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Cyclic Dipeptides from Bacillus vallismortis BS07 Require Key Components of Plant Immunity to Induce Disease Resistance in Arabidopsis against Pseudomonas Infection

  • Noh, Seong Woo (Department of Genetic Engineering, Dong-A University) ;
  • Seo, Rira (Department of Applied Bioscience, Dong-A University) ;
  • Park, Jung-Kwon (Department of Applied Bioscience, Dong-A University) ;
  • Manir, Md. Maniruzzaman (Department of Chemistry, Kongju National University) ;
  • Park, Kyungseok (National Institute of Agricultural Science, Rural Development Administration) ;
  • Sang, Mee Kyung (National Institute of Agricultural Science, Rural Development Administration) ;
  • Moon, Surk-Sik (Department of Chemistry, Kongju National University) ;
  • Jung, Ho Won (Department of Genetic Engineering, Dong-A University)
  • Received : 2016.12.02
  • Accepted : 2017.05.17
  • Published : 2017.08.01

Abstract

Cyclic dipeptides (CDPs) are one of the simplest compounds produced by living organisms. Plant-growth promoting rhizobacteria (PGPRs) also produce CDPs that can induce disease resistance. Bacillus vallismortis strain BS07 producing various CDPs has been evaluated as a potential biocontrol agent against multiple plant pathogens in chili pepper. However, plant signal pathway triggered by CDPs has not been fully elucidated yet. Here we introduce four CDPs, cyclo(Gly-L-Pro) previously identified from Aspergillus sp., and cyclo(L-Ala-L-Ile), cyclo(L-Ala-L-Leu), and cyclo(L-Leu-L-Pro) identified from B. vallismortis BS07, which induce disease resistance in Arabidopsis against Pseudomonas syringae infection. The CDPs do not directly inhibit fungal and oomycete growth in vitro. These CDPs require PHYTOALEXIN DEFICIENT4, SALICYLIC ACID INDUCTION DEFICIENT2, and NONEXPRESSOR OF PATHOGENESIS-RELATED PROTEINS1 important for salicylic acid-dependent defense to induce resistance. On the other hand, regulators involved in jasmonate-dependent event, such as ETHYLENE RECEPTOR1, JASMONATE RESPONSE1, and JASMONATE INSENSITIVE1, are necessary to the CDP-induced resistance. Furthermore, treatment of these CDPs primes Arabidopsis plants to rapidly express PATHOGENESIS-RELATED PROTEIN4 at early infection phase. Taken together, we propose that these CDPs from PGPR strains accelerate activation of jasmonate-related signaling pathway during infection.

