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http://dx.doi.org/10.4014/jmb.0906.06042

Movement of Rhizobia Inside Tobacco and Lifestyle Alternation from Endophytes to Free-Living Rhizobia on Leaves  

Ji, Kui-Xian (Key Laboratory of Photosynthesis & Environmental Molecular Physiology, Institute of Botany, Chinese Academy of Sciences)
Chi, Feng (Key Laboratory of Photosynthesis & Environmental Molecular Physiology, Institute of Botany, Chinese Academy of Sciences)
Yang, Ming-Feng (Key Laboratory of Photosynthesis & Environmental Molecular Physiology, Institute of Botany, Chinese Academy of Sciences)
Shen, Shi-Hua (Key Laboratory of Photosynthesis & Environmental Molecular Physiology, Institute of Botany, Chinese Academy of Sciences)
Jing, Yu-Xiang (Key Laboratory of Photosynthesis & Environmental Molecular Physiology, Institute of Botany, Chinese Academy of Sciences)
Dazzo, Frank B. (Department of Microbiology & Molecular Genetics, Michigan State University, East Lansing)
Cheng, Hai-Ping (Lehman College, the City University of New York)
Publication Information
Journal of Microbiology and Biotechnology / v.20, no.2, 2010 , pp. 238-244 More about this Journal
Abstract
Rhizobia are well-known for their ability to infect and nodulate legume roots, forming a nitrogen-fixing symbiosis of agricultural importance. In addition, recent studies have shown that rhizobia can colonize roots and aerial plant tissues of rice as a model plant of the Graminaceae family. Here we show that rhizobia can invade tobacco, a model plant belonging to the Solanaceae family. Inoculation of seedling. roots with five GFP-tagged rhizobial species followed by microscopy and viable plating analyses indicated their colonization of the surface and interior of the whole vegetative plant. Blockage of ascending epiphytic migration by coating the hypocotyls with Vaseline showed that the endophytic rhizobia can exit the leaf interior through stomata and colonize the external phyllosphere habitat. These studies indicate rhizobia can colonize both below- and above-ground tissues of tobacco using a dynamic invasion process that involves both epiphytic and endophytic lifestyles.
Keywords
Alternative lifestyle; endophytic and epiphytic rhizobia; tobacco; GFP tagging; rhizobial movement;
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1 Biswas, J. C., J. K. Ladha, and F. B. Dazzo. 2000. Rhizobia inoculation improves nutrient uptake and growth of lowland rice. Soil Sci. Soc. Amer. Journal 64: 1644-1650.   DOI
2 Cheng, H. P. and G. C. Walker. 1998. Succinoglycan is required for initiation and elongation of infection threads during nodulation of alfalfa by Rhizobium meliloti. J. Bacteriol. 180: 5183-5191.
3 Endre, G., A. Kereszt, Z. Kevei, S. Mihacea, P. Kalo, and G. B. Kiss. 2002. A receptor kinase gene regulating symbiotic nodule development. Nature 417: 962-966.   DOI   ScienceOn
4 Hilali, A., D. Prevost, W. J. Broughton, and H. Antoun. 2001. Effects of inoculation with strains of Rhizobium leguminosarum bv. trifolii on whieat cultivated in clover crop rotation agricultural soil in Morocco. Can. J. Microbiol. 47: 590-593.
5 Noel, T. C., C. Sheng, C. K. Yost, R. P. Pharis, and M. F. Hynes. 1996. Rhizobium leguminosarum as a plant growthpromoting rhizobacterium: Direct growth promotion of canola and lettuce. Can. J. Microbiol. 42: 279-283.   DOI   ScienceOn
6 Prayitno, J., J. Stefaniak, J. McIver, J. J. Weinman, F. B. Dazzo, J. K. Ladha, W. Barraquio, Y. G. Yanni, and B. G. Rolfe. 1999. Interactions of rice seedlings with bacteria isolated from rice roots. Austr. J. Plant Physiol. 26: 521-535.   DOI
7 Rahme, L. G., F. M. Ausubel, H. Cao, E. Drenkard, B. C. Goumnerov, G. W. Lau, S. Mahajan-Miklos, J. Plotnikova, M. W. Tan, et al. 2000. Plants and animals share functionally common bacterial virulence factors. Proc. Nat. Acad. Sci. U.S.A. 97: 8815-8821.   DOI   ScienceOn
8 Reddy, P. M., J. K. Ladha, R. B. So, R. J. Hernandez, M. C. Ramos, O. R. Angeles, F. B. Dazzo, and F. J. deBruijn. 1997. Rhizobial communication with rice roots: Induction of phenotypic changes, mode of invasion and extent of colonization. Plant and Soil 194: 81-98.   DOI
9 Sambrook, J. and D. W. Russel. 2001. Molecular Cloning: A Laboratory Manual, pp. 1.105-101.111.3 Ed. Cold Spring Harbor Laboratory Press, NY.
