DOI QR코드

DOI QR Code

Transcriptome Analysis of Induced Systemic Drought Tolerance Elicited by Pseudomonas chlororaphis O6 in Arabidopsis thaliana

  • Cho, Song-Mi (Department of Floriculture, Chunnam Techno University) ;
  • Kang, Beom Ryong (Environment-Friendly Agricultural Research Institute, Jeollanamdo Agricultural Research and Extension Services) ;
  • Kim, Young Cheol (Institute of Environmentally-Friendly Agriculture, College of Agriculture and Life Sciences, Chonnam National University)
  • Received : 2012.07.15
  • Accepted : 2012.09.30
  • Published : 2013.06.01

Abstract

Root colonization by Pseudomonas chlororaphis O6 induces systemic drought tolerance in Arabidopsis thaliana. Microarray analysis was performed using the 22,800-gene Affymetrix GeneChips to identify differentially-expressed genes from plants colonized with or without P. chlororaphis O6 under drought stressed conditions or normal growth conditions. Root colonization in plants grown under regular irrigation condition increased transcript accumulation from genes associated with defense, response to reactive oxygen species, and auxin- and jasmonic acid-responsive genes, but decreased transcription factors associated with ethylene and abscisic acid signaling. The cluster of genes involved in plant disease resistance were up-regulated, but the set of drought signaling response genes were down-regulated in the P. chlororaphis O6-colonized under drought stress plants compared to those of the drought stressed plants without bacterial treatment. Transcripts of the jasmonic acid-marker genes, VSP1 and pdf-1.2, the salicylic acid regulated gene, PR-1, and the ethylene-response gene, HEL, also were up-regulated in plants colonized by P. chlororaphis O6, but differed in their responsiveness to drought stress. These data show how gene expression in plants lacking adequate water can be remarkably influenced by microbial colonization leading to plant protection, and the activation of the plant defense signal pathway induced by root colonization of P. chlororaphis O6 might be a key element for induced systemic tolerance by microbes.