Keywords

References

  1. Bellezza, I., Peirce, M. J. and Minelli, A. 2014. Cyclic dipeptides: from bugs to brain. Trends Mol. Med. 20:551-558. https://doi.org/10.1016/j.molmed.2014.08.003
  2. Berger, S., Bell, E. and Mullet, J. E. 1996. Two methyl jasmonate-insensitive mutants show altered expression of AtVsp in response to methyl jasmonate and wounding. Plant Physiol. 111:525-531. https://doi.org/10.1104/pp.111.2.525
  3. Bleecker, A., Estelle, M., Somerville, C., and Kende, H. 1988. Insensitivity to ethylene conferred by a dominant mutation in Arabidopsis thaliana. Science 241:1086-1089. https://doi.org/10.1126/science.241.4869.1086
  4. Cao, H., Bowling, S.A., Gordon, A.S., and Dong, X. 1997. Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell 6:1583-1592.
  5. Choudhary, D. K. and Johri, B. N. 2009. Interactions of Bacillus spp. and plants-with special reference to induced systemic resistance (ISR). Microbiol. Res.164:493-513. https://doi.org/10.1016/j.micres.2008.08.007
  6. Choudhary, D. K., Prakash, A. and Johri, B. N. 2007. Induced systemic resistance (ISR) in plants: mechanism of action. Indian J. Microbiol. 47:289-297. https://doi.org/10.1007/s12088-007-0054-2
  7. Compant, S., Duffy, B., Nowak, J., Clement, C. and Barka, E. A. 2005. Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Appl. Environ. Microbiol. 71:4951-4959. https://doi.org/10.1128/AEM.71.9.4951-4959.2005
  8. Conrath, U. 2011. Molecular aspects of defence priming. Trends Plant Sci. 16:524-531. https://doi.org/10.1016/j.tplants.2011.06.004
  9. Conrath, U., Beckers, G. J., Langenbach, C. J. and Jaskiwicz, M. R. 2015. Priming for enhanced defense. Annu. Rev. Phytopathol. 53:97-119. https://doi.org/10.1146/annurev-phyto-080614-120132
  10. Conrath, U., Pierterse, C. M. and Mauch-Mani, B. 2002. Priming in plant-pathogen interactions. Trends Plant Sci. 7:210-216. https://doi.org/10.1016/S1360-1385(02)02244-6
  11. De Vos, M., van Oosten, V. R., van Peocke, R. M., van Pelt, J. A., Pozo, M. J., Mueller, M. J., Buchala, A. J., Métraux, J. P., van Loon, L. C., Dicke, M. and Pieterse, C. M. 2005. Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Mol. Plant-Microbe Interact. 18:923-937. https://doi.org/10.1094/MPMI-18-0923
  12. Dempsey, D. A. and Klessig, D. F. 2012. SOS - too many signals for systemic acquired resistance? Trends Plant Sci. 17:538-545. https://doi.org/10.1016/j.tplants.2012.05.011
  13. Gaffney, T., Friedrich, L., Vernooij, B., Negrotto, D., Nye, G., Uknes, S., Ward, E., Kessmann, H. and Ryals, J. 1993. Requirement of salicylic acid for the induction of systemic acquired resistance. Science 261:754-756. https://doi.org/10.1126/science.261.5122.754
  14. Hahn, M. G. 1996. Microbial elicitors and their receptors in plants. Annu. Rev. Phytopathol. 34:387-412. https://doi.org/10.1146/annurev.phyto.34.1.387
  15. Jirage, D., Tootle, T. L., Reuber, T. L., Frost, L. N., Feys, B. J., Parker, J. E., Ausubel, F. M. and Glazebrook, J. 1999. Arabidopsis thaliana PAD4 encodes a lipase-like gene that is important for salicylic acid signaling. Proc. Natl. Acad. Sci. U.S.A. 96:13583-13588. https://doi.org/10.1073/pnas.96.23.13583
  16. Jung, H. W., Tschaplinski, T. J., Wang, L., Glazebrook, J. and Greenberg, J. T. 2009. Priming in systemic plant immunity. Science 324:89-91. https://doi.org/10.1126/science.1170025
  17. Kloepper, J. W. 1994. Plant growth-promoting rhizobacteria (other systems). In: Azospirillum/Plant Associations, ed. by Y. Okon, pp. 111-118. CRC Press, Boca Raton, FL, USA.
  18. Kloepper, J. W. and Ryu, C. M. 2006. Bacterial endophytes as elicitors of induced systemic resistance. In: Microbial Root Endophytes, eds. by B. Schulz, C. Boyle and T. Siebern, pp. 33-51. Springer-Verglag, Heildelberg, Germany.
