Transposon mutagenesis of the plant-associated Bacillus amyloliquefaciens ssp. plantarum FZB42 revealed that the nfrA and RBAM17410 genes are involved in plant-microbe-interactions

PLoS ONE

Volumn 9, Issue 5, 2014, Pages

  Budiharjo, Anto ^a   Chowdhury, Soumitra Paul ^b   Dietel, Kristin ^c   Beator, Barbara ^a   Dolgova, Olga ^c   Fan, Ben ^a   Bleiss, Wilfrid ^a   Ziegler, Jörg ^d   Schmid, Michael ^b   Hartmann, Anton ^b   Borriss, Rainer ^a,c  

^a HUMBOLDT UNIVERSITY   (Germany)

^b INSTITUTE OF EPIDEMIOLOGY   (Germany)

^c ABITEP GMBH   (Germany)

^d LEIBNIZ INSTITUTE OF PLANT BIOCHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AUXIN; GREEN FLUORESCENT PROTEIN; BACTERIAL PROTEIN; NFRA1 PROTEIN, BACILLUS SUBTILIS; NITROREDUCTASE; TRANSPOSON;

ARTICLE; BACILLUS AMYLOLIQUEFACIENS; BACTERIAL GENE; BACTERIAL GENOME; BIOFILM; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; DEGU GENE; DNA SEQUENCE; GENE IDENTIFICATION; GENE INSERTION; GENE LIBRARY; GENETIC SCREENING; GENETIC VARIABILITY; LETTUCE; MUTAGENESIS; NFRA GENE; NONHUMAN; PLANT MICROORGANISM INTERACTION; RBAM17410 GENE; ROOT GROWTH; TRANSPOSON; BACILLUS; CONFOCAL MICROSCOPY; GENETIC COMPLEMENTATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; OXIDATIVE STRESS; PHYSIOLOGY; PLANT ROOT; RHIZOSPHERE; SCANNING ELECTRON MICROSCOPY;

BACILLUS; BACTERIAL PROTEINS; BIOFILMS; DNA TRANSPOSABLE ELEMENTS; GENE LIBRARY; GENETIC COMPLEMENTATION TEST; GREEN FLUORESCENT PROTEINS; LETTUCE; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, SCANNING; MUTAGENESIS; NITROREDUCTASES; OXIDATIVE STRESS; PLANT ROOTS; RHIZOSPHERE;

EID: 84901329562     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0098267     Document Type: Article

References (39)

1. Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Ann Rev Microbiol 63: 541-556.
2. Borriss R (2011) Use of plant-associated Bacillus strains as biofertilizers and biocontrol agents in agriculture. In: D. K. Maheshwari (ed.) Bacteria in Agrobiology: Plant growth responses. Springer-Verlag Berlin Heidelberg.
3. Weller DM (1988) Biological control of soilborne plant pathogens in the rhizosphere with bacteria. Ann Rev of Phytopathol 26: 379-407.
4. Chin-A-Woeng TFC, Bloemberg GV, Mulders LHM, Dekkers LC, Lugtenberg BJJ (2000) Root colonization by phenazine-1-carboxamide-producing bacterium Pseudomonas chlororaphis PCL1391 is essential for biocontrol of tomato foot and root rot. Mol Plant Microbe Interact 13: 1340-1345.
5. Chen Y, Yan F, Chai Y, Liu H, Kolter R, Losick R, Guo J (2013) Biocontrol of tomato wilt disease by Bacillus subtilis isolates from natural environments depends on conserved genes mediating biofilm formation. Environ Microbiol 15: 848-864.
6. Chen XH, Koumoutsi A, Scholz R, Eisenreich A, Schneider K, et al. (2007) Comparative analysis of the complete genome sequence of the plant growth-promoting bacterium Bacillus amyloliquefaciens FZB42. Nat Biotechnol 25: 1007-1014. (Pubitemid 47517636)
7. T: 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: 1786-1801.
8. Idris ESE, Makarewicz O, Farouk A, Rosner K, Greiner R, et al. (2002) Extracellular phytase activity of Bacillus amyloliquefaciens FZB45 contributes to its plant-growth-promoting effect. Microbiology 148: 2097-2109. (Pubitemid 34785294)
9. Idris ESE, Iglesias DJ, Talon M, Borriss R (2007) Tryptophan-dependent production of indole-3-acetic acid (IAA) affects level of plant-growth-promotion by Bacillus amyloliquefaciens FZB42. Mol Plant-Microbe Interact 20: 619-626. (Pubitemid 47011017)
10. Ryu CM, Farag MA, Hu CH, Reddy M, Wei HX, et al. (2003) Bacterial volatiles promote growth in Arabidopsis. Proc Natl Acad Sci USA 100: 4927-4932. (Pubitemid 36457830)
11. Koumoutsi A, Chen XH, Henne A, Liesegang H, Hitzeroth G, et al. (2004) Structural and functional characterization of gene clusters directing nonribosomal synthesis of bioactive cyclic lipopeptides in Bacillus amyloliquefaciens strain FZB42. J Bacteriol 186: 1084-1096. (Pubitemid 38209468)
12. Chen XH, Scholz R, Borriss M, Junge H, Mögel G, et al. (2009) Difficidin and bacilysin produced by plant-associated Bacillus amyloliquefaciens are efficient in controlling fire blight disease. J Biotechnol 140: 38-44.
13. Chowdhury SP, Dietel K, Rändler M, Schmid M, Junge H (2013) Effects of Bacillus amyloliquefaciens FZB42 on lettuce growth and health under pathogen pressure and its impact on the rhizosphere bacterial community. PLoS ONE 8(7): e68818. doi:10.1371/journal.pone.0068818
14. Fan B, Chen XH, Budiharjo A, Bleiss W, Vater J, et al. (2011) Efficient colonization of plant roots by the plant growth promoting bacterium Bacillus amyloliquefaciens FZB42, engineered to express green fluorescent protein. J Biotechnol 151: 303-11.
15. Fan B, Borriss R, Bleiss W, Wu XQ (2012) Gram-positive rhizobacterium Bacillus amyloliquefaciens FZB42 colonizes three types of plants in different patterns. J Microbiol 50: 38-44.
16. Dietel K, Beator B, Budiharjo A, Fan B, Borriss R (2013) Bacterial traits involved in colonization of Arabidopsis thaliana roots by Bacillus amyloliquefaciens FZB42. Plant Pathol J 29: 59-66.
17. Branda SS, Gonzalez-Pastor JE, Dervyn E, Ehrlich SD, Losick R, et al. (2004) Genes involved in the formation of structured multicellular communities by Bacillus subtilis. J Bacteriol 186: 3970-3979. (Pubitemid 38746073)
18. Pirson A, Seidel F (1950) Zell- und stoffwechselphysiologische Untersuchungen an der Wurzel von Lemna minor L. unter besonderer Berücksichtigung von Kalium- und Kalziummangel. Planta 38: 431-473.
19. LeBreton Y, Mohapatra N P, Haldenwang WG (2006) In vivo random mutagenesis of Bacillus subtilis by use of TnYLB-1, a mariner-based transposon. Appl Envir Microbiol 72: 327-333.
