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Synergistic effect of Cordia curassavica Jacq. essential oils association against the phytopathogen Xanthomonas campestris pv. campestris


The increased use of pesticides applied to treat diseases caused by bacteria has caused serious environmental problems. There are few fungicides/bactericides for the treatment of plant diseases caused by Xanthomonas campestris pv. campestris (Xcc), and only two natural products with general bactericidal/fungicidal use are available on the market. Thus, this study evaluated the antimicrobial activity of essential oils (EOs), and their combinations, from five distinct genotypes of Cordia curassavica (Jacq.) Roem. & Schult (Syn. Varronia curassavica Jacq.) (CCUR) against Xcc. GC/MS chemical analysis revealed α-pinene, sabinene, (E)-caryophyllene, ar-curcumene, β-sesquiphellandrene, 7-cyclodecen-1-one, and ar-Turmerone as the major compounds of the five EOs of CCUR. All EOs showed growth inhibition of Xcc with minimum inhibitory concentration between 500 and 1000 μg mL−1. The associations between two EOs from different CCUR genotypes showed that 70% of the total combinations had an additive effect. However, the combinations between CCUR-002 × (-302, -202) and CCUR-302 × (-601) showed a synergistic effect, with mean fractional inhibitory concentration FIC50 values of 0.28, 0.42, and 0.40, respectively. This study demonstrates that combinations of C. curassavica EOs have antimicrobial activity and a potential to be used in the control of black rot.

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  1. Abifra (2019), Brazilian Association of Essential Oils, Aromatic Chemicals, Fragrances and Aromas, Brazil. Acessed in http://www.abifra.org.br/wp/

  2. Adams RP (2007) Identification of essential oil components by gas chromatography/mass spectroscopy, 4th edn. Allured Publishing Corporation, Carol Stream, Illinois

  3. Agrofit (2019), Phytosanitary pesticide system, Brazil. Acessed in http://agrofit.agricultura.gov.br/primeira_pagina/extranet/AGROFIT.html

  4. Alexy R, Schöll A, Kümpel T, Kümmerer K (2004) What do we know about antibiotics in the environment? In: Pharmaceuticals in the Environment. Springer, Berlin

  5. Bajpai VK, Kang S-R, Xu H et al (2011) Potential roles of essential oils on controlling plant pathogenic bacteria Xanthomonas species: a review. Plant Pathol J 27:207–224

  6. Bizi RM, Grigoletti Junior A, Auer CG, May-De Mio LL (2008) Alternative products in the control of powdery mildew in eucalyptus seedlings. Summa Phytopathol 34:144–148

  7. Brandão DS, Mendes ADR, Santos RR et al (2015) Biologia floral e sistema reprodutivo da erva-baleeira (Cordia curassavica Jacq. Jacq.). Rev Bras Plantas Med 17:562–569

  8. Buchbauer G, Hemetsberger S (2015) Use of essential oils in agriculture. In: Handbook of essential oils: science, technology, and applications, second edn, New York

  9. Chavez-Dozal A, Morales-Morales HA et al (2012) Antibacterial activity of mexican oregano essential oil (Lippia berlandieri) against the phytopathogenic bacterium Xanthomonas euvesicatoria. Medio Ambient y Desarro sustentable VIII:109–121

  10. Cox SD, Mann CM, Markham JL (2001) Interactions between components of the essential oil of Melaleuca alternifolia. J Appl Microbiol 91:492–197

  11. da Frank MC, Rui SJ, de Fernandes AA, Mariana VL (2006) Efficiency of Kasugamycin and copper hydroxide in Acidovorax avenae subsp. citrulli, causal stain agent. Rev Biol E Ciencias Da Terra 6:132–138

  12. da Silva AC, de Souza PE, da Cruz Machado J et al (2012) Effectiveness of essential oils in the treatment of Colletotrichum truncatum-infected soybean seeds. Trop Plant Pathol 37:305–313

  13. da Silva RS, de Oliveira MMG, de Melo JO et al (2019) Antimicrobial activity of Lippia gracilis essential oils on the plant pathogen Xanthomonas campestris pv. campestris and their effect on membrane integrity. Pestic Biochem Physiol

  14. de Aguiar LA, Kimura O, Castilho AMC et al (2003) Effect of copper formulations on resident Xanthomonas campestris pv. vesicatoria populations on sweet pepper leaf surfaces. Hortic Bras 21:44–50

