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Microbial Ecology

, Volume 51, Issue 3, pp 257–266 | Cite as

Exploiting New Systems-Based Strategies to Elucidate Plant-Bacterial Interactions in the Rhizosphere

  • P. D. Kiely
  • J. M. Haynes
  • C. H. Higgins
  • A. Franks
  • G. L. Mark
  • J. P. Morrissey
  • F. O'GaraEmail author
Article

Abstract

The rhizosphere is the site of intense interactions between plant, bacterial, and fungal partners. In plant-bacterial interactions, signal molecules exuded by the plant affect both primary initiation and subsequent behavior of the bacteria in complex beneficial associations such as biocontrol. However, despite this general acceptance that plant-root exudates have an effect on the resident bacterial populations, very little is still known about the influence of these signals on bacterial gene expression and the roles of genes found to have altered expression in plant-microbial interactions. Analysis of the rhizospheric communities incorporating both established techniques, and recently developed “omic technologies” can now facilitate investigations into the molecular basis underpinning the establishment of beneficial plant-microbial interactomes in the rhizosphere. The understanding of these signaling processes, and the functions they regulate, is fundamental to understanding the basis of beneficial microbial–plant interactions, to overcoming existing limitations, and to designing improved strategies for the development of novel Pseudomonas biocontrol strains.

Keywords

Green Fluorescent Protein Microbe Rhizobium Omic Technology Functional Genomic Analysis 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We acknowledge Abdelhamid Abbas, Maeve Cullinane, Max Dow, and Pat Higgins for useful advice and discussions. We acknowledge the IMPACT, ECO-SAFE GM-RHIZO, and PSEUDOMICS EU-consortia for fruitful discussion and valuable scientific comment. Research in the authors' laboratories is supported in part by grants awarded by the European Union: BIO4-CT96-0027 (IMPACT 11), QLK3-CT-2000-31759 (ECO-SAFE) QLK3-2001-00101 (GM-RHIZO), QLRT-2001-00914 (PSEUDOMICS); The Higher Education Authority of Ireland (PRTI2, PRTI3); Enterprise Ireland, SC/02/517, SC/02/0420, and Science Foundation of Ireland (04/BR/B0597; 02/IN.1/B1261).

