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

Frontiers in Plant Science

Volumn 4, Issue MAY, 2013, Pages

  Yi, Hwe Su ^a   Yang, Jung Wook ^a   Ryu, Choong Min ^a,b  

^a Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

^b University of Science and Technology (UST)   (South Korea)

Author keywords

Biological control; Defense priming; ISR; PGPR; SAR

Indexed keywords

EID: 84886428282     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2013.00122     Document Type: Article

References (45)

1. Anith, K. N., Momol, M. T., Kloepper, J. W., Marios, J. J., Olson, S. M., and Jones, J. B. (2004). Efficacy of plant growth-promoting rhizobacteria, acibenzolar-s-methyl and soil amendment for integrated management of bacterial wilt on tomato. Plant Dis. 88, 669-673.
2. 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.
3. Conrath, U., Beckers, G. J. M., Flors, V., García-Agustín, P., Jakab, G., Mauch, F., et al. (2006). Priming: getting ready for battle. Mol. Plant Microbe Interact. 19, 1062-1071.
4. Dempsey, D. A., Shah, J., and Klessig, D. F. (1999). Salicylic acid and disease resistance in plants. Crit. Rev. Plant Sci. 18, 547-575.
5. Enebak, S. A., and Carey, W. A. (2000). Evidence for induced systemic protection to fusiform rust in loblolly pine by plant growth-promoting rhizobacteria. Plant Dis. 84, 306-308.
6. Hammerschmidt, R. (2009). Systemic acquired resistance. Adv. Bot. Res. 51, 173-222.
7. Heil, M., and Baldwin, I. (2002). Fitness costs of induced resistance: emerging experimental support for a slippery concept. Trends Plant Sci. 7, 61-67.
8. Heil, M., and Bostock, R. M. (2002). Induced systemic resistance (ISR) against pathogens in the context of induced plant defences. Ann. Bot. 89, 503-512.
9. 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.
10. 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.
11. 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.
12. Kang, S. H., Cho, H. S., Cheong, H., Ryu, C. M., Kim, J. F., and Park, S. H. (2007). Two bacterial endophytes eliciting both plant growth promotion and plant defense on pepper (Capsicum annuum L.). J. Microbiol. Biotechol. 17, 96-103.
13. Kloepper, J. W., Tuzun, S., and Kuc, J. A. (1992). Proposed definitions related to induced disease resistance. Biocon. Sci. Techol. 2, 349-351.
14. 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.
15. Kloepper, J. W., and Ryu, C. M. (2006). "Bacterial Endophytes as Elicitors of Induced Systemic Resistance, " in Who is an Endophyte? eds Schulz/Boyle/Sieber (Berlin: Springer-Verlag), 33-52.
16. 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.
17. Lee, B., Lee, S., and Ryu, C. M. (2012). Foliar aphid feeding recruits rhizosphere bacteria and primes plant immunity against pathogenic and non-pathogenic bacteria in pepper. Ann. Bot. 110, 281-290.
18. Liu, X., Schiff, M., Serino, G., Deng, X.-W., and Dinesh-Kumar, S. P. (2002). Role of SCF ubiqutin-ligase and the COP9 signalosome in the N gene-mediated resistance response to tobacco mosaic virus. Plant Cell 14, 483-496.
19. Murphy, J. F. (2006) "Applied aspects of induced resistance to plant virus infection, " in Natural Resistance Mechanisms of Plants to Viruses, eds. G. Loebenstein and J. P. Carr (Heidelberg: Springer).
20. Murphy, J. F., Reddy, M., 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.
21. Obradovic, A., Jones, J. B., Momol, M. T., Olson, S. M., Jackson, L. E., Balogh, B., et al. (2005). Integration of biological control agents and systemic acquired resistance inducers against bacterial spot on tomato. Plant Dis. 89, 712-716.
22. Peart, J. R., Lui, R., Sadanandom, A., Malcuit, I., Moffett, P., Brice, D. C., et al. (2002). Ubiquitin ligase-associated protein SGT1 is required for host and non-host disease resistance in plants. Proc. Natl. Acad. Sci. U.S.A. 99, 10865-10869.
23. Pieterse, C. M., Leon-Reyes, A., Van der Ent, S., and Van Wees, S. C. (2009). Networking by small-molecule hormones in plant immunity. Nat. Chem. Biol. 5, 308-316.
24. Press, C. M., Loper, J. E., and Kloepper, J. W. (2001). Role of iron in rhizobacteria-mediated induced systemic resistance. Phytopathology 91, 593-598.
