O gênero Bacillus aplicado ao controle biológico de doenças de plantas

Thiago Anchieta de  Melo; Ingrid Tayane Vieira da Silva do  Nascimento; Ilka Márcia Ribeiro de Souza  Serra

doi:10.33448/rsd-v10i9.17817

Authors

Thiago Anchieta de Melo Universidade Estadual do Maranhão https://orcid.org/0000-0003-0796-6388
Ingrid Tayane Vieira da Silva do Nascimento Universidade Estadual do Maranhão https://orcid.org/0000-0003-2858-4549
Ilka Márcia Ribeiro de Souza Serra Universidade Estadual do Maranhão https://orcid.org/0000-0003-1622-5434

DOI:

https://doi.org/10.33448/rsd-v10i9.17817

Keywords:

Biocontrol; Bacterium; Phytopathology; Biological management.

Abstract

To meet the growing world demand for food free of chemical residues, many microorganisms have been used as biocontrol agents for important phytopathogens and pests in important commercial crops. The genus Bacillus is widely used for this purpose, so the objective of this article was to concentrate the main updates on the genus, considering biological, taxonomic, genetic aspects and the applicability and potential of this group of prokaryotes in biological management actions of other organisms. The research demonstrates great versatility of the Bacillus genus with the capacity to occupy different niches, among them: soil, forage, water, and food; in addition to having many characteristics that define a good biological control agent, they are also widely applied in the management of phytomatomatoids. With technological advances, through studies of molecular biology, it became evident the possibility of using the genus Bacillus in biological management, thus being the focus of important scientific research.

Author Biographies

Thiago Anchieta de Melo, Universidade Estadual do Maranhão

Atua como professor da disciplina Microbiologia nos cursos de Engenharia Agronômica e Ciências Biológicas na Universidade Estadual do Maranhão (UEMA), Campus São Luís e também como professor das disciplinas Biologia de Fungos, Diversidade de Microrganismos, Microbiologia Ambiental e Fundamentos em Biotecnologia oferecidas ao curso de Ciências Biológicas da UEMA. É Engenheiro Agrônomo pela Universidade Estadual do Maranhão (UEMA) (2011) e licenciado para o ensino de Biologia, pela Universidade Cruzeiro do Sul (2020). Mestre (2013) e doutor (2017) em Ciências (Fitopatologia) pela Escola Superior de Agricultura Luiz de Queiroz/Universidade de São Paulo (ESALQ/USP). Tem experiência na área de Agronomia/Microbiologia/Fitopatologia com ênfase em Fisiologia do Parasitismo da interação planta-patógeno e Indução de Resistência dos vegetais, especialmente frutas e hortaliças na fase de pós-colheita. Colaborador na especialização em Ensino de Genética e Educação Especial/Educação Inclusiva pelo Núcleo de Tecnologias para Educação UEMANET/Universidade Estadual do Maranhão, UEMA. Membro do comitê de quarentena vegetal da Estação Quarentenária da SGS do Brasil LTDA. Consultor Acadêmico e Diretor da Easy Paper Consultoria, empresa que presta assessoria a todos os níveis acadêmicos e oferece cursos de aperfeiçoamento sendo estes: Metodologia da Pesquisa Científica, Escrita Científica, Prática aplicada à Plataforma Lattes e Estatística Experimental.

Ingrid Tayane Vieira da Silva do Nascimento, Universidade Estadual do Maranhão

Graduada em Ciências Biológicas (Licenciatura e Bacharelado) pela Universidade Estadual do Maranhão (UEMA), Mestra em Recursos Aquáticos e Pesca - UEMA. Possui experiência na área de Microbiologia, Educação Ambiental, Micologia, Saúde coletiva e Histopatologia. Ministrou disciplina no curso Tecnologia de Alimentos oferecido pela Universidade Estadual do Maranhão, Núcleo de Tecnologias para Educação - UemaNet. Desenvolveu dissertação na área de biopatologia de organismos aquáticos com ênfase em patologia de peixes causados por fungos. Atualmente é técnica responsável pelo laboratório de Microbiologia do curso de Ciências Biológicas da UEMA e atua como professora tutora no curso de especialização Ciência é 10 oferecido pela Universidade Aberta do Brasil (UAB) oferecido pela Núcleo de Tecnologias para Educação UEMANET/Universidade Estadual do Maranhão, UEMA.

