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Characterization of Pseudomonas chlororaphis from Theobroma cacao L. rhizosphere with antagonistic activity against Phytophthora palmivora (Butler)

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Acebo-Guerrero, Yanelis [Facultu of Biology, University of Havana, Cuba] Hernandez-Rodri­guez, A. [Facultu of Biology, University of Havana, Cuba] Vandeputte, O. [Laboratory of Plant biotechnoly, ULB, Gosselies] Miguélez-Sierra, Y. [Faculty of Agrogofrstry, University of Guantanamo, Cuba] Heydrich-Perez, M. [Faculty of Biology, University of Havana, Cuba] Bertin, Pierre [UCL] El Jaziri, M. [Laboratory of Plant biotechnoly, ULB, Gosselies]

Aim: To isolate and characterize rhizobacteria from Theobroma cacao with antagonistic activity against Phytophthora palmivora, the causal agent of the black pod rot, which is one of the most important diseases of T. cacao. Methods and Results: Among 127 rhizobacteria isolated from cacao rhizosphere, three isolates (CP07, CP24 and CP30) identified as Pseudomonas chlororaphis, showed in vitro antagonistic activity against P. palmivora. Direct antagonism tested in cacao detached leaves revealed that the isolated rhizobacteria were able to reduce symptom severity upon infection with P. palmivora Mab1, with Ps. chlororaphis CP07 standing out as a potential biocontrol agent. Besides, reduced symptom severity on leaves was also observed in planta where cacao root system was pretreated with the isolated rhizobacteria followed by leaf infection with P. palmivora Mab1. The production of lytic enzymes, siderophores, biosurfactants and HCN, as well as the detection of genes encoding antibiotics, the formation of biofilm, and bacterial motility were also assessed for all three rhizobacterial strains. By using a mutant impaired in viscosin production, derived from CP07, it was found that this particular biosurfactant turned out to be crucial for both motility and biofilm formation, but not for the in vitro antagonism against Phytophthora, although it may contribute to the bioprotection of T. cacao. Conclusions: In the rhizosphere of T. cacao, there are rhizobacteria, such as Ps. chlororaphis, able to protect plants against P. palmivora. Significance and Impact of the Study: This study provides a theoretical basis for the potential use of Ps. chlororaphis CP07 as a biocontrol agent for the protection of cacao plants from P. palmivora infection. © 2015 The Society for Applied Microbiology.

Document type Article de périodique (Journal article) – Article de recherche
Access type Accès restreint
Publication date 2015
Language Anglais
Journal information "Journal of Applied Microbiology" - Vol. 119, no.4, p. 1112-1126 (2015)
Peer reviewed yes
Publisher Wiley-Blackwell Publishing Ltd. ((United Kingdom) Chichester)
issn 1364-5072
e-issn 1365-2672
Publication status Publié
Affiliation UCL - SST/ELI/ELIA - Agronomy
Keywords Antagonism ; Phytophthora ; Phytophthora palmivora ; Pseudomonas ; Pseudomonas chlororaphis ; Rhizobiales ; Theobroma cacao ; Biocontrol ; Black pod rot ; Cacao ; Phytophthora ; Pseudomonas ; Rhizobacteria ; Viscosin ; Bacteria (microorganisms)
