Browse > Article
http://dx.doi.org/10.14348/molcells.2014.2239

Alleviation of Salt Stress by Enterobacter sp. EJ01 in Tomato and Arabidopsis Is Accompanied by Up-Regulation of Conserved Salinity Responsive Factors in Plants  

Kim, Kangmin (Division of Biotechnology, College of Environmental and Bioresource Sciences, Chonbuk National University)
Jang, Ye-Jin (Division of Biotechnology, College of Environmental and Bioresource Sciences, Chonbuk National University)
Lee, Sang-Myeong (Division of Biotechnology, College of Environmental and Bioresource Sciences, Chonbuk National University)
Oh, Byung-Taek (Division of Biotechnology, College of Environmental and Bioresource Sciences, Chonbuk National University)
Chae, Jong-Chan (Division of Biotechnology, College of Environmental and Bioresource Sciences, Chonbuk National University)
Lee, Kui-Jae (Division of Biotechnology, College of Environmental and Bioresource Sciences, Chonbuk National University)
Publication Information
Molecules and Cells / v.37, no.2, 2014 , pp. 109-117 More about this Journal
Abstract
Microbiota in the niches of the rhizosphere zones can affect plant growth and responses to environmental stress conditions via mutualistic interactions with host plants. Specifically, some beneficial bacteria, collectively referred to as Plant Growth Promoting Rhizobacteria (PGPRs), increase plant biomass and innate immunity potential. Here, we report that Enterobacter sp. EJ01, a bacterium isolated from sea china pink (Dianthus japonicus thunb) in reclaimed land of Gyehwa-do in Korea, improved the vegetative growth and alleviated salt stress in tomato and Arabidopsis. EJ01 was capable of producing 1-aminocy-clopropane-1-carboxylate (ACC) deaminase and also exhibited indole-3-acetic acid (IAA) production. The isolate EJ01 conferred increases in fresh weight, dry weight, and plant height of tomato and Arabidopsis under both normal and high salinity conditions. At the molecular level, short-term treatment with EJ01 increased the expression of salt stress responsive genes such as DREB2b, RD29A, RD29B, and RAB18 in Arabidopsis. The expression of proline biosynthetic genes (i.e. P5CS1 and P5CS2) and of genes related to priming processes (i.e. MPK3 and MPK6) were also up-regulated. In addition, reactive oxygen species scavenging activities were enhanced in tomatoes treated with EJ01 in stressed conditions. GFP-tagged EJ01 displayed colonization in the rhizosphere and endosphere in the roots of Arabidopsis. In conclusion, the newly isolated Enterobacter sp. EJ01 is a likely PGPR and alleviates salt stress in host plants through multiple mechanisms, including the rapid up-regulation of conserved plant salt stress responsive signaling pathways.
Keywords
Arabidopsis; Enterobacter; PGPR; ROS; salt stress;
Citations & Related Records
연도 인용수 순위
  • Reference
1 Achard, P., Cheng, H., De Grauwe, L., Decat, J., Schoutteten, H., Moritz, T., Van Der Straeten, D., Peng, J., and Harberd, N.P. (2006). Integration of plant responses to environmentally activated phytohormonal signals. Science 311, 91-94.   DOI   ScienceOn
2 Ahmad, M., Zahir, Z.A., Asghar, H.N., and Asghar, M. (2011). Inducing salt tolerance in mung bean through coinoculation with rhizobia and plant-growth-promoting rhizobacteria containing 1-aminocyclopropane-1-carboxylate deaminase. Can. J. Microbiol. 57, 578-589.   DOI   ScienceOn
3 Aroca, R., Ferrante, A., Vernieri, P., and Chrispeels, M.J. (2006). Drought, abscisic acid and transpiration rate effects on the regulation of PIP aquaporin gene expression and abundance in Phaseolus vulgaris plants. Ann. Bot. 98, 1301-1310.   DOI   ScienceOn
4 Cao, W.H., Liu, J., Zhou, Q.Y., Cao, Y.R., Zheng, S.F., Du, B.X., Zhang, J.S., and Chen, S.Y. (2006). Expression of tobacco ethylene receptor NTHK1 alters plant responses to salt stress. Plant Cell Environ. 29, 1210-1219.   DOI   ScienceOn
5 Beckers, G.J.M., Jaskiewicz, M., Liu, Y.D., Underwood, W.R., He, S.Y., Zhang, S.Q., and Conrath, U. (2009). Mitogen-activated protein kinases 3 and 6 are required for full priming of stress responses in Arabidopsis thaliana. Plant Cell 21, 944-953.   DOI   ScienceOn
