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Genomic Insights and Comparative Genomics of Bacillus Species Having Diverse Mechanisms of Biocontrol Against Fungal Phytopathogens

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Bacilli and Agrobiotechnology: Phytostimulation and Biocontrol

Abstract

Pathogenic fungi affect a large number of crop species that are the main threat to food production and storage. Generally, chemical-based pesticides are supposed to be effective in controlling pests in agriculture; however, intensive use of chemicals has led to the development of resistance of the pathogen. It is also a potential threat to all kinds of life on earth. Bacillus species, which are well-known to promote the growth of plants with antagonistic activity against phytopathogenic fungi, are considered as safer and sustainable control agents for crop management. Genome-based studies enable us to understand the genetic elements of Bacillus strains for the survival in the rhizosphere, plant growth promotion, root colonization, chemotaxis, and motility. To extend the understanding of the potential antifungal capacities, 286 Bacillus genome sequences having the ability of biocontrol have been described. The genomic analyses identified biosynthetic gene clusters encoding secondary metabolites associated with biocontrol activity. Different Bacillus strains were found to dedicate approximately 8.5–18% of the whole genome in the biosynthesis of non-ribosomal peptide synthetase (NRPS) clusters encoding lipopeptides surfactin (srf), iturin (itu), fengycin (fen), and siderophore bacillibactin (besA, dhbACEBF) which have antifungal activity. Emerging bioinformatics tools based on multiple protein-coding loci comparison and core genome phylogenomic analyses have been employed to distinguish novel species in Bacillus taxa. Comparative genome analysis of the publicly available Bacillus strains allows for identifying the closest relatives. It can identify unique genes associated with secondary metabolites biosynthesis encoded in a strain. The production of antimicrobial compounds indicates Bacillus sp. as an ideal candidate for use as a biocontrol agent.

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References

  • Alvarez F, Castro M, Principe A, Borioli G, Fischer S, Mori G, Jofre E (2012) The plant-associated Bacillus amyloliquefaciens strains MEP2 18 and ARP23 capable of producing the cyclic lipopeptides iturin or surfactin and fengycin are effective in biocontrol of sclerotinia stem rot disease. J Appl Microbiol 112(1):159–174

    Article  CAS  PubMed  Google Scholar 

  • Arguelles-Arias A, Ongena M, Halimi B, Lara Y, Brans A, Joris B et al (2009) Bacillus amyloliquefaciens GA1 as a source of potent antibiotics and other secondary metabolites for biocontrol of plant pathogens. Microb Cell Factories 8(1):63. https://doi.org/10.1186/1475-2859-8-63. PMID: 19941639

    Article  CAS  Google Scholar 

  • Arrebola E, Jacobs R, Korsten L (2010) Iturin A is the principal inhibitor in the biocontrol activity of Bacillus amyloliquefaciens PPCB004 against postharvest fungal pathogens. J Appl Microbiol 108(2):386–395

    Article  CAS  PubMed  Google Scholar 

  • Baysal O, Lai D, Xu H, Siragusa M, Casiskan M, Carimi F, Silva JAT, Tor M (2013) A proteomic approach provides new insights into the control of soil-borne plant pathogens by Bacillus species. PLoS One 8:e53182

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Belbahri L, Bouket AC, Rekik I, Alenezi FN, Vallat A, Luptakova L, Petrovova E, Oszako T, Cherrad S, Vacher S, Rateb ME (2017) Comparative genomics of Bacillus amyloliquefaciens strains reveals a core genome with traits for habitat adaptation and a secondary metabolites rich accessory genome. Front Microbiol 8:1438. https://doi.org/10.3389/fmicb.2017.01438

    Article  PubMed  PubMed Central  Google Scholar 

  • Benhamou N, Kloepper JW, Quadt-Hallmann A, Tuzun S (1996) Induction of defence-related ultrastructural modifications in pea root tissues inoculated with endophytic bacteria. Plant Physiol 112:919–929

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Benhamou N, Kloepper JW, Tuzun S (1998) Induction of resistance against Fusarium wilt of tomato by combination of chitosan with an endophytic bacterial strain: ultra structure and cytochemistry of the host response. Planta 204:153–168