Ilka Márcia Ribeiro de Souza Serra, Universidade Estadual do Maranhão

Possui graduação em Agronomia pela Universidade Estadual do Maranhão (2001), mestrado em Fitossanidade Com Transferencia Direta Para o Doutorado pela Universidade Federal Rural de Pernambuco (2003) e Doutorado em Fitopatologia pela Universidade Federal Rural de Pernambuco (2006). Pós Doutorado pela Universidade de Coimbra, em Tecnologias Digitais. Professora Adjunto IV DE MICROBIOLOGIA do Depto. de Química e Biologia- UEMA. Atua na área de Agronomia e Biologia, com ênfase em Fitopatologia, atuando principalmente nos seguintes temas: Taxonomia e Fisiologia de Fungos, Indução de Resistência, Microbiologia Geral e Microbiologia de Pescados e Ecologia de Recursos Pesqueiro. Cumulativamente, exerce a Coordenação Geral do Núcleo de Tecnologias para Educação da Universidade Estadual do Maranhão, representando-a junto ao Sistema Universidade Aberta do Brasil-UAB e à Rede e-Tec Brasil do Ministério da Educação. Nessa área, atua na pesquisa com enfoque em Gestão em EaD, TICS e EaD e Formação de Professores em cursos intermediados por tecnologias educacionais. Excerceu o cargo de Presidente do Forúm Nacional de Coordenadores da Universidade Aberta do Brasil-FORUAB/ CAPES de 2016 a 2019. E Integrante da Camara de EaD da Associação Brasileira dos Reitores das Universidades Estaduais e Municipais (ABRUEM). E editora chefe da Revista cientifica TICs e EaD em Foco - UEMA.

References

Almenar, E., Del Valle, V., Catala, R., & Gavara, R. (2007). Active package for wild strawberry fruit (Fragaria vesca L.). Journal of Agricultural and Food chemistry, 55(6), 2240-2245.

Alves, E. (2007). Mecanismos estruturais na resistência de plantas a patógenos. Summa Phytopathol, 33, 154-156.

Araujo, F. D. (2008). Inoculação de sementes com Bacillus subtilis, formulado com farinha de ostras e desenvolvimento de milho, soja e algodão. Ciência e Agrotecnologia, 32(2), 456-462.

Araújo, F. F. D., & Marchesi, G. V. P. (2009). Uso de Bacillus subtilis no controle da meloidoginose e na promoção do crescimento do tomateiro. Ciência Rural, 39(5), 1558-1561.

Araújo, F. F. D., Silva, J. F. V., & Araújo, A. S. F. D. (2002). Influência de Bacillus subtilis na eclosão, orientação e infecção de Heterodera glycines em soja. Ciência Rural, 32(2), 197-203.

Azevedo, J. L., Maccheroni Jr, W., Pereira, J. O., & de Araújo, W. L. (2000). Endophytic microorganisms: a review on insect control and recent advances on tropical plants. Electronic Journal of Biotechnology, 3(1), 15-16.

Bais, H. P., Fall, R., & Vivanco, J. M. (2004). Biocontrol of Bacillus subtilis against infection of Arabidopsis roots by Pseudomonas syringae is facilitated by biofilm formation and surfactin production. Plant physiology, 134(1), 307-319.

Bettucci, L., & Alonso, R. (1997). A comparative study of fungal populations in healthy and symptomatic twigs of Eucalyptus grandis in Uruguay. Mycological Research, 101(9), 1060-1064.

Bleich, R., Watrous, J. D., Dorrestein, P. C., Bowers, A. A., & Shank, E. A. (2015). Thiopeptide antibiotics stimulate biofilm formation in Bacillus subtilis. Proceedings of the National Academy of Sciences, 112(10), 3086-3091.

Bouton, J. H., & Hopkins, A. A. (2003). Commercial applications of endophytic fungi. Clavicipitalean fungi: evolutionary biology, chemistry, biocontrol and cultural impacts, 495-516.

Cankar, K., Kraigher, H., Ravnikar, M., & Rupnik, M. (2005). Bacterial endophytes from seeds of Norway spruce (Picea abies L. Karst). FEMS microbiology letters, 244(2), 341-345.

Cavaglieri, L. R., Passone, A., & Etcheverry, M. G. (2004). Correlation between screening procedures to select root endophytes for biological control of Fusarium verticillioides in Zea mays L. Biological Control, 31(3), 259-267.

Chen, H., Xiao, X., Wang, J., Wu, L., Zheng, Z., & Yu, Z. (2008). Antagonistic effects of volatiles generated by Bacillus subtilis on spore germination and hyphal growth of the plant pathogen, Botrytis cinerea. Biotechnology letters, 30(5), 919-923.

Choudhary, D. K., Prakash, A., & Johri, B. N. (2007). Induced systemic resistance (ISR) in plants: mechanism of action. Indian Journal of Microbiology, 47(4), 289-297.

Claus, D.R.; Berkeley, C.W. The genus Bacillus. SNEATH, P.H.A. (Eds.). (1986). Bergey’s manual of systematic bacteriology. v. 2. Baltimore: Williams and Wilkins.

