The genus Bacillus as a biological control agent and its implications in the agricultural biosecurity
Abstract
The genus Bacillus is widely distributed in agro-systems, being one of its main applications the control of diseases in agricultural crops. The present review describes and analyzes the genus Bacillus, and its main mechanisms of action, such the excretion of antibiotics, toxins, siderophores, lytic enzymes and Induced systemic resistance, focused on its ability to be used as biocontrol agent of pests and diseases in plants; as well as its use in formulations of biopesticides, which have been incorporated into Integrated Pest Management programs. In addition, the Bacillus genus is analyzed in terms of agricultural biosecurity, as well as the principal criteria for the effective selection of biocontrol agents, considering strains not pathogenic to humans, and that do not negatively impact the microbial communities of agro-ecosystems, as a side-effect by its non-specific biological activity against a particular plant pathogen.
Keywords
Full Text:
PDF (Español)References
AgraQuest. 2007. BALLAD PLUS, Biofungicide. Disponible en línea: http://fs1.agrian.com/pdfs/Ballad_Plus_(30_May_2007)_Label.pdf
Aguado-Santacruz GA, Moreno-Gómez B, Jiménez-Francisco B, García-Moya E y Preciado-Ortiz RE. 2012. Impacto de los sideróforos microbianos y fitosidéforos en la asimilación de hierro por las plantas: una síntesis. Revista Fitotecnia Mexicana. 35:9-21. Disponible en línea: http://www.scielo.org.mx/scielo.php?script=sci_arttext&pid=S0187-73802012000100004
Akram W, Anjum T and Ali B. 2016. Phenylacetic Acid Is ISR Determinant Produced by Bacillus fortis IAGS162, Which Involves Extensive Re-modulation in Metabolomics of Tomato to Protect against Fusarium Wilt. Frontiers in Plant Science. 7:1-12. https://doi.org/10.3389/fpls.2016.00498
Aktuganov GE, Galimzyanova NF, Melent’ev AI and Kuz’mina L. 2007. Extracellular hydrolases of strain Bacillus sp. 739 and their involvement in the lysis of micromycete cell walls. Microbiology. 76:413-120. http://dx.doi.org/10.1134/S0026261707040054
Alcaraz LD, Moreno-Hagelsieb G, Eguiarte LE, Souza V, Herrera-Estrella L and Olmedo G. 2010. Understanding the evolutionary relationships and major traits of Bacillus through comparative genomics. BMC Genomics. 11:332. http://dx.doi.org/10.1186/1471-2164-11-332
Aranda FJ, Teruel JA and Ortiz A. 2005. Further aspects on the hemolytic activity of the antibiotic lipopeptide iturin A. Biochimica et Biophysica Acta (BBA) - Biomembranes. 1713:51-56. http://dx.doi.org/10.1016/j.bbamem.2005.05.003
Arellano-Aguilar O y Rendón OJ. 2016. La huella de los plaguicidas en México. E. Martínez. Greenpeace México A. C. Las Flores 35 Col. Pueblo de Los Reyes, C.P. 04330, Coyoacán, México. 39 p. Disponible en línea: http://www.greenpeace.org/mexico/Global/mexico/Graficos/2016/comida-sana/Plaguicidas_en_agua_ok_EM.pdf
Badii MH, Tejada LO, Flores AE, Lopez CE y Quiróz H. 2000. Historia, fundamentos e importancia. Pp: 3-17. In: Badii MH, Flores AE y Galán LJ (eds.). Fundamentos y Perspectivas de Control Biológico. UANL, Monterrey.
Bais HP, Fall R and Vivanco JM. 2004. Biocontrol of Bacillus subtilis against infection of Arabidopsis roots by Pseudomonas syringae is facilitated by biofilm formation and surfactin production. Plant Physiology. 134:307-319. http://dx.doi.org/10.1104/pp.103.028712
Bayer AG. 2016. Serenade, Fungicida Biológico, Mejorando la Protección de Cultivos. Bayer Crop Science. Folleto Serenade. Santiago, Chile. 5p.