    Article  CAS  Google Scholar 

  • Bharathi S (2004) Development of botanical formulations for the management of major fungal diseases of tomato and onion. PhD thesis, Tamil Nadu Agricultural University, Coimbatore, India, p 152

    Google Scholar 

  • Bloemberg GV, Lugtenberg BJ (2001) Molecular basis of plant growth promotion and biocontrol by Rhizobacteria. Curr Opin Plant Biol 4:343–350

    Article  CAS  PubMed  Google Scholar 

  • Blom J, Rueckert C, Niu B, Wang Q, Borriss R (2012) The complete genome of Bacillus amyloliquefaciens subsp. plantarum CAU B946 contains a gene cluster for nonribosomal synthesis of iturin A. J Bacteriol 194(7):1845–1846

    Google Scholar 

  • Borriss R, Chen XH, Rueckert C, Blom J, Becker A, Baumgarth B, Fan B, Pukall R, Schumann P, Sproer C, Junge H, Vater J, Puhler A, Klenk HP (2011) Relationship of Bacillus amyloliquefaciens clades associated with strains DSM7T and FZB42T: a proposal for Bacillus amyloliquefaciens subsp. amyloliquefaciens subsp. nov. and Bacillus amyloliquefaciens subsp. plantarum subsp. nov. based on complete genome sequence comparisons. Int J Syst Evol Microbiol 61(8):1786–1801

    Article  CAS  PubMed  Google Scholar 

  • Brennan JM, Fagan B, Van Maanen A, Cooke BM, Doohan FM et al (2003) Studies on in vitro growth and pathogenicity of Fusarium fungi. Eur J Plant Pathol 109:577–587

    Article  Google Scholar 

  • Cai X, Li H, Xue Y, Liu C (2013) Study of endophytic Bacillus amyloliquefaciens CC09 and its antifungal cyclic lipopeptides. J Appl Biol Biotechnol 1(1):1–5

    Google Scholar 

  • Cai XC, Liu CH, Wang BT, Xue YR (2017) Genomic and metabolic traits endow Bacillus velezensis CC09 with a potential biocontrol agent in control of wheat powdery mildew disease. Microbiol Res 196:89–94

    Article  CAS  PubMed  Google Scholar 

  • Cassan F, Maiale S, Masciarelli O, Vidal A, Luna V, Ruiz O (2009) Cadaverine production by Azospirillum brasilense and its possible role in plant growth promotion and osmotic stress mitigation. Eur J Soil Biol 45(1):12–19

    Article  CAS  Google Scholar 

  • Chen X, Koumoutsi A, Scholz R, Eisenreich A, Schneider K, Heinemeyer I, Morgenstern B, Voss B, Hess W, Reva O, Junge H, Voigt B, Jungblut P, Vater J, Sussmuth R, Liesegang H, Strittmatter A, Gottschalk G, Borriss R (2007) Comparative analysis of the complete genome sequence of the plant growth-promoting bacterium Bacillus amyloliquefaciens FZB42. Nat Biotechnol 25:1007–1014

    Article  CAS  PubMed  Google Scholar 

  • Chen X, Koumoutsi A, Scholz R, Schneider K, Vater J, Süssmuth R, Piel J, Borriss R (2009) Genome analysis of Bacillus amyloliquefaciens FZB42 revealsits potential for biocontrol of plant pathogens. J Biotechnol 140(1–2):27–37

    Article  CAS  PubMed  Google Scholar 

  • Chen L, Li RJ, Qin SY, Huang L, Wei LC, Bian K (2017) Screening and inhibition effect of antagonistic strain against Fusarium head blight by Fusarium graminearum. China Plant Prot 37(5):12–17

    Google Scholar 

  • Chen L, Heng J, Qin S, Bian K (2018) A comprehensive understanding of the biocontrol potential of Bacillus velezensis LM2303 against Fusarium head blight. PLoS One 13(6):e0198560. https://doi.org/10.1371/journal.pone.0198560

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chowdhury SP, Dietel K, Randler M, Schmid M, Junge H, Borriss R, Hartmann A, Grosch R (2013) Effects of Bacillus amyloliquefaciens FZB42 on lettuce growth and health under pathogen pressure and its impact on therhizosphere bacterial community. PLoS One 8(7):e68818

