Skip to main content
Log in

Expression of β-1,3-glucanase (GLU) and phenylalanine ammonia-lyase (PAL) genes and their enzymes in tomato plants induced after treatment with Bacillus subtilis CBR05 against Xanthomonas campestris pv. vesicatoria

  • Host Responses
  • Published:
Journal of General Plant Pathology Aims and scope Submit manuscript

Abstract

When 4-week-old tomato plants, which developed from seeds treated with antagonist Bacillus subtilis CBR05 before sowing, were challenged with Xanthomonas campestris pv. vesicatoria (XCV), activities of plant-defense enzymes β-1,3-glucanase (GLU, 42.5%) and phenylalanine ammonia-lyase (PAL; 93.9%) were significantly higher than in control plants at 72 h after inoculation with XCV. Also, GLU- and PAL-related genes were upregulated 2- and 3-fold, respectively, in these plants. Our results suggest that expression of GLU- and PAL-related genes in plants from seeds pretreated with B. subtilis are pivotal for inducing disease resistance against XCV.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  • Areas MS, Gonçalves RM, Soman JM, Sakate RK, Gioria R, da Silva Júnior TAF, Maringoni AC (2015) Prevalence of Xanthomonas euvesicatoria on pepper in Brazil. J Phytopathol 163:1050–1054

    Article  Google Scholar 

  • Bardin M, Ajouz S, Comby M, Lopez-Ferber M, Graillot B, Siegwart M, Nicot PC (2015) Is the efficacy of biological control against plant diseases likely to be more durable than that of chemical pesticides? Front Plant Sci 6:566

    Article  PubMed  PubMed Central  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Byrne JM, Dianese AC, Ji P, Campbell HL, Cuppels DA, Louws FJ, Miller SA, Jones JB, Wilson M (2005) Biological control of bacterial spot of tomato under field conditions at several locations in North America. Biol Control 32:408–418

    Article  Google Scholar 

  • Chandrasekaran M, Chun SC (2016a) Induction of defence-related enzymes in tomato (Solanum lycopersicum) plants treated with Bacillus subtilis CBR05 against Xanthomonas campestris pv. vesicatoria. Biocontrol Sci Technol 26:1366–1378

    Article  Google Scholar 

  • Chandrasekaran M, Chun SC (2016b) Expression of PR-protein genes and induction of defense-related enzymes by Bacillus subtilis CBR05 in tomato (Solanum lycopersicum) plants challenged with Erwinia carotovora subsp. carotovora. Biosci Biotechnol Biochem 80:2277–2283

    Article  CAS  Google Scholar 

  • Chandrasekaran M, Ee Y, Chun SC (2015) Plant growth promoting bacteria (PGPR): potentials in biocontrol and signal transduction mechanism. Int J Medicobiol Res 1:405–410

    Google Scholar 

  • Chandrasekaran M, Dharaneedharan S, Ee Y, Taehoon K, Chun SC (2016) Meta-analysis reveals that the genus Pseudomonas can be a better choice of biological control agent against bacterial wilt disease caused by Ralstonia solanacearum. Plant Pathol J 32:216–227

    Article  PubMed  PubMed Central  Google Scholar 

  • Chithrashree R, Udayasankar AC, Nayaka SC (2011) Plant growth-promoting rhizobacteria mediate induced systemic resistance in rice against bacterial leaf blight caused by Xanthomonas oryzae pv. oryzae. Biol Control 59:114–122

    Article  CAS  Google Scholar 

  • El-Shora HM (2002) Properties of phenylalanine ammonia-lyase from marrow cotyledons. Plant Sci 162:1–7

    Article  CAS  Google Scholar 

  • Ferraz HGM, Resende RS, Andrade CCL, Milagres EA, Oliveira JR, Rodrigues FA (2014) Rhizobacteria induces resistance against Fusarium wilt of tomato by increasing the activity of defence enzymes. Bragantia 73:274–283

    Article  Google Scholar 

  • Ferraz HGM, Resende RS, Moreira PC, Silveira PR, Milagres EA, Oliveira JR, Rodrigues FA (2015) Antagonistic rhizobacteria and jasmonic acid induce resistance against tomato bacterial spot. Bragantia 74:417–427

    Article  Google Scholar 

  • Indiragandhi P, Anandham R, Kim KA, Yim W, Madhaiyan M, Sa T (2008) Induction of defence responses in tomato against Pseudomonas syringae pv. tomato by regulating the stress ethylene level with Methylobacterium oryzae CBMB20 containing 1-aminocyclopropane-1-carboxylate deaminase. World J Microbiol Biotechnol 24:1037–1045