Keywords

References

  1. Cartieaux, F., Thibaud, M. C., Zimmerli, L., Lessard, P., Sarrobert, C., David, P., Gerbaud, A., Robaglia, C., Somerville, S. and Nussaume, L. 2003. Transcriptome analysis of Arabidopsis colonized by a plant-growth promoting rhizobacterium reveals a general effect on disease resistance. Plant J. 36:177−188. https://doi.org/10.1046/j.1365-313X.2003.01867.x
  2. Cho, S. M., Kang, B. R., Han, S. H., Anderson, A. J., Park, J.-Y., Lee, Y.-H., Cho, B. H., Yang, K.-Y., Ryu, C.-M. and Kim, Y. C. 2008. 2R,3R-butanediol, a bacterial volatile produced by Pseudomonas chlororaphis O6, is involved in induction of systemic tolerance to drought in Arabidopsis thaliana. Mol. Plant-Microbe Interact. 21:1067−1075.
  3. Cho, S. M., Kang, B. R., Kim, J. J. and Kim, Y. C. 2012. Induced systemic drought and salt tolerance by Pseudomonas chlororaphis O6 root colonization is mediated by ABA-independent stomatal closure. Plant Pathol. J. 28:202−206.
  4. Cho, S. M., Park, J. Y., Han, S. H., Anderson, A. J., Yang, K. Y., McSpadden Gardener, B. and Kim, Y. C. 2011. Identification and transcriptional analysis of priming genes in Arabidopsis thaliana induced by root colonization with Pseudomonas chlororaphis O6. Plant Pathol. J. 27:272−279.
  5. Choi, H. I., Hong, J. H., Ha, J. O., Kang, J. Y. and Kim, S. Y. 2000. ABFs, a family of ABA-responsive element binding factors. J. Biol. Chem. 275:1723-1730. https://doi.org/10.1074/jbc.275.3.1723
  6. Cornelissen, B. J. C., Hooft van Huijsduijnen, R. A. and Bol, J. F. 1986. A tobacco mosaic virus-induced protein is homologous to the sweet-tasting protein thaumatin. Nature 321:531-532. https://doi.org/10.1038/321531a0
  7. Conrath, U., Pieterse, 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
  8. Defago, G. and Hass, D. 1990. Pseudomonads as antagonists of soilborne pathogens: modes of action and genetic analysis. In Soil Biochemistry, Vol. 6, ed. Bollag, J. M., and Stotzky, G., pp. 249−291. New York: Marcel Dekker.
  9. Edens, L., Hesling, L., Klock, R., Ledeboer, A. M., Maat, J., Toonen, M. Y., Visser, C. and Verrips, C. T. 1982. Cloning of cDNA encoding the sweet-tasting plant protein thaumatin and its expression in Escherichia coli. Gene 18:1-12. https://doi.org/10.1016/0378-1119(82)90050-6
  10. Epple, P., Apel, K. and Bohlmann, H. 1997. Overexpression of an endogenous thionin enhances resistance of Arabidopsis against Fusarium oxysporum. Plant Cell 9:509-520. https://doi.org/10.1105/tpc.9.4.509
  11. Epple, P., Vignutelli, A., Apel, K. and Bohlmann, H. 1998. Differential induction of the Arabidopsis thaliana Thi2.1 gene by Fusarium oxysporum f. sp. matthiolae. Mol. Plant-Microbe Interact. 11:523-239. https://doi.org/10.1094/MPMI.1998.11.6.523
  12. Fernandez de Caleya, R., Gonzalez-Pascual, B., Garcia-Olmedo, F. and Carbonero, P. 1972. Susceptibility of phytopathogenic bacteria to wheat purothionins in vitro. Appl. Microbiol. 23:998-1000.
  13. Glick, B. R. 1995. The enhancement of plant growth by free-living bacteria. Can. J. Microbiol. 41:109-117. https://doi.org/10.1139/m95-015
  14. Glick, B. R., Penrose, D. M. and Li, J. 1998. A model for the lowering of plant ethylene concentrations by plant growth-promoting bacteria. J. Theor. Biol. 190:63−68.
  15. Hajgaard, J., Jacobsen, S. and Svendsen, I. 1991. Two antifungal thaumatinlike proteins from barley grain. FEBS Lett. 291:127-131. https://doi.org/10.1016/0014-5793(91)81119-S
  16. Han, S. H., Lee, S. J., Moon, J. H., Park, K. H., Yang, K. Y., Cho, B. H., Kim, K. Y., Kim, Y. W., Lee, M. C., Anderson, A. J. and Kim, Y. C. 2006. GacS-dependent production of 2R, 3Rbutanediol by Pseudomonas chlororaphis O6 is a major determinant for eliciting systemic resistance against Erwinia carotovora but not against Pseudomonas syringae pv. tabaci in tobacco. Mol. Plant-Microbe Interact. 19:924−930.
  17. Hong, J. K. and Hwang, B. K. 2006. Promoter activation of pepper class II basic chitinase gene, CAChi2, and enhanced bacterial disease resistance and osmotic stress tolerance in the CAChi2-overexpressing Arabidopsis. Planta 22:433−448.
  18. Hong, J. K., Lee, S. C. and Hwang, B. K. 2005. Activation of pepper basic PR-1 gene promoter during defense signaling to pathogen, abiotic and environmental stresses. Gene 356:169−180. https://doi.org/10.1016/j.gene.2005.04.030
  19. Hontzeas, N., Saleh, S. S. and Glick, B. R. 2004. Changes in gene expression in canola roots induced by ACC-deaminse-containing plant-growth-promoting bacteria. Mol. Plant-Microbe Interact. 17:865−871.
  20. Irizarry, R. A. 2003. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4:249−264. https://doi.org/10.1093/biostatistics/4.2.249
  21. Kang, B. R., Yang, K. Y., Cho, B. H., Han, T. H., Kim, I. S. Lee, M. C., Anderson, A. J. and Kim, Y. C. 2006. Production of indole-3-acetic acid in the plant beneficial strain Pseudomonas chlororaphis O6 is negatively regulated by the global sensor kinase GacS. Curr. Microbiol. 52:473−476.
  22. 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 Biol. 6:105−108. https://doi.org/10.1055/s-2004-817803
  23. Kim, Y. C., Glick, B. R., Bashan, Y. and Ryu, C. M. 2012. Enhancement of plant drought tolerance by microbes. In: Plant responses to drought stress: From Morphological to molecular feature. Aroca, R. (ed), Springer-Verlag, Berlin Heidelberg, in press.
  24. Kim, Y. C., Leveau, J., McSpadden Gardener, B. B., Pierson, E. A., Pierson III, L. S. and Ryu, C. M. 2011. The factorial basis for plant health promotion by plant-associated bacteria. Appl. Environ. Microbiol. 77:1548−1555.
  25. Kloepper, J. W., Leong, J., Teintze, M. and Schroth, M. N. 1980. Enhanced plant growth by siderophores produced by plant growth-promoting rhizobacteria. Nature 286:885−886.
  26. 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.
  27. Mayak, S., Tirosh, T. and Glick, B. R. 2004. Plant growth-promoting bacteria confer resistance in tomato plants to salt stress. Plant Physiol. Biochem. 42:565−572.
  28. Pierpoint, W. S., Jackson, P. J. and Evans, R. M. 1990. The presence of a thaumatin-like protein, a chitinase and a glucanase among the pathogenesis-related proteins of potato (Solanum tuberosum). Physiol. Mol. Plant Pathol. 36:325-338. https://doi.org/10.1016/0885-5765(90)90062-3
  29. Ramamoorthy, V., Viswanathan, R., Raguchander, T., Prakasam, V. and Samiyappan, R. 2001. Induction of systemic resistance by plant growth promoting rhizobacteria in crop plants against pests and diseases. Crop Prot. 20:1−11.
  30. Ryu, C. M., Kang, B. R., Han, S. H., Cho, S. M., Kloepper, J. W., Anderson, A. J. and Kim, Y. C. 2007. Tobacco cultivars vary in induction of systemic resistance against Cucumber mosaic virus and growth promotion by Pseudomonas chlororaphis O6 and its gacS mutant. Eur. J. Plant Pathol. 119:383−390.
  31. Schardl, C. L., Leuchtmann, A. and Spiering, M. J. 2004. Symbioses of grasses with seedborne fungal endophytes. Annu. Rev. Plant Biol. 55:315−340.
  32. Shinozaki, K. and Yamaguchi-Schinozaki, K. 1997. Gene expression and signal transduction in water-stress response. Plant Physiol. 115:327−334. https://doi.org/10.1104/pp.115.2.327
  33. Spencer, M., Ryu, C. M., Yang, K. Y., Kim, Y. C., Kloepper, J. W. and Anderson, A. J. 2003. Induced defence in tobacco by Pseudomonas chlororaphis strain O6 involves at least the ethylene pathway. Physiol. Mol. Plant Pathol. 63:27−34.
  34. Timmusk, S. and Wagner, E. G. H. 1999. The plant-growth-promoting rhizobacterium Paenibacillus polymyxa induces changes in Arabidopsis thaliana gene expression: a possible connection between biotic and abiotic stress responses. Mol. Plant-Microbe Interact. 12:951−959.
  35. Van Loon, L. C., Bakker, P. A. H. M. and Pierterse, C. M. J. 1998. Systemic resistance induced by rhizosphere bacteria. Annu. Rev. Phytopathol. 36:453−483.
  36. Van Loon, L. C. and Glick, B. R. 2004. Increased plant fitness by rhizobacteria. In: Molecular ecotoxicology of plants, Sandermann, H. (ed), Springer-Verlag, Berlin Heidelberg, pp 177−205.
  37. Verhagen, B. W., Glazebrook, J., Zhu, T., Chang, H. S., van Loon, L. C. and Pieterse, C. M. J. 2004. The transcriptome of rhizobacteria-induced systemic resistance in Arabidopsis. Mol. Plant-Microbe Interact. 17:895−908.
  38. Vigers, J. A., Roberts, W. K. and Selitrennikoff, C. P. 1992. A new family of plant antifungal proteins. Mol. Plant-Microbe Interact. 4:315−323.
  39. Waller, F., Archatz, B., Baltruschat, H., Fodor, J., Becker, K., Fischer, M., Heier, T., Huckelhover, R., Neumann, C., von Wettstein, D., Franken, P. and Kogel, K.-H. 2005. The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc. Natl. Acad. Sci. USA 102:13386−13391.
  40. Wang, Y., Ohara, Y., Nakayashiki, H., Tosa, Y. and Mayama, S. 2005. Microarray analysis of the gene expression profile induced by the endophytic plant growth-promoting rhizobacteria, Pseudomonas fluorescens FPT9601-T5 in Arabidopsis. Mol. Plant-Microbe Interact. 18:385−396.
  41. Wittstock, U. and Halkier, B. A. 2002. Glucosinolate research in the Arabidopsis era. Trends Plant Sci. 7:263−270.

