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Research article

Microbial Ecology and Diversity

The Antibiosis Action and Rice-Induced Resistance, Mediated by a Lipopeptide from Bacillus amyloliquefaciens B014, in Controlling Rice Disease Caused by Xanthomonas oryzae pv. oryzae

Shu Bin Li 1*, Shi Ru Xu 1, Rui Ning Zhang 1, Yuan Liu 1 and Ren Chao Zhou 1

Guangdong Provincial Key Laboratory of Biotechnology for Plant Development, School of Life Sciences, South China Normal University, Guangzhou 510631, P.R. China

Received: October 21, 2015; Accepted: December 29, 2015

J. Microbiol. Biotechnol. 2016; 26(4): 748-756

Published April 28, 2016 https://doi.org/10.4014/jmb.1510.10072

Copyright © The Korean Society for Microbiology and Biotechnology.

Abstract

In the present study, a lipopeptide (named AXLP14) antagonistic to Xanthomonas oryzae pv. oryzae (Xoo) was obtained from the culture supernatant of Bacillus amyloliquefaciens B014. Matrix-assisted laser desorption/ionization time-of-flight mass spectrometry analysis demonstrated that AXLP14 consisted of surfactin homologs. The minimum inhibition concentration and minimum bactericidal concentration of AXLP14 against Xoo were determined to be 1.25 and 2.50 mg/ml, respectively. At a concentration of 0.613 mg/ml, AXLP14 strongly inhibited the formation of Xoo biofilm. AXLP14 also inhibited the motility of Xoo in a concentration-dependent manner. Applying AXLP14 to rice seedlings significantly reduced the incidence and severity of disease caused by Xoo. In Xoo-infected rice seedlings, AXLP14 strongly and continuously up-regulated the expression of both OsNPR1 and OsWRKY45. In addition, AXLP14 effectively inhibited the Xoo-induced up-regulation of the expression of the abscisic acid biosynthesis gene OsNECD3 and the abscisic acid signalingresponsive gene OsLip9, indicating that AXLP14 may protect rice against Xoo-induced disease by enhancing salicylic acid defense and interfering with the abscisic acid response to virulence.

Keywords

Rice, Xanthomonas oryzae pv. oryzae, Bacillus lipopeptide, Antibiosis action, Induced resistance

