Browse > Article
http://dx.doi.org/10.5423/PPJ.2009.25.4.389

Priming of Defense-Related Genes Confers Root-Colonizing Bacilli-Elicited Induced Systemic Resistance in Pepper  

Yang, Jung-Wook (Industrial Biotechnology and Bioenergy Research Center, KRIBB)
Yu, Seung-Hun (Department of Applied Biology, Chungnam National University)
Ryu, Choong-Min (Industrial Biotechnology and Bioenergy Research Center, KRIBB)
Publication Information
The Plant Pathology Journal / v.25, no.4, 2009 , pp. 389-399 More about this Journal
Abstract
A group of beneficial plant bacteria has been shown to increase crop growth referring to as plant growth-promoting rhizobacteria (PGPR). PGPR can decrease plant disease directly, through the production of antagonistic compounds, and indirectly, through the elicitation of a plant defense response termed induced systemic resistance (ISR). While the mechanism of PGPR-elicited ISR has been studied extensively in the model plant Arabidopsis, it is less well characterized in crop plants such as pepper. In an effort to better understand the mechanism of ISR in crop plants, we investigated the induction of ISR by Bacillus cereus strain BS107 against Xanthomonas axonopodis pv. vesicatoria in pepper leaves. We focused on the priming effect of B. cereus strain BS107 on plant defense genes as an ISR mechanism. Of ten known pepper defense genes that were previously reported to be involved in pathogen defense signaling, the expression of Capsicum annum pathogenesis-protein 4 and CaPR1 was systemically primed by the application of strain BS107 onto pepper roots confirming by quantitative-reverse transcriptase PCR. Our results provide novel genetic evidence of the priming effect of a rhizobacterium on the expression of pepper defense genes involved in ISR.
Keywords
induced systemic resistance; pepper; PGPR; priming;
Citations & Related Records
Times Cited By KSCI : 2  (Citation Analysis)
Times Cited By Web Of Science : 6  (Related Records In Web of Science)
연도 인용수 순위
1 Bakker, P. A. H. M., Pieterse, C. M. J. and Van Loon, L. C. 2007. Induced systemic resistance by fluorescent Pseudomonas spp. Phytopathology 97:239-243   DOI   ScienceOn
2 Beckers, G. J. and Comath, U. 2007. Priming for stress resistance: from the lab to the field. Curr. Opin. Plant BioI. 10:425-431   DOI   ScienceOn
3 Benhamou, N., Kloepper, J. W., Quadt-Hallman, A. and Tuzun, S. 1996. Induction of defenserelated ultrastructural modifications in pea root tissues inoculated with endophytic bacteria. Plant Physiol. 112:919-929   DOI   PUBMED
4 Comath, U., Pieterse, C. M. and Mauch-Mani, B. 2002. Priming in plant-pathogen interactions. Trends. Plant Sci. 7:210-216   DOI   ScienceOn
5 Comath, U., Beckers, G. J., Flors, V., Garcia-Agustin, P., Jakab, G., Mauch, F., Newman, M. A., Pieterse, C. M., Poinssot, B., Pozo, M. J., Pugin, A., Schaffrath, U., Ton, J., Wendehenne, D., Zimmerli, L. and Mauch-Mani, B. 2006. Priming: getting ready for battle. Mol. Plant-Microbe Interact. 19:1062-1071   DOI   ScienceOn
6 Kang, S. H., Cho, H. S., Cheong, H., Ryu, C. M., Kim, J. F. and Park, S. H. 2007. Two bacterial entophytes eliciting both plant growth promotion and plant defense on pepper (Capsicum annuum L.). J. Microbiol. Biotechnol. 17:96-103   PUBMED
7 Kim, K. J., Park, C. J., An, J. M., Ham, B. K, Lee, B. J. and Paek, K. H. 2005. CaAlaAT1 catalyzes the alanine: 2-oxoglutarate amonitransferase reaction during the resistance response against Tobacco mosaic virus in hot pepper. Planta 221:857-867   DOI   ScienceOn
8 Kim, K. J., Park, C. J., Ham, B. K., Choi, S. B., Lee, B. J. and Paek, K. H. 2006. Induction of a cytosolic pyruvatekinase 1 gene during the resistance response to Tobacco mosaic virus in Capsicum annuum. Plant Cell. Rep. 25:359-364   DOI   ScienceOn
