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Article

Bactericidal Activity of Larrea tridentata Hydroalcoholic Extract against Phytopathogenic Bacteria

by
Ana Lizet Morales-Ubaldo
1,
Nallely Rivero-Perez
2,*,
Fidel Avila-Ramos
3,
Eliazar Aquino-Torres
1,
Judith Prieto-Méndez
1,
Helal F. Hetta
4,
Gaber El-Saber Batiha
5 and
Adrian Zaragoza-Bastida
2,*
1
Área Académica de Ciencias Agrícolas y Forestales, Instituto de Ciencias Agropecuarias, Rancho Universitario Av. Universidad km 1, Universidad Autónoma del Estado de Hidalgo, EX-Hda de Aquetzalpa, Tulancingo, Hidalgo 43600, Mexico
2
Área Académica de Medicina Veterinaria y Zootecnia, Instituto de Ciencias Agropecuarias, Rancho Universitario Av. Universidad km 1, Universidad Autónoma del Estado de Hidalgo, EX-Hda de Aquetzalpa, Tulancingo, Hidalgo 43600, Mexico
3
Programa Educativo de Medicina Veterinaria y Zootecnia, División Ciencias de la Vida, Universidad de Guanajuato, Ex Hacienda El Copal km. 9, carretera Irapuato-Silao, A.P. 311, Irapuato 36500, Guanajuato, Mexico
4
Department of Medical Microbiology and Immunology, Faculty of Medicine, Assiut University, Assiut 71515, Egypt
5
Department of Pharmacology and Therapeutics, Faculty of Veterinary Medicine, Damanhour University, Damanhour 22511, Egypt
*
Authors to whom correspondence should be addressed.
Agronomy 2021, 11(5), 957; https://doi.org/10.3390/agronomy11050957
Submission received: 15 April 2021 / Revised: 5 May 2021 / Accepted: 10 May 2021 / Published: 12 May 2021
(This article belongs to the Special Issue Biological Control of Plant Disease)
Browse Figure
Versions Notes

Abstract

:
Due to the emergence of bacterial resistance in phytopathogenic microorganisms, it is necessary to search for new treatment alternatives for these pathogens. Natural extracts are a potential source of bioactive compounds that can act against such bacterial strains. The antibacterial activity of Larrea tridentata against bacteria with public health importance has been documented; however, few reports cover pathogens associated with the agricultural sector. The aim of the present study was to evaluate the antibacterial activity of Larrea tridentata hydroalcoholic extract (LTHE) and fractions against phytopathogenic bacteria. LTHE was obtained by the maceration technique and then subjected to bipartition using solvents of different polarities. Clavibacter michiganensis sbsp. michiganensis, Pseudomonas syringae, and Xanthomonas campestris strains were used, and their antibiotic sensitivity was determined. The minimal inhibitory concentration (MIC) and minimal bactericidal concentration (MBC) of LTHE and its fractions (aqueous: LTAq-F; organic: LTEtOAc-F) were determined. LTHE and its organic fraction showed bactericidal activity against the three bacteria, showing better activity against X. campestris, exhibiting an MIC of 0.39 mg/mL and an MBC of 0.78 mg/mL. The results show that LTHE and its organic fraction have bactericidal activity in vitro against Clavibacter michiganensis sbsp. michiganensis, Pseudomonas syringae, and Xanthomonas campestris.

Graphical Abstract

1. Introduction

The agricultural activities around the world are the main food suppliers, hence its great relevance. Over the years, this sector has undergone significant changes, such as adaptions to new demands by society, changes in soil conditions and climate, these changes have triggering fires, droughts, de-creased crop yield, and the emergence or reemergence of pests and diseases [1,2].
Production of tomato (Solanum lycopersicum L.), one of the most consumed vegetables, has been limited by several factors, including management practices, pests, and diseases [3,4]. Some reports state that more than 60 pathogens, including viruses, nematodes, fungi, and bacteria, can infect tomato crops, which results in severe problems that affect global production [5]. Among the most important diseases are bacterial canker, bacterial speck, and bacterial spot, whose etiological agents are Clavibacter michiganensis subsp. michiganensis, Pseudomonas syringae, and Xanthomonas campestris, respectively [4,6,7].
Controlling phytopathogenic bacteria currently represents a challenge due to the lack of effective antibacterial agents, since these microorganisms have developed resistance to the active ingredients, in addition to the environmental damage resulting from their application. This situation has impeded the treatment and control of several diseases, and in some cases, there are no chemical or biological treatments available with which to control them, as in the case of Xanthomonas campestris [8,9,10,11].
Due to the aforementioned problems, new treatment alternatives are being sought. Today, biocontrol is sociologically, commercially, and environmentally accepted as a legitimate tool for crop protection [12]. In this respect, medicinal plants, through the use of extracts, have attracted attention in the field of plant disease control, since they are considered biopesticides. Among the main advantages of botanical agents are that they are less toxic, biodegrade rapidly, are targeted to specific pests, and exhibit specific modes of action, thus maintaining the ecological balance [13,14].
Larrea tridentata is a perennial shrub with wide distribution (deserts in Mexico and USA) that survives in hostile environments and is characterized by resistance to pests and infections [15,16]. Is a botanical species well known in Mexican and American traditional medicine for its effectiveness against infertility, rheumatism, arthritis, diabetes, renal afflictions, pain, and inflammation [17,18].
Several studies have reported the pharmacological properties of Larrea tridentata, such as antioxidant [19,20,21,22,23,24,25], antitumoral [23], neuroprotective [26,27], regenerative [28], hepatoprotective [29,30,31], nephroprotective [32,33], antiviral [34], antifungal (mainly against fungi associated with agricultural crops, including tomatoes) [22,35,36,37,38], antiparasitic [39], and antibacterial (against Gram-positive and Gram-negative bacteria and Mycobacteria) effects [40,41,42,43,44,45,46,47,48,49]. However, there are no reports on the antibacterial activity of this plant against pathogens that affect agricultural production, so the aim of the present study was to evaluate the antibacterial activity of hydroalcoholic extract and fractions of Larrea tridentata against phytopathogenic bacteria.

2. Materials and Methods

2.1. Plant Material

Aerial parts from Larrea tridentata plants were collected in the municipality of Matehuala, San Luis Potosí, Mexico (23°38′47″ n 100°30′40″ O). For plant identification, the herbarium of the National Autonomous University of Mexico (UNAM) was consulted, and the plant was verified as Larrea tridentata (IBUNAM: MEXU: 1249920). Fresh material was dried at room temperature in the dark.

2.2. Preparation of Hydroalcoholic Extract

Hydroalcoholic extract was prepared according to the methodology described by Rivero-Perez et al. (2019) [50]. Dried aerial parts from L. tridentata (1500 g) were subjected to an extraction process through the maceration technique using a hydroalcoholic solution of ethanol:water (70:30 v/v) at room temperature for 24 h. Subsequently, it was filtered using Whatman filter paper (Whatman® 42). After filtration, the solvent was eliminated using a rotary evaporator to obtain a semisolid extract (Büchi R-300, Flawil, Switzerland), which, finally, was lyophilized (LABCONCO®) and stored at 4 °C until antibacterial evaluation.