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  1. Acebo-Guerrero Yanelis, Hernández-Rodríguez Annia, Heydrich-Pérez Mayra, El Jaziri Mondher, Hernández-Lauzardo Ana N., Management of black pod rot in cacao (Theobroma cacaoL.): a review, 10.1051/fruits/2011065
  2. Adebola, Afr Sci, 11, 235 (2010)
  3. Adesina Modupe F., Lembke Antje, Costa Rodrigo, Speksnijder Arjen, Smalla Kornelia, Screening of bacterial isolates from various European soils for in vitro antagonistic activity towards Rhizoctonia solani and Fusarium oxysporum: Site-dependent composition and diversity revealed, 10.1016/j.soilbio.2007.06.004
  4. Alsohim Abdullah S., Taylor Tiffany B., Barrett Glyn A., Gallie Jenna, Zhang Xue-Xian, Altamirano-Junqueira Astrid E., Johnson Louise J., Rainey Paul B., Jackson Robert W., The biosurfactant viscosin produced byPseudomonas fluorescens SBW25 aids spreading motility and plant growth promotion : Viscosin mediates sliding motility and plant protection, 10.1111/1462-2920.12469
  5. Barahona Emma, Navazo Ana, Yousef-Coronado Fátima, Aguirre de Cárcer Daniel, Martínez-Granero Francisco, Espinosa-Urgel Manuel, Martín Marta, Rivilla Rafael, Efficient rhizosphere colonization by Pseudomonas fluorescens f113 mutants unable to form biofilms on abiotic surfaces : Biofilm formation and rhizosphere colonization, 10.1111/j.1462-2920.2010.02291.x
  6. Barahona E., Navazo A., Martinez-Granero F., Zea-Bonilla T., Perez-Jimenez R. M., Martin M., Rivilla R., Pseudomonas fluorescens F113 Mutant with Enhanced Competitive Colonization Ability and Improved Biocontrol Activity against Fungal Root Pathogens, 10.1128/aem.00320-11
  7. Bashan, Terra, 14, 159 (1996)
  8. Berendsen Roeland L., Pieterse Corné M.J., Bakker Peter A.H.M., The rhizosphere microbiome and plant health, 10.1016/j.tplants.2012.04.001
  9. Bergsma-Vlami Maria, Prins Mieke E., Raaijmakers Jos M., Influence of plant species on population dynamics, genotypic diversity and antibiotic production in the rhizosphere by indigenous Pseudomonas spp., 10.1016/j.femsec.2004.10.007
  10. Bidot Martínez Igor, Riera Nelson Manuel, Flamand Marie-Christine, Bertin Pierre, Genetic diversity and population structure of anciently introduced Cuban cacao Theobroma cacao plants, 10.1007/s10722-014-0136-z
  11. Blin Kai, Medema Marnix H., Kazempour Daniyal, Fischbach Michael A., Breitling Rainer, Takano Eriko, Weber Tilmann, antiSMASH 2.0—a versatile platform for genome mining of secondary metabolite producers, 10.1093/nar/gkt449
  12. de Bruijn Irene, de Kock Maarten J. D., Yang Meng, de Waard Pieter, van Beek Teris A., Raaijmakers Jos M., Genome-based discovery, structure prediction and functional analysis of cyclic lipopeptide antibiotics inPseudomonasspecies : Cyclic lipopeptides inPseudomonas, 10.1111/j.1365-2958.2006.05525.x
  13. Buddrus-Schiemann Katharina, Schmid Michael, Schreiner Karin, Welzl Gerhard, Hartmann Anton, Root Colonization by Pseudomonas sp. DSMZ 13134 and Impact on the Indigenous Rhizosphere Bacterial Community of Barley, 10.1007/s00248-010-9720-8
  14. Calderón Claudia E., Ramos Cayo, de Vicente Antonio, Cazorla Francisco M., Comparative Genomic Analysis ofPseudomonas chlororaphisPCL1606 Reveals New Insight into Antifungal Compounds Involved in Biocontrol, 10.1094/mpmi-10-14-0326-fi
