of more than 50 botanical families, which represent more than 200 plant species, including tomato. It is difficult to control bacterial wilt due to following reasons: the bacterial wilt pathogen can grow inside the plant tissue, and it can also survive in soil for a long period; moreover, it has a wide host range and biological diversity. In most previous studies, scientists have focused on developing biological control agents, such as antagonistic microorganisms and botanical materials. However, biocontrol attempts are not successful. Plant-derived metabolites and extracts have been promising candidates to environmentally friendly control bacterial wilt diseases. Therefore, we review the plant extracts, essential oils, and secondary metabolites that show potent in vivo antibacterial activities (in potted plants or in field) against tomato bacterial wilt, which is caused by RSSC.

Keywords : Antibacterial activity, Botanical, Plant metabolite, Ralstonia solanacearum species complex, Tomato bacterial wilt
Introduction

Plant disease outbreaks cause global economic losses by reducing the quality and quantity of marketable plants and plant products. Plant diseases cause loss of crops, which leads to hunger and starvation of impoverished people, especially in less developed countries where there is limited access to disease control methods. In these countries, major crops usually suffer annual losses of about 30%–50% (Dubey et al., 2011). Although plant pathogenic bacteria are less harmful than fungi or viruses, they do cause many serious diseases in plants throughout the world (Anderson et al., 2004; Vidaver and Lambrecht, 2004).

Ralstonia solanacearum species complex (RSSC), formerly known as Pseudomonas solanacearum (Smith 1896) Smith (1914) or Burkholderia solanacearum (Smith 1896) (Safni et al., 2014) in the 20th century, was first described by Erwin F. Smith in 1896 as the causative agent of bacterial wilt in solanaceous plants (Genin, 2010; Mohumad Tahat and Sijam, 2010). It is one of the most important soil-borne plant pathogenic bacteria, and its appearance makes it the second most important bacterial pathogen on scientific and economic grounds (Mansfield et al., 2012). RSSC causes bacterial wilt on tomato and many other crops in tropical and subtropical regions, leading to huge economic losses. The bacterium, RSSC, has a large host range of more than 50 botanical families that represent more than 200 plant species, including tomato, potato, eggplant, pepper, peanut, tobacco, banana, groundnut, olive, and ginger (Genin, 2010; Ramsubhag et al., 2012; Vu et al., 2013).

RSSC is the cause of bacterial wilt disease that destroys many crops, leading to serious economic losses. Direct yield losses differ significantly according to the host, cultivar, climate, soil type, cropping pattern, and strain. Yield losses vary from 0%–91% for tomato, 33%–90% in potato, 10%–30% in tobacco, 80%–100% in banana, and up to 20% in groundnut (Elphinstone, 2005; Yuliar et al., 2015). Tomato crops have high economic value; therefore, it is essential to control bacterial wilt of tomato.

It is difficult to control bacterial wilt because of the complex nature of the pathogen. It can grow endophytically and survive in soil, and it has a wide host range and biodiversity (Singh et al., 2015; Yuliar et al., 2015). To control bacterial wilt disease, different methods have been precribed till date (Yuliar et al., 2015). Yuliar et al. (2015) reported that studies conducted between 1984 and 2014 described the following methods to control bacterial wilt: biological methods (54%) were most commonly used, followed by cultural practices (21%), chemical methods (8%), and physical methods (6%).

Most researchers are interested in developing biological methods that involve the use of biological control agents (BCAs) and organic matter. Modes of action of BCAs are characterized by various interactions, such as the competition for nutrients and space, antibiosis, parasitism, and induced systemic resistance (Yuliar et al., 2015). Previous studies reported that beneficial microbes, such as species of Pseudomonas, Bacteriophages, Streptomyces, Acinetobacter, Enterobacter, Bacillus, and Paenibacillus, suppressed the growth of RSSC in field conditions. Therefore, the interest of researchers in BCAs has increased steadily (Chen et al., 2013; Yuliar et al., 2015). However, the biocontrol efficiencies of some BCAs are too low to be commercially available. This might be due to the poor colonization ability of antagonistic strains under different field conditions. The performance of BCAs is hindered by some difficulties, which are associated with the production, storage, and subsequent application of BCAs (Singh et al., 2015; Yuliar et al., 2015). Many previous studies reported that bacterial wilt was suppressed by organic matter. To suppress bacterial wilt, plant residues (80%) such as fresh plant materials, plant extracts, isolated compounds, and essential oils, have been most commonly used, followed by animal wastes (10%), and simple organic compounds (10%) (Yuliar et al., 2015).