2.3. Fractionation of Larrea Tridentata Hydroalcoholic Extract

Hydroalcoholic extract was fractionated according to the methodology described by González-Alamilla et al. (2019), and Olmedo-Juárez et al. (2019), described below [51,52].
L. tridentata hydroalcoholic extract (LTHE) was processed for bipartition via liquid-liquid chromatography, using water: ethyl acetate (1:3) solvent (Merck, Darmstadt, Germany). Two fractions were obtained, aqueous fraction (LTAq-F) and organic fraction (LTEtOAc-F). Solvent in both fractions was eliminated by low-pressure distillation (Büchi R-300, Flawil, Switzerland). Both fractions were evaluated with a pharmacological antibacterial test.

2.4. Bacterial Strains and Culture Conditions

The strains used were Clavibacter michiganensis subsp. michiganensis, Pseudomonas syringae, and Xanthomonas campestris, which were obtained from AG laboratory in Celaya Guanajuato, México.
Bacterial strains were reactivated from cryopreservation in Müller–Hinton agar (BD Bioxon, Heidelberg, Germany) with the simple strain technique to obtain isolated colonies. Gram staining was performed to corroborate their morphology and purity. One colony of each strain was inoculated in nutritive broth (BD Bioxon) and incubated for 24 h at 26 °C.

2.5. Antibiotic Sensitivity Test

Antibiotic sensitivity was determined using the disk diffusion method in Müller–Hinton agar (BD Bioxon, Heidelberg, Germany), according to the methodology described by Rangel-López et al. (2020) [53].
For this process, 100 µL of each bacterium previously adjusted to a 0.5 McFarland standard (Remel, R20421, Lenexa, KS, USA) was inoculated and distributed on petri plates, and each plate was allowed to dry for 15 min. Once this period elapsed, multidiscs (PT-35, Mexico City, Mexico) were placed on the plate and incubated at 26 °C for 24 h. After the incubation period, growth inhibition halos were measured and compared with measures established by the Clinical and Laboratory Standards Institute (CLSI) [54].
Antibacterial active ingredients used were amikacin (30 µg), ampicillin (10 µg), carbenicillin (100 µg), cephalothin (30 µg), cefotaxime (30 µg), ciprofloxacin (5 µg), clindamycin (30 µg), chloramphenicol (30 µg), dicloxacillin (1 µg), erythromycin (15 µg), gentamicin (10 µg), netilmicin (30 µg), nitrofurantoin (300 µg), norfloxacin (10 µg), penicillin (10 U), sulfamethoxazole/trimethoprim (25 µg), tetracycline (30 µg), and vancomycin (30 µg).

2.6. Antibacterial Activity

The antibacterial activity of the L. tridentata hydroalcoholic extract and fractions was determined through the minimal inhibitory concentration (MIC) and minimal bactericidal concentration (MBC) in accordance with the CLSI guidelines, and as described by Zaragoza-Bastida et al. (2020) [54,55].

2.6.1. Minimal Inhibitory Concentration (MIC)

Microdilution technique was used to determine MIC, and different concentrations were evaluated (200–3.12 mg/mL for LTHE and 6.25–0.39 mg/mL for LTAq-F and LTEtOAc-F). Every concentration was prepared with nutritive broth, except for the organic fraction, which was solubilized in Dimethyl Sulfoxide Solvent (DMSO) (15%).
Into a sterile 96-well plate, 100 µL of each concentration were added along with 10 µL of bacterial cell suspension previously adjusted to a 0.5 McFarland standard (Remel, R20421, Lenexa, KS, USA). Plates were incubated at 26 °C during 24 h. Kanamycin (AppliChem 4K10421, Darmstadt, Germany) (16 to 0.125 µg/mL) and nutritive broth, were used as positive and negative controls, respectively. Treatments were evaluated by triplicate.
After incubation, 20 µL of a 0.04% (w/v) p-iodonitrotetrazolium (Sigma-Aldrich I8377, St. Louis, MO, USA.) solution was added into each well, and the plates were incubated for 30 min. The MIC was determined by the concentration at which the solution turned to a pinkish color.

2.6.2. Minimal Bactericidal Concentration (MBC)

After incubation and prior to adding p-iodonitrotetrazolium, 5 µL from each well was inoculated in Müller–Hinton agar (BD Bioxon) and incubated at 26 °C for 24 h. The MBC was considered as the lowest concentration where no visible growth of bacteria was observed on the plate.
In order to determine if the evaluated treatments had bactericidal or bacteriostatic effects, the ratio of MBC/MIC was determined. A bacteriostatic effect was considered when the ratio was greater than 4, and a bactericidal effect when values less than or equal to 4 were obtained [51].

2.7. Statistical Analysis

The MIC and MBC results were normalized using log10 and were analyzed by a completely randomized design through ANOVA using the general linear model (GLM). Differences among the means were assessed by Tukey’s multiple comparison statistical analysis at the p = 0.05 level of significance using the SAS program, version 9.0.

3. Results

3.1. Test of Antibiotic Sensitivity

The results for antibiotic sensitivity show that Clavibacter michiganensis subsp. michiganensis was resistant to 13 antimicrobials and had intermediate resistance to dicloxacillin, clindamycin, and norfloxacin, making it the most resistant of all the strains under study, followed by X. campestris, which was resistant to nine antibiotics and had intermediate resistance to amikacin, and P. syringae, which was resistant to eight antibiotics and had intermediate resistance to carbenicillin (Table 1).

3.2. Minimal Inhibitory Concentration (MIC)

As can be seen in Table 2, L. tridentata hydroalcoholic extract inhibited the growth of both Gram-positive and Gram-negative bacteria, and X. campestris was the most sensitive bacterium (p = 0.0001, MIC = 0.39 mg/mL) compared with C. michiganensis subsp. michiganensis and P. syringae (MIC = 6.25 mg/mL). LTEtOAc-F was the most active fraction, showing the best (p = 0.0001) MIC (0.39 mg/mL) against X. campestris, followed by C. michiganensis sbsp. michiganensis and P. syringae (MIC = 3.12 mg/mL). LTAq-F only showed activity against two of the strains at 6.25 mg/mL.

3.3. Minimal Bactericidal Concentration (MBC)

LTHE showed bactericidal activity against the three strains under study; the best activity (p = 0.0001) was observed for X. campestris, with an MBC of 0.78 mg/mL. LTEtOAc-F showed effects against the three strains, with a better MBC (0.0001) for X. campestris (0.78 mg/mL and 6.25 mg/mL for the others). LTAq-F did not show an MBC against any bacteria. These results are shown in Table 3.
Calculating the MBC/MIC ratio allowed us to determine that LTHE and LTEtOAc-F had bactericidal effects against C. michiganensis sbsp. michiganensis, P. syringae, and X. campestris, since the ratio was 2 for all strains.