Bayer CropScience. 2016. Serenade ASO. Disponible en línea : http://www.cropscience.bayer.cl/upfiles/etiquetas/SERENADE__ASO_20170517.pdf
Boller T and Felix G. 2009. A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annual Review Plant Biology. 60:379-406. http://dx.doi.org/10.1146/annurev.arplant.57.032905.105346
Bowman SM and Free SJ. 2006. The structure and synthesis of the fungal cell wall. BioEssays 28:799-808. http://dx.doi.org/10.1002/bies.20441
CALS, College of Agriculture and Life Sciences. 2016. Bacterial Endospores. Department of Microbiology. Cornell University. Ithaca, Nueva York 14850, EE. UU. Disponible en línea: https://micro.cornell.edu/research/epulopiscium/bacterial-endospores
Calvo P y Zúñiga D. 2010. Caracterización fisiológica de cepas de Bacillus spp. aisladas de la rizósfera de papa (Solanum tuberosum). Ecología Aplicada. 9:31-39. http://dx.doi.org/10.21704/rea.v9i1-2.393
Cawoy H, Debois D, Franzil L, De Pauw E, Thonart P and Ongena M. 2015. Lipopeptides as main ingredients for inhibition of fungal phytopathogens by Bacillus subtilis/amyloliquefaciens. Microbial Biotechnology. 8:281-295. http://dx.doi.org/10.1111/1751-7915.12238
Ceuppens S, Boon N and Uyttendaele M. 2013. Diversity of Bacillus cereus group strains is reflected in their broad range of pathogenicity and diverse ecological lifestyles. FEMS Microbiology Ecology. 84:433-450. https://dx.doi.org/10.1111/1574-6941.12110
Chandler D, Bailey AS, Tatchell GM, Davison G, Graves J and Grant WP. 2011. The development, regulation and use of biopesticides for integrated pest management. Philosophical Transactions of the Royal Society B, Biological Sciences. 366:1987-1998. http://dx.doi.org/10.1098/rstb.2010.0390
Chen CY, Wang YH and Huang CJ. 2004. Enhancement of the antifungal activity of Bacillus subtilis F29-3 by the chitinase encoded by Bacillus circulans chiA gene. Canadian Journal of Microbiology. 50:451-454. http://dx.doi.org/10.1139/w04-027
Chen YY, Chen PC, Tsay TT. 2016. The biocontrol efficacy and antibiotic activity of Streptomyces plicatus on the oomycete Phytophthora capsica. Biological Control. 98:34-42. http://dx.doi.org/10.1016/j.biocontrol.2016.02.011
Cheng XL, Liu CJ and Yao JW. 2010. The Current Status, Development Trend and Strategy of the Bio-pesticide Industry in China. Hubei Agricultural Sciences. 49:2287-2290. Disponible en línea: http://en.cnki.com.cn/Article_en/CJFDTOTAL-HBNY201009086.htm
Chien-Jui H, Tang-Kai W, Shu-Chung C and Chao-Ying C. 2004. Identification of an Antifungal Chitinase from a Potential Biocontrol Agent, Bacillus cereus 28-9. Journal of Biochemistry and Molecular Biology. 38:82-88. http://dx.doi.org/10.5483/BMBRep.2005.38.1.082
Choudhary DK and Johri BN. 2009. Interactions of Bacillus spp. and plants with special reference to induced systemic resistance (ISR). Microbiological Research. 164:493-513. http://dx.doi.org/10.1016/j.micres.2008.08.007
Chowdhury SP, Hartmann A, Gao X and Borriss R. 2015. Biocontrol mechanism by root-associated Bacillus amyloliquefaciens FZB42 - a review. Frontiers in Microbiology. 6:780. https://doi.org/10.3389/fmicb.2015.00780
Cohn F. 1872. Untersuchungen Über Bakterien. Beitrage zur Biologie Pflanz. 1:127-1224.