    Article  PubMed  PubMed Central  Google Scholar 

  • Chowdhury SP, Hartmann A, Gao X, Borriss R (2015) Biocontrol mechanism byroot-associated Bacillus amyloliquefaciens FZB42 – a review. Front Microbiol 6:1–11

    Article  Google Scholar 

  • Cook RJ (1993) Making greater use of microbial inoculants in agriculture. Annu Rev Phytopathol 31:53–80

    Article  CAS  PubMed  Google Scholar 

  • Cuervo-Parra JA, Sánchez-López V, Ramirez-Suero M, Ramírez-Lepe M (2011) Morphological and molecular characterization of Moniliophthora roreri causal agent of frosty pod rot of cocoa tree in Tabasco. Mexico Plant Pathol J 10:122–127

    Article  Google Scholar 

  • Danielsson J, Reva O, Meijer J (2007) Protection of oilseed rape (Brassica napus) toward fungal pathogens by strain of plant-associated Bacillus amyloliquefaciens. Microb Ecol 54(1):134–140

    Article  PubMed  Google Scholar 

  • Denner W, Gillanders T (1996) The legislative aspects of the use of industrial enzymes in the manufacture of food and food ingredients. In: Godfrey T, Reichelt J (eds) Industrial enzymology. Stockton Press, New York, pp 397–412

    Google Scholar 

  • Doornbos RF, Loon LC, Bakker PAHM (2012) Impact of root exudates and plant defense signaling on bacterial communities in the rhizosphere. Agron Sustain Dev 32:227–243

    Article  Google Scholar 

  • Driks A (2004) The Bacillus spore coat. Phytopathology 94(11):1249–1251

    Article  CAS  PubMed  Google Scholar 

  • Duan J, Jiang W, Cheng Z, Heikkila JJ, Glick BR (2013) The complete genome sequence of the plant growth-promoting bacterium Pseudomonas sp. UW4. PLoS One 8:462–469

    Google Scholar 

  • Dunlap CA, Bowman MJ, Schisler DA (2013) Genomic analysis and secondary metabolite production in Bacillus amyloliquefaciens AS 43.3: a biocontrol antagonist of Fusarium head blight. Biol Control 64:166–175

    Article  CAS  Google Scholar 

  • Dunlap CA, Kim SJ, Kwon SW, Rooney AP (2015) Phylogenomic analysis shows that Bacillus amyloliquefaciens subsp. plantarum is a later heterotypic synonym of Bacillus methylotrophicus. Int J Syst Evol Microbiol 65:2104–2109

    Article  CAS  PubMed  Google Scholar 

  • Fan B, Rainer B, Wilfrid B, Wu X (2012) Gram-positive rhizobacterium Bacillus amyloliquefaciens FZB42 colonizes three types of plants in different patterns. J Microbiol 50(1):38–44

    Article  PubMed  Google Scholar 

  • Fredrick KL, Helmann JD (1994) Dual chemotaxis signaling pathways in Bacillus subtilis: a sigma D-dependent gene encodes a novel protein with both CheW and CheY homologous domains. J Bacteriol 176(9):2727–2735

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fritze D (2004) Taxonomy of the genus Bacillus and related genera: the aerobic endospore-forming bacteria. Phytopathology 94:1245–1248

    Article  PubMed  Google Scholar 

  • Ghelardi E, Salvetti S, Ceragioli M, Gueye SA, Celandroni F, Senesi S (2012) Contribution of surfactin and SwrA to flagellin expression, swimming, and surface motility in Bacillus subtilis. Appl Environ Microbiol 78:6540–6544. https://doi.org/10.1128/AEM.01341-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gheler CF, Domingues ZT, de Soares MI (2013) Biological control of phytopathogenic fungi by endophytic actinomycetes isolated from maize (Zea mays L.). Braz Arch Biol Technol 56:948–955

    Article  Google Scholar 

  • Grosch R, Junge H, Krebs B, Bochow H (1999) Use of Bacillus subtilis as abiocontrol agent. III: influence of Bacillus subtilis on fungal root diseases Andon yield in soilless culture. J Plant Dis Protect 106(6):568–580

    Google Scholar 

  • Guo S, Li X, He P, Ho H, Wu Y, He Y (2015) Whole-genome sequencing of Bacillus subtilis XF-1 reveals mechanisms for biological control and multiple beneficial properties in plants. J Ind Microbiol Biotechnol 42(6):925–937. https://doi.org/10.1007/s10295-015-1612-y. PMID: 25860123