25. Press, C. M., Wilson, M., Tuzun, S., and Kloepper, J. W. (1997). Salicylic acid produced by Serratia marcescens 90-166 is not the primary determinant of induced systemic resistance in cucumber or tobacco. Mol. Plant Microbe Interact. 10, 761-768.
26. Quadt-Hallmann, A., Hallmann, J., and Kloepper, J. W. (1997). Bacterial endophytes in cotton: location and interaction with other plant-associated bacteria. Can. J. Microbiol. 43, 254-259.
27. Raaijmakers, J. M., Leeman, M., vanoorschot, M. M. P., Vander sluis, I., Schippers, B., and Bakker, P. A. H. M. (1995). Dose-response relationships in biological control of fusarium wilt of radish by Pseudomonas spp. Phytopathology 85, 1075-1081.
28. 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.
29. Ross, A. F. (1961). Systemic acquired resistance induced by localized virus infections in plants. Virology 14, 340-358.
30. Ryu, C. M., Murphy, J. F., Mysore, K. S., and Kloepper, J. W. (2004). Plant growth-promoting rhizobacteria systemically protect Arabidopsis thaliana against Cucumber mosaic virus by a salicylic acid and NPR1-independent and jasmonic acid-dependent signaling pathway. Plant J. 39, 381-392.
31. Song, G. C., Choi, H. K., and Ryu, C. M. (2013). The folate precursor para-aminobenzoic acid elicits induced resistance against Cucumber mosaic virus and Xanthomonas axonopodis. Ann. Bot. 111, 925-934.
32. Shin, R., Kim, M. J., and Paek, K. H. (2003). The CaTin1(Capsicum annuum TMV-induced Clone 1) and CaTin1-2 genes are linked head-to-head and share a bidirectional promoter. Plant Cell Physiol. 44, 549-554.
33. Tally, A., Oostendorp, M., Lawton, K., Staub, T., Bassi, B., Agrawal, A., et al. (1999) "Commercial development of elicitors of induced resistance to pathogens" in Induced Plant Defenses Against Pathogens and Herbivores: Biochemistry, Ecology, and Agriculture, eds A. A. Agrawal S. Tuzun, and E. Bent (St Paul: APS Press), 357-369.
34. Van Hulten, M., Pelser, M., Van Loon, L. C., Pieterse, C. M. J., and Ton, J. (2006). Costs and benefits of priming for defense in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 103, 5602-5607.
35. van Loon, L. C. (2007). Plant responses to plant growth-promoting rhizobacteria. Eur. J. Plant Pathol. 119, 243-254.
36. van Wees, S. C., de Swart, E. A., van Pelt, J. A., van Loon, L. C., and Pieterse, C. M. J. (2000). Enhancement of induced disease resistance by simultaneous activation of salicylate-and jasmonate-dependent defense pathways in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 97, 8711-8716.
37. Van Wees, S. C., Van der Ent, S., and Pieterse, C. M. J. (2008). Plant immune responses triggered by beneficial microbes. Curr. Opin. Plant Biol. 11, 443-438.
38. Wang, Y., Dang, F., Liu, Z., Wang, X., Eulgem, T., Lai, Y., et al. (2013). CaWRKY58, encoding a group I WRKY transcription factor of Capsicum annuum, negatively regulates resistance to Ralstonia solanacearum infection. Mol. Plant Pathol. 14, 131-144.
39. Wei, G., Kloepper, J. W., and Tuzun, S. (1996). Induced systemic resistance to cucumber diseases and increased plant growth by plant growth-promoting rhizobacteria under field conditions. Phytopathology 86, 221-224.
40. Yang, J. W., Yi, H. S., Kim, H., Lee, B., Lee, S., Ghim, S. Y., et al. (2011). Whitefly infestation of pepper plants elicits defence responses against bacterial pathogens in leaves and roots and changes the below-ground microflora. J. Ecol. 99, 46-56.
41. Yang, J. W., Yu, S. H., and Ryu, C. M. (2009). Priming of defense-related genes confers root-colonizing bacilli-elicited induced systemic resistance in pepper. Plant Pathol. J. 25, 303-440.
42. Yi, H. S., Heil, M., Adame-Alvarez, R. M., Ballhorn, D. J., and Ryu, C. M. (2009). Airborne induction and priming of plant defenses against a bacterial pathogen. Plant Physiol. 151, 2152-2161.
43. Yi, H.-S., Yang, J. W., Choi, H. K., Ghim, S.-Y., and Ryu, C.-M. (2012). Benzothiadiazole-elicited defense priming and systemic acquired resistance against bacterial and viral pathogens of pepper under field conditions. Plant Biotechnol. Rep. 6, 373-380.
44. Zehnder, G. W., Murphy, J. F., Sikora, E. J., and Kloepper, J. W. (2001). Application of rhizobacteria for induced resistance. Eur. J. Plant Pathol. 107, 39-50.
45. Zhang, S., Reddy, M. S., and Kloepper, J. 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.