20. Kunst F, Rapoport G (1995) Salt stress is an environmental signal affecting degradative enzyme synthesis in Bacillus subtilis. J Bacteriol 177: 2403-2407.
21. Kearns DB, Chu F, Rudner R, Losick R (2004) Genes governing swarming in Bacillus subtilis and evidence for phase variation mechanisms controlling surface motility. Mol Microbiol 52: 357-369. (Pubitemid 38520708)
22. Msadek T, Kunst F, Henner D, Klier A, Rapoport G, et al. (1990) Signal transduction pathway controlling synthesis of a class of degradative enzymes in Bacillus subtilis: expression of the regulatory genes and analysis of mutations in degS and degU. J Bacteriol 172: 824-834. (Pubitemid 20070395)
23. Dubnau D, Hahn J, Roggiani M, Piazza F, Weinrauch Y (1994) Two-component regulators and genetic competence in Bacillus subtilis. Res Microbiol 145: 403-411. (Pubitemid 24281569)
24. Koumoutsi A, Chen XH, Vater J, Borriss R (2007) DegU and YczE positively regulate the synthesis of bacillomycin D by Bacillus amyloliquefaciens strain FZB42. Appl Environ Microbiol 73: 6953-6964. (Pubitemid 350076816)
25. Mariappan A, Makarewicz O, Chen XH, Borriss R (2012) Two-component response regulator DegU controls the expression of bacilysin in plant-growth-promoting bacterium Bacillus amyloliquefaciens FZB42. J Mol Microbiol Biotechnol 22: 114-125.
26. Verhamme DT, Kiley TB, Stanley-Wall NR (2007) DegU co-ordinates multicellular behaviour exhibited by Bacillus subtilis. Mol Microbiol 65: 554-68 (Pubitemid 47052735)
27. Murray EJ, Kiley TB, Stanley-Wall NR (2009) A pivotal role for the response regulator DegU in controlling multicellular behavior. Microbiology 155: 1-8.
28. Calvio C, Osera C, Amati G, Galizzi A (2008) Autoregulation of swrAA and motility in Bacillus subtilis. J Bacteriol 190: 5720-5728.
29. Stanley NR, Lazzazera BA (2005) Defining the genetic differences between wild and domestic strains of Bacillus subtilis that affect poly-γ-dl- glutamic acid production and biofilm formation. Mol Microbiol 57: 1143-1158. (Pubitemid 41139872)
30. Ostrowski A, Mehert A, Prescott A, Kailey TB, Stanley-Wall NR (2011) YuaB functions synergistically with the exopolysaccharide and TasA amyloid fibers to allow biofilm formation by Bacillus subtilis. J Bacteriol 193: 4821-4831.
31. Ollinger J, Song KB, Antelmann H, Hecker M, Helmann JD (2006) Role of the Fur regulon in iron transport in Bacillus subtilis. J Bacteriol 188: 3664-3673. (Pubitemid 43726229)
32. Schadt HS, Schadt S, Oldach F, Süssmuth RD (2009) 2-Amino-2-deoxychorismate is a key intermediate in Bacillus subtilis p-aminobenzoic acid biosynthesis. JACS 131: 3481-3483.
33. Nicolas P, Mäder U, Dervyn E, Rochat T, Leduc A, et al. (2012) Condition-dependent transcriptome reveals high-level regulatory architecture in Bacillus subtilis. Science 335: 1103-1106.
34. Streker K, Freiberg C, Labischinski H, Hacker J, Ohlsen K (2005) Staphylococcus aureus NfrA (SA0367) is a flavin mononucleotide-dependent NADPH oxidase involved in oxidative stress response. J Bacteriol 187: 2249-2256. (Pubitemid 40389122)
35. Moch C, Schrogel O, Allmannsberger R (2000) Transcription of the nfrA-ywcH operon from Bacillus subtilis is specifically induced in response to heat. J. Bacteriol 182: 889-898.
36. Rudrappa T, Quinn WJ, Wall NRS, Bais HP (2007) A degradation product of the salicylic acid pathway triggers oxidative stress resulting in down regulation of Bacillus subtilis biofilm formation on Arabidopsis thaliana roots. Planta 226: 283-297. (Pubitemid 46889509)
37. Mostertz J, Scharf C, Hecker M, Homuth G (2004). Transcriptome and proteome analysis of Bacillus subtilis gene expression in response to superoxide and peroxide stress. Microbiology 150: 497-512. (Pubitemid 38220053)
38. Burroughs AM, Iyer LM, Aravind L (2011) Functional diversification of the RING finger and other binuclear treble clef domains in prokaryotes and the early evolution of the ubiquitin system. Mol Biosyst 7: 2261-77
39. Weng J, Wang Y, Li J, Shen Q, Zhang R (2013) Enhanced root colonization and biocontrol activity of Bacillus amyloliquefaciens SQR9 by abrB gene disruption. Appl Microbiol Biotechnol 97: 8823-8830.