9 Kim, Y. J. and Hwang, B. K. 2000. Pepper gene encoding a basic pathogenesis-related1 protein is pathogen and ethylene inducible. Physiol. Plant 108:51-60   DOI
10 Kloepper, J. W. 1993. Plant growth-promoting rhizobacteria as biological control agents. In: F. B. Metting Soil Microbial Ecology: Applications in Agricultural and Environmental Management, Marcel Dekker Inc., New York, pp 255-274
11 Kloepper, J. W., Ryu, C. M. and Zhang, S. 2004. Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 94:1259-1266   DOI   ScienceOn
12 Kloepper, J. W., Gutierrez-Estrada, A. and McInroy, J. A. 2007. Photoperiod regulates elicitation of growth promotion but not induced resistance by plant growth-promoting rhizobacteria. Can. J. Microbiol. 53:159-67   DOI   ScienceOn
13 Malolepsza, U. 2006. Induction of disease resistance by acibenzolar-S-methyl and o-hydroxyethylorutin against Botrytis cinerea in tomato plants. Crop Prot. 25:956-962   DOI   ScienceOn
14 Raupach, G. S. and Kloepper, J. W. 1998. Mixtures of plant growth-promoting rhizobacteria enhance biological control of multiple cucumber pathogens. Phytopathology 88:1158-1164   DOI   ScienceOn
15 Park, C. J., Kim, K. J., Shin, R., Park, J. M., Shin, Y. C. and Paek, K. H. 2004. Pathogenesis-related protein 10 isolated from hot pepper functions as a ribonuclease in an antivial pathway. Plant J. 37:186-198   DOI   PUBMED   ScienceOn
16 Pozo, M. J. and Azcon-Aguilar, C. 2007. Unraveling mycorrhiza-induced resistance. Curr. Opin. Plant Biol. 10:393-398   DOI   ScienceOn
17 Quilis, J., Pefias, G., Messeguer, J., Brugidou, C. and San Seg-undo, B. 2008. The Arabidopsis AtNPR1 inversely modulates defense responses against fungal, bacterial, or viral pathogens while conferring hypersensitivity to abiotic stresses in transgenic rice. Mol. Plant-Microbe Interact. 21:1215-1231   DOI   ScienceOn
18 Ryu, C. M., Kim, J. W., Choi, O. H., Park, S. Y., Park, S. H. and Park, C. S. 2005. Nature of a root-associated Paenibacillus polymyxa from field-grown winter barley in Korea. J. Microbiol. Biotechnol. 15:984-991
19 Slaughter, A. R, Hamiduzzaman, M. M., Gindro, K., Neuhaus, J. M. and Mauch-Mani, B. 2008. Beta-aminobutyric acid-induced resistance in grapevine against downy mildew: involvement of pterostilbene. Eur. J. Plant Pathol. 122:185-195   DOI   ScienceOn
20 Walters, D. R. and Boyle, C. 2005. Induced resistance and allocation costs: what is the impact of pathogen challenge? Physiol. Mol. Plant Pathol. 66:40-44   DOI   ScienceOn
21 Abu, I. P., Kim, S., Lee, Y. H. and Suh, S. C. 2007. Vitamin B1-induced priming is dependent on hydrogen peroxide and the NPR1 gene in Arabidopsis. Plant Physiol. 143:838-848   DOI   ScienceOn
22 Attaran, E., Rostas, M. and Zeier, J. 2008. Pseudomonas syringae elicits emission of the terpenoid (E,E)-4,8,12-trimethyl-1,3,7,1l-tridecatetraene in Arabidopsis leaves via jasmonate signaling and expression of the terpene synthase TPS4. Mol. Plant-Microbe. Interact. 21:1482-1497   DOI   ScienceOn
23 Chung, E., Ryu, C. M., Oh, S. K. and Choi, D. 2006. The essential role of pepper CaSgt1 and CaSkp1 genes in plant development and basal resistance. Physiol. Plant 126:605-612   DOI
24 Jetiyanon, K. and Kloepper, J. W. 2002. Mixtures of plant growth-promoting rhizobacteria for induction of systemic resistance against multiple plant diseases. Biol. Control 24:285-291   DOI   ScienceOn
25 Yi, S. Y., Kim, J. H., Joung, Y. H., Lee, S., Kim, W. T., Yu, S. H. and Choi, D. 2004. The pepper transcription factor CaPF1 confers pathogen and freezing tolerance in Arabidopsis. Plant Physiol. 136:2862-2874   DOI   ScienceOn
26 Heil, M. and Kost, C. 2006. Priming of indirect defences. Ecol. Lett. 9:813-817   DOI   ScienceOn