Coombs, J. T., & Franco, C. M. (2003). Visualization of an endophytic Streptomyces species in wheat seed. Applied and Environmental Microbiology, 69(7), 4260-4262.

Coombs, J. T., Michelsen, P. P., & Franco, C. M. (2004). Evaluation of endophytic actinobacteria as antagonists of Gaeumannomyces graminis var. tritici in wheat. Biological control, 29(3), 359-366.

Durham, D. R., Stewart, D. B., & Stellwag, E. J. (1987). Novel alkaline-and heat-stable serine proteases from alkalophilic Bacillus sp. strain GX6638. Journal of Bacteriology, 169(6), 2762-2768.

Durmaz, E., Hu, Y., Aroian, R. V., & Klaenhammer, T. R. (2016). Intracellular and extracellular expression of Bacillus thuringiensis crystal protein Cry5B in Lactococcus lactis for use as an anthelminthic. Applied and environmental microbiology, 82(4), 1286-1294.

El-Tarabily, K. A. (2003). An endophytic chitinase-producing isolate of Actinoplanes missouriensis, with potential for biological control of root rot of lupin caused by Plectosporium tabacinum. Australian Journal of Botany, 51(3), 257-266.

Eppinger, M., Bunk, B., Johns, M. A., Edirisinghe, J. N., Kutumbaka, K. K., Koenig, S. S., ... & Vary, P. S. (2011). Genome sequences of the biotechnologically important Bacillus megaterium strains QM B1551 and DSM319. Journal of bacteriology, 193(16), 4199-4213.

Estrela, C. (2018). Metodologia científica: ciência, ensino, pesquisa. Artes Médicas.

Fernandes, R. H., Vieira, B. S., Fuga, C. A. G., & Lopes, E. A. (2014). Pochonia chlamydosporia e Bacillus subtilis no controle de Meloidogyne incognita e M. javanica em mudas de tomateiro. Bioscience Journal, 30(1).

Ferraz, S., & VALLE, L. D. (1997). Controle de fitonematóides por plantas antagônicas. Viçosa: UFV.

Ficth, W. M., & Margoliash, E. (1967). Construction of phylogenetic trees: a method based on mutation distances as estimated from cytochrome c sequences is of general applicability. Science, 155, 279-284.

Fox, G. E., Pechman, K. R., & Woese, C. R. (1977). Comparative cataloging of 16S ribosomal ribonucleic acid: molecular approach to procaryotic systematics. International Journal of Systematic and Evolutionary Microbiology, 27(1), 44-57.

Freitas, L.G.; Oliveira, R.D.L.; Ferraz, S. (2001). Introdução à nematologia. Universidade Federal de Viçosa.

Germida, J. J., Siciliano, S. D., Renato de Freitas, J., & Seib, A. M. (1998). Diversity of root-associated bacteria associated with field-grown canola (Brassica napus L.) and wheat (Triticum aestivum L.). FEMS Microbiology Ecology, 26(1), 43-50.

Gordon, R. E. (1981). One hundred and seven years of the genus Bacillus. The Aerobic Endospore Forming Bacteria, 9-45.

Gordon, R. E., Haynes, W. C., & Pang, C. H. N. (1973). The genus bacillus (No. 427). Agricultural Research Service, US Department of Agriculture.

Griffitts, J. S., Haslam, S. M., Yang, T., Garczynski, S. F., Mulloy, B., Morris, H., ... & Aroian, R. V. (2005). Glycolipids as receptors for Bacillus thuringiensis crystal toxin. Science, 307(5711), 922-925.

Guettler, M., & Hanson, R. S. (1988, May). Characterization of a Methanol Oxidizing Thermophilic Member of the Genus Bacillus. In Poster Session Materials presented at the 88th Annual Meeting of the American Society for Microbiology, Wednesday.

Hallmann, J., Faupel, A., Krechel, A., Sikora, R., & Berg, G. (2004). Endophytic bacteria and biological control of nematodes. IOBC/WPRS Bulletin, 27, 83-95.

Hallmann, J., Quadt-Hallmann, A., Mahaffee, W. F., & Kloepper, J. W. (1997). Bacterial endophytes in agricultural crops. Canadian journal of microbiology, 43(10), 895-914.

Hammami, I., Rhouma, A., Jaouadi, B., Rebai, A., & Nesme, X. (2009). Optimization and biochemical characterization of a bacteriocin from a newly isolated Bacillus subtilis strain 14B for biocontrol of Agrobacterium spp. strains. Letters in applied microbiology, 48(2), 253-260.