Compant S, Duffy B, Nowak J, Clément C and Barka EA. 2005. Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Applied Environmental Microbiology. 71:4951-4959. http://dx.doi.org/10.1128/AEM.71.9.4951-4959.2005
Curtis TP, Sloan WT and Scannel JW. 2002. Estimating prokaryotic diversity and its limits. PNAS USA. 99:10494-10499. http://dx.doi.org/10.1073/pnas.142680199
de Olivar CG, Castillo CCE, Cañizales BLM y Olivar R. 2008. Control Biológico: Una herramienta para el desarrollo sustentable y sostenible. Academia Trujillo Venezuela. 7:50-74. Disponible en línea: http://erevistas.saber.ula.ve/index.php/academia/article/view/6030/5831
de Souza R, Ambrosini A and Passaglia LMP. 2015. Plant growth-promoting bacteria as inoculants in agricultural soils. Genetics and Molecular Biology. 38:401-419. http://dx.doi.org/10.1590/S1415-475738420150053
Environmental protection agency, EPA. 2004. Office of Pesticide Programs Biopesticides and Pollution Prevention Division (7511C). Disponible en línea: https://www3.epa.gov/pesticides/chem_search/ppls/070127-00012-20140207.pdf
Environmental protection agency, EPA. 2004. United States environmental protection agency. Disponible en línea: https://www3.epa.gov/pesticides/chem_search/ppls/069592-00012-20040902.pdf
Environmental protection agency, EPA. 2007. Office of Pesticide Programs Biopesticides and Pollution Prevention Division (7611C). Disponible en línea: https://www3.epa.gov/pesticides/chem_search/ppls/000004-00252-20070112.pdf
Environmental protection agency, EPA. 2013. Office of chemical safety and pollution prevention. Disponible en línea: https://www3.epa.gov/pesticides/chem_search/ppls/070127-00003-20130906.pdf
Errigton J. 2003. Regulation of endospore formation in Bacillus subtilis. Nature Reviews Microbiology. 1:117-126. http://dx.doi.org/10.1038/nrmicro750
European Food Safety Authority, EFSA. 2015. Statement on the update of the list of QPS-recommended biological agents intentionally added to food or feed as notified to EFSA. 2: Suitability of taxonomic units notified to EFSA until March 2015. EFSA Journal. 13:4138. http://dx.doi.org/10.2903/j.efsa.2015.4138
Falardeau J, Wise C, Novitsky L and Avis TJ. 2013. Ecological and mechanistic insights into the direct and indirect antimicrobial properties of Bacillus subtilis lipopeptides on plant pathogens. Journal of Chemical Ecology. 39:869-878. http://dx.doi.org/10.1007/s10886-013-0319-7
FAO, Food and Agriculture Organization of the United Nations. 2014. El estado mundial de la agricultura y la alimentación. FAO. Viale delle Terme di Caracalla 00153 Roma, Italia. Disponible en línea: http://www.fao.org/3/a-i4040s.pdf
Faraldo-Gómez JD and Sansom MS. 2003. Acquisition of siderophores in gram-negative bacteria. Nature Reviews Molecular Cell Biology. 4:105-116. http://dx.doi.org/10.1038/nrm1015
Fgaier H and Eberl HJ. 2011. Antagonistic control of microbial pathogens under iron limitations by siderophore producing bacteria in a chemostat setup. Journal of Theoretical Biology. 273:103-114. http://dx.doi.org/10.1016/j.jtbi.2010.12.034
Galindo E, Serrano-Carreón L, Gutiérrez CR, Balderas-Ruíz KA, Muñoz-Celaya AL, Mezo-Villalobos M y Arroyo-Colín J. 2015. Desarrollo histórico y los retos tecnológicos y legales para comercializar Fungifree AB®, el primer biofungicida 100% mexicano. TIP Revista Especializada en Ciencias Químico-Biológicas. 18:52-60. http://dx.doi.org/10.1016/j.recqb.2015.05.005
Glasset B, Herbin S, Guillier L, Vignaud M, Grout J, Pairaud S and Ramarao N. 2016. Bacillus cereus -induced food-borne outbreaks in France, 2007 to 2014: epidemiology and genetic characterisation. Eurosurveillance. 21:1-11. https://dx.doi.org/10.2807/1560-7917.es.2016.21.48.30413