References

  1. 1.
    Abbas, A, McGuire, JE, Crowley, D, Baysse, C, Dow, M, O'Gara, F (2004) The putative permease PhlE of Pseudomonas fluorescens F113 has a role in 2,4-diacetylphloroglucinol resistance and in general stress tolerance. Microbiology 150: 2443–2450CrossRefPubMedGoogle Scholar
  2. 2.
    Abbas, A, Morrissey, JP, Marquez, PC, Sheehan, MM, Delany, IR, O'Gara, F (2002) Characterization of interactions between the transcriptional repressor PhlF and its binding site at the phlA promoter in Pseudomonas fluorescens F113. J Bacteriol 184: 3008–3016CrossRefPubMedGoogle Scholar
  3. 3.
    Achouak, W, Conrod, S, Cohen, V, Heulin, T (2004) Phenotypic variation of Pseudomonas brassicacearum as a plant root-colonization strategy. Mol Plant Microb Interact 17: 872–879CrossRefGoogle Scholar
  4. 4.
    Allen, J, Davey, HM, Broadhurst, D, Heald, JK, Rowland, JJ, Oliver, SG, Kell, DB (2003) High-throughput classification of yeast mutants for functional genomics using metabolic footprinting. Nat Biotechnol 21: 692–696CrossRefPubMedGoogle Scholar
  5. 5.
    Artursson, V, Jansson, JK (2003) Use of bromodeoxyuridine immunocapture to identify active bacteria associated with arbuscular mycorrhizal hyphae. Appl Environ Microbiol 69: 6208 – 6215CrossRefPubMedGoogle Scholar
  6. 6.
    Barnett, MJ, Toman, CJ, Fisher, RF, Long, SR (2004) A dual-genome Symbiosis Chip for coordinate study of signal exchange and development in a prokaryote–host interaction. Proc Natl Acad Sci USA 101: 16636–16641CrossRefPubMedGoogle Scholar
  7. 7.
    Bestel-Corre, G, Dumas-Gaudot, E, Poinsot, V, Dieu, M, Dierick, JF, van, TD, Remacle, J, Gianinazzi-Pearson, V,Gianinazzi, S (2002) Proteome analysis and identification of symbiosis-related proteins from Medicago truncatula Gaertn. by two-dimensional electrophoresis and mass spectrometry. Electrophoresis 23: 122–137CrossRefPubMedGoogle Scholar
  8. 8.
    Bloemberg, GV, O'Toole, GA, Lugtenberg, BJ, Kolter, R (1997) Green fluorescent protein as a marker for Pseudomonas spp. Appl Environ Microbiol 63: 4543–4551PubMedGoogle Scholar
  9. 9.
    Buell, CR, Joardar, V, Lindeberg, M, Selengut, J, Paulsen, IT, Gwinn, ML, Dodson, RJ, Deboy, RT, Durkin, AS, Kolonay, JF, Madupu, R, Daugherty, S, Brinkac, L, Beanan, MJ, Haft, DH, Nelson, WC, Davidsen, T, Zafar, N, Zhou, L, Liu, J, Yuan, Q, Khouri, H, Fedorova, N, Tran, B, Russell, D, Berry, K, Utterback, T, Van Aken, SE, Feldblyum, TV, D’Ascenzo, M, Deng, WL, Ramos, AR, Alfano, JR, Cartinhour, S, Chatterjee, AK, Delaney, TP, Lazarowitz, SG, Martin, GB, Schneider, DJ, Tang, X, Bender, CL, White, O, Fraser, CM, Collmer, A (2003) The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000. Proc Natl Acad Sci USA 100: 10181–10186CrossRefPubMedGoogle Scholar
  10. 10.
    Cook, RJ, Thomashow, LS, Weller, DM, Fujimoto, D, Mazzola, M, Bangera, G, Kim, DS (1995) Molecular mechanisms of defense by rhizobacteria against root disease. Proc Natl Acad Sci USA 92: 4197–4201PubMedCrossRefGoogle Scholar
  11. 11.
    Delany, I, Sheehan, MM, Fenton, A, Bardin, S, Aarons, S, O'Gara, F (2000) Regulation of production of the antifungal metabolite 2,4-diacetylphloroglucinol in Pseudomonas fluorescens F113: genetic analysis of phlF as a transcriptional repressor. Microbiology 146(Pt 2): 537–543PubMedGoogle Scholar
  12. 12.
    Dumas-Gaudot, E, Amiour, N, Weidmann, S, Bestel-Corre, G, Valot, B, Lenogu, S, Gianinazzi-Pearson, V, Gianinazzi, S (2004) A technical trick for studying proteomics in parallel to transcriptomics in symbiotic root–fungus interactions. Proteomics 4: 451–453CrossRefPubMedGoogle Scholar
  13. 13.
    Gage, DJ (2002) Analysis of infection thread development using Gfp- and DsRed-expressing Sinorhizobium meliloti. J Bacteriol 184: 7042–7046CrossRefPubMedGoogle Scholar
  14. 14.
    Gage, DJ, Bobo, T, Long, SR (1996) Use of green fluorescent protein to visualize the early events of symbiosis between Rhizobium meliloti and alfalfa (Medicago sativa). J Bacteriol 178: 7159–7166PubMedGoogle Scholar
  15. 15.
