Abstract
Expression of HpaGxoo, a bacterial type-III effector protein, in transgenic plants induces disease resistance. Resistance also can be elicited by biocontrol bacteria. We studied effects of the biocontrolBacillus subtilis strain B-916 on the rice variety R109 and the thehpaG xoo -expressing rice line HER1. Colonisation of roots by B-916 caused 12.5±1.3% and 0.5±0.05% increases, in contrast to controls, in root growth of R109 and HER1. Growth of R109 leaves and stems was increased by 0.5±0.05% but that of HER1 was inhibited. When B-916 colonisation was subsequent to plant inoculation withRhizoctonia solani, a pathogen that causes sheath blight, the disease was less severe than controls in both R109 and HER1; HER1, nevertheless, was more resistant, suggesting that B-916 and HpaGxoo cooperate in inducing disease resistance. In R109 roots, theOsARF1 gene, which regulates plant growth, was expressed in consistence with growth promotion by B-916. Inversely, the depression ofOsARF1 expression was coincident with inhibition in growth of HER1 leaves and stems. In both plants, the expression ofOsEXP1, which encodes an expansin protein involved in plant growth, was concomitant with growth promotion in leaves and roots responding to B-916. We also studiedOsMAPK5b encoding a mitogen-activated protein kinase involved in multiple defence responses in rice. In response to B-916, early expression ofOsMAPK5b was coincident with R109 resistance to the disease, while HER1 expressed the gene similarly whether B-916 was present or not. Evidently, B916 and HER1 interact differently in rice growth and resistance. The combinative efffects should stimulate agricultural use and furthestudies on mechanisms that underlie the interaction.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Alfano J.R., Collmer A. (2004). Type III secretion system effector proteins: double agents in bacterial disease and plant defense. Annu. Rev. Phytopathol., 42: 385–414.
Belfield E.J., Ruperti B., Roberts J.A., McQueen-Mason S. (2005). Changes in expansin activity and gene expression during ethylene-promoted leaflet abscission inSambucus nigra. J. Exp. Bot., 56: 817–823.
Berberich T., Sugawara K., Harada M., Kusano T. (1995). Molecular cloning, characterization and expression of an elongation factor 1α gene in maize. Plant Mol. Biol., 28: 611–615.
Bostock R.M. (2005). Signal crosstalk and induced resistance: straddling the line between cost and benefit. Annu. Rev. Phytopathol., 43: 545–480.
Chen Z.Y., Mew T.W. (1998). Relationship between the colonisation, concentration and spray timing of antagonistic bacteria and sheath blight of rice. Jiang Su J. Agric. Sci., 14: 31–35.
Dangl J.L., Jones D.G. (2001). Plant pathogens and integrated defense responses to infection. Nature, 411: 826–833.
Dixon R.A. (2001). Natural products and plant disease resistance. Nature, 411: 843–847.
Dong H., Delaney T.P., Bauer D.W., Beer S.V. (1999). Harpin induces disease resistance inArabidopsis through the systemic acquired resistance pathway mediated by salicylic acid and theNIM1 gene. Plant J., 20: 207–215.
Dong X., Li X., Zhang Y., Fan W., Kinkema M., Clarke J. (2001). Regulation of systemic acquired resistance by NPR1 and its partners. Novartis Found. Symp., 236: 165–173.
Dong H.P., Peng J.L., Bao Z.L., Meng X., Bonasera J.M., Chen G., Beer S.V., Dong H. (2004). Downstream divergence of the ethylene signaling pathway for harpin-stimulatedArabidopsis growth and insect defense. Plant Physiol., 136: 3628–3638.
Dong H.P., Yu H.Q., Bao Z.L., Guo X., Peng J., Yao Z., Chen G., Qu S., Dong H. (2005). TheABI2-dependent abscissic acid signalling controls HrpN-induced drought tolerance inArabidopsis. Planta, 211: 313–327.