  15. de Araújo IMM, Oliveira AGRDC (2016) Agribusiness and pesticides: impacts on the health of agricultural workers in northeastern Brazil. Trab Educ e Saúde. https://doi.org/10.1590/1981-7746-sol00043

  16. de Carvalho PM, Rodrigues RFO, Sawaya ACHF et al (2004) Chemical composition and antimicrobial activity of the essential oil of Cordia verbenacea D.C. J Ethnopharmacol 95:297–301

  17. de Castro Nizio DA, Fujimoto RY, Maria AN et al (2018) Essential oils of Cordia curassavica Jacq. accessions have different activity against white spot disease in freshwater fish. Parasitol Res 117:97–105

  18. de Morais LAS (2009) Biocontrol of plant diseases: uses and perspectives. In: Wagnerbettio L, Morandi MAB (eds) Essential oils in phytosanitary control, Fundag, Embrapa Meio Ambiente, 1st edn. Jaguariúna, São Paulo

  19. de Oliveira BMS, Melo CR, Santos ACC, Nascimento LFA, Nízio DAC, Cristaldo PF, Blank AF, Bacci L (2019) Essential oils from Cordia curassavica Jacq. (Cordiaceae) accessions and their compounds (E)-caryophyllene and α-humulene as an alternative to control Dorymyrmex thoracius (Formicidae: Dolichoderinae). Environ Sci Pollut Res 26:6602–6612

  20. Delaquis P (2002) Antimicrobial activity of individual and mixed fractions of dill, cilantro, coriander and Eucalyptus essential oils. Int J Food Microbiol 74:101–109

  21. Dhifi W, Bellili S, Jazi S et al (2016) Essential oils’ chemical characterization and investigation of some biological activities: a critical review. Medicines 3:2–6

  22. dos Santos LA, Bandeira DDA, da Silva JP et al (2008) Characterization of strains of Xanthomonas campestris pv campestris from organic farming systems and reaction of brassicas to black rot. Hortic Bras 26:486–491

  23. Ehlert PAD, Blank AF, Arrigoni-Blank MF et al (2006) Hydrodistillation time for essential oil extraction of seven medicinal plant species. Rev Bras Plantas Med 8:79–80

  24. Farfán LM, Benítez SV, Carvajal LMH (2014) Sensibilidad de bacterias procedentes de pasifloras a antibióticos y productos cúpricos. Rev Colomb Ciencias Hortícolas 8:20–33

  25. Fernandes ES, Passos GF, Medeiros R, da Cunha FM, Ferreira J, Campos MM, Pianowski LF, Calixto JB (2007) Anti-inflammatory effects of compounds alpha-humulene and (−)-trans-caryophyllene isolated from the essential oil of Cordia verbenacea. Eur J Pharmacol 569:228–236

  26. Filho ELB, Luiz E, Filho B, Filho ELB (2004) Environmental impacts occurred by the use of agricultural pesticides: the scarcity of research in the Brazilian National Agricultural Research Program. XLII Congr da Soc Bras Econ e Sociol Rural

  27. Fivelman QL, Adagu IS, Warhurst DC (2004) Modified fixed-ratio isobologram method for studying in vitro interactions between Atovaquone and Proguanil or Dihydroartemisinin against drug-resistant strains of Plasmodium falciparum. Antimicrob Agents Chemother 48:4097–4102

  28. Fonseca MCM, Lehner MS, Gonçalves MG et al (2015) Potential of essential oils of medicinal plants in the control of phytopathogens. Rev Bras Plantas Med 17:45–50

  29. Gallucci MN, Oliva M, Casero C et al (2009) Antimicrobial combined action of terpenes against the food-borne microorganisms Escherichia coli, Staphylococcus aureus and Bacillus cereus. Flavour Fragr J 24:348–354

  30. Ghabraie M, Vu KD, Tata L et al (2016) Antimicrobial effect of essential oils in combinations against five bacteria and their effect on sensorial quality of ground meat. LWT Food Sci Technol 66:332–339

  31. Gholami D, Aminzadeh S, Alavi SM et al (2018) Comparison of antibiotics and bacteriocins antibacterial activity on Xanthomonas citri subsp.citri. Iran J Fish Sci 17:162–178