Plant kingdom is the most efficient producer of different biologically active compounds (Dubey et al., 2011). Plants contain abundant bioactive materials, such as secondary metabolites, volatile oils, and essential oils. Since plants are an important source of bioactive materials, they can be exploited to develop new biopesticides (Bhagat et al., 2014; Gurjar et al., 2012). In the development of novel pesticides, secondary metabolites could be used as lead compounds as they have novel modes of action (Bourgaud et al., 2001; Dubey et al., 2011). The extracts obtained from various plant species have promising potential applications: they can be used as natural products to fight plant pathogens in agriculture (Bhagat et al., 2014; Gurjar et al., 2012; Pretorius and van der Watt, 2011). However, very few natural plant products have been developed from screening programs on a commercial scale (Pretorius and van der Watt, 2011). Only a handful of pesticidal plant products have been successfully used on a commercial scale; they constitute a very small percentage (<0.1%) of total pesticide products (Glare et al., 2012; Isman, 2006; Sola et al., 2014). Pyrethrum, rotenone, neem, and essential oils are the four major types of botanical pesticide products currently used to control plant diseases. Furthermore, ryania, nicotine, and sabadilla are the other three botanical pesticides used to a limited extent in different countriesalong with plant extracts and oils, such as garlic oil (El-Wakeil, 2013; Tanwar et al., 2012).

In most research studies, scientists have performed in vitro assays in potted plants to determine the efficacy of various botanicals (extracts and isolated compounds) in controlling RSSC. However, only a handful of antibacterial substances were examined to determine whether they can control bacterial wilt disease in tomato. Most of studies have been focused on isolation and determination of antibacterial substances from plants to control bacterial wilt diseases. These plant-derived products are listed in Table 1 and Table 2, and chemical structures in Fig. 1. Several previous studies have reported that some plant materials, which were incorporated as organic amendments in soil, suppressed the growth of RSSC, such as Brassica sp. (cole) (Olivier et al., 2006), Azadirachta indica (neem) (Pontes et al., 2011), Cajanus cajan (pigeon pea), and Crotalaria juncea (sunn hemp) (Cardoso et al., 2006). The possible mechanism of action of plant residues primarily includes antimicrobial activities. Thereafter, the plant residues suppress pathogens indirectly by improving the physical, chemical, and biological soil properties (Cardoso et al., 2006). Presently, only a few isolated compounds have been used to control tomato bacterial wilt in planta or in field conditions (Li et al., 2016).

Plant extracts showing a potent in vitro antibacterial activity against Ralstonia solanacearum species complex (RSSC) causing bacterial wilt

Plant speciesPart usedPlant extract*Strain (host)MethodAntibacterial activityReference
Azadirachta indica (neem)LeafMeOHRSSC (tomato)Agar well diffusionDIZ: 18.4–21.6 mmMurthy et al., 2015b
Allium sativum (garlic)Leaf, bulbAq.RSSC (tomato)Agar well diffusionDIZ: 49 mmGopalakrishnan et al., 2014
Carica papaya (papaya)SeedAq.RSSC (n.d.)Agar well diffusionDIZ: 19 mmUma et al., 2012
Eugenia jambolana (Jamun)MeOHDIZ: 26 mm
Curcuma longa (turmeric)RhizomeAq.RSSC (tomato)Agar well diffusionDIZ: 20–26 mmMurthy et al., 2015a
Broth microdilutionMIC: 2–20 µg/ml
Rhus chinensis (Chinese sumac)GallnutAq.RSSC EPS-1 (eggplant)Agar dilutionMIC: 50 µg/mlFeng et al., 2012
Acacia auriculiformisLeafEtOH, Ac.RSSC Rs-08-17 (eggplant)Agar well diffusionDIZ: 23.6–25.0 mmGaitonde and Ramesh, 2016
Anacardium occidentalisLeafEtOH, MeOHDIZ: 20.3–24.6 mm
Boerhavia diffusaWhole plantEADIZ: 30.0 mm
Calotropis giganteaLeafEtOHDIZ: 20.0 mm
Cinnamomum zevlanciumLeafEtOH, EADIZ: 21.6–24.6 mm
Cymbopogon flexuosusLeafEADIZ: 31.6 mm
Garcinia indicaLeafEtOH, MeOH, Ac.DIZ: 20.6–30.0 mm
Lawsonia inermisLeafMeOHDIZ: 20.6 mm
Mimosa pudicaLeafEtOHDIZ: 20.6 mm
Psidium guajavaLeafEtOH, MeOH, Ac.DIZ: 28.0–31.6 mm
Tamarindus indicaLeafEtOH, MeOH, Ac.DIZ: 23.0–30.6 mm

*MeOH, methanol; Aq., aqueous; EtOH, ethanol; Ac., acetone; EA, ethyl acetate.

