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Planta

, Volume 229, Issue 4, pp 747–755 | Cite as

The class IId bacteriocin thuricin-17 increases plant growth

  • Kyung Dong Lee
  • Elizabeth J. Gray
  • Fazli Mabood
  • Woo-Jin Jung
  • Trevor Charles
  • Scott R. D. Clark
  • Anh Ly
  • Alfred Souleimanov
  • Xiaomin Zhou
  • Donald Lawrence SmithEmail author
Original Article

Abstract

The mechanisms by which many plant growth promoting rhizobacteria (PGPR) affect plants are unknown. We recently isolated a rhizosphere bacterium (Bacillus thuringiensis NEB17), that promotes soybean growth and screened the liquid growth medium in which it grew for plant growth stimulating materials. We have also shown that it produces a bacteriocin (named by us as thuricin-17 and a member of the recently described class IId bacteriocins). Here we show that application of this bacteriocin to leaves (spray) or roots (drench) directly stimulates the growth of both a C3 dicot (soybean) and a C4 monocot (corn). This growth stimulation is similar in nature to that previously seen when plants are treated with Nod factors. Strain NEB17 contains three copies of the gene for thuricin 17 that code for identical amino acid sequences. These two lines of evidence suggest that the dual functions of these proteins may have constrained their evolution. This is the first report of direct plant growth enhancement by a bacteriocin.

Keywords

Bacillus thuringiensis Bacteriocin Bradyrhizobium japonicum Corn Plant growth promoting rhizobacteria (PGPR) Soybean 

Abbreviations

HPLC

High pressure liquid chromatography

PGPR

Plant growth promoting rhizobacteria

ePGPR

Extracellular plant growth promoting rhizobacteria

iPGPR

Intracellular plant growth promoting rhizobacteria

kDa

Kilo Daltan

LCOs

Lipo-chitooligosaccharides

MALDI–QTOF

Matrix assisted laser desorption/ionization–quadrapole time of flight

Notes

Acknowledgments

This work was supported by an NSERC strategic grant, an NSERC Research Network Grant, an NSERC Discovery grant and funding from the SEVE centre, all held by D. Smith.