4. Discussion

In the present study, an antibiotic sensitivity test was performed with C. michiganensis subsp michiganensis, P. syringae, and X. campestris strains. The obtained data show that C. michiganensis subsp. michiganensis was resistant to 13 antimicrobials (amikacin, ampicillin, carbenicillin, cephalothin, cefotaxime, chloramphenicol, erythromycin, gentamicin, netilmicin, nitrofurantoin, penicillin sulfamethoxazole/trimethoprim, and vancomycin); X. campestris was resistant to 9 (ampicillin, cephalothin, cefotaxime, ciprofloxacin, dicloxacillin, gentamicin, netilmicin, nitrofurantoin, and norfloxacin); and P. syringae was resistant to 8 (cephalothin, cefotaxime, clindamycin, dicloxacillin, erythromycin, penicillin, sulfamethoxazole/trimethoprim, and vancomycin).
According to these results, all strains were classified as multidrug-resistant. López-Pueyo et al. (2011) noted that a bacterial strain can be considered to be in this category when it presents resistance to more than one family of antibiotics, such as C. michiganensis subsp michiganensis. Specifically for Gram-negative bacilli, it must be resistant to three or more families of antibiotics to which they are usually sensitive, such as beta-lactams, carbapenems, aminoglycosides, or quinolones, which was shown by P. syringae and X. campestris in the present study [56].
Antimicrobial resistance is a worldwide concern that involves not only human and animal bacteria, but also phytopathogenic bacterial strains. It has been reported that the overuse of antibiotics in crops, such as streptomycin, has led to the emergence of resistant phytopathogenic strains, and the severity of the issue has increased. According to the data obtained in the present study, phytopathogenic bacteria showed resistance to antibacterial agents that are not used in agricultural crops [10].
This problem may arise in association with the use of wastewater. Some studies reported that Mexico is among the countries that irrigate agricultural lands with untreated residual water (approximately 387,600 h per year). Some research reported the presence of pollutant organic materials, metals, detergents, antibiotics, and bacteria in residual water, which can cause public health problems and soil degradation, and promote antibiotic resistance in crops [57].
In some studies around the world, it was reported that wastewater treatment plants release antibiotics into the environment. In this sense, Bougnom et al. (2019) suggested that wastewater is associated with the generation and dissemination of antibiotic resistance, since drug-resistant plasmids and antibiotic resistance genes have been identified in wastewater. These genes may encode resistance to trimethoprim, aminoglycosides, β-lactams, macrolides, quinolones, amphenicols, and sulphonamides, which could explain the profiles of resistance to antimicrobials reported in the present study [58,59,60].
The results of antibiotic sensitivity testing demonstrate the emergence of multi-drug-resistant phytopathogenic strains for which treatment options are limited. In this sense, the hydroalcoholic extract of L. tridentata and its organic fraction showed important antibacterial activity.
The antibacterial activity of L. tridentata was previously reported Mendez et al. (2012) evaluated four L. tridentata leaf extracts (water, ethanol, cocoa butter, and lanolin), and their results revealed that ethanolic extract showed the same activity against Gram-positive and Gram-negative bacteria, similar to the activity observed in our study, with equal MIC and MBC determined for C. michiganensis subsp michiganensis and P. syringae [61].
In another study, Martins et al. (2013) evaluated the antibacterial activity of crude methanolic extract against both Gram-positive and Gram-negative bacteria. They determined a concentration range (MIC) from 62.5 to 250 µg/mL, lower concentrations than those reported in our study (0.39–6.25 mg/mL). Similarly, Snowden et al. (2014) evaluated L. tridentata extract (leaves and flowers) against S. aureus and obtained MIC of 60 µg/mL [42,43].
Gerstel et al. (2018) tested antibacterial activity against nonantibiotic-resistant and antibiotic-resistant Gram-positive strains, determining an MIC range from 0.35 to 15 µg/mL for L. tridentata extract; even though these results cannot be compared with ours, the activity of the species against drug-resistant bacterial strains supports our results [47].
The data obtained in all of these studies support our results, despite the determination of different concentrations. In this sense, it has been reported that solvents used during the extraction process have an influence on the nature and amount of secondary metabolites extracted from medicinal plants. In addition, the yield of extraction depends not only on the solvent, but on the pH, temperature, extraction time, and composition of the sample, and this could explain the different concentrations determined between the studies discussed and the present research [62,63].
L. tridentata aqueous fraction only showed inhibitory activity against C. michiganensis subsp michiganensis and P. syringae (6.25 mg/mL). Organic fraction (ethyl acetate) showed better activity than LTHE and LTAq-F, with an MIC of 3.12 mg/mL against both C. michiganensis subsp michiganensis and P. syringae, and a concentration of 0.39 mg/mL for X. campestris.
Martins et al. (2013) evaluated the antibacterial activity of L. tridentata methanolic extract and ethyl acetate fraction and determined lower concentrations for the organic fraction. Other studies also determined lower concentrations when ethyl acetate fractions were evaluated, such as those performed by Olmedo-Juarez et al. (2019) and González-Alamilla et al. (2019), which showed lower concentrations of Caesalpinia coriaria and Salix babylonica ethyl acetate fractions against a wide range of Gram-positive and Gram-negative bacterial strains than those obtained with hydroalcoholic extracts [42,51,52].
Cartaya and Reynaldo (2001) and Martínez-Aguilar et al. (2012) explained that, due to the polarity of ethyl acetate, better extraction could be performed, with higher concentrations of bioactive compounds. Similarly, Gomez-Guiñán et al. (2003) reported that medium and low polarity compounds eluted using ethyl acetate could pass easily through bacterial cell walls, which could explain why better activity was observed with the L. tridentata organic fraction [64,65,66].
With respect to the minimal bactericidal concentrations, obtained in the present study, it was observed that LTHE showed bactericidal activity, with a concentration of 12.5 mg/mL, against C. michiganensis sbsp. michiganensis and P. syringae, and a concentration of 0.78 mg/mL for X. campestris. The aqueous fraction did not show any bactericidal effects, while the organic fraction exhibited bactericidal effects on all the evaluated strains, showing MBC values ranging from 0.78 to 6.25 mg/mL.
In the studies carried out by Snowden et al. (2014) and Gerstel et al. (2018), bactericidal effects of L. tridentata were observed, but they did not report at which concentrations the activity was determined. The current lack of studies in which the MBC values of plant extracts or fractions are determined limit the discussion of our results [43,47].
The use of bactericidal agents is desirable and preferred, since killing the bacteria allows the infection to be eliminated, and most importantly, minimizes the possible emergence of resistance and the spread of infections; in this sense, L. tridentata represents a promising alternative treatment for phytopathogenic bacteria [8,67].
As can be seen, several studies evaluated the antibacterial activity of L. tridentata; in some of them, the secondary metabolites associated with its antibacterial activity are reported. The chemical composition of L. tridentata indicates the presence of terpenes, saponins, tannins, quercetin, kaempferol, ellagic acid, gallic acid, methyl gallate, resorcinol, cinnamic acid, catechins, and lignans [19,42,45,61,68,69,70,71].
Determining the tannin content revealed that L. tridentata contains 17.3769 and 37.153 mg/g of hydrolyzable and condensed tannins, respectively; also quantified was a thymol concentration of 4.3033 and a carvacrol concentration of 7.7986 mg/mL. In addition, the total phenolic compounds were estimated, determining an amount of 237.60 mg/GAE/g dry wt. plant in ethanolic extract (70%). Other studies determined the content of quercetin, kaempferol, and Nordihydroguaiaretic acid (NDGA) in methanolic extracts and ethyl acetate fractions, determining concentrations of 8.67, 21.52, and 35.72, and 8.45, 11.89 and 16.51 mg of plant material, respectively [42,45,61,69].
Other studies stated that major antibacterial activity of L. tridentata is associated with the presence of lignans, and some of them determined the mechanism of action. Favela-Hernández et al. (2012) reported that the antibacterial activity of chloroform extract from L. tridentata leaves was conferred by a lignan identified as 3-demethoxy-6-O-demethylisoguaiacin. The authors reported that the compound is able to affect proteins of the ATP binding cassette transport system, causing bacterial death. Clemente-Soto et al. (2014) determined that MDGA caused membrane destabilization and consequently death of Mycobacterium tuberculosis, and similar activity was reported by Guzmán-Beltrán et al. (2016); these authors found that NDGA in high concentrations inhibited the growth of M. tuberculosis [40,41,48,49].
Similarly, Cunningham-Oakes et al. (2015) [44] evaluated the antibacterial activity of NDGA in combination with a commercial antibiotic against Staphylococcus aureus, obtaining promising results; this lignan enhanced the antibacterial activity of the commercial antibiotic due to its capacity to damage the bacterial cell membrane. Gnabre et al. (2015) [72] stated that the use of L. tridentata lignans could be a way to treat and prevent new diseases, some of which have no cure to date.
According to these reports, we suggest that the antibacterial activity of hydroalcoholic extract and organic fraction of L. tridentata could be associated with the presence of lignans, which may exhibit similar mechanisms of action. However, further studies should be performed to identify the bioactive compounds associated with the antibacterial activity reported in the present study.