  32. Gilbert B, Favoreto R (2012) Cordia verbenacea DC. Boraginaceae. Rev Fitos 7:9–15

  33. Habbadi K, Meyer T, Vial L, Gaillard V, Benkirane R, Benbouazza A, Kerzaon I, Achbani EH, Lavire C (2018) Essential oils of Origanum compactum and Thymus vulgaris exert a protective effect against the phytopathogen Allorhizobium vitis. Environ Sci Pollut Res 25:29943–29952

  34. Hazzit M, Baaliouamer A, Veríssimo AR et al (2009) Chemical composition and biological activities of Algerian thymus oils. Food Chem 116:714–721

  35. Hernandez T, Canales M, Teran B, Avila O, Duran A, Garcia AM, Hernandez H, Angeles-Lopez O, Fernandez-Araiza M, Avila G (2007) Antimicrobial activity of the essential oil and extracts of Cordia curassavica (Boraginaceae). J Ethnopharmacol 111:137–141

  36. Hoyos JMÁ, Alves E, Rozwalka LC et al (2012) Antifungal activity and ultrastructural alterations in Pseudocercospora griseola treated with essential oils. Ciência e Agrotecnologia 36:270–284

  37. Iacobellis N, Lo Cantore P, Capasso F et al (2005) Antimicrobial activity of Cuminum cyminum L.and Carum carvi L. essential oils. J Agric Food Chem 53:57–61

  38. Iglesias-Bernabé L, Madloo P, Rodríguez VM et al (2019) Dissecting quantitative resistance to Xanthomonas campestris pv. campestris in leaves of Brassica oleracea by QTL analysis. Sci Rep 9:–2015

  39. Isman MB, Machial CM (2006) Chapter 2 Pesticides based on plant essential oils: from traditional practice to commercialization. In: Rai, Carpinella (eds) Advances in phytomedicine. Naturally occurring bioactive compounds, Oxford

  40. Isman MB, Miresmailli S, MacHial C (2011) Commercial opportunities for pesticides based on plant essential oils in agriculture, industry and consumer products. Phytochem Rev 10:197–204

  41. Jacques M-A, Arlat M, Boulanger A, Boureau T, Carrère S, Cesbron S, Chen NW, Cociancich S, Darrasse A, Denancé N, Fischer-le Saux M, Gagnevin L, Koebnik R, Lauber E, Noël LD, Pieretti I, Portier P, Pruvost O, Rieux A, Robène I, Royer M, Szurek B, Verdier V, Vernière C (2016) Using ecology, physiology, and genomics to understand host specificity in Xanthomonas. Annu Rev Phytopathol 54:163–187

  42. Jarva J, Ottesen RT, Tarvainen T (2014) Geochemical studies on urban soil from two sampling depths in Tampere Central Region, Finland. Environ Earth Sci 71:4783–4799

  43. Junior SS, De Lalla JG, Goto R et al (2013) Black rot susceptibility and broccoli yield as a function of nitrogen and potassium doses. Hortic Bras 31:426–431

  44. Kim J, Marshall MR, Wei C (1995) Antibacterial activity of some essential oil components against five foodborne pathogens. J Agric Food Chem 43:2839–2845

  45. Lambert RJW, Skandamis PN, Coote PJ, Nychas G-JE (2001) A study of the minimum inhibitory concentration and mode of action of oregano essential oil, thymol and carvacrol. J Appl Microbiol 91:453–462

  46. Liu K, Garrett C, Fadamiro H, Kloepper JW (2016) Induction of systemic resistance in Chinese cabbage against black rot by plant growth-promoting rhizobacteria. Biol Control 99:8–13

  47. Lopes CVA, de Albuquerque GSC (2018) Agrochemicals and their impacts on human and environmental health: a systematic review. Saúde em Debate 42:518–534

  48. Mari M, Bautista-Baños S, Silvakumar D (2016) Decay control in the postharvest system: Role of microbial and plant volatile organic compounds. Pastharvest Biol Technol 122:70–81

  49. Matias EFF, Alves EF, Santos BS et al (2013) Biological activities and chemical characterization of Cordia verbenacea DC. as tool to validate the ethnobiological usage. Evid Based Complement Altern Med 2013:1–7