    Article  CAS  PubMed  Google Scholar 

  • Hammerschmidt R, Kuc J (1995) Induced resistance to disease in plants. Kluwer Academic, Dordrecht, p 182

    Book  Google Scholar 

  • Hao K, He P, Blom J, Rueckert C, Mao Z, Wu Y, He Y, Borriss R (2012) The genome of plant growth-promoting Bacillus amyloliquefaciens subsp. plantarum strain YAU B9601-Y2 contains a gene cluster for mersacidin synthesis. J Bacteriol 194:3264–3265

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He P, Hao K, Blom J, Rückert C, Vater J, Mao Z, Wu Y, Hou M, He P, He Y, Borriss R (2012) Genome sequence of the plant growth promoting strain Bacillus amyloliquefaciens subsp. plantarum B9601-Y2 and expression of mersacidin and other secondary metabolites. J Biotechnol 164:281–291

    Article  CAS  PubMed  Google Scholar 

  • Hofemeister J, Conrad B, Adler B, Hofemeister B, Feesche J, Kucheryava N, Steinborn G, Franke P, Grammel N, Zwintscher A, Leenders F, Hitzeroth G, Vater J (2004) Genetic analysis of the biosynthesis of non-ribosomal peptide- and polyketide-like antibiotics, iron uptake and biofilm formation by Bacillus subtilis A1/3. Mol Genet Genomics 272:363–378

    Article  CAS  PubMed  Google Scholar 

  • Jamalizadeh M, Etebarian HR, Aminian H, Alizadeh A (2011) A review of mechanisms of action of biological control organisms against post-harvest fruit spoilage. EPPO Bull 41:65–71

    Article  Google Scholar 

  • Khan NI, Schisler DA, Boehm MJ, Slininger PJ, Bothast RJ (2001) Selection and evaluation of microorganisms for biocontrol of Fusarium head blight of wheat incited by Gibberella zeae. Plant Dis 85:1253–1258

    Article  CAS  PubMed  Google Scholar 

  • Kim HS, Park J, Choi SW, Choi KH, Lee GL, Ban SJ, Lee CH, Kim CS (2003) Isolation and characterization of Bacillus strains for biological control. J Microbiol 41(3):196

    CAS  Google Scholar 

  • Kim SY, Lee SY, Weon HY, Sang MK, Song J (2017) Complete genome sequence of Bacillus velezensis M75, a biocontrol agent against fungal plant pathogens, isolated from cotton waste. J Biotechnol 241:112–115

    Article  CAS  PubMed  Google Scholar 

  • Kinsinger R, Shirk M, Fall R (2003) Rapid surface motility in Bacillus subtilis is dependent on extracellular surfactin and potassium ion. J Bacteriol 185:5627–5631

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kloepper JW, Ryu CM, Zhang S (2004) Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 94(11):1259–1266. https://doi.org/10.1094/PHYTO.2004.94.11.1259

    Article  CAS  PubMed  Google Scholar 

  • Kotan R, Dikbas N, Bostan H (2009) Biological control of post-harvest disease caused by Aspergillus flavus on stored lemon fruits. Afr J Biotechnol 8:209–214

    Google Scholar 

  • Leclere V, Bechet M, Adam A, Guez JS, Wathelet B, Ongena M, Thonart P, Gancel F, Chollet-Imbert M, Jacques P (2005) Mycosubtilin overproduction by Bacillus subtilis BBG100 enhances the organism’s antagonistic and biocontrol activities. Appl Environ Microbiol 71:4577–4584

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leslie JF, Marasas WF, Shephard GS, Sydenham EW, Stockenstrom S et al (1996) Duckling toxicity and the production of fumonisin and moniliformin by isolates in the A and E mating populations of Gibberella fujikuroi (Fusarium moniliforme). Appl Environ Microbiol 62:1182–1187

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li XY, Yang JJ, Mao ZC, Ho HH, Wu YX, He YQ (2014) Enhancement of biocontrol activities and cyclic lipopeptides production by chemical mutagenesis of Bacillus subtilis XF-1, a biocontrol agent of Plasmodiophora brassicae and Fusarium solani. Indian J Microbiol 54:476–479