5. Conclusions

To date, there are no studies reporting the antibacterial activity of L. tridentata against multidrug-resistant phytopathogenic bacteria. The present study shows that LTHE and its organic fraction have bactericidal activity in vitro against Clavibacter michiganensis sbsp. michiganensis, Pseudomonas syringae, and Xanthomonas campestris, bacteria that affect tomato (Solanum lycopersicum L.) crops. Better results were obtained against X. campestris. Therefore, the hydroalcoholic extract of Larrea tridentata and its organic fraction could be used as an alternative treatment against diseases caused by these bacteria in crops. However, it is necessary to carry out tests in situ.

Author Contributions

Conceptualization and methodology, N.R.-P., A.L.M.-U., E.A.-T. and A.Z.-B.; validation and formal analysis, N.R.-P., A.Z.-B., A.L.M.-U. and J.P.-M.; investigation and resources, N.R.-P. and A.Z.-B.; data curation, A.Z.-B., A.L.M.-U. and F.A.-R.; writing—original draft preparation, A.L.M.-U., H.F.H. and N.R.-P.; writing—review and editing, A.Z.-B., F.A.-R., E.A-T. and G.E.-S.B.; supervision, N.R.-P. and A.Z.-B.; project administration, N.R.-P. and A.Z.-B.; funding acquisition, N.R.-P. and A.Z.-B. All authors have read and agreed to the published version of the manuscript.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sector.

Data Availability Statement

Not applicable.

Acknowledgments

The authors would like to acknowledge the Universidad Autónoma del Estado de Hidalgo (UAEH) for the support provided to carry out the study at its facilities. This study forms part of the thesis of Ana Lizet Ubaldo Morales (Maestría en Ciencias y Tecnología Agrícola y Forestal Sustentable, Universidad Autónoma del Estado de Hidalgo).