DIZ, diameter of inhibition zone; MIC, minimum inhibitory concentration.

n.d., not determined.


Plant metabolites showing a potent in vitro antibacterial activity against Ralstonia solanacearum species complex (RSSC) causing bacterial wilt

Plant speciesPart usedPlant metabolite*Strain (host)MethodAntibacterial activityReference
Macleaya cordataLeafEssential oilRSSC GMI 1000 (tomato)Broth microdilutionMIC: 125 µg/mlLi and Yu, 2015
Syzygium aromaticum (clove)n.d.Essential oilRSSC (tomato)Agar well diffusionDIZ: 52 mmGopalakrishnan et al., 2014
Clausena lansiumSeedLansiumamide BRSSC (tobacco)Agar dilutionMIC: 125 µg/mlLi et al., 2014
Cryptomeria japonicaWoodFerruginolRSSC no. 8224 (n.d.)Agar dilutionMIC: 32 µg/mlMatsushita et al., 2006
SandaracopimarinolMIC: 8 µg/ml
Dalbergia odoriferaWoodLiquiritigeninRSSC (n.d.)Agar disc diffusionDIZ: 12.2 mmZhao et al., 2011
IsoliquiritigeninDIZ: 14.2 mm
(3R)-vestitolDIZ: 16.6 mm
n.d.n.d.DaphnetinRSSC CCT818 (n.d.)Broth microdilutionMIC: 64 µg/mlYang et al., 2016
EsculetinMIC: 192 µg/ml
Salvia miltiorrhizaeRootProtocatechualdehydeRSSC (tobacco)Agar dilutionMIC: 20 µg/mlLi et al., 2016
MBC: 40 µg/ml
Sedum takesimenseArial partGallic acidRSSC (tomato)Broth microdilutionMIC: 50 µg/mlVu et al., 2013
Methyl gallateMIC: 30 µg/ml
4,6-di-O-galloylarbutinMIC: 100 µg/ml
2,6-di-O-galloylarbutinMIC: 80 µg/ml
2,4,6-tri-O-galloyl-glucoseMIC 40 µg/ml
1,3,4,6-tetra-O-galloyl-β-glucoseMIC: 30 µg/ml
1,2,4,6-tetra-O-galloyl-β-glucoseMIC: 30 µg/ml
1,2,3,6-tetra-O-galloyl-β-glucoseMIC: 20 µg/ml
Syringa oblata (lilac)Flower budEugenolRSSC (tobacco)Oxford cupDIZ: 18.5 mmBai et al., 2016
Warbugia ugandensisStem barkMukaadialRSSC (sweet potato)Agar disc diffusionMIC: 25 µg/mlOpiyo et al., 2011
MuzigadialMIC: 25 µg/ml
PolygodialMIC: 25 µg/ml
UgandensidialMIC: 100 µg/ml
UgandensolideMIC: 100 µg/ml
WarburganalMIC: 50 µg/ml

*Plant metabolite includes essential oil and isolated compound.

MIC, minimum inhibitory concentration; DIZ, diameter of inhibition zone; MBC, minimum bactericidal concentration.

n.d., not determined.


Fig. 1.

Chemical structures of isolated compounds showing a potent in vitro antibacterial activity against Ralstonia solanacearum species complex causing bacterial wilt.


To the best of our knowledge, there are no effective chemical treatments and commercially available botanical productsto control tomato bacterial wilt. In this study, we review plant-derived bactericides, including plant extracts (or residues), essential oils, and secondary metabolites, showing a potent in vivo antibacterial activities (in potted plants or in field) against tomato bacterial wilt caused by RSSC. Please note that these plant-derived bactericides have not yet been commercialized.