References

  1. Abd-Alla MH (2001) Regulation of nodule formation in soybean-Bradyrhizobium symbiosis is controlled by shoot or/and root signals. Plant Growth Reg 34:241–250CrossRefGoogle Scholar
  2. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402PubMedCrossRefGoogle Scholar
  3. Atlas RM (1995) Handbook of media for environmental microbiology. CRC Press, Boca RatonGoogle Scholar
  4. Bai Y, D’Aoust F, Smith DL, Driscoll BT (2002) Isolation of plant-growth-promoting Bacillus strains from soybean root nodules. Can J Microbiol 48:230–238PubMedCrossRefGoogle Scholar
  5. Bai Y, Zhou X, Smith DL (2003) Enhanced soybean plant growth resulting from co-inoculation of Bacillus strains with Bradyrhizobium japonicum. Crop Sci 43:1774–1781CrossRefGoogle Scholar
  6. Bhuvaneawari TV, Turgeon BG, Bauer WD (1980) Early events in the infection of soybean [Glycine max (L.) Merr.] by Rhizobium japonicum I. location of infectible root cells. Plant Physiol 66:1027–1031CrossRefGoogle Scholar
  7. Fehr WR, Caviness CE, Burmood DT, Pennington JS (1971) Stage of development descriptions for soybeans, Glycine max (L.) Merrill. Crop Sci 11:929–931Google Scholar
  8. Gray E, Di Falco M, Souleimanov A, Smith DL (2006a) Proteomic analysis of the bacteriocin, thuricin-17 produced by Bacillus thuringiensis NEB17. FEMS Microbiol Lett 255:27–32PubMedCrossRefGoogle Scholar
  9. Gray EJ, Lee KD, Di Falco MR, Souleimanov AM, Zhou X, Ly A, Charles T, Driscoll B, Smith DL (2006b) A novel bacteriocin, thuricin-17, produced by PGPR strain Bacillus thuringiensis NEB17: isolation and classification. J Appl Microbiol 100:545–554PubMedCrossRefGoogle Scholar
  10. Gray EJ, Smith DL (2005) Intracellular and extracellular PGPR: commonalities and distinctions in the plant-bacterium signaling processes. Soil Biol Biochem 37:395–412CrossRefGoogle Scholar
  11. Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. California Agric Exp St Circ 347:1–32Google Scholar
  12. Jack WR, Tagg JR, Ray B (1995) Bacteriocins of Gram-positive bacteria. Microbiol Rev 59:171–200PubMedGoogle Scholar
  13. Kamoun F, Mejdoub H, Aouissaoui H, Reinbolt J, Hammami A, Jaoua S (2005) Purification, amino acid sequence and characterization of bacthuricin F4, a new bacteriocin produced by Bacillus thuringiensis. J Appl Microbiol 98:881–888PubMedCrossRefGoogle Scholar
  14. Kunst F, Ogasawara N, Moszer I, Albertini AM, Alloni G, Azevedo V, Bertero MG, Bessières P, Bolotin A, Borchert S, Borriss R, Boursier L, Brans A, Braun M, Brignell SC, Bron S, Brouillet S, Bruschi CV, Caldwell B, Capuano V, Carter NM, Choi S-K, Codani J-J, Connerton IF, Cummings NJ, Daniel RA, Denizot F, Devine KM, Düsterhöft A, Ehrlich SD, Emmerson PT, Entian KD, Errington J, Fabret C, Ferrari E, Foulger D, Fritz C, Fujita M, Fujita Y, Fuma S, Galizzi A, Galleron N, Ghim S-Y, Glaser P, Goffeau A, Golightly EJ, Grandi G, Guiseppi G, Guy BJ, Haga K, Haiech J, Harwood CR, Hénaut A, Hilbert H, Holsappel S, Hosono S, Hullo M-F, Itaya M, Jones L, Joris B, Karamata D, Kasahara Y, Klaerr-Blanchard M, Klein C, Kobayashi Y, Koetter P, Koningstein G, Krogh S, Kumano M, Kurita K, Lapidus A, Lardinois S, Lauber J, Lazarevic V, Lee S-M, Levine A, Liu H, Masuda S, Mauël C, Médigue C, Medina N, Mellado RP, Mizuno M, Moestl D, Nakai S, Noback M, Noone D, O’Reilly M, Ogawa K, Ogiwara A, Oudega B, Park S-H, Parro V, Pohl TM, Portetelle D, Porwollik S, Prescott AM, Presecan E, Pujic P, Purnelle B, Rapoport G, Rey M, Reynolds S, Rieger M, Rivolta C, Rocha E, Roche B, Rose M, Sadaie Y, Sato T, Scanlan E, Schleich S, Schroeter R, Scoffone F, Sekiguchi J, Sekowska A, Seror SJ, Serror P, Shin B-S, Soldo B, Sorokin A, Tacconi E, Takagi T, Takahashi H, Takemaru K, Takeuchi M, Tamakoshi A, Tanaka T, Terpstra P, Tognoni A, Tosato V, Uchiyama S, Vandenbol M, Vannier F, Vassarotti A, Viari A, Wambutt R, Wedler E, Wedler H, Weitzenegger T, Winters P, Wipat A, Yamamoto H, Yamane K, Yasumoto K, Yata K, Yoshida K, Yoshikawa H-F, Zumstein E, Yoshikawa H, Danchin A (1997) The complete genome sequence of the Gram-positive bacterium Bacillus subtilis. Nature 390:237–238CrossRefGoogle Scholar