Handoo, Z.A. (1998). Plant parasitic nematodes. Disponível em <http://www.ars.usda.gov/ Services/docs/htm>. Acesso em 20 mai. 2015.

Henning, K.; Villforth, F. (1995). Experimentalle untersuchungen zur frage der bacteriensymbiose in Höeheren Pflanzen und Ihre Beeinflussung durch “Leitemente”. Biochemische Zeitschrift 350(1), 117-125.

Huang, X. W., Niu, Q. H., Zhou, W., & Zhang, K. Q. (2005). Bacillus nematocida sp. nov., a novel bacterial strain with nematotoxic activity isolated from soil in Yunnan, China. Systematic and applied microbiology, 28(4), 323-327.

Hunger, W., & Claus, D. (1981). Taxonomic studies on Bacillus megaterium and on agarolytic Bacillus strains. The aerobic endospore-forming bacteria: classification and identification, 217-239.

Iatsenko, I., Corton, C., Pickard, D. J., Dougan, G., & Sommer, R. J. (2014). Draft genome sequence of highly nematicidal Bacillus thuringiensis DB27. Genome announcements, 2(1).

Ivanova, N., Sorokin, A., Anderson, I., Galleron, N., Candelon, B., Kapatral, V., ... & Kyrpides, N. (2003). Genome sequence of Bacillus cereus and comparative analysis with Bacillus anthracis. Nature, 423(6935), 87-91.

De Vrind, J. P., Boogerd, F. C., & de Vrind-de Jong, E. W. (1986). Manganese reduction by a marine Bacillus species. Journal of bacteriology, 167(1), 30-34.

Kado, C.I. (1992). Plant pathogenic bacteria. In: Balows, A.; Trüper, H.G.; Dworkin, M.; Harder, W.; Schleifer, K.H. (Ed.). The prokaryotes. New York: Springer-Verlag, 660-662.

Kai, M., Effmert, U., Berg, G., & Piechulla, B. (2007). Volatiles of bacterial antagonists inhibit mycelial growth of the plant pathogen Rhizoctonia solani. Archives of microbiology, 187(5), 351-360.

Keynan, A., & Sandler, N. (1983). Spore research in historical perspective.

Kiraly, Z., & Hornok, L. (1997). Molecular aspects of plant-pathogen interactions in relation to novel strategies of breeding for disease resistance. Acta phytopathologica et entomologica hungarica, 32(1-2), 1-28.

Kitada, M. A. K. I. O., & Horikoshi, K. O. K. I. (1987). Bioenergetic properties of alkalophilic Bacillus sp. strain C-59 on an alkaline medium containing K2CO3. Journal of bacteriology, 169(12), 5761-5765.

Kitada, M. A. K. I. O., Onda, K. E. N. S. U. K. E., & Horikoshi, K. O. K. I. (1989). The sodium/proton antiport system in a newly isolated alkalophilic Bacillus sp. Journal of bacteriology, 171(4), 1879-1884.

Kunst, F., Debarbouille, M., Msadek, T., Young, M., Mauel, C., Karamata, D., ... & Dedonder, R. (1988). Deduced polypeptides encoded by the Bacillus subtilis sacU locus share homology with two-component sensor-regulator systems. Journal of bacteriology, 170(11), 5093-5101.

Koch, D.; Mirza, Z.; Hu, Y. (2016). Crystal protein Cry5B as a novel and powerful anthelmintic. Massachusetts: Center for Clinical and Translational Science. Disponível em <http://escholarship.umassmed.edu/cgi/viewcontent.cgi?article=1397&context=cts_retreat>. Acesso em 27 jul. 2016.

Kunkel, B. A., & Grewal, P. S. (2003). Endophyte infection in perennial ryegrass reduces the susceptibility of black cutworm to an entomopathogenic nematode. Entomologia Experimentalis et Applicata, 107(2), 95-104.

Kupper, K. C., Gimenes-Fernandes, N., & Goes, A. D. (2003). Controle biológico de Colletotrichum acutatum, agente causal da queda prematura dos frutos cítricos. Fitopatologia brasileira, 28(3), 251-257.

Lanna Filho, R., Ferro, H. M., & de Pinho, R. S. C. (2010). Controle biológico mediado por Bacillus subtilis. Revista Trópica: Ciências Agrárias e Biológicas, 4(2).

Leelasuphakul, W., Hemmanee, P., & Chuenchitt, S. (2008). Growth inhibitory properties of Bacillus subtilis strains and their metabolites against the green mold pathogen (Penicillium digitatum Sacc.) of citrus fruit. Postharvest Biology and Technology, 48(1), 113-121.