Gong M, Wang JD, Zhang J, Yang H, Lu XF, Pei Y and Cheng JQ. 2006. Study of the Antifungal Ability of Bacillus subtilis Strain PY-1 in vitro and Identification of its Antifungal Substance (Iturin A). Acta Biochimica et Biophysica Sinica. 38:233–240. http://dx.doi.org/10.1111/j.1745-7270.2006.00157.x
Hayat R, Ali S, and Amara U. 2010. Soil beneficial bacteria and their role in plant growth promotion: a review. Annals of Microbiology. 60:579-598. http://dx.doi.org/10.1007/s13213-010-0117-1
Hoffmaster AR, Hill KK, Gee JE, Marston CK, De B K, Popovic T, Sue D, Wilkins PP, Avashia SB, Drumgoole R, Helma CH, Ticknor LO, Okinaka RT and Jackson PJ. 2006. Characterization of Bacillus cereus isolates associated with fatal pneumonias: strains are closely related to Bacillus anthracis and harbor B. anthracis virulence genes. Journal of Clinical Microbiology. ca44:3352-3360. https://dx.doi.org/10.1128/jcm.00561-06
Höfte H and Whiteley H. 1989. Insecticidal crystal proteins of Bacillus thuringiensis. Microbiological Reviews. 53:242-255. Disponible en línea: http://mmbr.asm.org/content/53/2/242.long
ISAGRO. 2017. Isagro, TAEGRO 2, biofungicide – Product Training. Disponible en línea: http://www.isagro-usa.com/assets/taegro-2-training-presentation-usa-final-2017-05-02.pdf
Jaaffar AKM, Parejko JA, Paulitz TC, Weller DM and Thomashow LS. 2017. Sensitivity of Rhizoctonia Isolates to Phenazine-1-Carboxylic Acid and Biological Control by Phenazine-Producing Pseudomonas spp. Phytopathology. 107:692-703. http://dx.doi.org/10.1094/PHYTO-07-16-0257-R
Kim JS, Lee J, Lee CH, Woo SY, Kamg H, Seo SG and Kim SH. 2015. Activation of pathogenesis-related genes by the rhizobacterium, Bacillus sp. JS, which induces systemic resistance in tobacco plants. Plant Pathology Journal. 31:195-201. http://dx.doi.org/10.5423/PPJ.NT.11.2014.0122
Kim MJ, Han JK, Park JS, Lee JS, Lee SH, Cho JI and Kim KS. 2016. Various Enterotoxin and Other Virulence Factor Genes Widespread Among Bacillus cereus and Bacillus thuringiensis Strains. Journal of Microbiology and Biotechnology. 25:872-879 https://dx.doi.org/10.4014/jmb.1502.02003
Kim Y, Kim H, Kim K, Chon J, Kim D and Seo K. 2016. High Occurrence Rate and Contamination Level of Bacillus cereus in Organic Vegetables on Sale in Retail Markets. Foodborne Pathogens and Disease. 13:656-660. https://dx.doi.org/10.1089/fpd.2016.2163
Kinsinger RF, Shirk MC and Fall R. 2003. Rapid surface motility in Bacillus subtilis is dependent on extracellular surfactin and potassium ion. Journal of Bacteriology. 185:5627-5631. Disponible en línea: http://jb.asm.org/content/185/18/5627.long
Kishore GK, Pande S and Podile AR. 2005. Biological Control of Late Leaf Spot of Peanut (Arachis hypogaea) with Chitinolytic Bacteria. Phytopathology. 95:1157-1165. http://dx.doi.org/10.1094/PHYTO-95-1157
Kumar A, Prakash A and Johri BN. 2011. Bacillus as PGPR in Crop Ecosystem. Bacteria in Agrobiology: Crop Ecosystems. 37-59. http://dx.doi.org/10.1007/978-3-642-18357-7_2
Latgé JP. 2007. The cell wall: a carbohydrate armour for the fungal cell. Molecular Microbiology. 66:279-290. http://dx.doi.org/10.1111/j.1365-2958.2007.05872.x
Layton C, Maldonado E, Monroy L, Corrales LC y Sánchez LC. 2011. Bacillus spp.; perspectiva de su efecto biocontrolador mediante antibiosis en cultivos afectados por fitopatógenos. Revista NOVA Publicación Científica en Ciencias Biomédicas. 9:177-187. http://dx.doi.org/10.22490/24629448.501
Li B, Li Q, Xu Z, Zhang N, Shen Q and Zhang R. 2014. Response of beneficial Bacillus amyloliquefaciens SQR9 to different soilborne fungal pathogens through the alteration of antifungal compounds production. Frontiers in Microbiology. 5:636. http://dx.doi.org/10.3389/fmicb.2014.00636
Li L, Ma J, Ibekwe AM, Wang Q and Yang C. 2016. Cucumber Rhizosphere Microbial Community Response to Biocontrol Agent Bacillus subtilis B068150. Agriculture. 6:1-15. https://dx.doi.org/10.3390/agriculture6010002