27 Kim, Y. C., Yi, S. Y., Mang, H. G., Seo, Y. S., Kim, W. T. and Choi, D. 2001. Pathogen-induced expression of cyclo-oxygenase homologue in hot pepper (Capsicum annuum cv. Pukang). J. Exp. Bot. 53:383-385   DOI   ScienceOn
28 Verhagen, B. W, Glazebrook, J., Zhu, T., Chang, H. S., van Loon, L. C. and Pieterse, C. M. 2004. The transcriptome of Rhizobacteria-Induced Systemic Resistance in Arabidopsis. Mol. Plant Microbe Interact. 17:895-908   DOI   ScienceOn
29 Akram, A., Ongena, M., Duby, F., Dommes, J. and Thonart, P. 2008. Systemic resistance and lipooxygenase-related defence response induced in tomato by Pseudomonas putida strain BTP1. BMC Plant BioI. 8:113-124   DOI   ScienceOn
30 Oh, S. K., Lee, S., Chung, E., Park, J. M., Yu, S. H., Ryu, C. M. and Choi, D. 2006. Insight into Types I and II nonhost resistance using expression patterns of defense-related genes in tobacco. Planta 213:1102-1107   DOI
31 Conn, V. M., Walker, A. R. and Franco, C. M. 2008. Endophytic actinobacteria induce defense pathways in Arabidopsis thaliana. Mol. Plant-Microbe Interact. 21:208-218   DOI   ScienceOn
32 Hossain, M. M., Sultana, F., Kubota, M. and Hyakumachi, M. 2008. Differential inducible defense mechanisms against bacterial speck pathogen in Arabidopsis thaliana by plant-growth-promoting fungus Penicillium. Plant Soil 304:227-239   DOI
33 Cartieaux, F., Contesto, C., Gallou, A., Desbrosses, G, Kopka, J., Taconnat, L., Renou, J. P. and Touraine, B. 2008. Simultaneous interaction of Arabidopsis thaliana with Bradyrhizobium Sp. strainORS278 and Pseudomonas syringae pv. tomato DC3000 leads to complex transcriptome changes. Mol. Plant-Microbe Interact. 21:244-259   DOI   ScienceOn
34 Kim, Y. C., Kim, S. Y, Paek, K. H., Choi, D. and Park, J. M. 2006. Suppression of CaCYP1, a novel cytochrome P450 gene, compromises the basal pathogen defense response of pepper plants. Biochem. Biophys. Res. Commun. 345:638-645   DOI   ScienceOn
35 Kokalis-Burelle, N., Vavrina, C. S., Rosskopf, E. N. and Shelby, R. A. 2002. Field evaluation of plantgrowth-promoting rhizobacteria amended transplant mixes and soil solarization for tomato and pepper production in Florida. Plant Soil 238:257-266   DOI   ScienceOn
36 Park, C. J., Shin, Y. C., Lee, B. J., Kim, K. J., Kim, J. K. and Paek, K. H. 2006. A hot pepper gene encoding WRKY transcription factor is induced during hypersensitive response to Tobacco mosaic virus and Xanthomonas campestris. Planta 223:168-179   DOI
37 Ton, J., Jakab, G., Toquin, V., Iavicoli, V., Maeder, M., Metraux, J. P. and Mauch-Mania, B. 2005. Dissecting the b-aminobutyric acid-induced priming phenomenon in Arabidopsis. Plant Cell 17:987-999   DOI   ScienceOn
38 Jakab, G, Ton, J., Flors, V., Zimmerli, L., Metraux, J. P. and MauchMani, B. 2005. Enhancing Arabidopsis salt and drought stress tolerance by chemical priming for its abscisic acid responses Plant Physiol. 139:267-274   DOI   ScienceOn
39 Bais, H. P., Weir, T. L., Perry, L. G, Gilroy, S. and Vivanco, J. M. 2006. The role of root exudates in rhizosphere interactions with plants and other organisms. Annu. Rev. Plant Biol. 57:233-266   DOI   PUBMED   ScienceOn
40 Hacisalihoglu, G., Longo, P., Olson, S. and M, Momol. T. 2007. Bacterial wilt induced changes in nutrient distribution and biomass and the effect of acibenzolar-S-methyl on bacterial wilt in tomato. Crop Prot. 26:978-982   DOI   ScienceOn
41 Goellner, K. and Comath, U. 2008. Priming: it's all the world to induced disease resistance. Eur. J. Plant Pathol. 121:233-242   DOI   ScienceOn
42 van Hulten, M., PeIser, M., van Loon, L. C., Pieterse, C. M. and Ton, J. 2006. Costs and benefits of priming for defense in Arabidopsis. Proc. Natl. Acad. Sci. USA 103:5602-5607   DOI   ScienceOn