Li, J., Zou, C., Xu, J., Ji, X., Niu, X., Yang, J., ... & Zhang, K. Q. (2015). Molecular mechanisms of nematode-nematophagous microbe interactions: basis for biological control of plant-parasitic nematodes. Annual review of phytopathology, 53, 67-95.

Li, X. Q., Wei, J. Z., Tan, A., & Aroian, R. V. (2007). Resistance to root‐knot nematode in tomato roots expressing a nematicidal Bacillus thuringiensis crystal protein. Plant biotechnology journal, 5(4), 455-464.

Ludwig, J., Moura, A. B., & Gomes, C. B. (2013). Potencial da microbiolização de sementes de arroz com rizobactérias para o biocontrole do nematoide das galhas. Tropical Plant Pathology, 38(3), 264-268.

Luo, H., Xiong, J., Zhou, Q., Xia, L., & Yu, Z. (2013). The effects of Bacillus thuringiensis Cry6A on the survival, growth, reproduction, locomotion, and behavioral response of Caenorhabditis elegans. Applied microbiology and biotechnology, 97(23), 10135-10142.

Maciel, S. L., & Ferraz, L. C. C. B. (1996). Reprodução de Meloidogyne incognita raça 2 e de Meloidogyne javanica em oito espécies de plantas medicinais. Scientia Agricola, 53(2-3), 232-236.

Maget-Dana, R., Thimon, L., Peypoux, F., & Ptak, M. (1992). Surfactin/iturin A interactions may explain the synergistic effect of surfactin on the biological properties of iturin A. Biochimie, 74(12), 1047-1051.

Manjula, K., & Podile, A. R. (2005). Increase in seedling emergence and dry weight of pigeon pea in the field with chitin-supplemented formulations of Bacillus subtilis AF 1. World Journal of Microbiology and Biotechnology, 21(6), 1057-1062.

Mcafee, B.J.; Taylor, A. (2001). Some aspects of the ecology and physiology off ungi isolated predominently from the wood of trees of the northern temperate forest. Proceedings of the Nova Scotian Institute of Science, 41(1), 160-213.

McInroy, J. A., & Kloepper, J. W. (1995). Survey of indigenous bacterial endophytes from cotton and sweet corn. Plant and soil, 173(2), 337-342.

McNeill, M. R., Proffitt, J. R., Barlow, N. D., & Goldson, S. L. (2003). Population regulation of Argentine stem weevil Listronotus bonariensis (Kuschel)(Coleoptera: Curculionidae) in dryland New Zealand pastures: a multitrophic interaction. Environmental entomology, 32(4), 771-779.

Monteiro, A. R. (1970). Dorylaimoidea de cafezais paulistas (Nemata, Dorylaimida). Escola Superior de Agricultura Luiz de Queiroz, Piracicaba, SP (Brasil).

Musson, G. (1994). Ecology and effects of endophytic bacteria in plants (Doctoral dissertation, Auburn University).

Nakamura, L. K. (1987). Bacillus alginolyticus sp. nov. and Bacillus chondroitinus sp. nov., two alginate-degrading species. International Journal of Systematic and Evolutionary Microbiology, 37(3), 284-286.

Nakamura, L.K. (1984). Bacillus pulvifasciens sp. nov., nom. rev. International Journal of Systematic Bacteriology 34(1), 410-413.

Nakamura, L. K., Blumenstock, I., & Claus, D. (1988). Taxonomic Study of Bacillus coagulans Hammer 1915 with a Proposal for Bacillus smithii sp. nov. International Journal of Systematic and Evolutionary Microbiology, 38(1), 63-73.

Ngugi, H. K., Dedej, S., Delaplane, K. S., Savelle, A. T., & Scherm, H. (2005). Effect of flower-applied Serenade biofungicide (Bacillus subtilis) on pollination-related variables in rabbiteye blueberry. Biological Control, 33(1), 32-38.

Niu, Q., Huang, X., Zhang, L., Xu, J., Yang, D., Wei, K., ... & Zhang, K. Q. (2010). A Trojan horse mechanism of bacterial pathogenesis against nematodes. Proceedings of the National Academy of Sciences, 107(38), 16631-16636.

Norris, J. R., Berkeley, R. C. W., Logan, N. A., & O'donnell, A. G. (1981). The genera Bacillus and Sporolactobacillus. The prokaryotes, 2, 1711-1742.

Nunes, H. T., Monteiro, A. C., & Pomela, A. W. V. (2010). Uso de agentes microbianos e químico para o controle de Meloidogyne incognita em soja. Acta Scientiarum. Agronomy, 32(3), 403-409.

Ongena, M., Duby, F., Jourdan, E., Beaudry, T., Jadin, V., Dommes, J., & Thonart, P. (2005). Bacillus subtilis M4 decreases plant susceptibility towards fungal pathogens by increasing host resistance associated with differential gene expression. Applied Microbiology and Biotechnology, 67(5), 692-698.