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Food and Agriculture Organization (FAO). México Ante el Desafío del Cambio Climático. Available online: https://www.google.com/url?sa=t&rct=j&q=&esrc=s&source=web&cd=1&cad=rja&uact=8&ved=2ahUKEwjN0NWd5MTlAhUCba0KHbGpBbIQFjAAegQIAhAC&url=http%3A%2F%2Fwww.fao.org%2F3%2Fa-i4093s.pdf&usg=AOvVaw07YIaI-PTHin1zf0D3bY-A (accessed on 17 February 2021).
  2. Food and Agriculture Organization (FAO). Sustainable Small-Scale Livestock Production. Available online: http://www.fao.org/3/ca7660en/CA7660EN.pdf (accessed on 17 February 2021).
  3. Du, Y.Z.; Wood, L.L.; Saavedra, S.S. Growth behavior and structure of alkyltrichlorosilane monolayers bearing thioacetate and acetate tailgroups. Mater. Sci. Eng. C 1999, 7, 161–169. [Google Scholar] [CrossRef]
  4. Wang, Y.; Zhang, Y.; Gao, Z.; Yang, W. Breeding for Resistance to Tomato Bacterial Diseases in China: Challenges and Prospects. Hortic. Plant J. 2018, 4, 193–207. [Google Scholar] [CrossRef]
  5. Jones, J.; Lacy, G.H.; Bouzar, H.; Minsavage, G.; Stall, R.; Schaad, N.W. Bacterial Spot—Worldwide Distribution, Importance and Review. Acta Hortic. 2004, 695, 27–234. [Google Scholar] [CrossRef]
  6. Preston, G.M. Pseudomonas syringae pv. tomato: The right pathogen, of the right plant, at the right time. Mol. Plant Pathol. 2000, 1, 263–275. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  7. Kolomiets, J.V.; Grygoryuk, I.P.; Butsenko, L.M. Bacterial diseases of tomato plants in terms of open and covered growing of Ukraine. Ann. Agrar. Sci. 2017, 15, 213–216. [Google Scholar] [CrossRef]
  8. Soberón, J.R.; Sgariglia, M.A.; Dip Maderuelo, M.R.; Andina, M.L.; Sampietro, D.A.; Vattuone, M.A. Antibacterial activities of Ligaria cuneifolia and Jodina rhombifolia leaf extracts against phytopathogenic and clinical bacteria. J. Biosci. Bioeng. 2014, 118, 599–605. [Google Scholar] [CrossRef]
  9. Griffin, K.; Gambley, C.; Brown, P.; Li, Y. Copper-tolerance in Pseudomonas syringae pv. tomato and Xanthomonas spp. and the control of diseases associated with these pathogens in tomato and pepper. A systematic literature review. J. Crop Prot. 2017, 96, 144–150. [Google Scholar] [CrossRef]
  10. McManus, P.S.; Stockwell, V.O.; Sundin, G.W.; Jones, A.L. Antibiotic use in plant agriculture. Annu. Rev. Phytopathol. 2002, 40, 443–465. [Google Scholar] [CrossRef] [PubMed]
  11. da Silva, R.S.; de Oliveira, M.M.G.; de Melo, J.O.; Blank, A.F.; Corrêa, C.B.; Scher, R. Antimicrobial activity of Lippia gracilis essential oils on the plant pathogen Xanthomonas campestris pv. campestris and their effect on membrane integrity. Pestic. Biochem. Phys. 2019, 160, 40–48. [Google Scholar] [CrossRef]
  12. Lazarovits, G.; Turnbull, A.; Johnston-Monje, D. Plant Health Management: Biological Control of Plant Pathogens. In Encyclopedia of Agriculture and Food Systems; Van-Alfen, N.K., Ed.; Academic Press: Oxford, UK, 2014; pp. 388–399. [Google Scholar]
  13. Shaheen, H.A.; Issa, M.Y. In vitro and in vivo activity of Peganum harmala L. alkaloids against phytopathogenic bacteria. Sci. Hortic. 2020, 264, 1–10. [Google Scholar] [CrossRef]
  14. Marutescu, L.; Popa, M.; Saviuc, C.; Lazar, V.; Chifiriuc, M.C. 8—Botanical pesticides with virucidal, bactericidal, and fungicidal activity. In New Pesticides and Soil Sensors; Grumezescu, A.M., Ed.; Academic Press: San Diego, CA, USA, 2017; pp. 311–335. [Google Scholar]
  15. Woodson, R.E.; Schery, R.W.; Porter, D.M. Flora of Panama: Part VI. Family 88. Zygophyllaceae. Ann. Mo. Bot. Gard. 1969, 56, 1–7. [Google Scholar] [CrossRef]
  16. Ross, I.A. Chemical constituents, traditional and modern medicinal uses. In Medicinal Plants of the World; Springer’s Humana Press: Totowa, NJ, USA, 2007; Volume 3. [Google Scholar]
  17. Lira-Saldívar, R.H. Estado Actual del Conocimiento sobre las Propiedades Biocidas de la Gobernadora [Larrea tridentata (D.C.) Coville]. Rev. Mex. Fitopatol. 2003, 21, 214–222. [Google Scholar]
  18. Arteaga, S.; Andrade-Cetto, A.; Cárdenas, R. Larrea tridentata (Creosote bush), an abundant plant of Mexican and US-American deserts and its metabolite nordihydroguaiaretic acid. J. Ethnopharmacol. 2005, 98, 231–239. [Google Scholar] [CrossRef] [PubMed]
  19. Martins, S.; Mussatto, S.I.; Aguilar, C.N.; Teixeira, J.A. Antioxidant capacity and NDGA content of Larrea tridentata (a desert bush) leaves extracted with different solvents. J. Biotechnol. 2010, 150, 500. [Google Scholar] [CrossRef]
  20. Xue, H.; Zhang, X.-Y.; Liu, J.M.; Song, Y.; Liu, T.T.; Chen, D. NDGA reduces secondary damage after spinal cord injury in rats via anti-inflammatory effects. Brain Res. 2013, 1516, 83–92. [Google Scholar] [CrossRef]
  21. Rahman, S.; Ansari, R.A.; Rehman, H.; Parvez, S.; Raisuddin, S. Nordihydroguaiaretic Acid from Creosote Bush (Larrea tridentata) Mitigates 12-O-Tetradecanoylphorbol-13-Acetate-Induced Inflammatory and Oxidative Stress Responses of Tumor Promotion Cascade in Mouse Skin. Evid. Based Complement. Altern. Med. 2011, 2011, 1–11. [Google Scholar] [CrossRef] [Green Version]
  22. Aguirre-Joya, J.A.; Pastrana-Castro, L.; Nieto-Oropeza, D.; Ventura-Sobrevilla, J.; Rojas-Molina, R.; Aguilar, C.N. The physicochemical, antifungal and antioxidant properties of a mixed polyphenol based bioactive film. Heliyon 2018, 4, e00942. [Google Scholar] [CrossRef] [Green Version]
  23. Skouta, R.; Morán-Santibañez, K.; Valenzuela, C.A.; Vasquez, A.H.; Fenelon, K. Assessing the Antioxidant Properties of Larrea tridentata Extract as a Potential Molecular Therapy against Oxidative Stress. Molecules 2018, 23, 1826. [Google Scholar] [CrossRef] [Green Version]
  24. Morán-Santibañez, K.; Vasquez, A.H.; Varela-Ramirez, A.; Henderson, V.; Sweeney, J.; Odero-Marah, V. Larrea tridentata Extract Mitigates Oxidative Stress-Induced Cytotoxicity in Human Neuroblastoma SH-SY5Y Cells. Antioxidants 2019, 8, 427. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  25. Probst, L.; Dächert, J.; Schenk, B.; Fulda, S. Lipoxygenase inhibitors protect acute lymphoblastic leukemia cells from ferroptotic cell death. Biochem. Pharmacol. 2017, 140, 41–52. [Google Scholar] [CrossRef]