  15. Calderón Claudia E., Pérez-García Alejandro, de Vicente Antonio, Cazorla Francisco M., ThedarGenes ofPseudomonas chlororaphisPCL1606 Are Crucial for Biocontrol Activity via Production of the Antifungal Compound 2-Hexyl, 5-Propyl Resorcinol, 10.1094/mpmi-01-13-0012-r
  16. Cazorla Francisco M., Duckett Simon B., Bergström Ed T., Noreen Sadaf, Odijk Roeland, Lugtenberg Ben J. J., Thomas-Oates Jane E., Bloemberg Guido V., Biocontrol of Avocado Dematophora Root Rot by AntagonisticPseudomonas fluorescensPCL1606 Correlates With the Production of 2-Hexyl 5-Propyl Resorcinol, 10.1094/mpmi-19-0418
  17. Chen Yawen, Shen Xuemei, Peng Huasong, Hu Hongbo, Wang Wei, Zhang Xuehong, Comparative genomic analysis and phenazine production of Pseudomonas chlororaphis, a plant growth-promoting rhizobacterium, 10.1016/j.gdata.2015.01.006
  18. Compant Stéphane, Brader Günter, Muzammil Saima, Sessitsch Angela, Lebrihi Ahmed, Mathieu Florence, Use of beneficial bacteria and their secondary metabolites to control grapevine pathogen diseases, 10.1007/s10526-012-9479-6
  19. Das I.K., Indira S., Annapurna A., Prabhakar, Seetharama N., Biocontrol of charcoal rot in sorghum by fluorescent pseudomonads associated with the rhizosphere, 10.1016/j.cropro.2008.07.001
  20. Deberdt P., Mfegue C.V., Tondje P.R., Bon M.C., Ducamp M., Hurard C., Begoude B.A.D., Ndoumbe-Nkeng M., Hebbar P.K., Cilas C., Impact of environmental factors, chemical fungicide and biological control on cacao pod production dynamics and black pod disease (Phytophthora megakarya) in Cameroon, 10.1016/j.biocontrol.2007.10.026
  21. Drancourt, J Clin Microbiol, 38, 3623 (2000)
  22. Efombagn M.I.B., Bieysse D., Nyassé S., Eskes A.B., Selection for resistance to Phytophthora pod rot of cocoa (Theobroma cacao L.) in Cameroon: Repeatability and reliability of screening tests and field observations, 10.1016/j.cropro.2010.10.012
  23. Ghirardi Sandrine, Dessaint Fabrice, Mazurier Sylvie, Corberand Thérèse, Raaijmakers Jos M., Meyer Jean-Marie, Dessaux Yves, Lemanceau Philippe, Identification of Traits Shared by Rhizosphere-Competent Strains of Fluorescent Pseudomonads, 10.1007/s00248-012-0065-3
  24. González-Sánchez, J Appl Microbiol, 109, 65 (2010)
  25. Hebbar Prakash K., Cacao Diseases: A Global Perspective from an Industry Point of View, 10.1094/phyto-97-12-1658
  26. Hernandez-Rodriguez , A. Acebo-Guerrero , Y. Rives-Rodriguez , N. Almaguer Chavez , M. Heydrich-Pérez , M. El Jaziri , M. Vandeputte , O.M. 2011 Fluorescent pseudomonads isolated from rice rhizosphere have in vitro antagonistic activity and induce in vivo plant resistance against Pyricularia grisea (Sacc) 63rd International Symposium on Crop Protection
  27. Hubeaux, Caracterisation du Phytophthora, agent de la pourriture brune de la cabosse, à Cuba, 90 (2010)
  28. Hultberg Malin, Holmkvist Anna, Alsanius Beatrix, Strategies for administration of biosurfactant-producing pseudomonads for biocontrol in closed hydroponic systems, 10.1016/j.cropro.2011.04.012
  29. Iavicoli Annalisa, Boutet Emmanuel, Buchala Antony, Métraux Jean-Pierre, Induced Systemic Resistance inArabidopsis thalianain Response to Root Inoculation withPseudomonas fluorescensCHA0, 10.1094/mpmi.2003.16.10.851