References

  1. Andrews JM. 2011. Determination of minimum inhibitory concentrations. J. Antimicrob. Chemother. 48: 5-16.
    CrossRef
  2. Banas J, Hazlett KRO, Mazurkiewicz JE. 2001. An in vitro model for studying the contributions of the Streptococcus mutans glucan-binding protein-A to biofilm structure. Methods Enzymol. 337: 425-433.
    CrossRef
  3. Bang SWI, Park SH, Jeong JS, Kim YS, Jung H, Ha SH, Kim JK. 2013. Characterization of the stress-inducible OsNCED3 promoter in different transgenic rice organs and over three homozygous generations. Planta 237: 211-224.
    Pubmed CrossRef
  4. Bionda N, Fleeman RM, Shaw LN, Cudic P. 2013. Effect of ester to amide or N-methyl amide substitution on bacterial membrane depolarization and antibacterial activity of novel cyclic lipopeptides. Chem. Med. Chem. 8: 1394-1402.
    Pubmed PMC CrossRef
  5. Cawoy H, Mariutto M, Guillaume H, Fisher C, Vasilyeva N, Thonart P, et al. 2014. Plant defense stimulation by natural isolates of Bacillus depends on efficient surfactin production. Mol. Plant Microbe Interact. 27: 87-100.
    Pubmed CrossRef
  6. Cawoy H, Debois D, Franzil L, Edwin DP, Thonart P, Ongena M. 2015. Lipopeptides as main ingredients for inhibition of fungal phytopathogens by Bacillus subtilis/amyloliquefaciens. Microb. Biotechnol. 8: 281-295.
    Pubmed PMC CrossRef
  7. Chithrashree AC, Udayashankar AC, Chandra NS, Reddy MS, Srinivas C. 2011. Plant growth-promoting rhizobacteria mediate induced systemic resistance in rice against bacterial leaf blight caused by Xanthomonas oryzae pv. oryzae. Biocontrol 59: 114-22.
    CrossRef
  8. Chowdhury SP, Hartmann A, Gao X, Borriss R. 2015. Biocontrol mechanism by root-associated Bacillus amyloliquefaciens FZB42 - a review. Front. Microbiol. 6: 780.
    Pubmed PMC CrossRef
  9. De Vleesschauwer D, Xu J, Höfte M. 2014. Making sense of hormone-mediated defense networking: from rice to Arabidopsis. Front. Plant Sci. 5: 611.
    Pubmed PMC CrossRef
  10. Desoignies N, Schramme F, Ongena M, Legrève A. 2013. Systemic resistance induced by Bacillus lipopeptides in Beta vulgaris reduces infection by the rhizomania disease vector Polymyxa betae. Mol. Plant Pathol. 14: 416-421.
    Pubmed CrossRef
  11. Farace G, Fernandez O, Jacquens L, Coutte F, Krier F, Jacques P, et al. 2015. Cyclic lipopeptides from Bacillus subtilis activate distinct patterns of defence responses in grapevine. Mol. Plant Pathol. 16: 177-187.
    Pubmed CrossRef
  12. Gonzalez JF, Myers MP, Venturi V. 2013. The inter-kingdom solo OryR regulator of Xanthomonas oryzae is important for motility. Mol. Plant Pathol. 14: 211-221.
    Pubmed CrossRef
  13. Hwang SH, Lee IA, Yie SW, Hwang DJ. 2008. Identification of an OsPR10a promoter region responsive to salicylic acid. Planta 227: 1141-1150.
    Pubmed PMC CrossRef
  14. Kauffman HE, Reddy APK, Hsieh SPY, Merca SD. 1973. An improved technique for evaluating resistance of rice varieties to Xanthomonas oryzae. Plant Dis. Rep. 57: 537-541.
  15. Khan MA, Naeem M, Iqbal M. 2014. Breeding approaches for bacterial leaf blight resistance in rice (Oryza sativa L.), current status and future directions. Eur. J. Plant Pathol. 139:27-37.
    CrossRef
  16. Kim PI, Pyoung IL, Jaewon R, Young HK, Youn TC. 2010. Production of biosurfactant lipopeptides iturin A, fengycin, and surfactin A from Bacillus subtilis CMB32 for control of Colletotrichum gloeosporioides. J. Microbiol. Biotechnol. 20:138-145.
    Pubmed
  17. Li S, Fang M, Zhou RC, Huang J. 2012. Characterization and evaluation of endophytic Bacillus B014 as potential biocontrol agent for controlling bacterial blight of Anthurium caused by Xanthomonas axonopodis pv. dieffenbachiae. Biocontrol 63: 9-16.
  18. Liu J, Hagberg I, Novitsky L, Hadj-Moussa H, Avis TJ. 2014. Interaction of antimicrobial cyclic lipopeptides from Bacillus subtilis influences their effect on spore germination and membrane permeability in fungal plant pathogens. Fungal Biol. 118: 855-861.
    Pubmed CrossRef
  19. Mora I, Cabrefiga J, Montesinos E. 2015. Cyclic lipopeptide biosynthetic genes and products, and inhibitory activity of plant-associated Bacillus against phytopathogenic bacteria. PLoS One 10: e0127738.
    Pubmed PMC CrossRef
  20. Perez-Garcia A, Romero D, de Vicente A. 2011. Plant protection and growth stimulation by microorganisms:biotechnological applications of Bacilli in agriculture. Curr. Opin. Biotechnol. 22: 187-193.
    Pubmed CrossRef
  21. Raaijmakers JM, De Bruijn I, Nybroe O, Ongena M. 2010. Natural functions of lipopeptides from Bacillus and Pseudomonas: more than surfactants and antibiotics. FEMS Microbiol. Rev. 34: 1037-1062.
    Pubmed CrossRef
  22. Rahman A, Uddin W, Wenner N. 2015. Induced systemic resistance responses in perennial ryegrass against Magnaporthe oryzae elicited by semi-purified surfactin lipopeptides and live cells of Bacillus amyloliquefaciens. Mol. Plant Pathol. 16:546-558.
    Pubmed CrossRef
  23. Takatsuji H. 2014. Development of disease-resistant rice using regulatory components of induced disease resistance. Front. Plant Sci. 5: 630.
    Pubmed PMC CrossRef
  24. Waewthongrak W, Leelasuphakul W, McCollum G. 2014. Cyclic lipopeptides from Bacillus subtilis ABS-S14 elicit defense-related gene expression in citrus fruit. PLoS One 9: e109386.
    Pubmed PMC CrossRef
  25. Xu J, Audenaert K, Hofte M, De Vleesschauwer D. 2013. Abscisic acid promotes susceptibility to the rice leaf blight pathogen Xanthomonas oryzae pv oryzae by suppressing salicylic acid-mediated defenses. PLoS One 8: e67413.
    Pubmed PMC CrossRef
  26. Xu HM, Rong YJ, Zhao MX, Song B, Chi ZM. 2014. Antibacterial activity of the lipopetides produced by Bacillus amyloliquefaciens M1 against multidrug-resistant Vibrio spp. isolated from diseased marine animals. Appl. Microbiol. Biotechnol. 98: 127-136.
    Pubmed CrossRef
  27. Xu J, Zhou L, Venturi V, He YW, Kojima M, Sakakibari H, et al. 2015. Phytohormone-mediated interkingdom signaling shapes the outcome of rice-Xanthomonas oryzae pv. oryzae interactions. BMC Plant Biol. 15: 10-18.
    Pubmed PMC CrossRef
  28. Yamamoto S, Shiraishi S, Suzuki S. 2015. Are cyclic lipopeptides produced by Bacillus amyloliquefaciens S13-3 responsible for the plant defence response in strawberry against Colletotrichum gloeosporioides? Lett. Appl. Microbiol. 60: 379-386.
    Pubmed CrossRef
  29. Yi HS, Yang JW, Ryu CM. 2013. ISR meets SAR outside:additive action of the endophyte Bacillus pumilus INR7 and the chemical inducer, benzothiadiazole, on induced resistance against bacterial spot in field-grown pepper. Front. Plant Sci. 4: 122.
    Pubmed PMC CrossRef
  30. Zeriouh H, Romero D, Garcia-Gutierrez L, Cazorla FM, de Vicente A, Perez-Garcia A. 2011. The iturin-like lipopeptides are essential components in the biological control arsenal of Bacillus subtilis against bacterial diseases of cucurbits. Mol. Plant Microbe Interact. 24: 1540-1552.
    Pubmed CrossRef
  31. Zhang R S, L iu YF, L uo CP . 2012. Bacillus amyloliquefaciens Lx-11, a potential biocontrol agent against rice bacterial leaf streak. J. Plant Pathol. 94: 609-619.