  50. Mello M, Silveira E, Viana I et al (2011) Use of antibiotics and yeasts for controlling Chinese cabbage soft rot. Hortic Bras 29:78–83

  51. Michielin EMZ, Salvador AA, Riehl CAS, Smânia A Jr, Smânia EF, Ferreira SR (2009) Chemical composition and antibacterial activity of Cordia verbenacea extracts obtained by different methods. Bioresour Technol 100:6615–6623

  52. Migliore L (1995) Effect on plants of sulphadimethoxine used in intensive farming (Panicum miliaceum, Pisum sativum and Zea mays). Agric Ecosyst Environ 52:103–110

  53. Miranda CASF, Cardoso M das G, Batista LR, et al (2016) Essential oils from leaves of various species: antioxidant and antibacterial properties on growth in pathogenic species. Rev Ciência agronômica 47:213–220

  54. Mirzaei-Najafgholi H, Tarighi S, Golmohammadi M, Taheri P (2017) The effect of citrus essential oils and their constituents on growth of Xanthomonas citri subsp. citri. Molecules 22:1–14

  55. Nizio DAC, de Andrade Brito F, Sampaio TS et al (2015) Chemical diversity of native populations of Cordia curassavica Jacq. Jacq. and antifungal activity against Lasiodoplodia theobromae. Ind Crop Prod 76:437–448

  56. Nuñez AMP, Rodríguez GAA, Monteiro FP et al (2018) Bio-based products control black rot (Xanthomonas campestris pv. campestris) and increase the nutraceutical and antioxidant components in kale. Sci Rep 8:1–11

  57. Ouedrhiri W, Mounyr B, Harki EH et al (2017) Synergistic antimicrobial activity of two binary combinations of Marjoram, Lavender, and wild Thyme essential oils. Int J Food Prop 20:3149–3158

  58. Pandey AK, Kumar P, Singh P et al (2017) Essential oils: sources of antimicrobials and food preservatives. Front Microbiol 7:1–14

  59. Parisotto EB, Michielin EMZ, Biscaro F et al (2012) The antitumor activity of extracts from Cordia verbenacea D.C. obtained by supercritical fluid extraction. J Supercrit Fluids 61:101–107

  60. Queiroz TBB, Mendes ADRDR, Silva JCRL et al (2016) Content and chemical composition of whales (Varronia curassavica Jaqc.) essential oil as a function of collection times. Rev Bras Plant Med 18:356–362

  61. Quezado-Duval AM, Gazzoto Filho A, Leite Júnior RP, Camargo LEA (2003) Sensitivity to copper streptomycin and oxitetracyclin of Xanthomonas associated to bacterial spot in processing tomatoes. Hortic Bras 21:670–675

  62. Quijano CE, Pino JA (2009) Volatile compounds of Kumquat (Fortunella margarita (Lour.) Swingle) leaf oil. J Essent Oil Res 21:194–196

  63. Regitano JB, Leal RMP (2010) Performance and environmental impact of antibiotics in animal production in Brazil. Rev Bras Ciência do Solo 34:601–616

  64. Rodrigues FG, Rodrigues FG, Almeida SX et al (2012) Chemical composition, antibacterial and antifungal activities of essential oil from Cordia verbenacea DC leaves. Pharmacognosy 4:161–165

  65. Ryan RP, Vorhölter F-J, Potnis N, Jones JB, van Sluys M, Bogdanove AJ, Dow JM (2011) Pathogenomics of Xanthomonas: understanding bacterium–plant interactions. Nat Rev Microbiol 9:344–355

  66. Saddiq AA, Khayyat SA (2010) Chemical and antimicrobial studies of monoterpene: Citral. Pestic Biochem Physiol 98:89–93

  67. Salehi B, Zakaria ZA, Gyawali R et al (2019) Piper species: a comprehensive review on their phytochemistry, biological activities and applications. Molecules 24:2–118

  68. Sampietro DA, Lizarraga EF, Ibatayev ZA et al (2016) Chemical composition and antimicrobial activity of essential oils from Acantholippia deserticola , Artemisia proceriformis, Achillea micrantha and Libanotis buchtormensis against phytopathogenic bacteria and fungi. Nat Prod Res 30:1950–1955

  69. Santos RP, Nunes EP, Nascimento RF et al (2006) Chemical composition and larvicidal activity of the essential oils of Cordia leucomalloides and Cordia curassavica from the Northeast of Brazil. J Braz Chem Soc 17:1027–1030