  26. Zhang, L.J.; Wu, J.; Xing, D.M.; Liu, Y.; Jia, F.H.; Li, D.T. Nordihydroguaiaretic Acid (NDGA) Promotes Functional Recovery after Transient Focal Cerebral Ischemia in Rats. Lat. Am. J. Pharm. 2014, 33, 994–1000. [Google Scholar]
  27. Siddique, Y.H.; Ali, F. Protective effect of nordihydroguaiaretic acid (NDGA) on the transgenic Drosophila model of Alzheimer’s disease. Chem. Biol. Interact. 2017, 269, 59–66. [Google Scholar] [CrossRef]
  28. Tovar-Carrillo, K.L.; Saucedo-Acuña, R.A.; Ríos-Arana, J.; Tamayo, G.; Guzmán-Gastellum, D.A.; Díaz-Torres, B.A. Synthesis, Characterization, and In Vitro and In Vivo Evaluations of Cellulose Hydrogels Enriched with Larrea tridentata for Regenerative Applications. Biomed. Res. Int. 2020, 2020, 1–10. [Google Scholar] [CrossRef] [PubMed]
  29. Del Vecchyo-Tenorio, G.; Rodríguez-Cruz, M.; Andrade-Cetto, A.; Cárdenas-Vázquez, R. Creosote Bush (Larrea tridentata) Improves Insulin Sensitivity and Reduces Plasma and Hepatic Lipids in Hamsters Fed a High Fat and Cholesterol Diet. Front. Pharmacol. 2016, 7, 194. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  30. Han, L.; Bittner, S.; Dong, D.; Cortez, Y.; Dulay, H.; Arshad, S. Creosote bush-derived NDGA attenuates molecular and pathological changes in a novel mouse model of non-alcoholic steatohepatitis (NASH). Mol. Cell. Endocrinol. 2019, 498, 110538. [Google Scholar] [CrossRef] [PubMed]
  31. Chan, J.K.W.; Bittner, S.; Bittner, A.; Atwal, S.; Shen, W.J.; Inayathullah, M. Nordihydroguaiaretic Acid, a Lignan from Larrea tridentata (Creosote Bush), Protects Against American Lifestyle-Induced Obesity Syndrome Diet-Induced Metabolic Dysfunction in Mice. J. Pharmacol. Exp. Ther. 2018, 365, 281–290. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  32. Zuntilde, A.; Tapia, E.; Zazueta, C.; Correa, F.; Zatarain-Barron, Z.L.; Hernandez, P.R. Nordihydroguaiaretic acid pretreatment prevents ischemia and reperfusion induced renal injury, oxidant stress and mitochondrial alterations. J. Med. Plant Res. 2012, 6, 2938–2947. [Google Scholar]
  33. Rojo, A.I.; Medina-Campos, O.N.; Rada, P.; Zúñiga-Toalá, A.; López-Gazcón, A.; Espada, S. Signaling pathways activated by the phytochemical nordihydroguaiaretic acid contribute to a Keap1-independent regulation of Nrf2 stability: Role of glycogen synthase kinase-3. Free Radic. Biol. Med. 2012, 52, 473–487. [Google Scholar] [CrossRef] [PubMed]
  34. Pollara, J.J.; Laster, S.M.; Petty, I.T.D. Inhibition of poxvirus growth by Terameprocol, a methylated derivative of nordihydroguaiaretic acid. Antivir. Res. 2010, 88, 287–295. [Google Scholar] [CrossRef] [PubMed]
  35. Castillo, F.; Hernández, D.; Gallegos, G.; Mendez, M.; Rodríguez, R.; Reyes, A. In vitro antifungal activity of plant extracts obtained with alternative organic solvents against Rhizoctonia solani Kühn. Ind. Crop. Prod. 2010, 32, 324–328. [Google Scholar] [CrossRef]
  36. Osorio, E.; Flores, M.; Hernández, D.; Ventura, J.; Rodríguez, R.; Aguilar, C.N. Biological efficiency of polyphenolic extracts from pecan nuts shell (Carya Illinoensis), pomegranate husk (Punica granatum) and creosote bush leaves (Larrea tridentata Cov.) against plant pathogenic fungi. Ind. Crop. Prod. 2010, 31, 153–157. [Google Scholar] [CrossRef]
  37. Chávez-Solís, A.L.; Pedroza-Sandoval, A.; Nava-Díaz, C.; Cano-Rios, P.; Castro-Franco, R. Control de la cenicilla del melón (Podosphaera xanthii) mediante el uso de extracto de Larrea tridentata (D.C.) Coville (L.). Rev. Chapingo Ser. Zonas Áridas 2014, 13, 103–113. [Google Scholar] [CrossRef] [Green Version]
  38. Valero Galván, J.; González-Díaz, C.A.; González-Fernández, R. Efecto de los extractos acuosos de hojas de plantas de gobernadora (Larreas tridentata), hojasen (Flourensia cernua) y encino (Quercus pungens), sobre el crecimiento micelial in vitro de hongos fitopatógenos. Acta Univ. 2014, 24, 13–19. [Google Scholar]
  39. Bashyal, B.; Li, L.; Bains, T.; Debnath, A.; LaBarbera, D.V. Larrea tridentata: A novel source for anti-parasitic agents active against Entamoeba histolytica, Giardia lamblia and Naegleria fowleri. PLoS Negl. Trop. Dis. 2017, 11, e0005832. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  40. Favela-Hernández, J.M.; García, A.; Garza-González, E.; Rivas-Galindo, V.M.; Camacho-Corona, M.R. Antibacterial and antimycobacterial lignans and flavonoids from Larrea tridentata. Phytother. Res. 2012, 26, 1957–1960. [Google Scholar] [CrossRef] [PubMed]
  41. Favela-Hernández, J.M.; Clemente-Soto, A.F.; Balderas-Rentería, I.; Garza-González, E.; Camacho-Corona, M.D.R. Potential mechanism of action of 3’-demethoxy-6-O-demethyl-isoguaiacin on methicillin resistant Staphylococcus aureus. Molecules 2015, 20, 12450–12458. [Google Scholar] [CrossRef]
  42. Martins, S.; Amorim, E.L.C.; Sobrinho, T.J.S.P.; Saraiva, A.M.; Pisciottano, M.N.C.; Aguilar, C.N. Antibacterial activity of crude methanolic extract and fractions obtained from Larrea tridentata leaves. Ind. Crop. Prod. 2013, 41, 306–311. [Google Scholar] [CrossRef] [Green Version]
  43. Snowden, R.; Harrington, H.; Morrill, K.; Jeane, L.; Garrity, J.; Orian, M. A comparison of the anti-Staphylococcus aureus activity of extracts from commonly used medicinal plants. J. Altern. Complement. Med. 2014, 20, 375–382. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  44. Cunningham-Oakes, E.; Soren, O.; Moussa, C.; Rathor, G.; Liu, Y.; Coates, A. Nordihydroguaiaretic acid enhances the activities of aminoglycosides against methicillin-sensitive and resistant Staphylococcus aureus in vitro and in vivo. Front. Microbiol. 2015, 6, 1195. [Google Scholar] [CrossRef] [Green Version]