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Article

Research article

J. Microbiol. Biotechnol. 2016; 26(4): 748-756

Published online April 28, 2016 https://doi.org/10.4014/jmb.1510.10072

Copyright © The Korean Society for Microbiology and Biotechnology.

The Antibiosis Action and Rice-Induced Resistance, Mediated by a Lipopeptide from Bacillus amyloliquefaciens B014, in Controlling Rice Disease Caused by Xanthomonas oryzae pv. oryzae

Shu Bin Li 1*, Shi Ru Xu 1, Rui Ning Zhang 1, Yuan Liu 1 and Ren Chao Zhou 1

Guangdong Provincial Key Laboratory of Biotechnology for Plant Development, School of Life Sciences, South China Normal University, Guangzhou 510631, P.R. China

Received: October 21, 2015; Accepted: December 29, 2015

Abstract

In the present study, a lipopeptide (named AXLP14) antagonistic to Xanthomonas oryzae pv.
oryzae (Xoo) was obtained from the culture supernatant of Bacillus amyloliquefaciens B014.
Matrix-assisted laser desorption/ionization time-of-flight mass spectrometry analysis
demonstrated that AXLP14 consisted of surfactin homologs. The minimum inhibition
concentration and minimum bactericidal concentration of AXLP14 against Xoo were
determined to be 1.25 and 2.50 mg/ml, respectively. At a concentration of 0.613 mg/ml,
AXLP14 strongly inhibited the formation of Xoo biofilm. AXLP14 also inhibited the motility of
Xoo in a concentration-dependent manner. Applying AXLP14 to rice seedlings significantly
reduced the incidence and severity of disease caused by Xoo. In Xoo-infected rice seedlings,
AXLP14 strongly and continuously up-regulated the expression of both OsNPR1 and
OsWRKY45. In addition, AXLP14 effectively inhibited the Xoo-induced up-regulation of the
expression of the abscisic acid biosynthesis gene OsNECD3 and the abscisic acid signalingresponsive gene OsLip9, indicating that AXLP14 may protect rice against Xoo-induced disease by enhancing salicylic acid defense and interfering with the abscisic acid response to
virulence.