Li Y, Gu Y, Li J, Xu M, Wei Q and Wang Y. 2015. Biocontrol agent Bacillus amyloliquefaciens LJ02 induces systemic resistance against cucurbits powdery mildew. Frontiers Microbiology. 6:883. http://dx.doi.org/10.3389/fmicb.2015.00883
Liu D, Cai J, Xie C, Liu C and Chen Y. 2010. Purification and partial characterization of a 36-kDa chitinase from Bacillus thuringiensis subsp. colmeri, and its biocontrol potential. Enzyme Microbial Technology. 46:252-256. http://dx.doi.org/10.1016/j.enzmictec.2009.10.007
Liu Y, Lai Q, Göker M, Meier-kolthoff JP, Wang M, Sun Y and Shao Z. 2015. Genomic insights into the taxonomic status of the Bacillus cereus group. Scientific Reports. 5:1-11. http://dx.doi.org/10.1038/srep14082
López-Fernández S, Compat S, Vrhovsek U, Bianchedi PL, Sessitsch A, Pertot I and Campisano A. 2016. Grapevine colonization by endophytic bacteria shifts secondary metabolism and suggests activation of defense pathways. Plant and Soil. 405:155-175. http://dx.doi.org/10.1007/s11104-015-2631-1
LPSN, List of Prokaryotic names with Standing in Nomenclature. 2016. Genus Bacillus. Microbiology Society. Charles Darwin House, 12 Roger St, London WC1N 2JU, United Kingdom. http://www.bacterio.net/bacillus.html (consulta, mayo 2017)
Martínez-Absalón S, Rojas-Solís D, Hernández-León R, Prieto-Barajas C, Orozco-Mosqueda MC, Peña-Cabriales JJ, Sakuda S, Valencia-Cantero E and Santoyo G. 2014. Potential use and mode of action of the new strain Bacillus thuringiensis UM96 for the biological control of the gray mold phytopathogen Botrytis cinerea. Biocontrol Science Technology. 24:1349-1362. http://dx.doi.org/10.1080/09583157.2014.940846
Maughan H and van der Auwera G. 2011. Bacillus taxonomy in the genomic era finds phenotypes to be essential though often misleading. Infection, Genetics and Evolution. 11:789-797. http://dx.doi.org/10.1016/j.meegid.2011.02.001
May JJ, Wendrich TM and Marahiel MA. 2001. The dhb operon of Bacillus subtilis encodes the biosynthetic template for the catecholic siderophore 2,3-dihydroxybenzoate-glycine-threonine trimeric ester bacillibactin. Journal of Biological Chemistry. 276:7209-7217. http://dx.doi.org/10.1074/jbc.M009140200
Mc Spadden GBB. 2004 Ecology of Bacillus and Paenibacillus spp. in Agricultural Systems. Phytopathology. 94:1252-1258. http://dx.doi.org/10.1094/PHYTO.2004.94.11.1252
Meena KR and Kanwar SS. 2015. Lipopeptides as the Antifungal and Antibacterial Agents: Applications in Food Safety and Therapeutics. BioMed Research International. 2015:1-9. http://dx.doi.org/10.1155/2015/473050
Moebius N, Üzüm Z, Dijksterhuis J, Lackner G and Hertweck C. 2014. Active invasion of bacteria into living fungal cells. Microbiology and infectious disease. 1:1-20. http://dx.doi.org/10.7554/eLife.03007
Mora I, Cabrefiga J and Montesinos E. 2015. Cyclic Lipopeptide Biosynthetic Genes and Products, and Inhibitory Activity of Plant-Associated Bacillus against Phytopathogenic Bacteria. PLoS One. 10: e0127738. http://dx.doi.org/10.1371/journal.pone.0127738
Neilands JB. 1995. Siderophores: structure and function of microbial iron transport compounds. Journal of Biological Chemistry. 270:26723-26726. http://dx.doi.org/10.1074/jbc.270.45.26723
Niedmann LL y Meza-Basso L. 2006. Evaluación de Cepas Nativas de Bacillus thuringiensis Como una Alternativa de Manejo Integrado de la Polilla del Tomate (Tuta absoluta Meyrick; Lepidoptera: Gelechiidae) en Chile. Agricultura Técnica. 66:235-246. http://dx.doi.org/10.4067/S0365-28072006000300002
Novozymes. 2017. EcoGuard-GN, BioFungicide. Disponible en línea: http://www.kellysolutions.com/erenewals/documentsubmit/KellyData%5CNC%5Cpesticide%5CProduct%20Label%5C70127%5C70127-3%5C70127-3_ROOTS_ECOGUARD_GN_BIOFUNGICIDE_12_9_2010_2_33_14_PM.pdf