  30. ICCO 2014 Production of cocoa beans, Cocoa year 2013/14 ICCO Quarterly Bulletin of Cocoa Statistics
  31. Jiao, Ann Appl Biol, 163, 444 (2013)
  32. Karthikeyan V., Gnanamanickam S.S., Biological control of Setaria blast (Magnaporthe grisea) with bacterial strains, 10.1016/j.cropro.2007.05.013
  33. Koranteng, Afr J Agric Res, 6, 67 (2011)
  34. Kremer Robert J., Souissi Thouraya, Cyanide Production by Rhizobacteria and Potential for Suppression of Weed Seedling Growth, 10.1007/s002840010284
  35. Kroon Laurens P. N. M., Brouwer Henk, de Cock Arthur W. A. M., Govers Francine, The Genus Phytophthora Anno 2012, 10.1094/phyto-01-11-0025
  36. Kuiper Irene, Lagendijk Ellen L., Pickford Russell, Derrick Jeremy P., Lamers Gerda E. M., Thomas-Oates Jane E., Lugtenberg Ben J. J., Bloemberg Guido V., Characterization of two Pseudomonas putida lipopeptide biosurfactants, putisolvin I and II, which inhibit biofilm formation and break down existing biofilms : Putisolvins inhibit biofilm formation and break down existing biofilms, 10.1046/j.1365-2958.2003.03751.x
  37. Le C.N., Kruijt M., Raaijmakers J.M., Involvement of phenazines and lipopeptides in interactions between Pseudomonas species and Sclerotium rolfsii, causal agent of stem rot disease on groundnut : Suppression of stem rot by Pseudomonas, 10.1111/j.1365-2672.2011.05205.x
  38. Bin Li, Rongrong Yu, Qiaomei Tang, Xiaoling Chen, Zhiyi Wu, Yanli Wang, Guanlin Xie, Hongye Li, Guochang Sun Both, Carbon adaptation influence the antagonistic ability of Pseudomonas aeruginosa against Fusarium oxysporum f. sp. melonis, 10.5897/ajb10.2280
  39. Lim Chee Kent, Hassan Karl A., Tetu Sasha G., Loper Joyce E., Paulsen Ian T., The Effect of Iron Limitation on the Transcriptome and Proteome of Pseudomonas fluorescens Pf-5, 10.1371/journal.pone.0039139
  40. Loper Joyce E., Hassan Karl A., Mavrodi Dmitri V., Davis Edward W., Lim Chee Kent, Shaffer Brenda T., Elbourne Liam D. H., Stockwell Virginia O., Hartney Sierra L., Breakwell Katy, Henkels Marcella D., Tetu Sasha G., Rangel Lorena I., Kidarsa Teresa A., Wilson Neil L., van de Mortel Judith E., Song Chunxu, Blumhagen Rachel, Radune Diana, Hostetler Jessica B., Brinkac Lauren M., Durkin A. Scott, Kluepfel Daniel A., Wechter W. Patrick, Anderson Anne J., Kim Young Cheol, Pierson Leland S., Pierson Elizabeth A., Lindow Steven E., Kobayashi Donald Y., Raaijmakers Jos M., Weller David M., Thomashow Linda S., Allen Andrew E., Paulsen Ian T., Comparative Genomics of Plant-Associated Pseudomonas spp.: Insights into Diversity and Inheritance of Traits Involved in Multitrophic Interactions, 10.1371/journal.pgen.1002784
  41. Lugtenberg Ben, Kamilova Faina, Plant-Growth-Promoting Rhizobacteria, 10.1146/annurev.micro.62.081307.162918
  42. Matos, Rev Prot Veg, 26, 198 (2011)
  43. Mavrodi Olga V., McSpadden Gardener Brian B., Mavrodi Dmitri V., Bonsall Robert F., Weller David M., Thomashow Linda S., Genetic Diversity ofphlDfrom 2,4-Diacetylphloroglucinol-Producing FluorescentPseudomonasspp., 10.1094/phyto.2001.91.1.35