6 Bharti, N., Yadav, D., Barnawal, D., Maji, D., and Kalra, A. (2013). Exiguobacterium oxidotolerans, a halotolerant plant growth promoting rhizobacteria, improves yield and content of secondary metabolites in Bacopa monnieri (L.) Pennell under primary and secondary salt stress. World J. Microb. Biot. 29, 379-387.   DOI   ScienceOn
7 Blois, M.S. (1958). Antioxidant determination by the use of a stable free radical. Nature 181, 1199-1200.   DOI   ScienceOn
8 Chakraborty, U., Chakraborty, B.N., Chakraborty, A.P., and Dey, P.L. (2013). Water stress amelioration and plant growth promotion in wheat plants by osmotic stress tolerant bacteria. World J. Microbiol. Biotechnol. 29, 789-803.   DOI   ScienceOn
9 Choi, K.H., and Schweizer, H.P. (2006). mini-Tn7 insertion in bacteria with secondary, non-glmS-linked attTn7 sites: example Proteus mirabilis HI4320. Nat. Protoc. 1, 170-178.   DOI   ScienceOn
10 Dodd, I.C., and Perez-Alfocea, F. (2012). Microbial amelioration of crop salinity stress. J. Exp. Bot. 63, 3415-3428.   DOI   ScienceOn
11 Dworkin, M., and Foster, J.W. (1958). Experiments with some microorganisms which utilize ethane and hydrogen. J. Bacteriol. 75, 592-603.
12 Hirano, S.S., and Upper, C.D. (2000). Bacteria in the leaf ecosystem with emphasis on Pseudomonas syringae - a pathogen, ice nucleus, and epiphyte. Microbiol. Mol. Biol. Rev. 64, 624-653.   DOI   ScienceOn
13 Hoagland, D.R., and Arnon, D.I. (1950). The water-culture method for growing plants without soil. Vol. 347 revised. California Agriculture Experimental Station Center.
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.   DOI   ScienceOn
15 Gordon, S.A., and Weber, R.P. (1951). Colorimetric estimation of indoleacetic acid. Plant Physiol. 26, 192-195.   DOI   ScienceOn
16 Jahromi, F., Aroca, R., Porcel, R., and Ruiz-Lozano, J.M. (2008). Influence of salinity on the In vitro development of Glomus intraradices and on the In vivo physiological and molecular responses of mycorrhizal lettuce plants. Microb. Ecol. 55, 45-53.   DOI
17 Kloepper, J.W., and Schroth, M.N. (1978). Plant growth-promoting rhizobacteria on radishes. pp. 879-882 in: Proc. of the 4th Internat. Conf. on Plant Pathogenic Bacter. Vol 2, Station de Pathologie Vegetale et Phytobacteriologie, INRA, Angers, France.
18 Liu, Y., Shi, Z.Q., Yao, L.X., Yue, H.T., Li, H., and Li, C. (2013). Effect of IAA produced by Klebsiella oxytoca Rs-5 on cotton growth under salt stress. J. Gen. Appl. Microbiol. 59, 59-65.   DOI
19 Kloepper, J.W., Ryu, C.M., and Zhang, S.A. (2004). Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 94, 1259-1266.   DOI   ScienceOn
20 Koch, B., Jensen, L.E., and Nybroe, O. (2001). A panel of Tn7-based vectors for insertion of the gfp marker gene or for delivery of cloned DNA into Gram-negative bacteria at a neutral chromosomal site. J. Microbiol. Meth. 45, 187-195.   DOI   ScienceOn
21 Koussevitzky, S., Suzuki, N., Huntington, S., Armijo, L., Sha, W., Cortes, D., Shulaev, V., and Mittler, R. (2008). Ascorbate peroxidase 1 plays a key role in the response of Arabidopsis thaliana to stress combination. J. Biol. Chem. 283. 34197-34203.   DOI   ScienceOn
22 Krasensky, J., and Jonak, C. (2012). Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J. Exp. Bot. 63, 1593-1608.   DOI   ScienceOn
23 Lata, C., and Prasad, M. (2011). Role of DREBs in regulation of abiotic stress responses in plants. J. Exp. Bot. 62, 4731-4748.   DOI   ScienceOn
24 Mayak, S., Tirosh, T., and Glick, B.R. (2004a). Plant growth-promoting bacteria confer resistance in tomato plants to salt stress. Plant Physiol. Bioch. 42, 565-572.   DOI   ScienceOn
25 Mayak, S., Tirosh, T., and Glick, B.R. (2004b). Plant growth-promoting bacteria that confer resistance to water stress in tomatoes and peppers. Plant Sci. 166, 525-530.   DOI   ScienceOn
26 Nakano, Y., and Asada, K. (1981). Hydrogen-peroxide is scavenged by ascorbate-specific Peroxidase in spinach-chloroplasts. Plant Cell Physiol. 22, 867-880.