10 Verkhusha, V. V., I. M. Kuznetsova, O. V. Stepanenko, A. G. Zaraisky, M. M. Shavlovsky, K. K. Turoverov, and V. N. Uversky. 2003. High stability of Discosoma DsRed as compared to Aequorea EGFP. Biochemistry 42: 7879-7884.   DOI   ScienceOn
11 Weidner, S., A. Puhler, and H. Kuster. 2003. Genomics insights into symbiotic nitrogen fixation. Curr. Opin. Biotechnol. 14: 200-205.   DOI   ScienceOn
12 Yanni, Y. G., R. Y. Rizk, V. Corich, A. Squartini, K. Ninke, S. Philip-Hollingsworth, G. Orgambide, F. deBruijn, J. Stoltzfus, D. Buckley, T. M. Schmidt, P. F. Mateos, J. K. Ladha, and F. B. Dazzo. 1997. Natural endophytic association between Rhizobium leguminosarum bv. trifolii and rice roots and assessment of its potential to promote rice growth. Plant and Soil 194: 99-114.
13 Biswas, J. C., J. K. Ladha, F. B. Dazzo, Y. G. Yanni, and B. G. Rolfe. 2000. Rhizobial inoculation influences seedling vigor and yield of rice. Agron. J. 92: 880-886.   DOI
14 Ditta, G., S. Stanfield, D. Corbin, and D. R. Helinski. 1980. Broad host range DNA cloning system for Gram-negative bacteria - construction of a gene bank of Rhizobium meliloti. Proc. Natl. Acad. Sci. U.S.A. 77: 7347-7351.   DOI   ScienceOn
15 Long, S. R. 2001. Genes and signals in the Rhizobium-legume symbiosis. Plant Physiology 125: 69-72.   DOI   ScienceOn
16 Dong, Y. M., A. L. Iniguez, B. M. M. Ahmer, and E. W. Triplett. 2003. Kinetics and strain specificity of rhizosphere and endophytic colonization by enteric bacteria on seedlings of Medicago sativa and Medicago truncatula. Appl. Environ. Microbiol. 69: 1783-1790.   DOI   ScienceOn
17 Yanni, Y. G., R. Y. Rizk, F. K. Abd El-Fattah, A. Squartini, V. Corich, A. Giacomini, F. de Bruijn, J. Rademaker, J. Maya-Flores, P. Ostrom, M. Vega-Hernandez, R.I. Hollingsworth, E. Martinez-Molina, P. Mateos, E. Velazquez, J. Wopereis, E. Triplett, M. Umali-Garcia, J. A., Anarna, B. G. Rolfe, J. K. Ladha, J. Hill, R. Mujoo, P. K. Ng, and F. B. Dazzo. 2001. The beneficial plant growth-promoting association of Rhizobium leguminosarum bv. trifolii with rice roots. Aust. J. Plant Physiol. 28: 845-870.