Gielen S., Aerts R., Seels B. (2004). Biocontrol agents ofBotrytis cinerea tested in climate chambers by making artificial infection on tomato leaves. Commun. Agric. Appl. Biol. Sci., 69: 631–639.
Johri B.N., Sharma A., Virdi J.S. (2003). Rhizobacterial diversity in India and its influence on soil and plant health. Adv. Biochem. Eng. Biotechnol. 84: 49–89.
Kim J.F., Beer S.V. (2000).hrp genes and harpins ofErwinia amylovora: a decade of discovery; in Fire Blight and Its Causative Agent,Erwinia amylovora (J.L. Vanneste eds), CAB International, Wallingford, UK, pp: 141–162.
Kim J.G., Park B.K., Yoo C.H., Jeon E., Oh J., Hwang I. (2003). Characterization of theXanthomonas axonopodis pv.glycines HpaG pathogenicity island. J. Bacteriol., 185: 3155–3166.
Li Y., Jones L., McQueen-Mason S. (2003). Expansins and cell growth. Curr. Opin. Plant Biol., 6: 603–610.
Lin D., Qu L.J., Gu H., Chen Z. (2001). A 3.1-kb genomic fragment ofBacillus subtilis encodes the protein inhibiting growth ofXanthomonas oryzae pv.oryzae. J. Appl. Microbiol., 91: 1044–1050.
Maleck K., Dietrich R.A. (1999). Defense on multiple fronts: how do plants cope with diverse enemies? Trends Plant Sci., 4: 215–219.
Nandakumar R., Babu S., Viswanathan R., Raguchander T., Samiyappan R. (2001). Induction of systemic resistance in rice against sheath blight disease byPseudomonas fluorescens. Soil Biol. Biochem., 33: 603–612.
Noel L., Thieme F., Nennstiel D., Bonas U. (2002). Two novel type III-secreted proteins ofXanthomonas campestris pv.vesicatoria are encoded within the HpaG pathogenicity island. J. Bacteriol., 184: 1340–1348.
Ongena M., Duby F., Jourdan E., Beaudry T., Jadin V., Dommes J., Thonart P. (2005).Bacillus subtilis M4 decreases plant susceptibility towards fungal pathogens by increasing host resistance associated with differential gene expression. Appl. Microbiol. Biotechnol., 67: 692–698.
Peng J.L., Dong H.S., Dong H.P., Delaney T.P., Bonasera J.M., Beer S.V. (2003). Harpin-elicited hypersensitive cell death and pathogen resistance require theNDR1 andEDS1 genes. Physiol. Mol. Plant Pathol., 62: 317–326.
Peng J., Bao Z., Li P., Chen G., Wang J., Dong H. (2004a). Harpin and its functional domains activate pathogen-inducible plant promoters inArabidopsis. Acta Bot. Sinica, 46: 1083–1090.
Peng J., Bao Z., Ren H., Wang J., Dong H. (2004b). Expression of harpinxoo in transgenic tobacco induces pathogen defense in the absence of hypersensitive response. Phytopathology, 94: 1048–1055.
Pieterse C.M., van Wees S.C., Hoffland E., van Pelt J.A., van Loon L.C. (1996). Systemic resistance inArabidopsis induced by biocontrol bacteria is independent of salicylic acid accumulation and pathogenesis-related gene expression. Plant Cell, 8: 1225–1237.
Pionnat S., Keller H., Hericher D., Bettachini A., Dessaux Y., Nesme X., Poncet C. (1999). Ti plasmids fromAgrobacterium characterize rootstock clones that initiated a spread of crown gall disease in Mediterranean countries. Appl. Environ. Microbiol., 65: 4197–4206.
Podile A.R., Prakash A.P. (1996). Lysis and biological control ofAspergillus niger byBacillus subtilis AF1. Can. J. Microbiol., 42: 533–538.
Rohilla R., Singh U.S., Singh R.L. (2002). Mode of action of acibenzolar-S-methyl against sheath blight of rice, caused byRhizoctonia solani Kuhn. Pest Manag. Sci., 58: 63–69.