27 Ryu, C.M., Farag, M.A., Hu, C.H., Reddy, M.S., Wei, H.X., Pare, P. W., and Kloepper, J.W. (2003). Bacterial volatiles promote growth in Arabidopsis. Proc. Natl. Acad. Sci. USA 100, 4927-4932.   DOI   ScienceOn
28 Naz, I., Bano, A., and Ul-Hassan, T. (2009). Isolation of phytohormones producing plant growth promoting rhizobacteria from weeds growing in Khewra salt range, Pakistan and their implication in providing salt tolerance to Glycine max L. Afr. J. Biotechnol. 8, 57-62.
29 Spaepen, S., and Vanderleyden, J. (2011). Auxin and plantmicrobe Interactions. Cold Spring Harb. Perspect. Biol. 3, 1-13.
30 Penrose, D.M., and Glick, B.R. (2003). Methods for isolating and characterizing ACC deaminase-containing plant growth-promoting rhizobacteria. Physiol. Plant 118, 10-15.   DOI   ScienceOn
31 Shen, M., Kang, Y.J., Wang, H.L., Zhang, X.S., and Zhao, Q.X. (2012). Effect of plant growth-promoting rhizobacteria (PGPRs) on plant growth, yield, and quality of tomato (Lycopersicon esculentum Mill.) under simulated seawater irrigation. J. Gen. Appl. Microbiol. 58, 253-262.   DOI
32 Teige, M., Scheikl, E., Eulgem, T., Doczi, F., Ichimura, K., Shinozaki, K., Dangl, J.L., and Hirt, H. (2004). The MKK2 pathway mediates cold and salt stress signaling in Arabidopsis. Mol. Cell 15, 141-152.   DOI   ScienceOn
33 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.   DOI   ScienceOn
34 Xiong, L.M., Schumaker, K.S., and Zhu, J.K. (2002). Cell signaling during cold, drought, and salt stress. Plant Cell 14, S165-S183.   DOI   ScienceOn
35 Zhang, H., Kim, M.S., Krishnamachari, V., Payton, P., Sun, Y., Grimson, M., Farag, M.A., Ryu, C.M., Allen, R., Melo, I.S., et al. (2007). Rhizobacterial volatile emissions regulate auxin homeostasis and cell expansion in Arabidopsis. Planta 226, 839-851.   DOI   ScienceOn
36 Yang, J., Kloepper, J.W., and Ryu, C.M. (2009). Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci. 14, 1-4.   DOI   ScienceOn
37 Zhu, J.K. (2002). Salt and drought stress signal transduction in plants. Annu. Rev. Plant Biol. 53, 247-273.   DOI   ScienceOn
38 Yoshiba, Y., Kiyosue, T., Nakashima, K., Yamaguchi-Shinozaki, K., and Shinozaki, K. (1997). Regulation of levels of proline as an osmolyte in plants under water stress. Plant Cell Physiol. 38, 1095-1102.   DOI   ScienceOn
39 Zhang, H., Kim, M.S., Sun, Y., Dowd, S.E., Shi, H.Z., and Pare, P. W. (2008). Soil bacteria confer plant salt tolerance by tissuespecific regulation of the sodium transporter HKT1. Mol. Plant Microbe Interact. 21, 737-744.   DOI   ScienceOn
40 Bulgarelli, D., Schlaeppi, K., Spaepen, S., Ver Loren van Themaat, E., and Schulze-Lefert, P. (2013). Structure and functions of the bacterial microbiota of plants. Annu. Rev. Plant Biol. 64, 807-838.   DOI   ScienceOn
41 Msanne, J., Lin, J.S., Stone, J.M., and Awada, T. (2011). Characterization of abiotic stress-responsive Arabidopsis thaliana RD29A and RD29B genes and evaluation of transgenes. Planta 234, 97-107.   DOI
42 Spaepen, S., Vanderleyden, J., and Remans, R. (2007). Indole-3-acetic acid in microbial and microorganism-plant signaling. Fems. Microbiol. Rev. 31, 425-448.   DOI   ScienceOn