  44. Mavrodi O. V., Mavrodi D. V., Parejko J. A., Thomashow L. S., Weller D. M., Irrigation Differentially Impacts Populations of Indigenous Antibiotic-Producing Pseudomonas spp. in the Rhizosphere of Wheat, 10.1128/aem.07968-11
  45. Mazzola M., Zhao X., Cohen M. F., Raaijmakers J. M., Cyclic Lipopeptide Surfactant Production by Pseudomonas fluorescens SS101 Is Not Required for Suppression of Complex Pythium spp. Populations, 10.1094/phyto-97-10-1348
  46. Melnick Rachel L., Zidack Nina K., Bailey Bryan A., Maximova Siela N., Guiltinan Mark, Backman Paul A., Bacterial endophytes: Bacillus spp. from annual crops as potential biological control agents of black pod rot of cacao, 10.1016/j.biocontrol.2008.01.022
  47. Melnick Rachel L., Suárez Carmen, Bailey Bryan A., Backman Paul A., Isolation of endophytic endospore-forming bacteria from Theobroma cacao as potential biological control agents of cacao diseases, 10.1016/j.biocontrol.2011.03.005
  48. MEYER J. M., ABDALLAH M. A., The Fluorescent Pigment of Pseudomonas fluorescens: Biosynthesis, Purification and Physicochemical Properties, 10.1099/00221287-107-2-319
  49. van de Mortel J. E., Tran H., Govers F., Raaijmakers J. M., Cellular Responses of the Late Blight Pathogen Phytophthora infestans to Cyclic Lipopeptide Surfactants and Their Dependence on G Proteins, 10.1128/aem.00241-09
  50. Mpika, Afr J Biotechnol, 8, 5280 (2009)
  51. Mpika, Biodiversity Loss in a Changing Planet, 303 (2011)
  52. Nyadanu D., Akromah R., Adomako B., Kwoseh C., Dzahini-Ob H., Lowor S.T., Akrofi A.Y., Assuah M.K., Host Plant Resistance to Phytophthora Pod Rot in Cacao (Theobroma cacao L.): The Role of Epicuticular Wax on Pod and Leaf Surfaces, 10.3923/ijb.2012.13.21
  53. Nyassé S., Cilas C., Herail C., Blaha G., Leaf inoculation as an early screening test for cocoa (Theobroma cacao L.) resistance to Phytophthora black pod disease, 10.1016/0261-2194(95)00054-2
  54. Olorunleke, Faculty of Bioscience Engineering, 58 (2011)
  55. Opoku, Afr J Agric Res, 2, 601 (2007)
  56. Palleroni, Bergey's Manual of Systematic Bacteriology, 323 (2005)
  57. Perneel M., Heyrman J., Adiobo A., De Maeyer K., Raaijmakers J.M., De Vos P., Höfte M., Characterization of CMR5c and CMR12a, novel fluorescentPseudomonasstrains from the cocoyam rhizosphere with biocontrol activity, 10.1111/j.1365-2672.2007.03345.x
  58. Perneel Maaike, D'hondt Liesbet, De Maeyer Katrien, Adiobo Amayana, Rabaey Korneel, Höfte Monica, Phenazines and biosurfactants interact in the biological control of soil-borne diseases caused by Pythium spp., 10.1111/j.1462-2920.2007.01501.x
  59. Poritsanos, Department of Microbiology, 154 (2005)
  60. Raaijmakers Jos M., De Bruijn Irene, Nybroe Ole, Ongena Marc, Natural functions of lipopeptides fromBacillusandPseudomonas: more than surfactants and antibiotics, 10.1111/j.1574-6976.2010.00221.x
  61. Raio A., Puopolo G., Cimmino A., Danti R., Della Rocca G., Evidente A., Biocontrol of cypress canker by the phenazine producer Pseudomonas chlororaphis subsp. aureofaciens strain M71, 10.1016/j.biocontrol.2011.04.012
  62. Ramarathnam Rajesh, Fernando W. G. Dilantha, de Kievit Teresa, The role of antibiosis and induced systemic resistance, mediated by strains of Pseudomonas chlororaphis, Bacillus cereus and B. amyloliquefaciens, in controlling blackleg disease of canola, 10.1007/s10526-010-9324-8