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Loper JE, Buyer JS (1991) Siderophores in microbial interactions on plant-surfaces. Mol Plant Microbe Interact 4:5–13

    Article  CAS  Google Scholar 

  • M’Piga P, Belanger RR, Paulitz TC, Benhamou N (1997) Increased resistance to Fusarium oxysporum f. sp. radicis-lycopersici in tomato plants treated with the endophytic bacterium Pseudomonas fluorescens strain 63-28. Physiol Mol Plant Pathol 50:301–320

    Article  Google Scholar 

  • MacLean D, Jones JD, Studholme DJ (2009) Application of ‘next-generation’ sequencing technologies to microbial genetics. Nat Rev Microbiol 7:287–296

    Article  PubMed  Google Scholar 

  • Madhaiyan M, Poonguzhali S, Kwon SW, Sa TM (2010) Bacillus methylotrophicus sp. nov, a methanol-utilizing, plant-growth-promoting bacterium isolated from rice rhizosphere soil. Int J Syst Evol Microbiol 60(10):2490–2495

    Article  CAS  PubMed  Google Scholar 

  • 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 74:1047–1051

    Article  CAS  PubMed  Google Scholar 

  • May JT, Wendrich TM, 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. J Biol Chem 276:7209–7217

    Article  CAS  PubMed  Google Scholar 

  • McQuilken MP, Gemmell J (2004) Enzyme production by the mycoparasite Verticillium biguttatum against Rhizoctonia solani. Mycopathologia 157:201–205

    Article  CAS  PubMed  Google Scholar 

  • Microbiology UDoPa (2016) Antimicrob Pept database; 18 April. Available from: http://aps.unmc.edu/AP/main.php

  • Miedaner T (1997) Breeding wheat and rye for resistance to Fusarium diseases. Plant Breed 116:201–220

    Article  Google Scholar 

  • Moyne AL, Cleveland TE, Tuzun S (2004) Molecular characterization and analysis of the operon encoding the antifungal lipopeptide bacillomycin D. FEMS Microbiol Lett 234:43–49

    Article  CAS  PubMed  Google Scholar 

  • Nasraoui B, Hajlaoui MR, Aïssa AD, Kremer RJ (2007) Biological control of wheat take-all disease: I-characterization of antagonistic bacteria from diverse soils toward Gaeumannomyces graminis var. tritici. Tunisian J Plant Prot 2:23–34

    Google Scholar 

  • Niazi A, Manzoor S, Asari S, Bejai S, Meijer J, Bongcam-Rudloff E (2014) Genome analysis of Bacillus amyloliquefaciens subsp. plantarum UCMB5113: a rhizobacterium that improves plant growth and stress management. PLoS One 9(8):e104651. https://doi.org/10.1371/journal.pone.0104651. PMID: 25119988

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ongena M, Jacques P (2008) Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiol 16:115–125. https://doi.org/10.1016/j.tim.2007.12.009

    Article  CAS  PubMed  Google Scholar 

  • Ozer EA, Allen JP, Hauser AR (2014) Characterization of the core and accessory genomes of Pseudomonas aeruginosa using bioinformatic tools Spine and AGEnt. BMC Genomics 15:737. https://doi.org/10.1186/1471-2164-15-737

    Article  PubMed  PubMed Central  Google Scholar 

  • Palazzini JM, Dunlap CA, Bowman MJ, Chulze SN (2016) Bacillus velezensis RC 218 as a biocontrol agent to reduce Fusarium head blight and deoxynivalenol accumulation: genome sequencing and secondary metabolite cluster profiles. Microbiol Res 192:30–36

    Article  CAS  PubMed  Google Scholar 

  • Park K, Paul D, Kim YK et al (2007) Induced systemic resistance by Bacillus vallismortis EXTN-1 suppressed bacterial wilt in tomato caused by Ralstonia solanacearum. Plant Pathol J 23(1):22

    Article  Google Scholar 

  • Parry DW, Jenkinson P, McLeod L (1995) Fusarium ear blight (scab) in small-grain cereals – a review. Plant Pathol 44:207–238

    Article  Google Scholar 

  • Pelletier A, Sygusch J (1990) Purification and characterization of three chitosanase activities from Bacillus megaterium P1. Appl Environ Microbiol 56(4):844–848