Keywords: Rice, Xanthomonas oryzae pv. oryzae, Bacillus lipopeptide, Antibiosis action, Induced resistance

References

  1. Andrews JM. 2011. Determination of minimum inhibitory concentrations. J. Antimicrob. Chemother. 48: 5-16.
    CrossRef
  2. Banas J, Hazlett KRO, Mazurkiewicz JE. 2001. An in vitro model for studying the contributions of the Streptococcus mutans glucan-binding protein-A to biofilm structure. Methods Enzymol. 337: 425-433.
    CrossRef
  3. Bang SWI, Park SH, Jeong JS, Kim YS, Jung H, Ha SH, Kim JK. 2013. Characterization of the stress-inducible OsNCED3 promoter in different transgenic rice organs and over three homozygous generations. Planta 237: 211-224.
    Pubmed CrossRef
  4. Bionda N, Fleeman RM, Shaw LN, Cudic P. 2013. Effect of ester to amide or N-methyl amide substitution on bacterial membrane depolarization and antibacterial activity of novel cyclic lipopeptides. Chem. Med. Chem. 8: 1394-1402.
    Pubmed KoreaMed CrossRef
  5. Cawoy H, Mariutto M, Guillaume H, Fisher C, Vasilyeva N, Thonart P, et al. 2014. Plant defense stimulation by natural isolates of Bacillus depends on efficient surfactin production. Mol. Plant Microbe Interact. 27: 87-100.
    Pubmed CrossRef
  6. Cawoy H, Debois D, Franzil L, Edwin DP, Thonart P, Ongena M. 2015. Lipopeptides as main ingredients for inhibition of fungal phytopathogens by Bacillus subtilis/amyloliquefaciens. Microb. Biotechnol. 8: 281-295.
    Pubmed KoreaMed CrossRef
  7. Chithrashree AC, Udayashankar AC, Chandra NS, Reddy MS, Srinivas C. 2011. Plant growth-promoting rhizobacteria mediate induced systemic resistance in rice against bacterial leaf blight caused by Xanthomonas oryzae pv. oryzae. Biocontrol 59: 114-22.
    CrossRef
  8. Chowdhury SP, Hartmann A, Gao X, Borriss R. 2015. Biocontrol mechanism by root-associated Bacillus amyloliquefaciens FZB42 - a review. Front. Microbiol. 6: 780.
    Pubmed KoreaMed CrossRef
  9. De Vleesschauwer D, Xu J, Höfte M. 2014. Making sense of hormone-mediated defense networking: from rice to Arabidopsis. Front. Plant Sci. 5: 611.
    Pubmed KoreaMed CrossRef
  10. Desoignies N, Schramme F, Ongena M, Legrève A. 2013. Systemic resistance induced by Bacillus lipopeptides in Beta vulgaris reduces infection by the rhizomania disease vector Polymyxa betae. Mol. Plant Pathol. 14: 416-421.
    Pubmed CrossRef
  11. Farace G, Fernandez O, Jacquens L, Coutte F, Krier F, Jacques P, et al. 2015. Cyclic lipopeptides from Bacillus subtilis activate distinct patterns of defence responses in grapevine. Mol. Plant Pathol. 16: 177-187.
    Pubmed CrossRef
  12. Gonzalez JF, Myers MP, Venturi V. 2013. The inter-kingdom solo OryR regulator of Xanthomonas oryzae is important for motility. Mol. Plant Pathol. 14: 211-221.
    Pubmed CrossRef
  13. Hwang SH, Lee IA, Yie SW, Hwang DJ. 2008. Identification of an OsPR10a promoter region responsive to salicylic acid. Planta 227: 1141-1150.
    Pubmed KoreaMed CrossRef
  14. Kauffman HE, Reddy APK, Hsieh SPY, Merca SD. 1973. An improved technique for evaluating resistance of rice varieties to Xanthomonas oryzae. Plant Dis. Rep. 57: 537-541.
  15. Khan MA, Naeem M, Iqbal M. 2014. Breeding approaches for bacterial leaf blight resistance in rice (Oryza sativa L.), current status and future directions. Eur. J. Plant Pathol. 139:27-37.
    CrossRef
  16. Kim PI, Pyoung IL, Jaewon R, Young HK, Youn TC. 2010. Production of biosurfactant lipopeptides iturin A, fengycin, and surfactin A from Bacillus subtilis CMB32 for control of Colletotrichum gloeosporioides. J. Microbiol. Biotechnol. 20:138-145.
    Pubmed