  45. Delgadillo-Ruiz, L.; Bañuelos-Valenzuela, R.; Delgadillo-Ruiz, O.; Silva-Vega, M.; Gallegos-Flores, P. Chemical composition and antibacterian effect in vitro of extracts of Larrea tridentata, Origanum vulgare, Artemisa ludoviciana and Ruta graveolens. Nova Sci. 2017, 9, 273–290. [Google Scholar] [CrossRef] [Green Version]
  46. Reyes-Melo, K.; García, A.; Romo-Mancillas, A.; Garza-González, E.; Rivas-Galindo, V.M.; Miranda, L.D. Meso-Dihydroguaiaretic acid derivatives with antibacterial and antimycobacterial activity. Bioorg. Med. Chem. 2017, 25, 5247–5259. [Google Scholar] [CrossRef] [PubMed]
  47. Gerstel, J.; Turner, T.; Ruiz, G.; Wise, J.; Stein, A.; Jones, G. Identification of botanicals with potential therapeutic use against methicillin-resistant Staphylococcus aureus (MRSA) infections. Phytother. Res. 2018, 32, 2577–2585. [Google Scholar] [CrossRef] [PubMed]
  48. Clemente-Soto, A.F.; Balderas-Rentería, I.; Rivera, G.; Segura-Cabrera, A.; Garza-González, E.; del Rayo Camacho-Corona, M. Potential mechanism of action of meso-dihydroguaiaretic acid on Mycobacterium tuberculosis H37Rv. Molecules 2014, 19, 20170–20182. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  49. Guzmán-Beltrán, S.; Rubio-Badillo, M.Á.; Juárez, E.; Hernández-Sánchez, F.; Torres, M. Nordihydroguaiaretic acid (NDGA) and α-mangostin inhibit the growth of Mycobacterium tuberculosis by inducing autophagy. Int. Immunopharmacol. 2016, 31, 149–157. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  50. Rivero-Perez, N.; Hernández-Alvarado, J.L.; Valladares-Carranza, B.; Delgadillo-Ruiz, L.; Ojeda-Ramírez, D.; Sosa-Gutiérrez, C.G.; Morales-Ubaldo, A.L.; Vega-Sánchez, V.; Zaragoza- Bastida, A. Salix babylonica L. as a Natural Anticoccidial Alternative in Growing Rabbits. Evid. Based Complement. Altern. Med. 2019, 2019, 1–10. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  51. González-Alamilla, E.N.; Gonzalez-Cortazar, M.; Valladares-Carranza, B.; Rivas-Jacobo, M.A.; Herrera-Corredor, C.A.; Ojeda-Ramírez, D.; Zaragoza-Bastida, A.; Rivero-Perez, N. Chemical Constituents of Salix babylonica L. and their Antibacterial Activity Against Gram-Positive and Gram-Negative Animal Bacteria. Molecules 2019, 24, 2992. [Google Scholar] [CrossRef] [Green Version]
  52. Olmedo-Juárez, A.; Briones-Robles, T.I.; Zaragoza-Bastida, A.; Zamilpa, A.; Ojeda-Ramírez, D.; Mendoza de Gives, P.; Olivarez-Pérez, J.; Rivero-Perez, N. Antibacterial activity of compounds isolated from Caesalpinia coriaria (Jacq) Willd against important bacteria in public health. Microb. Pathog. 2019, 136, 103–660. [Google Scholar] [CrossRef] [PubMed]
  53. Rangel-López, L.; Zaragoza-Bastida, A.; Valladares-Carranza, B.; Peláez-Acero, A.; Sosa-Gutiérrez, C.G.; Hetta, H.F.; Batiha, G.E.S.; Alqahtani, A.; Rivero-Perez, N. In Vitro Antibacterial Potential of Salix babylonica Extract against Bacteria that Affect Oncorhynchus mykiss and Oreochromis spp. Animals 2020, 10, 1340. [Google Scholar] [CrossRef] [PubMed]
  54. Clinical and Laboratory Standards Institute. Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria that Grow Aerobically; Approved Standards; CLSI Document M7-A5; CLSI: Wayne, PA, USA, 2012. [Google Scholar]
  55. Zaragoza-Bastida, A.; Flores-Aguilar, S.C.; Aguilar-Castro, L.M.; Morales-Ubaldo, A.L.; Valladares-Carranza, B.; Rangel-López, L.; Olmedo-Juárez, A.; Rosenfeld-Miranda, C.E.; Rivero-Perez, N. Antibacterial and Hemolytic Activity of Crotalus Triseriatus and Crotalus Ravus Venom. Animals 2020, 10, 281. [Google Scholar] [CrossRef] [Green Version]
  56. López-Pueyo, M.J.; Barcenilla-Gaite, F.; Amaya-Villar, R.; Garnacho-Montero, J. Multirresistencia antibiótica en unidades de críticos. Med. Intensiv. 2011, 35, 41–53. [Google Scholar] [CrossRef]
  57. García-Salazar, E.M. El agua residual como generadora del espacio de la actividad agrícola en el Valle del Mezquital, Hidalgo, México. Estud. Soc. REVISTA Aliment. Contemp. Desarro. Reg. 2019, 29, 2–34. [Google Scholar] [CrossRef]
  58. Michael, I.; Rizzo, L.; McArdell, C.S.; Manaia, C.M.; Merlin, C.; Schwartz, T.; Dagot, C.; Fatta-Kassinos, D. Urban wastewater treatment plants as hotspots for the release of antibiotics in the environment: A review. Water Res. 2013, 47, 957–995. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  59. Bougnom, B.P.; Zongo, C.; McNally, A.; Ricci, V.; Etoa, F.X.; Thiele-Bruhn, S.; Piddock, L.J.V. Wastewater used for urban agriculture in West Africa as a reservoir for antibacterial resistance dissemination. Environ. Res. 2019, 168, 14–24. [Google Scholar] [CrossRef] [PubMed]
  60. Bougnom, B.P.; McNally, A.; Etoa, F.X.; Piddock, L.J.V. Antibiotic resistance genes are abundant and diverse in raw sewage used for urban agriculture in Africa and associated with urban population density. Environ. Pollut. 2019, 251, 146–154. [Google Scholar] [CrossRef] [PubMed]
  61. Mendez, M.; Rodríguez, R.; Ruiz, J.; Morales-Adame, D.; Castillo, F.; Hernández-Castillo, F.D.; Aguilar, C.N. Antibacterial activity of plant extracts obtained with alternative organics solvents against food-borne pathogen bacteria. Ind. Crop. Prod. 2012, 37, 445–450. [Google Scholar] [CrossRef]
  62. Dirar, A.I.; Alsaadi, D.H.M.; Wada, M.; Mohamed, M.A.; Watanabe, T.; Devkota, H.P. Effects of extraction solvents on total phenolic and flavonoid contents and biological activities of extracts from Sudanese medicinal plants. S. Afr. J. Bot. 2019, 120, 261–267. [Google Scholar] [CrossRef]
  63. Do, Q.D.; Angkawijaya, A.E.; Tran-Nguyen, P.L.; Huynh, L.H.; Soetaredjo, F.E.; Ismadji, S.; Yi-Hsu, J. Effect of extraction solvent on total phenol content, total flavonoid content, and antioxidant activity of Limnophila aromatica. J. Food Drug Anal. 2014, 22, 296–302. [Google Scholar] [CrossRef] [Green Version]
  64. Cartaya, O.; Reynaldo, I. Flavonoides: Características químicas y aplicaciones. Cult. Trop. 2001, 22, 5–14. [Google Scholar]