43 Yoo, T. H., Park, C. l., Ham, B. K., Kim, K. l. and Paek, K. H. 2004. Ornithine decarboxylase gene (CaODCl) is specifically induced during TMV-mediated but salicylate-independent resistant response in hot pepper. Plant Cell Physiol. 45:1537-1542   DOI   ScienceOn
44 Park, C. J., Shin, R., Park, J. M., Lee, G. J., Yoo, T. H. and Paek, K.H. 2001. Hot pepper cDNA encoding a ge-at-valuation of plant pathogenesis-related protein 4 is induced during the resistance response to tobacco mosaic virus. Mol. Cells. 11:122-127   PUBMED
45 Edreva, A. 2005. Pathogenesis-related proteins: research progress in the last 15years. Plant Physiol. 31:105-124
46 Murphy, J. F., Reddy, M. S., Ryu, C. M., Kloepper, J. W. and Li, R. 2003. Rhizobacteria-mediated growth promotion of tomato leads to protection against Cucumber mosaic virus. Phytopathology 93:1301-1307   DOI   ScienceOn
47 Shin, R., Kim, M. J. and Paek, K. H. 2003. The CaIinl(Capsicum annuum TMV-induced Clone 1) and CaTml-2 genes are linked head-to-head and share a bidirectional promoter. Plant Cell Physiol. 44:549-554   DOI   ScienceOn
48 Alstrom, S. 1991. Induction of disease resistance in common bean susceptible to halo blight bacterial pathogen after seed bacterization with rhizosphere pseudomonads. J. Gen. Appl. MicrobioI. 37:495-501   DOI
49 Jetiyanon, K., Fowler, W. D. and Kloepper, J. W. 2003. Broad-spectrum protection against several pathogens by PGPR mixtures under field conditions in Thailand. Plant Dis. 87:1390-1394   DOI   ScienceOn
50 Sadd, B. M., Kleinlogel, Y., Schmid-Hempel, R and SchmidHempel, P. 2005. Trans-generational immune priming in a social insect. Biol. Lett. 1:386-388   DOI   ScienceOn
51 Ryu, C. M., Anand, A., Kang, L. and Mysore, K. S. 2004. Agrodrench: a novel and effective agroinoculation method for virus-induced gene silencing in roots and diverse Solanaceous species. Plant J. 40:322-331   DOI   ScienceOn
52 van Peer, R, Niemann, G. J. and Schippers, B. 1991. Induced resistance and phytoalexin accumulation in biological control of Fusarium wilt of carnation by Pseudomonas sp. strain WCS417r. Phytopathology 81:728-734   DOI
53 van Loon, L. C. 2007. Plant responses to plant growth-promoting rhizobacteria Eur. J. Plant Pathol. 119:243-254   DOI   ScienceOn
54 Weller, D. M. 1988. Biological control of soilborne plant pathogens in the rhizosphere with bacteria. Annu. Rev. Phytopathol. 26:379-407   DOI   ScienceOn
55 D'Arcy, W. G. 1986. Solanaceae biology and systematic, Columbia University Press
56 Gomez-Ariza, J., Campo, S., Rufat, M., Estopa, M., Messeguer, J., San Segundo, B. and Coca, M. 2007. Sucrose-mediated priming of plant defense responses and broad-spectrum disease resistance by overexpression of the maize pathogenesis-related PRms protein in rice plants. Mol. Plant-Microbe Interact. 20:832-842   DOI   ScienceOn
57 Park, C. J., An, J. M., Shin, Y. C., Kim, K. J., Lee, B. J. and Paek, K. H. 2004b. Molecular characterization of pepper germinlike protein as the novel PR -16 family of pathogenesis-related proteins isolated during the resistance response to viral and bacterial infection. Planta 219:797-806   PUBMED
58 Ryu, C. M., Murphy, J. F., Reddy, M. S. and Kloepper, J. W. 2007. A two-strain mixture of rhizobacteria elicits inducation of systemic resistance against Pseudomonas syringae and Cucumber mosaic virus coupled to promotion of plant growth on Arabidopsis thaliana. J. Microbiol. Biotechnol. 17:280-286   PUBMED
59 Nam, Y. W. and Paek, K. H. 2001. Isolation of pepper mRNAs differentially expressed during the hypersensitive response to tobacco mosaic virus and characterization of a proteinase inhibitor gene. Plant Sci. 161:727-737   DOI   ScienceOn
60 De Vleesschauwer, D., Djavaheri, M., Bakker, P. A. and Hofie, M. 2008. Pseudomonas fluorescens WCS 374r-induced systemic resistance in rice against Magnaporthe oryzae is based on pseudobactin-mediated priming for a salicylic acid-repressible multifaceted defense response. Plant Physiol. 148:1996-2012   DOI   ScienceOn