    Article  CAS  Google Scholar 

  • Jetiyanon K (2007) Defensive-related enzyme response in plants treated with a mixture of Bacillus strains (IN937a and IN937b) against different pathogens. Biol Control 42:178–185

    Article  Google Scholar 

  • Ji P, Campbell HL, Kloepper JW, Jones JB, Suslow TV, Wilson M (2006) Integrated biological control of bacterial speck and spot of tomato under field conditions using foliar biological control agents and plant growth-promoting rhizobacteria. Biol Control 36:358–367

    Article  Google Scholar 

  • Ji SH, Gururani MA, Chun SC (2014) Isolation and characterization of plant growth promoting endophytic diazotrophic bacteria from Korean rice cultivars. Microbiol Res 169:83–98

    Article  CAS  PubMed  Google Scholar 

  • Jones JB, Lacy GH, Bouzar H, Stall RE, Schaad NW (2004) Reclassification of the xanthomonads associated with bacterial spot disease of tomato and pepper. Syst Appl Microbiol 27:755–762

    Article  CAS  PubMed  Google Scholar 

  • Keen NT, Yoshikawa M (1983) Beta-1,3-endoglucanase from soybean releases elicitor active carbohydrates from fungus cell walls. Plant Physiol 71:460–465

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim D, Hwang B (2014) An important role of the pepper phenylalanine ammonia-lyase gene (PAL1) in salicylic acid-dependent signalling of the defence response to microbial pathogens. J Exp Bot 65:2295–2306

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kloepper JW, Rodríguez-Kábana R, Zehnder GW, Murphy JF, Sikora E, Fernández C (1999) Plant root–bacterial interactions in biological control of soilborne diseases and potential extension to systemic and foliar diseases. Aust Plant Pathol 28:21–26

    Article  Google Scholar 

  • Kloepper JW, Ryu CM, Zhang SA (2004) Induced systemic resistance and promotion of growth by Bacillus spp. Phytopathology 94:1259–1266

    Article  CAS  PubMed  Google Scholar 

  • Kocal N, Sonnewald U, Sonnewald S (2008) Cell wall-bound invertase limits sucrose export and is involved in symptom development and inhibition of photosynthesis during compatible interaction between tomato and Xanthomonas campestris pv vesicatoria. Plant Physiol 148:1523–1536

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lanna RF, Souza RM, Ferreira A, Quecine MC, Alves E, Azevedo JL (2013a) Biocontrol activity of Bacillus against a GFP-marked Pseudomonas syringae pv. tomato on tomato phylloplane. Aust Plant Pathol 42:643–651

    Article  Google Scholar 

  • Lanna RF, Souza RM, Marcelo M, Villela L, Edgar RJ, Pedro M, Resende LV (2013b) Induced defence responses in tomato against bacterial spot by proteins synthesized by endophytic bacteria. Trop Plant Pathol 38:295–302

    Article  Google Scholar 

  • Lee HJ, Park KH, Shim JH, Park R, Kim Y, Cho J, Hwangbo H, Kim Y, Cha G, Krishnan H, Kim K (2005) Quantitative changes of plant defense enzymes in biocontrol of pepper (Capsicium annuum L.) late blight by antagonistic Bacillus subtilis HJ927. J Microbiol Biotechnol 15:1073–1079

    CAS  Google Scholar 

  • Li SB, Fang M, Zhou RC, Huang J (2012) Characterization and evaluation of the endophyte Bacillus B014 as a potential biocontrol agent for the control of Xanthomonas axonopodis pv. dieffenbachiae induced blight of Anthurium. Biol Control 63:9–16

    Article  CAS  Google Scholar 

  • Li Y, Gu Y, Li J, Xu M, Wei Q, Wang Y (2015) Biocontrol agent Bacillus amyloliquefaciens LJ02 induces systemic resistance against cucurbits powdery mildew. Front Microbiol 6:883

    PubMed  PubMed Central  Google Scholar 

  • Liang ZC, Hseu RS, Wang HH (1995) Partial purification and characterization of a 1,3-β-d-glucanase from Ganoderma tsugae. J Ind Microbiol 14:5–9

    Article  CAS  Google Scholar 

  • MacDonald MJ, D’Cunha GB (2007) A modern view of phenylalanine ammonia lyase. Biochem Cell Biol 85:273–282