  19. Kloepper, J.W., and Schroth, M.N., 1981. Relationship of in vitro antibiosis of plant growth promoting rhizobacteria to plant growth and the displacement of root microflora. Phytopathology 71:1020-1024. https://doi.org/10.1094/Phyto-71-1020
  20. Kumar, S. N., Nambisan, B. and Mohandas, C. 2014. Purification and identification of two antifungal cyclic dipeptides from Bacillus cereus subsp. thuringiensis associated with a rhabditid entomopathogenic nematode especially against Fusarium oxysporum. J. Enzyme Inhib. Med. Chem. 29:190-197. https://doi.org/10.3109/14756366.2013.765414
  21. Lawton, K. A., Friedrich, L., Hunt, M., Weymann, K., Delaney, T., Kessmann, H., Staub, T. and Ryals, J. 1996. Benzothiadiazole induces disease resistance in Arabidopsis by activation of the systemic acquired resistance signal transduction pathway. Plant J. 10:71-82. https://doi.org/10.1046/j.1365-313X.1996.10010071.x
  22. Lee, M. W., Seo, R., Lee, Y. J., Bae, J. H., Park, J. K., Yoon, J. H., Lee, J. W. and Jung, H. W. 2016. ALTERED MERISTEM PROGRAM1 has conflicting effects on the tolerance to heat shock and symptom development after Pseudomonas syringae infection. Biochem. Biophys. Res. Commun. 480:296-301. https://doi.org/10.1016/j.bbrc.2016.10.025
  23. Li, X. J., Zhang, Q., Zhang, A. L. and Gao, J. M. 2012. Metabolites from Aspergillus fumigatus, an endophytic fungus associated with Melia azedarach, and their antifungal, antifeedant, and toxic activities. J. Agric. Food Chem. 60:3424-3431. https://doi.org/10.1021/jf300146n
  24. Livak, K. and Schmittgen, T. D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the $2-{{\Delta}{\Delta}C_T}$ method. Methods 25:402-408. https://doi.org/10.1006/meth.2001.1262
  25. Lorenzo, O. and Solano, R. 2005. Molecular players regulating the jasmonate signalling network. Curr. Opin. Plant Biol. 8:532-540. https://doi.org/10.1016/j.pbi.2005.07.003
  26. Lugtenberg, B. and Kamilova, F. 2009. Plant-growth-promoting rhizobacteria. Annu. Rev. Microbiol. 63:541-556. https://doi.org/10.1146/annurev.micro.62.081307.162918
  27. Malamy, J., Carr, J. P., Klessig, D. F. and Raskin, I. 1990. Salicylic acid: a likely endogenous signal in the resistance response of tobacco to viral infection. Science 250:1002-1004. https://doi.org/10.1126/science.250.4983.1002
  28. Nawrath, C. and Metraux, J. P. 1999. Salicylic acid inductiondeficient mutants of Arabidopsis express PR-2 and PR-5 and accumulate high levels of camalexin after pathogen inoculation. Plant Cell 11:1393-1404.
  29. Ongena, M. and Jacques, P. 2008. Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiol. 16:115-125. https://doi.org/10.1016/j.tim.2007.12.009
  30. Ortiz-Castro, R., Diaz-Perez, C., Martinez-Trujillo, M., del Rio, R. E., Campos-Garcia, J. and Lopez-Bucio, J. 2011. Transkingdom signaling based on bacterial cyclodipeptides with auxin activity in plants. Proc. Natl. Acad. Sci. U.S.A. 108:7253-7258. https://doi.org/10.1073/pnas.1006740108
  31. Park, J.-W., Balaraju, K., Kim, J.-W., Lee, S.-W. and Park, K. 2013. Systemic resistance and growth promotion of chili pepper induced by an antibiotic producing Bacillus vallismortis strain BS07. Biol. Control 65:246-257. https://doi.org/10.1016/j.biocontrol.2013.02.002
  32. Park, K. S., Ahn, I. P. and Kim, C. H. 2001. Systemic resistance and expression of the pathogenesis-related genes mediated by the plant growth-promoting rhizobacterium Bacillus amyloliquefaciens EXTN-1 against anthracnose disease in cucumber. Mycobiology 29:48-53. https://doi.org/10.1080/12298093.2001.12015759