Ongena, M., Jourdan, E., Adam, A., Paquot, M., Brans, A., Joris, B., ... & Thonart, P. (2007). Surfactin and fengycin lipopeptides of Bacillus subtilis as elicitors of induced systemic resistance in plants. Environmental microbiology, 9(4), 1084-1090.

Pal, K. K., & Gardener, B. M. (2006). Biological control of plant pathogens. The plant health instructor, 2, 1117-1142.

Pascholati, S.F. (2011). Fisiologia do parasitismo: como os patógenos atacam as plantas. In: Amorin, L.; Rezende, J.A.M.; Bergamin Filho, A. Manual de Fitopatologia: princípios e conceitos 1(1), 545-591.

Pascholati, S. F., Melo, T. D., & Dalio, R. J. D. (2015). Indução de resistência contra patógenos: definição e perspectivas de uso. Visão agrícola nº13 jul, 110-112.

Patiño-Navarrete, R.; Sanchis, V. (2016). Evolutionary processes and environmental factors underlying the genetic diversity and lifestyles of Bacillus cereus group bacteria. Research in Microbiology. Disponível em <http://www.sciencedirect.com/science/article/pii/S092325081 6300754>. Acesso em 25 de jul. 2016.

Perchat, S., Dubois, T., Zouhir, S., Gominet, M., Poncet, S., Lemy, C., ... & Lereclus, D. (2011). A cell–cell communication system regulates protease production during sporulation in bacteria of the Bacillus cereus group. Molecular microbiology, 82(3), 619-633.

Persello‐Cartieaux, F., Nussaume, L., & Robaglia, C. (2003). Tales from the underground: molecular plant–rhizobacteria interactions. Plant, Cell & Environment, 26(2), 189-199.

Pettit, R. E., Taber, R. A., & Foster, B. G. (1968). Occurrence of Bacillus subtilis in peanut kernels. Phytopathology, 58(2), 254-255.

Pichinoty, F., Asselineau, J., & Mandel, M. (1984, September). Caractérisation biochimique de Bacillus benzoevorans sp. nov., une nouvelle espèce filamenteuse, engainée et mésophile, dégradant divers acides aromatiques et phénols. In Annales de l'Institut Pasteur/Microbiologie (Vol. 135, No. 2, pp. 209-217). Elsevier Masson.

Pichinoty, F., Waterbury, J. B., Mandel, M., & Asselineau, J. (1986, January). Bacillus gordonae sp. nov., une nouvelle espece appartenant au second groupe morphologique, dégradant divers composés aromatiques. In Annales de l'Institut Pasteur/Microbiologie (Vol. 137, No. 1, pp. 65-78). Elsevier Masson.

Pieterse, C. M., & Van Loon, L. C. (2004). NPR1: the spider in the web of induced resistance signaling pathways. Current opinion in plant biology, 7(4), 456-464.

Prasad, S. S. S. V., Tilak, K. V. B. R., & Gollakota, K. G. (1972). Role of Bacillus thuringiensis var. thuringiensis on the larval survivability and egg hatching of Meloidogyne spp., the causative agent of root knot disease. J Invertebrate Pathol.

Preston, J. F., Dickson, D. W., Maruniak, J. E., Nong, G., Brito, J. A., Schmidt, L. M., & Giblin-Davis, R. M. (2003). Pasteuria spp.: systematics and phylogeny of these bacterial parasites of phytopathogenic nematodes. Journal of Nematology, 35(2), 198.

Raaijmakers, J. M., De Bruijn, I., Nybroe, O., & Ongena, M. (2010). Natural functions of lipopeptides from Bacillus and Pseudomonas: more than surfactants and antibiotics. FEMS microbiology reviews, 34(6), 1037-1062.

Ravichandra, N.G. (2014). Phytonematodes: treat to horticulture. Horticultural Nematology 2(1), 5-16.

Redlin, S.C.; Carris, L. M. (1996). Endophytic fungi in grasses and woody plants: systematics, ecology and evolution. Minneapolis: APS Press, 231.

Riggs, P. J., Chelius, M. K., Iniguez, A. L., Kaeppler, S. M., & Triplett, E. W. (2001). Enhanced maize productivity by inoculation with diazotrophic bacteria. Functional Plant Biology, 28(9), 829-836.

Romeiro, R. D. S. (2007). Controle biológico de doenças de plantas: fundamentos. Universidade Federal de Viçosa.

Rosson, R. A., & Nealson, K. H. (1982). Manganese binding and oxidation by spores of a marine bacillus. Journal of Bacteriology, 151(2), 1027-1034.