  65. Martínez- Aguilar, Y.; Soto-Rodríguez, F.; Almeida-Saavedra, M.; Hermosilla-Espinosa, R.; Martínez-Yero, O. Metabolitos secundarios y actividad antibacteriana in vitro de extractos de hojas de Anacardium occidentale L. (marañón). Rev. Cuba. Plantas Med. 2012, 17, 320–329. [Google Scholar]
  66. Gómez-Guiñán, Y.; Hidalgo, J.; Jiménez, M.; Salcedo, J. Obtención de extractos orgánicos con actividad antimicrobiana a partir de Penicillium sp. (Moniliales) aislado de la esponja Ircinia felix (Porifera: Demospongiae). Rev. Biol. Trop. 2003, 51, 141–147. [Google Scholar]
  67. Rivas-Cáceres, R.R.; Luis Stephano-Hornedo, J.; Lugo, J.; Vaca, R.; Del Aguila, P.; Yañez-Ocampo, G.; Mora-Herrera, M.E.; Camacho-Díaz, L.M.; Cipriano-Salazar, M.; Alaba, P.A. Bactericidal effect of silver nanoparticles against propagation of Clavibacter michiganensis infection in Lycopersicon esculentum Mill. Microb. Pathog. 2018, 115, 358–362. [Google Scholar] [CrossRef] [PubMed]
  68. Bañuelos-Valenzuela, R.; Delgadillo-Ruiz, L.; Echavarría-Cháirez, F.; Delgadillo-Ruiz, O.; Meza-López, C. Composición química y FTIR de extractos etanólicos de Larrea tridentata, Origanum vulgare, Artemisa ludoviciana y Ruta graveolens. Agrociencia 2018, 52, 309–321. [Google Scholar]
  69. Martins, S.; Aguilar, C.N.; Teixeira, J.A.; Mussatto, S.I. Bioactive compounds (phytoestrogens) recovery from Larrea tridentata leaves by solvents extraction. Sep. Purif. Technol. 2012, 88, 163–167. [Google Scholar] [CrossRef] [Green Version]
  70. Ruiz, J.; Ascacio-Valdés, J.; Rodriguez, R.; Morales, D.; Aguilar, C. Phytochemical screening of extracts from some Mexican plants used in traditional medicine. J. Med. Plants 2011, 5, 2791–2797. [Google Scholar]
  71. Ascacio-Valdés, J.A.; Aguilera-Carbó, A.; Rodríguez-Herrera, R.; Aguilar-González, C. Análisis de ácido elágico en algunas plantas del semidesierto Mexicano. Rev. Mex. Cienc. Farm. 2013, 44, 36–40. [Google Scholar]
  72. Gnabre, J.; Bates, R.; Huang, R.C. Creosote bush lignans for human disease treatment and prevention: Perspectives on combination therapy. J. Tradit. Complement. Med. 2015, 5, 119–126. [Google Scholar] [CrossRef] [Green Version]
Table
Table 1. Inhibition halos (mm) and antibiotic sensitivity of C. michiganensis sbsp. michiganensis, P. syringae, and X. campestris.
Table 1. Inhibition halos (mm) and antibiotic sensitivity of C. michiganensis sbsp. michiganensis, P. syringae, and X. campestris.
AntimicrobialBacteria
C. michiganensis subsp. MichiganensisP. syringaeX. campestris
Amikacin10 (R)20 (S)15 (I)
Ampicillin7 (R)15 (S)7 (R)
Carbenicillin7 (R)16 (I)22(S)
Cephalothin7 (R)11 (R)7 (R)
Cefotaxime7 (R)7 (R)7 (R)
Ciprofloxacin30 (S)30 (S)7 (R)
Clindamycin15 (I)7 (R)34 (S)
Chloramphenicol8 (R)31 (S)30 (S)
Dicloxacillin12 (I)7 (R)7 (R)
Erythromycin7 (R)7 (R)23 (S)
Gentamicin7 (R)21 (S)12 (R)
Netilmicin8 (R)20 (S)10 (R)
Nitrofurantoin9 (R)22 (S)8 (R)
Norfloxacin15 (I)20 (S)7 (R)
Penicillin7 (R)7 (R)22 (S)
Sulfamethoxazole/trimethoprim7 (R)7 (R)17 (S)
Tetracycline20 (S)20 (S)20 (S)
Vancomycin7 (R)7 (R)21 (S)
R, resistant; I, intermediate; S, sensitive.
Table
Table 2. Minimal inhibitory concentration (mg/mL) of hydroalcoholic extract and fractions obtained from Larrea tridentata.
Table 2. Minimal inhibitory concentration (mg/mL) of hydroalcoholic extract and fractions obtained from Larrea tridentata.
Evaluated TreatmentBacteria
C. michiganensis sbsp. MichiganensisP. syringaeX. campestrisp-Value
LTHE6.25 cB6.25 cB0.39 bA0.0001
LTAq-F6.25 cA6.25 cANA0.0001
LTEtOAc-F3.12 bB3.12 bB0.39 bA0.0001
Kanamycin0.25 a*0.25 a*8 a*
p-value0.00010.00010.0001
NA, no activity; LTHE, L. tridentata hydroalcoholic extract; LTAq-F, aqueous fraction; LTEtOAc-F, organic fraction. * Values are expressed in µg/mL. a,b,c Different letters in columns indicate significant statistical differences (p ≤ 0.05) between treatments, A,B Different letters in rows indicate significant statistical differences (p ≤ 0.05) between bacteria.
Table
Table 3. Minimal bactericidal concentrations (mg/mL) of extract and fractions obtained from Larrea tridentata.
Table 3. Minimal bactericidal concentrations (mg/mL) of extract and fractions obtained from Larrea tridentata.
Evaluated TreatmentBacteria
C. nichiganensis sbsp. MichiganensisP. syringaeX. campestrisp-Value
LTHE12.5 cB12.5 cB0.78 bA0.0001
LTAq-FNANANA
LTEtOAc-F6.25 bB6.25 bB0.78 bA0.0001
Kanamycin0.5 a*0.5 a*16 a*
p-value0.00010.00010.0001
NA, no activity; LTHE, L. tridentata hydroalcoholic extract; LTAq-F, aqueous fraction; LTEtOAc-F, organic fraction. * Values are expressed in µg/mL. a,b,c Different letters in columns indicate significant statistical differences (p ≤ 0.05) between treatments. A,B Different letters in rows indicate significant statistical differences (p ≤ 0.05) between bacteria.
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Morales-Ubaldo, A.L.; Rivero-Perez, N.; Avila-Ramos, F.; Aquino-Torres, E.; Prieto-Méndez, J.; Hetta, H.F.; El-Saber Batiha, G.; Zaragoza-Bastida, A. Bactericidal Activity of Larrea tridentata Hydroalcoholic Extract against Phytopathogenic Bacteria. Agronomy 2021, 11, 957. https://doi.org/10.3390/agronomy11050957

AMA Style

Morales-Ubaldo AL, Rivero-Perez N, Avila-Ramos F, Aquino-Torres E, Prieto-Méndez J, Hetta HF, El-Saber Batiha G, Zaragoza-Bastida A. Bactericidal Activity of Larrea tridentata Hydroalcoholic Extract against Phytopathogenic Bacteria. Agronomy. 2021; 11(5):957. https://doi.org/10.3390/agronomy11050957

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Morales-Ubaldo, Ana Lizet, Nallely Rivero-Perez, Fidel Avila-Ramos, Eliazar Aquino-Torres, Judith Prieto-Méndez, Helal F. Hetta, Gaber El-Saber Batiha, and Adrian Zaragoza-Bastida. 2021. "Bactericidal Activity of Larrea tridentata Hydroalcoholic Extract against Phytopathogenic Bacteria" Agronomy 11, no. 5: 957. https://doi.org/10.3390/agronomy11050957

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