OECD, Organization for Economic Co-operation and Development. 2009. Series on pesticides no. 44. Report of Workshop on the Regulation of Biopesticides: Registration and Communication Issues. Disponible en línea: http://www.oecd.org/env/ehs/pesticides-biocides/ENV-JM-MONO(2009)19-ENG.pdf
Oh, M., Ham, J. and Cox, J. M. 2012. Diversity and toxigenicity among members of the Bacillus cereus group. International Journal of Food Microbiology, 152:1-8. https://dx.doi.org/10.1016/j.ijfoodmicro.2011.09.018
Olson S, Ranade A, Kurkjy N, Pang K and Hazekamp C. 2013. Green Dreams or Growth Opportunities: Assessing the Market Potential for “Greener” Agricultural Technologies. Lux Research Inc, Boston, MA, USA. Disponible en línea: https://portal.luxresearchinc.com/research/tidbit/15753
Olson S. 2015. An analysis of the biopesticide market now and where it is going. Outlooks on Pest Management. 26:203-206. http://dx.doi.org/10.1564/v26_oct_04
Ongena M and Jacques P. 2008. Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiolgy. 16:115-125. http://dx.doi.org/10.1016/j.tim.2007.12.009
Pal KK and Gardener BM. 2006. Biological Control of Plant Pathogens. The Plant Health Instructor. 1:1-25. http://dx.doi.org/10.1094/PHI-A-2006-1117-02
Pavic S, Brett M, Petric N, Lastre D, Smoljanovic M and Atkinson M. 2005. An outbreak of food poisoning in a kindergarten caused by milk powder containing toxigenic Bacillus subtilis and Bacillus licheniformis. Archiv Fur Lebensmittelhygiene. 56:20-22. Disponible en línea: https://www.tib.eu/en/search/id/BLSE%3ARN163847095/An-outbreak-of-food-poisoning-in-a-kindergarten/
Pérez-García A, Romero D and de Vicente A. 2011. Plant protection and growth stimulation by microorganisms: biotechnological applications of Bacilli in agriculture. Current Opinion in Biotechnology. 22:187-193. http://dx.doi.org/10.1016/j.copbio.2010.12.003
Pérez-Montaño F, Alías-Villegas RA, Bellogín RA, del Cerro P, Espuny MR, Jiménez-Guerrero I, López-Baena FJ, Ollero FJ and Cubo T. 2014. Plant growth promotion in cereal and leguminous agricultural important plants: From microorganism capacities to crop production. Microbiological Research. 169:325-336. http://dx.doi.org/10.1016/j.micres.2013.09.011
Piechulla B, Lemfack MC and Kai M. 2017. Effects of discrete bioactive microbial volatiles on plants and fungi. Plant, Cell & Environment. 40: 2042-2067. http://dx.doi.org/10.1111/pce.13011
Pieterse CMJ, Zamioudis C, Berendsen RL, Weller DM, Van Wees SC and Bakker PA. 2014. Induced Systemic Resistance by Beneficial Microbes. Annual Review of Phytopathology, 52:347-375. http://dx.doi.org/10.1146/annurev-phyto-082712-102340
Pieterse CMJ. 1998. A Novel Signaling Pathway Controlling Induced Systemic Resistance in Arabidopsis. The Plant cell. 10:1571-1580. https://doi.org/10.1105/tpc.10.9.1571
Porcar M y Juárez V. 2004. Aislamiento y establecimiento de una colección de Bacillus thuringiensis. Pp:69-100. In: Bravo A y Cerón J (eds). Bacillus thuringiensis en el control biológico. Universidad Nacional de Colombia, Bogotá.
Portela-Dussán DD, Chaparro-Giraldo A y López-Pazos SA. 2013. La biotecnología de Bacillus thuringiensis en la agricultura. Revista NOVA Publicación Científica en Ciencias Biomédicas. 11:87-96. http://dx.doi.org/10.22490/24629448.1031
Pretali L, Bernardo L, Butterfield TS, Trevisan M and Lucini L. 2016. Botanical and biological pesticides elicit a similar Induced Systemic Response in tomato (Solanum lycopersicum) secondary metabolism. Phytochemistry, 130:56-63. https://doi.org/10.1016/j.phytochem.2016.04.002
Raaijmakers JM and Mazzola M. 2012. Diversity and Natural Functions of Antibiotics Produced by Beneficial and Plant Pathogenic Bacteria. Annual Reviews of Phytopathology. 50:403-424. http://dx.doi.org/10.1146/annurev-phyto-081211-172908