Plant Extracts

Allium fistulosum

Allium genus plants have antimicrobial properties, so they have been used in traditional medicine. Disease control efficacy of the aqueous extracts of A. fistulosum was evaluated against tomato bacterial wilt in a growth chamber. The soil pretreated with A. fistulosum extracts significantly reduced RSSC populations. The extracts also significantly reduced the incidence of tomato bacterial wilt (Deberdt et al., 2012).

Chamaecyparis obtusa (hinoki)

Chamaecyparis obtuse (hinoki) is a perennial tree widely grown in the forests of Asian countries. The bark of this plant hardly decomposes. The bark has a fibrous structure and suggested rephrase ans an acidic pH (5.6), so it is used as a substrate in soilless culture, which decreases the losses caused by root-infecting pathogens (Terada, 1993). Ethanol extracts of the hinoki bark exhibited significant in vitro antibacterial activity against RSSC. The proliferation of RSSC was mainly inhibited by volatile oils and non-volatile substances of the bark. However, the activity of non-volatile substances was greater in inhibiting RSSC. In addition, the incidence of tomato bacterial wilt was greatly reduced by hinoki bark (Yu and Komada, 1999). Yu and Komada (1999) also found that hinoki bark could greatly reduce the crown and root rot of tomato, which is caused by the fungus Fusarium oxysporum f. sp. radicis-lycopersici.

Eichhorina crassipes and other invasive alien species (IAS) in Ethiopia

Invasive alien species (IAS) such as Eichhorina crassipes are a major problem in Ethiopia. They have a negative impact on the environment, especially hampering the country’s biodiversity. Alemu et al. (2013) reported that E. crassipes showed the highest antibacterial activity against RSSC as compared to other IAS, including Mimosa diplotricha, Lantana camara, and Prosopis juliflora. In the in vivo experiment, the three extracts applied at the time of inoculation showed the best antibacterial activity against tomato bacterial wilt with a control value of 91% for E. crassipes, and 71%–85% for the other plant extracts.

Sedum takesimense

The methanol extract of S. takesimense showed potent in vitro antibacterial activity against RSSC (Vu et al., 2013). Eight antibacterial gallotannins were isolated from the plant extract and identified as follows: gallic acid (1), methyl gallate (2), 4,6-di-O-galloylarbutin (3), 2,6-di-O-galloylarbutin (4), 2,4,6-tri-O-galloylglucose (5), 1,3,4,6-tetra-O-galloyl-β-glucose (6), 1,2,4,6-tetra-O-galloyl-β-glucose (7), and 1,2,3,6-tetra-O-galloyl-β-glucose (8). The minimum inhibitory concentration (MIC) values of these eight chemicals against RSSC varied between 0.02 to 0.10 g/l. Compound 8 showed maximum antibacterial activity against the plant pathogen. The antibacterial activity of galloylarbutins and galloylglucoses was enhanced by increasing the number of galloyl groups and substituents at 1 or 2 position of the glucose ring, respectively. Furthermore, the several combinations of compounds showed synergistic or partial synergistic effects.

On the other hand, the wettable powder formulation of the ethyl acetate layer of S. takesimense (ST-WP) effectively suppressed the development of tomato bacterial wilt in greenhouse experiment (Vu et al., 2013). Seven and 14 days after inoculation, the control efficacy of the formulation was 93.9% and 53.9% at 400-fold dilution, respectively. Its disease control efficacy was higher than that of agricultural streptomycin sulfate (200 μ/ml).

Plant Metabolites

Thymol, palmarosa oil, and lemongrass oil

Pradhanang et al. (2003) reported that thymol (a major component of thyme oil that is produced synthetically), palmarosa, and lemongrass oils were effective in reducing RSSC populations in infested soil, thereby minimizing the incidence of tomato bacterial wilt. The growth of RSSC in infested soils was completely inhibited seven days after the soil was treated with these essential oils and thymol component at a concentration of 0.4 ml (or g) per liter. Plants grown in this oil-treated soil did not wilt throughout the experiment (28 days after inoculation). Futhermore, plants grown in soil treated with 700 μ/ml of thymol were free from wilt and RSSC. Ten percent of plants grown in soil treated with palmarosa or lemongrass oil harbored the bacteria but did not wilt (Pradhanang et al., 2003). Ji et al. (2005) also reported that the incidence of bacterial wilt was significantly reduced by application of 0.7% thymol on the susceptible cultivar Solar Set. They suugested that thymol can be be used as a soil biofumigant for the management of RSSC.