  63. Rasamiravaka T., Jedrzejowski A., Kiendrebeogo M., Rajaonson S., Randriamampionona D., Rabemanantsoa C., Andriantsimahavandy A., Rasamindrakotroka A., Duez P., El Jaziri M., Vandeputte O. M., Endemic Malagasy Dalbergia species inhibit quorum sensing in Pseudomonas aeruginosa PAO1, 10.1099/mic.0.064378-0
  64. Rokni-Zadeh H., Li W., Sanchez-Rodriguez A., Sinnaeve D., Rozenski J., Martins J. C., De Mot R., Genetic and Functional Characterization of Cyclic Lipopeptide White-Line-Inducing Principle (WLIP) Production by Rice Rhizosphere Isolate Pseudomonas putida RW10S2, 10.1128/aem.00335-12
  65. Sayyed R. Z., Chincholkar S. B., Reddy M. S., Gangurde N. S., Patel P. R., Siderophore Producing PGPR for Crop Nutrition and Phytopathogen Suppression, Bacteria in Agrobiology: Disease Management (2013) ISBN:9783642336386 p.449-471, 10.1007/978-3-642-33639-3_17
  66. Shanks R. M. Q., Caiazza N. C., Hinsa S. M., Toutain C. M., O'Toole G. A., Saccharomyces cerevisiae-Based Molecular Tool Kit for Manipulation of Genes from Gram-Negative Bacteria, 10.1128/aem.00682-06
  67. Sonwa Denis J., Coulibaly Ousmane, Weise Stephan F., Akinwumi Adesina A., Janssens Marc J.J., Management of cocoa: Constraints during acquisition and application of pesticides in the humid forest zones of southern Cameroon, 10.1016/j.cropro.2008.02.004
  68. Tahi G. M., Kébé B. I., Sangare A., Cilas C., Eskes A. B., Foliar resistance of cacao (Theobroma cacao) to Phytophthora palmivora as an indicator of pod resistance in the field: the effect of light intensity and time of day of leaf collection, 10.1111/j.1365-3059.2006.01547.x
  69. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S., MEGA5: Molecular Evolutionary Genetics Analysis Using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods, 10.1093/molbev/msr121
  70. Thevenin Jean-Marc, Rossi Vivien, Ducamp Michel, Doare Fabien, Condina Virgile, Lachenaud Philippe, Numerous Clones Resistant to Phytophthora palmivora in the “Guiana” Genetic Group of Theobroma cacao L, 10.1371/journal.pone.0040915
  71. Whistler C. A., Stockwell V. O., Loper J. E., Lon Protease Influences Antibiotic Production and UV Tolerance of Pseudomonas fluorescens Pf-5, 10.1128/aem.66.7.2718-2725.2000
  72. Widmer T. L., Infective Potential of Sporangia and Zoospores ofPhytophthora ramorum, 10.1094/pdis-93-1-0030
  73. Yang Dongjing, Wang Bo, Wang Jianxin, Chen Yu, Zhou Mingguo, Activity and efficacy of Bacillus subtilis strain NJ-18 against rice sheath blight and Sclerotinia stem rot of rape, 10.1016/j.biocontrol.2009.05.021
  74. Zerbino D. R., Birney E., Velvet: Algorithms for de novo short read assembly using de Bruijn graphs, 10.1101/gr.074492.107
Bibliographic reference Acebo-Guerrero, Yanelis ; Hernandez-Rodri­guez, A. ; Vandeputte, O. ; Miguélez-Sierra, Y. ; Heydrich-Perez, M. ; et. al. Characterization of Pseudomonas chlororaphis from Theobroma cacao L. rhizosphere with antagonistic activity against Phytophthora palmivora (Butler). In: Journal of Applied Microbiology, Vol. 119, no.4, p. 1112-1126 (2015)
Permanent URL http://hdl.handle.net/2078.1/165560