Reyes A, Ricón G, López L, Martínez ZE y Quiñones E. 2015. Lucha entre microbios: una herramienta para el control de enfermedades de plantas. Revista Digital Universitaria UNAM. 16:2-15. Disponible en línea: http://www.revista.unam.mx/vol.16/num11/art92/
Rudrappa T, Czymme KJ, Paré PW and Bais HP. 2008. Root-Secreted Malic Acid Recruits Beneficial Soil Bacteria. Plant Physiology. 148:1547-1556. http://dx.doi.org/10.1104/pp.108.127613
Ryu C-M, Hu C-H, Reddy MS and Kloepper JW. 2003. Different signaling pathways of induced resistance by rhizobacteria in Arabidopsis thaliana against two pathovars of Pseudomonas syringae. New Phytologist. 160:413-20. http://dx.doi.org/10.1046/j.1469-8137.2003.00883.x
Sainju UM, Lenssen AW, Allen BL, Stevens WB and Jabro J. 2016. Nitrogen balance in response to dryland crop rotations and cultural practices. Agriculture, Ecosystems and Environment. 233:25-32. http://dx.doi.org/10.1016/j.agee.2016.08.023
Sauka DH y Benintende GB. 2008. Bacillus thuringiensis: generalidades. Un acercamiento a su empleo en el biocontrol de insectos lepidópteros que son plagas agrícolas. Revista argentina de microbiología. 40:124-140. Disponible en línea: http://www.scielo.org.ar/pdf/ram/v40n2/v40n2a13.pdf
Scharf DH, Heinekamp T and Brakjage AA. 2014. Human and Plant Fungal Pathogens: The Role of Secondary Metabolites. PLoS Pathogens. 10(1):e1003859. http://dx.doi.org/10.1371/journal.ppat.1003859
Selim HMM, Gomaa NM and Essa AMM. 2016. Application of endophytic bacteria for the biocontrol of Rhizoctonia solani (Cantharellales: Ceratobasidiaceae) damping-off disease in cotton seedlings. Biocontrol Science and Technology. 27:81-95. http://dx.doi.org/10.1080/09583157.2016.1258452
Shafi J, Tian H and Ji M. 2017. Bacillus species as versatile weapons for plant pathogens: a review. Biotechnology and Biotechnological Equipment. 31:446-459. http://dx.doi.org/10.1080/13102818.2017.1286950
Singh UB, Malvivya D, Wasiullah, Singh S, Imran M, Pathak N, Alam M, Rai JP, Singh RK, Sarma Bk, Sharma PK and Sharma AK. 2016. Compatible salt-tolerant rhizosphere microbe-mediated induction of phenylpropanoid cascade and induced systemic responses against Bipolaris sorokiniana (Sacc.) Shoemaker causing spot blotch disease in wheat (Triticum aestivum L.). Applied Soil Ecology: 108:300-306. http://dx.doi.org/10.1016/j.apsoil.2016.09.014
Soberón M y Bravo A. 2007. Las toxinas Cry de Bacillus thuringiensis: modo de acción y consecuencias de su aplicación. Biotecnología. 14:303-314. Disponible en línea: http://www.ibt.unam.mx/computo/pdfs/libro_25_aniv/capitulo_27.pdf
Tamez GP, Galán WLJ, Medrano RH, García GC, Rodríguez PC, Gómez FRA y Tamez GGRS. 2001. Bioinsecticidas: su empleo, producción y comercialización en México. Ciencia UANL. 4:143-152. Disponible en línea: http://www.redalyc.org/pdf/402/40240205.pdf
Tejera-Hernández B, Rojas-Badía MM y Heydrich-Pérez M. 2011. Potencialidades del género Bacillus en la promoción del crecimiento vegetal y el control de hongos fitopatógenos. Revista CENIC Ciencias Biológicas. 42:131-138. Disponible en línea: http://www.redalyc.org/pdf/1812/181222321004.pdf
Thyagarajan SI, Ramanathan G, Singaravelu S, Kandhasamy S, Perumal PT and Sivagnam UT. 2017. Microbial Siderophore as MMP inhibitor: An interactive approach on wound healing application. Wound Medicine. 17:7-14. http://dx.doi.org/10.1016/j.wndm.2016.12.002
Touré Y, Ongena M, Jacques P, Guiro A and Thonart P. 2004. Role of lipopeptides produced by Bacillus subtilis GA1 in the reduction of grey mould disease caused by Botrytis cinerea on apple. Journal of Applied Microbiology. 96: 1151-1160. http://dx.doi.org/ 10.1111/j.1365-2672.2004.02252.x
Trabelsi D and Mhamdi R. 2013. Microbial Inoculants and Their Impact on Soil Microbial Communities: A Review. BioMed Research International. ID 863240:1-11. http://dx.doi.org/10.1155/2013/863240