Cited by

  1. Nitric Oxide and Hydrogen Peroxide Production are Involved in Systemic Drought Tolerance Induced by 2R,3R-Butanediol in Arabidopsis thaliana vol.29, pp.4, 2013, https://doi.org/10.5423/PPJ.OA.07.2013.0069
  2. Modulation of Spartina densiflora plant growth and metal accumulation upon selective inoculation treatments: A comparison of gram negative and gram positive rhizobacteria 2017, https://doi.org/10.1016/j.marpolbul.2017.07.072
  3. Alleviation of environmental stress in plants: The role of beneficial Pseudomonas spp. vol.47, pp.6, 2017, https://doi.org/10.1080/10643389.2017.1318619
  4. Soil memory as a potential mechanism for encouraging sustainable plant health and productivity vol.38, 2016, https://doi.org/10.1016/j.copbio.2016.01.014
  5. Enhancement of drought stress tolerance in crops by plant growth promoting rhizobacteria vol.184, 2016, https://doi.org/10.1016/j.micres.2015.12.003
  6. The identification of presence/absence variants associated with the apparent differences of growth period structures between cultivated and wild soybeans vol.15, pp.2, 2016, https://doi.org/10.1016/S2095-3119(15)61048-6
  7. Remodeling of root morphology by CuO and ZnO nanoparticles: effects on drought tolerance for plants colonized by a beneficial pseudomonad vol.96, pp.3, 2018, https://doi.org/10.1139/cjb-2017-0124
  8. Rhizosphere pseudomonads as probiotics improving plant health vol.19, pp.10, 2018, https://doi.org/10.1111/mpp.12693
  9. Cytokinin at the Crossroads of Abiotic Stress Signalling Pathways vol.19, pp.8, 2018, https://doi.org/10.3390/ijms19082450
  10. Interactions Between a Plant Probiotic and Nanoparticles on Plant Responses Related to Drought Tolerance vol.14, pp.3, 2018, https://doi.org/10.1089/ind.2017.0033
  11. Transcriptomic profiling of maize (Zea mays L.) seedlings in response to Pseudomonas putida stain FBKV2 inoculation under drought stress vol.68, pp.6, 2018, https://doi.org/10.1007/s13213-018-1341-3