  15. Meade HM, Long SR, Ruvkun GB, Brown SE, Ausubel T (1982) Physical and genetic characterization of symbiotic and auxotrophic mutants of Rhizobium meliloti induced by transposon Tn5 mutagenesis. J Bacteriol 149:114–122PubMedGoogle Scholar
  16. Nelson LM (2004) Plant growth promoting rhizobacteria (PGPR): prospects for new inoculants. Online. Crop Manag. doi: 10.1094/CM-2004-0301-05-RV. http://www.plantmanagementnetwork.org/pub/cm/review/2004/rhizobacteria/
  17. Norman J (1977) Opiates, receptors and endorphins. Br J Anaesth 49:523–524PubMedCrossRefGoogle Scholar
  18. Oresnik IJ, Twelker S, Hynes MF (1999) Cloning and characterization of a Rhizobium leguminosarum gene encoding a bacteriocin with similarities to RTX toxins. Appl Environ Microbiol 65:2833–2840PubMedGoogle Scholar
  19. Oresnik IJ, Charles TC, Finan TM (1994) Second site mutations specifically suppress the Fix- phenotype of Rhizobium meliloti ndvF mutations on alfalfa: identification of a conditional ndvF-dependent mucoid colony phenotype. Genetics 136:1233–1244PubMedGoogle Scholar
  20. Oscariz JC, Lasa I, Pisabarro AG (1999) Detection and characterization of cerein 7, a new bacteriocin produced by Bacillus cereus with a broad spectrum of activity. FEMS Microbiol Lett 178:337–341PubMedCrossRefGoogle Scholar
  21. Parret AHA, De Mot R (2002) Bacteria killing their own kind: novel bacteriocins of Pseudomonas and other γ-proteobacteria. Trends Microbiol 10:107–112PubMedCrossRefGoogle Scholar
  22. Prithiviraj B, Zhou X, Souleimanov A, Khan WM, Smith DL (2003) A host-specific bacteria-to-plant signal molecule (Nod factor) enhances germination and early growth of diverse crop plants. Planta 216:437–445PubMedGoogle Scholar
  23. Prithiviraj B, Souleimanov A, Zhou X, Smith DL (2000) Differential response of soybean (Glycine max (L.) Merr.) genotypes to lipo-chito-oligosaccharide Nod Bj-V (C18:1 MeFuc). J Exp Bot 51:2045–2051PubMedCrossRefGoogle Scholar
  24. Ragauskas AJ, Williams CK, Davison BH, Britovsek G, Cairney J, Eckert CA, Frederick WJ Jr, Hallett JP, Leak DJ, Liotta CL, Mielenz JR, Murphy R, Templer R, Tschaplinski T (2006) The path forward for biofuels. Biomat Sci 331:484–489Google Scholar
  25. Souleimanov A, Prithiviraj B, Smith DL (2002) The major Nod factor of Bradyrhizobium japonicum promotes early growth of soybean and corn. J Exp Bot 53:1929–1934PubMedCrossRefGoogle Scholar
  26. Vincent JM (1970) A manual for the practical study of root nodule bacteria. Blackwell Scientific Publ., OxfordGoogle Scholar
  27. Whipps JM (2001) Microbial interactions and biocontrol in the rhizosphere. J Exp Bot 52:487–511PubMedGoogle Scholar
  28. Wilson RA, Handley BA, Beringer JE (1998) Bacteriocin production and resistance in a field population of Rhizobium leguminosarum biovar viciae. Soil Biol Biochem 30:413–417CrossRefGoogle Scholar
  29. Zhang F, Smith DL (1995) Preincubation of Bradyrhizobium japonicum with genistein accelerates nodule development of soybean at suboptimal root zone temperatures. Plant Physiol 108:961–968PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Kyung Dong Lee
    • 1
  • Elizabeth J. Gray
    • 2
  • Fazli Mabood
    • 3
  • Woo-Jin Jung
    • 4
  • Trevor Charles
    • 5
  • Scott R. D. Clark
    • 5
  • Anh Ly
    • 5
  • Alfred Souleimanov
    • 3
  • Xiaomin Zhou
    • 3
  • Donald Lawrence Smith
    • 3
    Email author
  1. 1.Department of Oriental Medicine MaterialsDongshin UniversityNajuSouth Korea
  2. 2.Department of Molecular Genetics, Samuel Lunenfeld Research Institute, Mt Sinai HospitalUniversity of TorontoTorontoCanada
  3. 3.Plant Science Department, Macdonald CampusMcGill UniversitySte-Anne-de-BellevueCanada
  4. 4.Division of Applied Bioscience and Biotechnology, Environment-Friendly Agriculture Research Center (EFARC), Institute of Agricultural Science and Technology, College of Agriculture and Life ScienceChonnam National UniversityGwangjuSouth Korea
  5. 5.Department of BiologyUniversity of WaterlooWaterlooCanada

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