Valent BioSciences. 2017. DiPel WG (Bacillus thuringiensis). Disponible en línea: http://www.cropscience.bayer.cl/upfiles/etiquetas/Dipel_WG.pdf
Van der Heijden M, Bardgett R and van Straalen N. 2008. The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecology Letters. 11: 296-310. http://dx.doi.org/10.1111/j.1461-0248.2007.01139.x
Vargas-Ayala R, Rodríguez-Kábana R, Morgan-Jones G, Mclnroy JA and Kloepper JW. 2000. Shifts in Soil Microflora Induced by Velvetbean (Mucuna deeringiana) in Cropping Systems to Control Root-Knot Nematodes. Biological Control. 17:11-22. https://doi.org/10.1006/bcon.1999.0769
Vázquez-Ramírez MF, Rangel-Nnúñez JC, Ibarra JE y del Rincón-Castro MC. 2015. Evaluación como agentes de control biológico y caracterización de cepas mexicanas de Bacillus thuringiensis contra el gusano cogollero del maíz Spodoptera frugiperda. Interciencia. 40:397-402. Disponible en línea: http://www.redalyc.org/pdf/339/33938675006.pdf
Vlot AC, Dempsey DA and Klessig DF. 2009. Salicylic acid, a multifaceted hormone to combat disease. Annual Review of Phytopathology. 47:177–206 http://doi.org/10.1146/annurev.phyto.050908.135202
Wang W, Chen LN, Wu H, Zang H, Yang Y, Xie S and Gao X. 2013. Comparative proteomic analysis of rice seedlings in response to inoculation with Bacillus cereus. Letters in Applied Microbiology. 56(3):208-215. http://dx.doi.org/10.1111/lam.12035
Wang X, Wang L, Wang J, Jin P, Liu H and Zheng Y. 2014. Bacillus cereus AR156-Induced Resistance to Colletotrichum acutatum Is Associated with Priming of Defense Responses in Loquat Fruit. PLos ONE. 9(11):e112494. http://dx.doi.org/10.1371/journal.pone.0112494
Wilson BR, Bogdan AR, Miyazawa M, Hashimoto K and Tsuji Y. 2016. Siderophores in Iron Metabolism: From Mechanism to Therapy Potential. Trends in Molecular Medicine. 22:1077-1090. http://dx.doi.org/10.1016/j.molmed.2016.10.005
Xu C, Wang BC, Yu Z and Sun M. 2014. Structural Insights into Bacillus thuringiensis Cry, Cyt and Parasporin Toxins. Toxins. 6:2732-2770. http://dx.doi.org/10.3390/toxins6092732
Xu Z, Shao J, Li B, Yan X, Shen Q and Zhang R. 2013. Contribution of bacillomycin D in Bacillus amyloliquefaciens SQR9 to antifungal activity and biofilm formation. Applied Environmental Microbiology. 79:808-815. http://dx.doi.org/10.1128/aem.02645-12
Yan L, Jing T, Yujun Y, Bin L, Hui L and Chun L. 2011. Biocontrol Efficiency of Bacillus subtilis SL-13 and Characterization of an Antifungal Chitinase. Chinese Journal Chemical Engineering. 19:128-134. http://dx.doi.org/10.1016/s1004-9541(09)60188-9
You C, Zhang C, Kong F, Feng C and Wang J. 2016. Comparison of the effects of biocontrol agent Bacillus subtilis and fungicide metalaxyl – mancozeb on bacterial communities in tobacco rhizospheric soil. Ecological Engineering. 91:119-125. http://dx.doi.org/10.1016/j.ecoleng.2016.02.011
Yu X, Ai C, Xin L and Zhou G. 2011. The siderophore-producing bacterium, Bacillus subtilis CAS15, has a biocontrol effect on Fusarium wilt and promotes the growth of pepper. European Journal of Soil Biology. 47:138-145. http://dx.doi.org/10.1016/j.ejsobi.2010.11.001
Zhang B, Qin Y, Han Y, Dong C, Li P and Shang Q. 2016. Comparative proteomic analysis reveals intracellular targets for bacillomycin L to induce Rhizoctonia solani Kühn hyphal cell death. Biochimica Biophysica Acta (BBA), Proteins and Proteomics. 1864:1152-1159. http://dx.doi.org/10.1016/j.bbapap.2016.06.003
Zhang X, Huang Y, Harvey PR, Ren Y, Zhang G, Zhou H and Yang H. 2012. Enhancing plant disease suppression by Burkholderia vietnamiensis through chromosomal integration of Bacillus subtilis chitinase gene chi113. Biotechnology Letters. 34:287-293. http://dx.doi.org/10.1007/s10529-011-0760-z
DOI: http://dx.doi.org/10.18781/R.MEX.FIT.1706-5
Refbacks
- There are currently no refbacks.