  33. Park, K. S., Diby, P., Kim Y. K., Nam, K. W., Lee, Y. K., Choi, H. W. and Lee, S. Y. 2007. Induced systemic resistance by Bacillus vallismortis EXTN-1 suppressed bacterial wilt in tomato caused by Ralstonia solanacearum. Plant Pathol. J. 23:22-25. https://doi.org/10.5423/PPJ.2007.23.1.022
  34. Park, K. S., Paul, D., Ryu, K. R., Kim, E. Y. and Kim, Y. K. 2006a. Bacillus vallismortis strain EXTN-1 mediated systemic resistance against potato virus Y and X in the field. Plant Pathol. J. 22:360-363. https://doi.org/10.5423/PPJ.2006.22.4.360
  35. Park, K. S., Paul, D. and Yeh, W. H. 2006b. Bacillus vallismortis EXTN-1-mediated growth promotion and disease suppression in rice. Plant Pathol. J. 22:278-282. https://doi.org/10.5423/PPJ.2006.22.3.278
  36. Park, K., Park, Y. S., Ahamed, J., Dutta, S., Ryu, H., Lee, S. H., Balaraju, K., Manir, M. and Moon, S. S. 2016. Elicitation of induced systemic resistance of chili pepper by iturin A analogs derived from Bacillus vallismortis EXTN-1. Can. J. Plant Sci. 96:564-570.
  37. Parniske, M. 2008. Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat. Rev. Microbiol. 6:763-775. https://doi.org/10.1038/nrmicro1987
  38. Pieterse, C. M., van Wees, S. C., van Pelt, J. A., Knoester, M., Laan, R., Greeits, 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. https://doi.org/10.1105/tpc.10.9.1571
  39. Pirozynski, K. A. and Malloch, D. W. 1975. The origin of land plants: A matter of mycotrophism. Biosystems 6:153-164. https://doi.org/10.1016/0303-2647(75)90023-4
  40. Prasad, C. 1995. Bioactive cyclic dipeptides. Peptides 16:151-164. https://doi.org/10.1016/0196-9781(94)00017-Z
  41. Ross, A. F. 1961. Systemic acquired resistance induced by localized virus infections in plants. Virology 14:340-358. https://doi.org/10.1016/0042-6822(61)90319-1
  42. Ryals, J. A., Neuenschwander, U. H., Willits, M. G., Molina, A., Steiner, H. Y. and Hunt, M. D. 1996. Systemic acquired resistance. Plant Cell 8:1809-1819. https://doi.org/10.1105/tpc.8.10.1809
  43. Staswick, P. E., Su, W. and Howell, S.H. 1992. Methyl jasmonate inhibition of root growth and induction of a leaf protein are decreased in an Arabidopsis thaliana mutant. Proc. Natl. Acad. Sci. U.S.A. 89:6837-6840. https://doi.org/10.1073/pnas.89.15.6837
  44. Thajudin, H., Park, K., Moon, S. S. and Hong, I. S. 2010. An efficient green synthesis of proline-based cyclic dipeptides under water-mediated catalyst-free conditions. Tetrahedron Lett. 51:1303-1305. https://doi.org/10.1016/j.tetlet.2009.12.134
  45. Van Hulten, M., Pelser, 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. U.S.A. 103:5602-5607. https://doi.org/10.1073/pnas.0510213103
  46. Walters, D. R., Ratsep, J. and Havis, N. D. 2013. Controlling crop diseases using induced resistance: challenges for the future. J. Exp. Bot. 64:1263-1280. https://doi.org/10.1093/jxb/ert026
  47. Wattana-Amorn, P., Charoenwongsa, W., Williams, C., Crump, M. P. and Apichaisataienchote, B. 2016. Antibacterial activity of cyclo(L-Pro-L-Tyr) and cyclo(D-Pro-L-Tyr) from Streptomyces sp. strain 22-4 against phytopathogenic bacteria. Nat. Prod. Res. 30:1980-1983. https://doi.org/10.1080/14786419.2015.1095747
  48. Wiesel, L., Newton, A. C., Elliott, I., Booty, D., Gilroy, E. M., Birch, P. R. J. and Hein, I. 2014. Molecular effects of resistance elicitors from biological origin and their potential for crop protection. Front. Plant Sci. 5:655.
  49. Zamioudis, C. and Pieterse, C. M. 2012. Modulation of host immunity by beneficial microbes. Mol. Plant-Microbe Interact. 25:139-150. https://doi.org/10.1094/MPMI-06-11-0179

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