  70. Santos MM, Peixoto AR, de Sousa Pessoa E et al (2014) Studies of the chemical constituents and antibacterial activity of the essential oil of Lippia gracilis a Xanthomonas campestris pv. viticolain vitro”. Summa Phytopathol 40:277–280

  71. Sarah Shafiei SN, Ahmad K, Fatin Mohd Ikhsan N et al (2017) Antibacterial activity of Acacia spp leaves extracts against Xanthomonas oryzae pv oryzae and screening for active phytochemical contents. 10:49–60

  72. Sartoratto A, Machado ALM, Delarmelina C et al (2004) Composition and antimicrobial activity of essential oils from aromatic plants used in Brazil. Braz J Microbiol 35:275–280

  73. Shi C, Song K, Zhang X et al (2016) Antimicrobial activity and possible mechanism of action of Citral against Cronobacter sakazakii. PLoS One 11:1–12

  74. Soković MD, Vukojević J, Marin PD et al (2009) Chemical composition of essential oils of Thymus and mentha species and their antifungal activities. Molecules 14:238–249

  75. Van Den Dool H, Dec Kratz P (1963) A Generalization of the Retention Index System Including Linear Temperature Programmed Gas-Liquid Partition Chromatography. Journal of Chromatography A 11:463–471

  76. Viero CM, Camponogara S, Cezar-Vaz MR et al (2016) Risk society: the use of pesticides and implications for the health of rural workers. Esc Anna Nery - Rev Enferm 20:99–105

  77. Vigo-Schultz SC, Stangarlin JR, Franzener G et al (2006) Effect of alcoholic extract of guaco (Mikania glomerata) on the control of dark rot (Xanthomonas campestris pv. campestris) in cauliflower. Semin Ciências Agrárias 27:515–524

  78. Viljoen A, van Vuuren S, Ernst E et al (2003) Osmitopsis asteriscoides (Asteraceae)-the antimicrobial activity and essential oil composition of a Cape-Dutch remedy. J Ethnopharmacol 88:137–143

  79. Whitman WB, Rainey F, Kämpfer P et al (eds) (2015) Bergey’s manual of systematics of Archaea and Bacteria. Wiley, Chichester

  80. Worthington RJ, Rogers SA, Huigens RW et al (2012) Foliar-applied small molecule that suppresses biofilm formation and enhances control of copper-resistant Xanthomonas euvesicatoria on pepper. Plant Dis 96:1637–1644

  81. Zhou F, Baoping JI, Zhang H et al (2007) The antibacterial effect of cinnamaldehyde, thymol, carvacrol and their combinations against the foodborne pathogen Salmonella typhimurium. J Food Saf 27:124–133

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The authors would like to thank Dr. Elmo Eduardo de Almeida Amaral for the valuable discussion and suggestions in the association experiments and Professor Paulo C. Nogueira for help with the identification of the compounds.


This study was funded, in part by Brazil’s Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq); Fundação de Apoio à Pesquisa e a Inovação Tecnológica do Estado de Sergipe (Fapitec/SE); Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES; Finance Code 001); and Financiadora de Estudos e Projetos (FINEP).

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Correspondence to Roberta Pereira Miranda Fernandes.

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• Essential oils from all five genotypes of C. curassavica showed growth inhibition of Xanthomonas campestris pv. campestris (Xcc).

• 70% of the total combinations between the five EOs from CCUR genotypes had an additive effect.

• The combinations between CCUR-002 × (-302, -202) and CCUR -302 × (-601) are efficient; in vitro bacteria inhibited 100% of X. campestris 629 IBSBF growth.

• Synergistic and additive combinations of EOs from C. curassavica might be a strategy for the control of black rot.

Responsible editor: Giovanni Benelli

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Da Silva, R.S., De Oliveira, M.M.G., Silva, K.P. et al. Synergistic effect of Cordia curassavica Jacq. essential oils association against the phytopathogen Xanthomonas campestris pv. campestris. Environ Sci Pollut Res 27, 4376–4389 (2020). https://doi.org/10.1007/s11356-019-06631-8

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  • Black rot
  • Cruciferous
  • Biological control
  • Medicinal plants
  • Interaction
  • Phytobacteria
  • Antimicrobial activity