18 Beringer, J. E. 1974. R factor transfer in Rhizobium leguminosarum. J. Gen. Microbiol. 84: 188-198.   DOI   ScienceOn
19 Stone, P. J., K. J. O'Callaghan, M. R. Davey, and E. C. Cocking. 2001. Azorhizobium caulinodans ORS571 colonizes the xylem of Arabidopsis thaliana. Mol. Plant-Microbe Interact. 14: 93-97.   DOI   ScienceOn
20 Lupwayi, N. Z., G. W. Clayton, K. G. Hanson, W. A. Rice, and V. O. Biederbeck. 2004. Endophytic rhizobia in barley, wheat and canola roots. Can. J. Plant Sci. 84: 37-45.   DOI   ScienceOn
21 Biological Nitrogen Fixation: The Global Challenge & Future Needs. A Position Paper. Discussed at The Rockefeller Foundation Bellagio Conference Centre. Lake Como, Italy. April 8-12, 1997
22 Chaintreuil, C., E. Giraud, Y. Prin, J. Lorquin, A. Ba, M. Gillis, P. de Lajudie, and B. Dreyfus. 2000. Photosynthetic bradyrhizobia are natural endophytes of the African wild rice Oryza breviligulata. Appl. Environ. Microbiol. 66: 5437-5447.   DOI   ScienceOn
23 Chi, F., S. H. Shen, H. P. Cheng, Y. X. Jing, Y. G. Yanni, and F. B. Dazzo. 2005. Ascending migration of endophytic rhizobia, from roots to leaves, inside rice plants and assessment of benefits to rice growth physiology. Appl. Environ. Microbiol. 71: 7271-7278.
24 Gutierrez-Zamora, M. L. and E. Martinez-Romero. 2001. Natural endophytic association between Rhizobium etli and maize (Zea mays L.). J. Biotechnol. 91: 117-126.   DOI   ScienceOn
25 Inouye, S. and F. I. Tsuji. 1994. Aequorea green fluorescent protein, expression of the gene and fluorescence characteristics of the recombinant protein. FEBS Letters 341: 277-280.   DOI
26 Luby-Phelps, K., G. Ning, J. Fogerty, and J. C. Besharse. 2003. Visualization of dentified GFP-expressing cells by light and electron microscopy. J. Histochem. Cytochem. 51: 271-274.   DOI   ScienceOn
27 Murashige, T. and F. Skoog. 1962. A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. Plantarum 15: 473-479.   DOI
28 Gyaneshwar, P., N. Mathan, Q. L. Barraquio, P. M. Reddy, P. P. M. Iannetta, F. L. Olivares, and J. K. Ladha. 2002. Infection and colonization of rice seedlings by the plant growth-promoting bacterium Herbaspirillum seropedicae Z67. Mol. Plant-Microbe Interact. 15: 894-906.   DOI   ScienceOn
29 Hallmann, J., A. QuadtHallmann, W. F. Mahaffee, and J. W. Kloepper. 1997. Bacterial endophytes in agricultural crops. Can. J. Microbiol. 43: 895-914.   DOI   ScienceOn
30 Dazzo, F. B. 2004. Applications of quantitative microscopy in studies of plant surface microbiology, pp. 503-550. In A. Varma, L. Abbott, D. Werner, and R. Hampp (eds.). Plant surface microbiology. Springer-Verlag, Berlin, Germany.
31 Sabry, S. R. S., S. A. Saleh, C. A. Batchelor, J. Jones, J. Jotham, G. Webster, S. L. Kothari, M. R. Davey, and E. C. Cocking. 1997. Endophytic establishment of Azorhizobium caulinodans in wheat. Proc. R. Soc. Lond. Series B-Biol. Sci. 264: 341-346.   DOI   ScienceOn
32 James, E. K., F. L. Olivares, A. L. M. de Oliveira, F. B. dos Reis, L. G. da Silva, and V. M. Reis. 2001. Further observations on the interaction between sugar cane and Gluconacetobacter diazotrophicus under laboratory and greenhouse conditions. J. Exp. Botany 52: 747-760.
33 Stracke, S., C. Kistner, S. Yoshida, L. Mulder, S. Sato, T. Kaneko, S. Tabata, N. Sandal, J. Stougaard, et al. 2002. A plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature 417: 959-962.   DOI   ScienceOn
34 Kurokawa, M., Hatano, M., Kashiwagi, N., Saito, T., Ishida, S., and R. Homma.1962. A new method for the turbidimetric measurement of bacterial density. J. Bacteriol. 83: 14-19.
35 Fahraeus, G. 1957. The infection of clover root hairs by nodule bacteria studied by a simple glass slide technique. J. Gen. Microbiol. 16: 374-381.   DOI   ScienceOn