Ryu, C. M., Farag, M. A., Hu, C. H., Reddy, M. S., Kloepper, J. W., & Paré, P. W. (2004). Bacterial volatiles induce systemic resistance in Arabidopsis. Plant physiology, 134(3), 1017-1026.

Saitou, N., & Nei, M. (1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular biology and evolution, 4(4), 406-425.

Sanahuja, G., Banakar, R., Twyman, R. M., Capell, T., & Christou, P. (2011). Bacillus thuringiensis: a century of research, development and commercial applications. Plant biotechnology journal, 9(3), 283-300.

Schendel, F. J., Bremmon, M. G., Flickinger, M. G., & RS, H. (1989). L-Lysine production from methanol at high cell densities of MGA3, a thermophilic Bacillus. In Abstract from 1989 ASM Annual Meeting (published Mar. 21, 1989).

Schulthess, F. M., & Faeth, S. H. (1998). Distribution, abundances, and associations of the endophytic fungal community of Arizona fescue (Festuca arizonica). Mycologia, 90(4), 569-578.

Scott, B.; Young, C. (2003). Genetic manipulation of clavicipitalean endophytes. In: ___. Clavicipitalean fungi: evolutionary biology, chemistry, biocontrole and cultural impacts. New York USA: Marcel Dekker Inc., 425-443.

Sikora, R. A. (1992). Management of the antagonistic potential in agricultural ecosystems for the biological control of plant parasitic nematodes. Annual review of phytopathology, 30, 245-270.

Padgham, J. L., & Sikora, R. A. (2007). Biological control potential and modes of action of Bacillus megaterium against Meloidogyne graminicola on rice. Crop protection, 26(7), 971-977.

Slepecky, R.A. (1972). Ecology of bacterial sporeformers. In: Halvorson, H.G.; Hanson, R.; Campbell, L.L. (Ed.). Spores V. Washington, DC: American Society of Microbiology, 297-313.

Slepecky, R.A.; Hemphill, H.E. (2006). The genus Bacillus – nonmedical. In: Dworkin, M.; Falkov, S.; Rosenberg, E.; Schileifer, K-H.; Stackebrandt, E. (Ed.). The prokaryotes. A handbook on the biology of bacteria. Bacteria: Frimicutes, Cyanobacteria. 3rd. Ed. v.4. Minneapolis: Springer.

Slepecky, R.A.; Leadbetter, E.R. (1984). On the prevalence and roles of sporeforming bacteria and their spores in nature. Hurst, A.; Gould, G.W. (Ed.). The bacterial spore. v.2. London: Academic Press, 79-99.

Slepecky, R.A.; Leadbetter, E.R. (1977). The diversity of spore-forming bacteria: some ecological implications. In: Barker, A.N.; Wolf, J.; Ellar, D.J.; Dring, G.J.; Gould, G.W. (Ed.). Spore Research. London: Academic Press, 869-877.

Smith, H., Wingfield, M. J., & Petrini, O. (1996). Botryosphaeria dothidea endophytic in Eucalyptus grandis and Eucalyptus nitens in South Africa. Forest ecology and management, 89(1-3), 189-195.

Smith, N. R., Gordon, R. E., & Clark, F. E. (1946). Aerobic mesophilic sporeforming bacteria (Vol. 552). US Department of Agriculture.

Smith, N. R., Gordon, R. E., & Clark, F. E. (1952). Aerobic sporeforming bacteria (No. 16). US Government Printing Office.

Sneath, P.H.A.; Sokal, R.R. (1973). Numerical taxonomy. San Francisco: W.H. Freeman.

Stackebrandt, E., Ludwig, W., Weizenegger, M., Dorn, S., McGill, T. J., Fox, G. E., ... & Schleifer, K. H. (1987). Comparative 16S rRNA oligonucleotide analyses and murein types of round-spore-forming bacilli and non-spore-forming relatives. Microbiology, 133(9), 2523-2529.

Stackebrandt, E., & Woese, C. R. (1979). A phylogenetic dissection of the family Micrococcaceae. Current Microbiology, 2(6), 317-322.

Stackebrandt, E.; Woese, C.R. (1981).The evolution of prokaryotes. In: Carlile, M.J.; Collings, J.F.; Moseley, B.E.B. (Ed.). Molecular and cellular aspects of microbial evolution. Cambridge: Cambridge University Press, 1-31.

Stein, T. (2005). Bacillus subtilis antibiotics: structures, syntheses and specific functions. Molecular microbiology, 56(4), 845-857.

Stirling, G. R., Nicol, J. M., & Reay, F. (1998). Advisory services for nematodes pests–operational guide (Rural Industries Research and Development Corporation Publication No. 99/41, 120 pp.). Whitehead, AG Plant nematode control. Wallingford: CAB.