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Phillips-Mora W, Coutino A, Ortiz CF, Lopez AP, Hernandez J et al (2006) First report of Moniliophthora roreri causing frosty pod rot (moniliasis disease) of cacao in Mexico. Plant Pathol 55:584

    Google Scholar 

  • Popovski S, Celar FA (2013) The impact of environmental factors on the infection of cereals with Fusarium species and mycotoxin production – a review. Acta Agric Slov 101:105–116

    Article  Google Scholar 

  • Pozo MJ, Azcón-Aguilar C (2007) Unravelling mycorrhiza-induced resistance. Curr Opin Plant Biol 10:393–398

    Article  CAS  PubMed  Google Scholar 

  • Qiao JQ, Wu HJ, Huo R, Gao XW, Borriss R (2014) Stimulation of plant growth and biocontrol by Bacillus amyloliquefaciens subsp. plantarum FZB42 engineered for improved action. Chem Biol Technol Agric 1:1–14

    Article  CAS  Google Scholar 

  • Rai R, Dash PK, Prasanna BM, Singh A (2007) Endophytic bacterial flora in the stem tissue of a tropical maize (Zea mays L.) genotype: isolation, identification and enumeration. World J Microbiol Biotechnol 23:853–858

    Article  Google Scholar 

  • Rate DN, Cuenca JV, Bowman GR, Guttman DS, Greenberg JT (1999) The gain-of-function Arabidopsis thaliana acd6 mutant reveals novel regulation and function of the salicylic acid signaling pathway in controlling cell death, defenses and cell growth. Plant Cell 11:1695–1708

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reva ON, Dixelius C, Meijer J, Priest FG (2004) Taxonomic characterization and plant colonizing abilities of some bacteria related to Bacillus amyloliquefaciens and Bacillus subtilis. FEMS Microbiol Ecol 48:249–259

    Article  CAS  PubMed  Google Scholar 

  • Ribera AE, Zuniga G (2012) Induced plant secondary metabolites for phytopatogenic fungi control: a review. J Soil Sci Plant Nutr 12:893–911

    Google Scholar 

  • Romero D, Perez-Garcia A, Rivera ME, Cazorla FM, de Vicente A (2004) Isolation and evaluation of antagonistic bacteria towards the cucurbit powdery mildew fungus Podosphaera fusca. Appl Microbiol Biotechnol 64(2):263–269

    Article  CAS  PubMed  Google Scholar 

  • Romero D, de Vicente A, Rakotoaly RV, Dufour SE, Veening JW, Arrebola E et al (2007) The iturin and fengycin families of lipopeptides are key factors in antagonism of Bacillus subtilis toward Podosphaera fusca. Mol Plant-Microbe Interact 20:430–440

    Article  CAS  PubMed  Google Scholar 

  • Ryu CM, Hu CH, Reddy MS, Kloepper W (2003) Different signaling pathways of induced resistance by rhizobacteria in Arabidopsis thaliana against two pathovars of Pseudomonas syringae. New Phytol 160:413–420

    Article  CAS  PubMed  Google Scholar 

  • Ryu CM, Farag MA, Hu CH, Reddy MS, Kloepper JW et al (2004) Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol 134:1017–1026

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sarosh BR, Danielsson J, Meijer J (2009) Transcript profiling of oilseed rape (Brassica napus) primed for biocontrol differentiate genes involved in microbial interactions with beneficial Bacillus amyloliquefaciens from pathogenic Botrytis cinerea. Plant Mol Biol 70(1–2):31–45

    Article  CAS  PubMed  Google Scholar 

  • Santos VB, Araujo SF, Leite LF, Nunes LA, Melo JW (2012) Soil microbial biomass and organic matter fractions during transition from conventional to organic farming systems. Geoderma 170:227–231

    Article  CAS  Google Scholar 

  • Scherm B, Balmas V, Spanu F, Pani G, Delogu G, Pasquali M, Migheli Q (2013) Fusarium culmorum: causal agent of foot and root rot and head blight on wheat. Mol Plant Pathol 14:323–341

    Article  CAS  PubMed  Google Scholar 

  • Schisler DA, Khan NI, Boehm MJ, Slininger PJ (2002) Greenhouse and field evaluation of biological control of Fusarium head blight on durum wheat. Plant Dis 86:1350–1356