Romanenko V.M., Alimov D.M. (2000). Ability of representatives ofPantoea agglomerans, as well asBacillus subtilis and somePseudomonas species to suppress the development of phytopathgenic bacteria and micromycetes in regulating plant growth. Mikrobiol. Z., 62: 29–37.
Shi Y.H., Zhu S.W., Mao X.Z., Feng J.X., Qin Y.M., Zhang L., Cheng J., Wei L.P., Wang Z.Y., Zhu Y.X. (2006). Transcriptome profiling, molecular biological, and physiological studies reveal a major role for ethylene in cotton fiber cell elongation. Plant Cell, 18: 651–664.
Staskawicz B.J., Mudgett M.B., Dangl J.L., Galan J.E. (2001). Common and contrasting themes of plant and animal diseases Science, 292: 2285–2289.
Strobel R.N., Gopalan J.S., Kuc J.A., He S.Y. (1996). Induction of systemic acquired resistance in cucumber byPseudomonas syringae pv.syringae 61 HrpZpss protein. Plant J., 9: 431–439.
Stuiver M.H., Custers J.H.H.V. (2001). Engineering disease resistance in plants. Nature, 411: 865–868.
Tjamos S.E. (2005). Induction of resistance toVerticillium dahliae inArabidopsis thaliana by the biocontrol agent K-165 and pathogenesis-related proteins gene expression. Mol. Plant-Microbe Interact., 18: 555–561.
Toure Y., Ongena M., Jacques P., Guiro A., Thonart P. (2004). Role of lipopeptides produced byBacillus subtilis GA1 in the reduction of grey mould disease caused byBotrytis cinerea on apple. J. Appl. Microbiol., 96: 1151–1160.
Vijayan P., Shockey J., Levesque C.A., Cook R.J., Browse, J. (1998). A role for jasmonate in pathogen defense ofArabidopsis. Proc. Natl. Acad. Sci. USA, 95: 7209–7214.
Vreeburg R.A., Benschop J.J., Peeters A.J., Colmer T.D., Ammerlaan A.H., Staal M., Elzenga T.M., Staals R.H., Darley C.P., McQueen-Mason S.J., Voesenek L.A. (2005). Ethylene regulates fast apoplastic acidification and expansin α transcription during submergence-induced petiole elongation inRumex palustris. Plant J., 43: 597–610.
Waller F., Furuya M., Nick P. (2002).OsARF1, an auxin response factor from rice, is auxin-regulated and classifies as a primary auxin responsive gene. Plant Mol. Biol., 50: 415–425.
Wang Z. and Tan G. (2005). Effects of fungicide on temporal and spatial niches ofRhizoctonia solani; Ying Yong Sheng Tai Xue Bao, 16: 1493–1496.
Xiong L., Yang Y. (2003). Disease resistance and abiotic stress tolerance in rice are inversely modulated by an abscisic acid-inducible mitogen-activated protein kinase. Plant Cell, 15: 745–759.
Xu D., Duan X., Wang B., Hong B., Ho T., Wu R. (1996). Expression of a late embryogenesis abundant protein gene,HVA1, from barley confers tolerance to water deficit and salt stress in transgenic rice. Plant Physiol., 110: 249–257.
Yao S., Gao X., Fuchsbauer N., Hillen W., Vater J., Wang J. (2003). Cloning, sequencing, and characterization of the genetic region relevant to biosynthesis of the lipopeptides iturin A and surfactin inBacillus subtilis. Curr. Microbiol., 47: 272–277.
Zasloff M. (2001). Antimicrobial peptides of multicellular organisms. Nature, 415: 389–395.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Ren, H., Song, T., Wu, T. et al. Effects of a biocontrol bacterium on growth and defence of transgenic rice plants expressing a bacterial type-III effector. Ann. Microbiol. 56, 281–287 (2006). https://doi.org/10.1007/BF03175019
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF03175019