    Germaine, K, Keogh, E, Garcia-Cabellos, G, Borremans, B, van der Lelie, D, Barac, T, Oeyen, L, Vangronsveld, J, Porteus-Moore, F, Moore, ERB, Campblee, CD, Ryan, D, Dowling, DN (2004) Colonisation of poplar trees by gfp expressing bacterial endophytes. FEMS Microbiol Ecol 48: 109–118CrossRefGoogle Scholar
  16. 16.
    Giddings, G, Allison, G, Brooks, D, Carter, A (2000) Transgenic plants as factories for biopharmaceuticals. Nat Biotechnol 18: 1151–1155CrossRefPubMedGoogle Scholar
  17. 17.
    Griffiths, RI, Manefield, M, Ostle, N, McNamara, N, O'Donnell, AG, Bailey, MJ, Whiteley, AS (2004) 13CO2 pulse labelling of plants in tandem with stable isotope probing: methodological considerations for examining microbial function in the rhizosphere. J Microbiol Methods 58: 119–129CrossRefPubMedGoogle Scholar
  18. 18.
    Gygi, SP, Rochon, Y, Franza, BR, Aebersold, R (1999) Correlation between protein and mRNA abundance in yeast. Mol Cell Biol 19: 1720–3170PubMedGoogle Scholar
  19. 19.
    Humphery-Smith, I, Cordwell, SJ, Blackstock, WP (1997) Proteome research: complementarity and limitations with respect to the RNA and DNA worlds. Electrophoresis 18: 1217–1242CrossRefPubMedGoogle Scholar
  20. 20.
    Ivanova, PT, Cerda, BA, Horn, DM, Cohen, JS, McLafferty, FW, Brown, HA (2001) Electrospray ionization mass spectrometry analysis of changes in phospholipids in RBL-2H3 mastocytoma cells during degranulation. Proc Natl Acad Sci USA 98: 7152–7157CrossRefPubMedGoogle Scholar
  21. 21.
    Jeon, CO, Park, W, Padmanabhan, P, DeRito, C, Snape, JR, Madsen, EL (2003) Discovery of a bacterium, with distinctive dioxygenase, that is responsible for in situ biodegradation in contaminated sediment. Proc Natl Acad Sci USA 100: 13591–13596CrossRefPubMedGoogle Scholar
  22. 22.
    Kim, ST, Cho, KS, Jang, YS, Kang, KY (2001) Two-dimensional electrophoretic analysis of rice proteins by polyethylene glycol fractionation for protein arrays. Electrophoresis 22: 2103–2109CrossRefPubMedGoogle Scholar
  23. 23.
    Kim, ST, Cho, KS, Yu, S, Kim, SG, Hong, JC, Han, CD, Bae, DW, Nam, MH, Kang, KY (2003) Proteomic analysis of differentially expressed proteins induced by rice blast fungus and elicitor in suspension-cultured rice cells. Proteomics 3: 2368–2378CrossRefPubMedGoogle Scholar
  24. 24.
    Kuske, CR, Ticknor, LO, Miller, ME, Dunbar, JM, Davis, JA, Barns, SM, Belnap, J (2002) Comparison of soil bacterial communities in rhizospheres of three plant species and the interspaces in an arid grassland. Appl Environ Microbiol 68: 1854–1863CrossRefPubMedGoogle Scholar
  25. 25.
    Loy, A, Schultz, C, Lucker, S, Schopfer-Wendels, A, Stoecker, K, Baranyi, C, Lehner, A, Wagner, M (2004) 16S rRNA gene-based oligonucleotide microarray for environmental monitoring of the betaproteobacterial order Rhodocyclales. Appl Environ Microbiol 71.3: 1373–1386Google Scholar
  26. 26.
    Lueders, T, Manefield, M, Friedrich, MW (2004) Enhanced sensitivity of DNA- and rRNA-based stable isotope probing by fractionation and quantitative analysis of isopycnic centrifugation gradients. Environ Microbiol 6: 73–78CrossRefPubMedGoogle Scholar
  27. 27.
    Lueders, T, Pommerenke, B, Friedrich, MW (2004) Stable-isotope probing of microorganisms thriving at thermodynamic limits: syntrophic propionate oxidation in flooded soil. Appl Environ Microbiol 70: 5778–5786CrossRefPubMedGoogle Scholar
  28. 28.
    Lueders, T, Wagner, B, Claus, P, Friedrich, MW (2004) Stable isotope probing of rRNA and DNA reveals a dynamic methylotroph community and trophic interactions with fungi and protozoa in oxic rice field soil. Environ Microbiol 6: 60–72CrossRefPubMedGoogle Scholar
  29. 29.
    Maier, W, Schmidt, J, Nimitz, M, Wray, V, Strack, D (2000) Secondary products in mycorrhizal roots of tobacco and tomato. Phytochemistry 54: 473–479CrossRefPubMedGoogle Scholar
  30. 30.
    Maleck, K, Levine, A, Eulgem, T, Morgan, A, Schmid, J, Lawton, KA, Dangl, JL, Dietrich, RA (2000) The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nat Genet 26: 403–410PubMedCrossRefGoogle Scholar
  31. 31.
    Manefield, M, Whiteley, AS, Griffiths, RI, Bailey, MJ (2002) RNA stable isotope probing, a novel means of linking microbial community function to phylogeny. Appl Environ Microbiol 68: 5367–5373PubMedCrossRefGoogle Scholar