    Article  CAS  PubMed  Google Scholar 

  • Schuster SC (2008) Next-generation sequencing transforms today’s biology. Nat Methods 5:16–18

    Article  CAS  PubMed  Google Scholar 

  • Song JY et al (2012) Genome sequence of the plant growth-promoting rhizobacterium Bacillus sp. strain JS. J Bacteriol 194:3760–3761

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stein T (2005) Bacillus subtilis antibiotics: structure syntheses and specific functions. Mol Microbiol 56:845–857

    Article  CAS  PubMed  Google Scholar 

  • Stein T, Vater J, Krufts V, Otto A, Wittmann-Liebold B, Franke P, Panico M, McDowell R, Morriss HR (1996) The multiple carrier model of nonribosomal peptide biosynthesis at modular multienzymatic templates. J Biol Chem 271:15428–15435

    Article  CAS  PubMed  Google Scholar 

  • Suarez-López F (2010) Evaluación de microorganismos promotores de crecimiento en jitomate (L. esculentum L.) bajo condiciones de invernadero. Tesis de Licenciatura, Universidad Autónoma Agraria Antonio Narro, Buenavista, Saltillo, Coahuila

    Google Scholar 

  • Sutton JC (1982) Epidemiology of wheat head blight and maize ear rot caused by Fusarium graminearum. Can J Plant Pathol 4:195–209

    Article  Google Scholar 

  • Szczech M, Shoda M (2006) The effect of mode of application of Bacillus subtilis RB14-C on its efficacy as a biocontrol agent against Rhizoctonia solani. Phytopathology 154:370–377

    Article  CAS  Google Scholar 

  • Tekauz A, McCallum B, Gilbert J (2000) Review: Fusarium head blight of barley in western Canada. Can J Plant Pathol 22:9–16

    Article  Google Scholar 

  • Timmusk S, Grantcharova N, Wagner EGH (2005) Paenibacillus polymyxa invades plant roots and forms biofilms. Appl Environ Microbiol 71(11):7292

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Torres AM, Reynoso MM, Rojo FG, Ramirez ML, Chulze SN (2001) Fusarium species (section Liseola) and its mycotoxins in maize harvested in northern Argentina. Food Addit Contam 18:836–843

    Article  CAS  PubMed  Google Scholar 

  • Toure Y, Ongena M, Jacques P, Guiro A, Thonart P (2004) Role of lipopeptides produced by Bacillus subtilis GA1 in the reduction of grey mould disease caused by Botrytis cinerea on apple. J Appl Microbiol 96:1151–1160. https://doi.org/10.1111/j.1365-2672.2004.02252.x

    Article  CAS  PubMed  Google Scholar 

  • Tournas V (2005) Spoilage of vegetable crops by bacteria and fungi and related health hazards. Crit Rev Microbiol 31:33–44

    Article  CAS  PubMed  Google Scholar 

  • Van-Loon LC, Bakker PAHM, Pieterse CMJ (1998) Systemic resistance induced by rhizosphere bacteria. Annu Rev Phytopathol 36:453–483

    Article  CAS  PubMed  Google Scholar 

  • Velluti A, Marín S, Bettucci L, Ramos AJ, Sanchis V et al (2000) The effect of fungal competition on colonisation of maize grain by Fusarium moniliforme, F. proliferatum and F. graminearum and on fumonisin B1 and zearalenone formation. Int J Food Microbiol 59:59–66

    Article  CAS  PubMed  Google Scholar 

  • Vessey JK (2003) Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255(2):571–586

    Article  CAS  Google Scholar 

  • Vlamakis H, Chai Y, Beauregard P, Losick R, Kolter R (2013) Sticking together: building a biofilm the Bacillus subtilis way. Nat Rev Microbiol 11:157–168. https://doi.org/10.1038/nrmicro2960

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang LT, Lee FL, Tai CJ, Kuo HP (2008) Bacillus velezensis is a later heterotypic synonym of Bacillus amyloliquefaciens. Int J Syst Evol Microbiol 58:671–675. https://doi.org/10.1099/ijs.0.65191-0

    Article  CAS  PubMed  Google Scholar 

  • Wang S, Wu H, Qiao J, Ma L, Liu J, Xia Y, Gao X (2009a) Molecular mechanism of plant growth promotion and induced systemic resistance to tobacco mosaic virus by Bacillus spp. J Microbiol Biotechnol 19(10):1250–1258