61 Wei, G., Kloepper, J. W. and Tuzun, S. 1991. Induction of systemic resistance of cucumber to Colletotrichum orbiculare by select strains of plant growth- promoting rhizobacteria. Phytopathology 81:1508-1512   DOI
62 Kim, M. S., Cho, S, M., Kang, E. Y., Im, Y. J., Hwangbo, H., Kim, Y. C., Ryu, C. M., Yang, K. Y., Chung, G. C. and Cho, B. H. 2008. Galactinol is a signaling component of the induced systemic resistance caused by Pseudomonas chlororaphis O6 root colonization. Mol. Plant-Microbe Interact. 21:1643-1653   DOI   ScienceOn
63 Aime, S., Cordier. C., Alabouvette, C. and Olivain C. 2008. Comparative analysis of PR gene expression in tomato inoculated with virulent Fusarium oxysporum f. sp. lycopersici and the biocontrol strain F oxysporum Fo47. Physiol. Mol. Plant Pathol. 73:9-15   DOI   ScienceOn
64 Jung, W. J., Jin, Y. L., Kim, K. Y., Park, R. D. and Kim, T. H. 2005. Changes in pathogenesis-related proteins in pepper plants with regard to biological control of phytophthor a blight with Paenibacillus illinoisensis. Biocontrol. 50:165-178   DOI   ScienceOn
65 Ton, J., D'Alessandro, M., Jourdie, V., Jakab, G., Karlen, D., Held, M., Mauch-Mani, B., Turlings, T. C. and Turlings, T. 2006. Priming by airborne signals boosts direct and indirect resistance in maize. Plant J. 49:16-26   DOI   ScienceOn
66 Zhang, S., Reddy, M. S. and Kloepper, l. W. 2004. Tobacco growth enhancement and blue mold protection by rhizobacteria: relationship between plant growth promotion and systemic disease protection by PGPR strain 90-166. Plant Soil 262:277-288   DOI   ScienceOn
67 Heil, M. 1999. Systemic acquired resistance available information and open ecological questions. J. Ecol. 87:341-346   DOI   ScienceOn
68 Pieterse, C. M. J., van Wees, S. C., van Pelt, J. A., Knoester, M., Laan, R., Gerrits, H., Weisbeek, P. J. and van Loon, L. C. 1998. A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 10:1571-1580   DOI   ScienceOn
69 Emmert, E. A. and Handelsman, J. 1999. Biocontrol of plant disease: a (gram-) positive perspective. FEMS Microbiol. Lett. 171:1-9   DOI   ScienceOn
70 Heil, M. 2001. The ecological concept of costs of induced systemic resistance (ISR). Eur. J. Plant Pathol. 107:137-146   DOI   ScienceOn
71 Ramamoorthy, V., Raguchander, T. and Samiyappan, R. 2002. Enhancing resistance of tomato and hotpepper to Pythium diseases by seed treatment with fluorescent pseudomonads. Eur. J. Plant Pathol. 108:429-441   DOI   ScienceOn
72 Heil, M., Hilpert, A., Kaiser, W. and Linsenmair, K. E. 2000. Reduced growth and seed set following chemical induction of pathogen defence: does systemic acquired resistance (SAR) incur allocation costs? J. Ecol. 88:645-654   DOI   ScienceOn
73 Park, C. J., Shin, R., Park, J. M., Lee, G. J., You, J. S. and Paek, K. H. 2002a. Induction of pepper cDNA encoding a lipid transfer protein during the resistance response to tobacco mosaic virus. Plant Mol. Biol. 48:243-254   DOI   ScienceOn
74 Pflieger, S., Palloix, A., Caranta, C., Blattes, A. and Lefebvre, V. 2001. Defense response genes colocalize with quantitative disease resistance loci in pepper. Theor. Appl. Genet. 103:920-929   DOI   ScienceOn
75 Kim, M. S., Kim, Y. C. and Cho, B. H. 2004. Gene expression analysis in cucumber leaves primed by root colonization with Pseudomonas chlororaphis O6 upon challenge-inoculation with Corynespora cassiicola. Plant BioI. 6:105-108   DOI   ScienceOn
76 Chassot, C., Buchala, A., Schoonbeek, H. J., M6traux, J. P. and Lamotte, O. 2008. Wounding of Arabidopsis leaves causes a powerful but transient protection against Botrytis infection. Plant J. 55:555-567   DOI   ScienceOn