  17. Li S, Fang M, Zhou RC, Huang J. 2012. Characterization and evaluation of endophytic Bacillus B014 as potential biocontrol agent for controlling bacterial blight of Anthurium caused by Xanthomonas axonopodis pv. dieffenbachiae. Biocontrol 63: 9-16.
  18. Liu J, Hagberg I, Novitsky L, Hadj-Moussa H, Avis TJ. 2014. Interaction of antimicrobial cyclic lipopeptides from Bacillus subtilis influences their effect on spore germination and membrane permeability in fungal plant pathogens. Fungal Biol. 118: 855-861.
    Pubmed CrossRef
  19. Mora I, Cabrefiga J, Montesinos E. 2015. Cyclic lipopeptide biosynthetic genes and products, and inhibitory activity of plant-associated Bacillus against phytopathogenic bacteria. PLoS One 10: e0127738.
    Pubmed KoreaMed CrossRef
  20. Perez-Garcia A, Romero D, de Vicente A. 2011. Plant protection and growth stimulation by microorganisms:biotechnological applications of Bacilli in agriculture. Curr. Opin. Biotechnol. 22: 187-193.
    Pubmed CrossRef
  21. Raaijmakers JM, De Bruijn I, Nybroe O, Ongena M. 2010. Natural functions of lipopeptides from Bacillus and Pseudomonas: more than surfactants and antibiotics. FEMS Microbiol. Rev. 34: 1037-1062.
    Pubmed CrossRef
  22. Rahman A, Uddin W, Wenner N. 2015. Induced systemic resistance responses in perennial ryegrass against Magnaporthe oryzae elicited by semi-purified surfactin lipopeptides and live cells of Bacillus amyloliquefaciens. Mol. Plant Pathol. 16:546-558.
    Pubmed CrossRef
  23. Takatsuji H. 2014. Development of disease-resistant rice using regulatory components of induced disease resistance. Front. Plant Sci. 5: 630.
    Pubmed KoreaMed CrossRef
  24. Waewthongrak W, Leelasuphakul W, McCollum G. 2014. Cyclic lipopeptides from Bacillus subtilis ABS-S14 elicit defense-related gene expression in citrus fruit. PLoS One 9: e109386.
    Pubmed KoreaMed CrossRef
  25. Xu J, Audenaert K, Hofte M, De Vleesschauwer D. 2013. Abscisic acid promotes susceptibility to the rice leaf blight pathogen Xanthomonas oryzae pv oryzae by suppressing salicylic acid-mediated defenses. PLoS One 8: e67413.
    Pubmed KoreaMed CrossRef
  26. Xu HM, Rong YJ, Zhao MX, Song B, Chi ZM. 2014. Antibacterial activity of the lipopetides produced by Bacillus amyloliquefaciens M1 against multidrug-resistant Vibrio spp. isolated from diseased marine animals. Appl. Microbiol. Biotechnol. 98: 127-136.
    Pubmed CrossRef
  27. Xu J, Zhou L, Venturi V, He YW, Kojima M, Sakakibari H, et al. 2015. Phytohormone-mediated interkingdom signaling shapes the outcome of rice-Xanthomonas oryzae pv. oryzae interactions. BMC Plant Biol. 15: 10-18.
    Pubmed KoreaMed CrossRef
  28. Yamamoto S, Shiraishi S, Suzuki S. 2015. Are cyclic lipopeptides produced by Bacillus amyloliquefaciens S13-3 responsible for the plant defence response in strawberry against Colletotrichum gloeosporioides? Lett. Appl. Microbiol. 60: 379-386.
    Pubmed CrossRef
  29. Yi HS, Yang JW, Ryu CM. 2013. ISR meets SAR outside:additive action of the endophyte Bacillus pumilus INR7 and the chemical inducer, benzothiadiazole, on induced resistance against bacterial spot in field-grown pepper. Front. Plant Sci. 4: 122.
    Pubmed KoreaMed CrossRef
  30. Zeriouh H, Romero D, Garcia-Gutierrez L, Cazorla FM, de Vicente A, Perez-Garcia A. 2011. The iturin-like lipopeptides are essential components in the biological control arsenal of Bacillus subtilis against bacterial diseases of cucurbits. Mol. Plant Microbe Interact. 24: 1540-1552.
    Pubmed CrossRef
  31. Zhang R S, L iu YF, L uo CP . 2012. Bacillus amyloliquefaciens Lx-11, a potential biocontrol agent against rice bacterial leaf streak. J. Plant Pathol. 94: 609-619.