Sturz, A.V.; Kimpinski, J. (2003). Endoroot bacteria derived from marigolds (Tagetes spp.) can decrease soil population densities of root-lesion activity. World Journal of Microbiology and Biotechnology 19 (1), 381-385.

Trevet, I. W. (1948). Bacteria in the storage organs of healthy plants. Phytopathology, 38, 960-967.

Tsavkelova, E. A., Klimova, S. Y., Cherdyntseva, T. A., & Netrusov, A. I. (2006). Microbial producers of plant growth stimulators and their practical use: a review. Applied biochemistry and microbiology, 42(2), 117-126.

Tuzun, S. (2001). The relationship between pathogen-induced systemic resistance (ISR) and multigenic (horizontal) resistance in plants. European Journal of Plant Pathology, 107(1), 85-93.

US Congress Office of Technology Assessment (1995). Biologically-based technologies for pest control. OTA-ENV-636. Washington, DC: US Government Printing Office.

Vachon, V., Laprade, R., & Schwartz, J. L. (2012). Current models of the mode of action of Bacillus thuringiensis insecticidal crystal proteins: a critical review. Journal of invertebrate pathology, 111(1), 1-12.

Vaz, M. V., Canedo, E. J., Machado, J. C., Vieira, B. S., & Lopes, E. A. (2011). Controle biológico de Meloidogyne javanica e Meloidogyne incognita com Bacillus subtilis. Perquirere, 8, 203-212.

Voss, G. B. (2013). Produção de Bacillus subtilis em biorreator airlift e sua aplicação no controle de nematoide de galhas do tomateiro.

Wang, J., Liu, J., Wang, X., Yao, J., & Yu, Z. (2004). Application of electrospray ionization mass spectrometry in rapid typing of fengycin homologues produced by Bacillus subtilis. Letters in applied microbiology, 39(1), 98-102.

Wei, J. Z., Hale, K., Carta, L., Platzer, E., Wong, C., Fang, S. C., & Aroian, R. V. (2003). Bacillus thuringiensis crystal proteins that target nematodes. Proceedings of the National Academy of Sciences, 100(5), 2760-2765.

Wu, C. C., Hu, Y., Miller, M., Aroian, R. V., & Sailor, M. J. (2015). Protection and delivery of anthelmintic protein Cry5B to nematodes using mesoporous silicon particles. ACS nano, 9(6), 6158-6167.

Xiong, J., Zhou, Q., Luo, H., Xia, L., Li, L., Sun, M., & Yu, Z. (2015). Systemic nematicidal activity and biocontrol efficacy of Bacillus firmus against the root-knot nematode Meloidogyne incognita. World Journal of Microbiology and Biotechnology, 31(4), 661-667.

Yanni, Y. G., Rizk, R. Y., Abd El-Fattah, F. K., Squartini, A., Corich, V., Giacomini, A., ... & Dazzo, F. B. (2001). The beneficial plant growth-promoting association of Rhizobium leguminosarum bv. trifolii with rice roots. Functional Plant Biology, 28(9), 845-870.

Yao, A.; Bochow, H.; Karimov, S.; Boturov, U.; Sanginboy, S.; Sharipov, A. (2006). Effect of FZB 24 Bacillus subtilis as a biofertilizer on cotton yields in field tests. Archives of Phytopathology and Plant Protection, 39(1),323-328.

Yu, Z., Luo, H., Xiong, J., Zhou, Q., Xia, L., Sun, M., ... & Yu, Z. (2014). B acillus thuringiensis C ry6 A exhibits nematicidal activity to C aenorhabditis elegans bre mutants and synergistic activity with C ry5 B to C. elegans. Letters in applied microbiology, 58(6), 511-519.

Zarilla, K. A., & Perry, J. J. (1987). Bacillus thermokovorans, sp. nov., a species of obligately thermophilic hydrocarbon utilizing endospore-forming bacteria. Systematic and applied Microbiology, 9(3), 258-264.

Zinniel, D. K., Lambrecht, P., Harris, N. B., Feng, Z., Kuczmarski, D., Higley, P., ... & Vidaver, A. K. (2002). Isolation and characterization of endophytic colonizing bacteria from agronomic crops and prairie plants. Applied and environmental microbiology, 68(5), 2198-2208.

The Bacillus genus applied to the biological control of plant diseases

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Thiago Anchieta de Melo, Universidade Estadual do Maranhão

Ingrid Tayane Vieira da Silva do Nascimento, Universidade Estadual do Maranhão

Ilka Márcia Ribeiro de Souza Serra, Universidade Estadual do Maranhão

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