Clove oil

Clove oil is an essential oil that is extracted from the buds of Eugenia caryophyllata (or formerly Syzygium aromaticum). It is widely used in traditional medicine and in the fragrance and flavoring industries. The major components of clove oil include eugenol, β-caryophyllene, and eugenyl acetate. It also contains lesser amounts of other components. Previous studies have reported that clove oil and its components possess many biological activities, including antibacterial, antifungal, antiviral, antioxidant, anaesthetic, and insecticidal activities (Chaieb et al., 2007).

Lee et al. (2012) proved that clove oil exhibited potent in vitro antibacterial activities against RSSC. The disease suppression efficacy of the essential oil was evaluated in planta using detached tomato leaves. The incidence of tomato bacterial wilt was significantly decreased using 0.005%−0.01% clove oil (Lee et al., 2012).

Cinnamon oil

Cinnamon belongs to Cinnamomum genus of the Lauraceae family. Most members of this family are used as spices. Cinnamon has been used as a spice in food preparations and in traditional medicine since ancient times. It has strong antioxidant, antibacterial, antifungal, antipyretic, anticancer, and anti-inflammatory properties. Cinnamon essential oil is extracted from the bark of cinnamon trees. Cinnamaldehyde (about 64%–90%) is the major component of cinnamon essential oil (Hamidpour et al., 2015).

In the series of experiments performed by Lee et al. (2012), cinnamon oil exhibited the highest in vitro antibacterial activity against RSSC, compared with other essential oils. In planta, cinnamon oil (0.01%) also significantly decreased the development of bacterial wilt disease three days after inoculation, and the disease protection effect still existed five days after inoculation. However, cinnamon oil (0.02%) caused phytotoxic effect on tomato petioles (Lee et al., 2012).

Methyl gallate

Methyl gallate was isolated from the methanol extract of Toxicodendron sylvestre. It significantly inhibited RSSC in vitro and in planta (Yuan et al., 2012). It exhibited antibacterial activity against RSSC, with MIC and minimum bacteriocidal concentration values of 20 and 30 μ/ml, respectively. In greenhouse experiments, its control efficacy, at 500 μ/ml, was 65.2%, which was significantly higher than that of agricultural streptomycin sulfate.

In other study, methyl gallate was isolated from the aqueous extract of Rhus chinensis (Chinese sumac or gallnut). Using agar dilution method, it was found that methyl gallet exhibits potent in vitro antibacterial activities against RSSC and other plant pathogens, including Acidovorax citrulli, Xanthomonas citri pv. citri, and X. euvesicatoria (MIC=50–100 μ/ml) (Feng et al., 2012). The mechanism of action of methyl gallate against RSSC was found to be as follows: the structure of cell walls in RSSC was damaged by methyl gallate; it also inhibited protein synthesis and succinate dehydrogenase activity in the pathogen (Fan et al., 2014).

Conclusions

The demand for environmentally acceptable, safe and effective pesticides is increasing in agriculture because of numerous problems associated with danger of human health and environment, poisonous effects by pesticide residues on food, and antibiotic resistance caused by using chemical pesticides. As one of biocontrol methods for the control of bacterial wilt caused by RSSC, botanical bacteriocides can be promising tools. Most recent studies that revealed plant-derived products and metabolites showing potent antibacterial activity against RSSC were conducted in in vitro tests or in potted plants, but not in fields. Additionally, several problems such as the limitation of information available on application, efficacy and safety of most of botanical products, and the narrow range of formulation types and antimicrobial spectra should still be overcome for the development of commercial products using botanicals (Sola et al., 2014). Therefore, future areas of interest consist of field trials to assess the practical applicability of the botanical pesticides, development of optimized fomulations with enhanced activity, and biosafety studies to ascertain their toxicity to humans, animals and crop plants. On the other hands, plant secondary metabolites can play an important role as lead molecules for chemical synthesis. This requires the continuous studies on the discovery of novel bacteriocidal compounds.

Acknowledgements

This research study was supported by Korea Research Institute of Chemical Technology (project no. KK1606-M02). This work was also supported by Korea Institute of Planning and Evaluation for Technology in Food, Agriculture, Forestry and Fisheries (IPET) through the Advanced Production Technology Development Program, funded by Ministry of Agriculture, Food and Rural Affairs (MAFRA) (315007-03).

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