    Article  CAS  PubMed  Google Scholar 

  • Mauch-mani B, Slusarenko AJ (1996) Production of salicylic acid precursors is a major function of phenylalanine ammonia-lyase in the resistance of Arabidopsis to Peronospora parasitica. Plant Cell 8:203–212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moss WP, Byrne JM, Campbell HL, Ji P, Bonas U, Jones JB, Wilson M (2007) Biological control of bacterial spot of tomato using hrp mutants of Xanthomonas campestris pv. vesicatoria. Biol Control 41:199–206

    Article  Google Scholar 

  • Niu DD, Liu HX, Jiang CH, Wang YP, Wang QY, Jin HL, Guo JH (2011) The plant growth-promoting rhizobacterium Bacillus cereus AR156 induces systemic resistance in Arabidopsis thaliana by simultaneously activating salicylate and jasmonate/ethylene-dependent signaling pathways. Mol Plant Microbe Interact 24:533–542

    Article  CAS  PubMed  Google Scholar 

  • Podile AR, Laxmi VD (1998) Seed bacterization with Bacillus subtilis AF 1 increase phenylalanine ammonia-lyase and reduces the incidence of Fusarium wilt in pigeon pea. J Phytopathol 146:255–259

    Article  CAS  Google Scholar 

  • Prathuangwong S, Buensanteai N (2007) Bacillus amyloliquefaciens induced systemic resistance against bacterial pustule pathogen with increased phenols, phenylalanine ammonia lyase, peroxidases and β-1,3-glucanases in soybean plants. Acta Phytopathol et Entomol Hungarica 42:321–330

    Article  CAS  Google Scholar 

  • Ryan RP, Germaine K, Franks A, Ryan DJ, Dowling DN (2008) Bacterial endophytes: recent developments and applications. FEMS Microbiol Lett 278:1–9

    Article  CAS  PubMed  Google Scholar 

  • Van Loon LC (2007) Plant responses to plant growth-promoting rhizobacteria. Eur J Plant Pathol 119:243–254

    Article  Google Scholar 

  • Van Loon LC, Pieterse CMJ (2006) Significance of inducible defense-related proteins in infected plants. Ann Rev Phytopathol 44:135–162

    Article  Google Scholar 

  • van Wees SCM, de Swart EAM, van Pelt JA, van Loon LC, Pieterse CMJ (2000) Enhancement of induced disease resistance by simultaneous activation of salicylate- and jasmonate-dependent defense pathways in Arabidopsis thaliana. Proc Natl Acad Sci USA 97:8711–8716

    Article  PubMed  PubMed Central  Google Scholar 

  • Verhagen BWM, Glazebrook J, Zhu T, Chang HS, van Loon LC, Pieterse CMJ (2004) The transcriptome of rhizobacteria-induced systemic resistance in Arabidopsis. Mol Plant-Microbe Interact 17:895–908

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Wang L, Wang J, Jin P, Liu H, Zheng Y (2014) Bacillus cereus AR156-induced resistance to Colletotrichum acutatum is associated with priming of defence responses in loquat fruit. PLoS One 9:e112494

    Article  PubMed  PubMed Central  Google Scholar 

  • Yim WJ, Kim KY, Lee YW, Sundaram SP, Lee Y, Sa T (2014) Real time expression of ACC oxidase and PR-protein genes mediated by Methylobacterium spp. in tomato plants challenged with Xanthomonas campestris pv. vesicatoria. J Plant Physiol 171:1064–1075

    Article  CAS  PubMed  Google Scholar 

  • Zeamanek AB, Ko TS, Thimmapuram J, Hammerschlang FA, Korban SS (2002) Changes in β-1,3-glucanase mRNA levels in peach in response to treatment with pathogen culture filtrates wounding, and other elicitor. J Plant Physiol 159:877–889

    Article  Google Scholar 

Download references

Acknowledgements

This paper was written as part of Konkuk University’s research support program for its faculty on sabbatical leave in 2015.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Se Chul Chun.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chandrasekaran, M., Belachew, S.T., Yoon, E. et al. Expression of β-1,3-glucanase (GLU) and phenylalanine ammonia-lyase (PAL) genes and their enzymes in tomato plants induced after treatment with Bacillus subtilis CBR05 against Xanthomonas campestris pv. vesicatoria . J Gen Plant Pathol 83, 7–13 (2017). https://doi.org/10.1007/s10327-016-0692-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10327-016-0692-5

Keywords

Navigation