    Article  CAS  PubMed  Google Scholar 

  • Wang H, Wen K, Zhao X, Wang X, Li A, Hong H (2009b) The inhibitory activity of endophytic Bacillus sp. strain CHM1 against plant pathogenic fungi and its plant growth-promoting effect. Crop Prot 28:634–639

    Article  Google Scholar 

  • Werhane H, Lopez P, Mendel M, Zimmer M, Ordal G, Márquez-Magaña L (2004) The last gene of the fla/che operon in Bacillus subtilis, ylxL, is required for maximal σD function. J Bacteriol 186(12):4025–4029

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • White JF, Torres MS, Sullivan RF, Jabbour RE, Chen Q, Tadych M et al (2014) Microscopy research and technique: occurrence of Bacillus amyloliquefaciens as a systemic endophyte of vanilla orchids. Microsc Res Tech. https://doi.org/10.1002/jemt.22410

  • Wilson D (1995) Endophyte: the evolution of a term, and clarification of its use and definition. Oikos 73(2):274–276

    Article  Google Scholar 

  • Woo SM, Kim SD (2008) Structural identification of siderophore from Bacillus subtilis AH18, a biocontrol agent of phytophthora blight disease in red pepper. Korean J Microbiol Biotechnol 36:326–335

    CAS  Google Scholar 

  • Wood GAR, Lass RA (2001) Cacao, 4th edn. Blackwell Science, Oxford

    Google Scholar 

  • Xiong G, Zhao G, Fan C, He Y (2009) Identification and fungistatic effect of a biocontrol strain. J Yunnan Agric Univ 24:190–194

    CAS  Google Scholar 

  • Yang H, Xue Y, Yu X, Liu C (2014) Colonization of Bacillus amyloliquefaciens CC09 in wheat leaf and its biocontrol effect on powdery mildew disease. Microbiol China 30(4):481–488

    Google Scholar 

  • Yao A, Bochow H, Karimov S, Boturov U, Sanginboy S, Sharipov AK (2006) Effect of FZB 24 Bacillus subtilis as a biofertilizer on cotton yields in field tests. Arch Phytopathol Plant Protect 39(4):323–328

    Article  Google Scholar 

  • Yu GY, Sinclair JB, Hartman GL, Bertagnolli BL (2002) Production of iturin A by Bacillus amyloliquefaciens suppressing Rhizoctonia solani. Soil Biol Biochem 34:955–963

    Article  CAS  Google Scholar 

  • Zeigler D (2003) Gene sequences useful for predicting relatedness of whole genomes in bacteria. Int J Syst Evol Microbiol 53:1893–1900

    Article  CAS  PubMed  Google Scholar 

  • Zeriouh H, de Vicente A, Perez-Garcia A, Romero D (2014) Surfactin triggers biofilm formation of Bacillus subtilis in melon phylloplane and contributes to the biocontrol activity. Environ Microbiol 16(7):2196–2211. https://doi.org/10.1111/1462-2920.12271. PMID: 24308294

    Article  CAS  PubMed  Google Scholar 

  • Zhang JX, Xue AG, Tambong JT (2009) Evaluation of seed and soil treatments with novel Bacillus subtilis strains for control of soybean root rot caused by Fusarium oxysporum and F. graminearum. Plant Dis 93(12):1317–1323

    Article  CAS  PubMed  Google Scholar 

  • Zhao X, Zhou ZJ, Han Y et al (2013) Isolation and identification of antifungal peptides from Bacillus BH072, a novel bacterium isolated from honey. Microbiol Res 168(9):598–606

    Article  CAS  PubMed  Google Scholar 

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Rajkumari, J., Pandey, P. (2019). Genomic Insights and Comparative Genomics of Bacillus Species Having Diverse Mechanisms of Biocontrol Against Fungal Phytopathogens. In: Islam, M., Rahman, M., Pandey, P., Boehme, M., Haesaert, G. (eds) Bacilli and Agrobiotechnology: Phytostimulation and Biocontrol. Bacilli in Climate Resilient Agriculture and Bioprospecting. Springer, Cham. https://doi.org/10.1007/978-3-030-15175-1_12

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