  32. 32.
    Mark, GL, Dow, JM, Kiely, PD, Higgins, H, Haynes, J, Baysse, C, Abbas, A, Foley, T, Franks, A, Morrissey, J, O'Gara, F (2005) Transcriptome profiling of bacterial responses to root exudates identifies novel genes involved in microbe–plant interactions. Proc Natl Acad Sci USA 102(48): 17454–17459CrossRefPubMedGoogle Scholar
  33. 33.
    Morris, AC, Djordjevic, MA (2001) Proteome analysis of cultivar-specific interactions between Rhizobium leguminosarum biovar trifolii and subterranean clover cultivar Woogenellup. Electrophoresis 22: 586–598CrossRefPubMedGoogle Scholar
  34. 34.
    Morrissey, JP, Dow, JM, Mark, LG, O'Gara, F (2004) Are microbes at the root of a solution to world food production? EMBO Reports 5: 922–926CrossRefPubMedGoogle Scholar
  35. 35.
    Larrainzar, E, O'Gara, F, Morrissey, JP (2005) Applications of autofluorescent proteins for in situ studies in microbial ecology. Annu Rev Microbiol 59: 257–277CrossRefPubMedGoogle Scholar
  36. 36.
    Muyzer, G (1999) DGGE/TGGE a method for identifying genes from natural ecosystems. Curr Opin Microbiol 2: 317–322CrossRefPubMedGoogle Scholar
  37. 37.
    Narasimhan, K, Basheer, C, Bajic, VB, Swarup, S (2003) Enhancement of plant–microbe interactions using a rhizosphere metabolomics-driven approach and its application in the removal of polychlorinated biphenyls. Plant Physiol 132: 146–153CrossRefPubMedGoogle Scholar
  38. 38.
    Ndimba, BK, Chivasa, S, Hamilton, JM, Simon, WJ, Slabas, AR (2003) Proteomic analysis of changes in the extracellular matrix of Arabidopsis cell suspension cultures induced by fungal elicitors. Proteomics 3: 1047–1059CrossRefPubMedGoogle Scholar
  39. 39.
    Nelson, KE, Weinel, C, Paulsen, IT, Dodson, RJ, Hilbert, H, Martins dos Santos, VA, Fouts, DE, Gill, SR, Pop, M, Holmes, M, Brinkac, L, Beanan, M, DeBoy, RT, Daugherty, S, Kolonay, J, Madupu, R, Nelson, W, White, O, Peterson, J, Khouri, H, Hance, I, Chris Lee, P, Holtzapple, E, Scanlan, D, Tran, K, Moazzez, A, Utterback, T, Rizzo, M, Lee, K, Kosack, D, Moestl, D, Wedler, H, Lauber, J, Stjepandic, D, Hoheisel, J, Straetz, M, Heim, S, Kiewitz, C, Eisen, JA, Timmis, KN, Dusterhoft, A, Tummler, B, Fraser, CM (2002) Complete genome sequence and comparative analysis of the metabolically versatile Pseudomonas putida KT2440. Environ Microbiol 4: 799 –808CrossRefPubMedGoogle Scholar
  40. 40.
    Normander, B, Hendriksen, NB, Nybroe, O (1999) Green fluorescent protein-marked Pseudomonas fluorescens: localization, viability, and activity in the natural barley rhizosphere. Appl Environ Microbiol 65: 4646–4651PubMedGoogle Scholar
  41. 41.
    Oliver, SG, Winson, MK, Kell, DB, Baganz, F (1998) Systematic functional analysis of the yeast genome. Trends Biotechnol 16: 373–378CrossRefPubMedGoogle Scholar
  42. 42.
    Palma, M, Worgall, S, Quadri, LE (2003) Transcriptome analysis of the Pseudomonas aeruginosa response to iron. Arch Microbiol 180: 374–379CrossRefPubMedGoogle Scholar
  43. 43.
    Peck, SC, Nuhse, TS, Hess, D, Iglesias, A, Meins, F, Boller, T (2001) Directed proteomics identifies a plant-specific protein rapidly phosphorylated in response to bacterial and fungal elicitors. Plant Cell 13: 1467–1475CrossRefPubMedGoogle Scholar
  44. 44.
    Puhler, A, Arlat, M, Becker, A, Gottfert, M, Morrissey, JP, O'Gara, F (2004) What can bacterial genome research teach us about bacteria–plant interactions? Curr Opin Plant Biol 7: 137–147CrossRefPubMedGoogle Scholar
  45. 45.
    Raamsdonk, LM, Teusink, B, Broadhurst, D, Zhang, N, Hayes, A, Walsh, MC, Berden, JA, Brindle, KM, Kell, DB, Rowland, JJ, Westerhoff, HV, van Dam, K, Oliver, SG (2001) A functional genomics strategy that uses metabolome data to reveal the phenotype of silent mutations. Nat Biotechnol 19: 45–50CrossRefPubMedGoogle Scholar
  46. 46.
    Radajewski, S, Ineson, P, Parekh, NR, Murrell, JC (2000) Stable-isotope probing as a tool in microbial ecology. Nature 403: 646–649CrossRefPubMedGoogle Scholar
  47. 47.
    Rainey, PB (1999) Adaptation of Pseudomonas fluorescens to the plant rhizosphere. Environ Microbiol 1: 243–257CrossRefPubMedGoogle Scholar
  48. 48.
    Ramos, C, Molbak, L, Molin, S (2000) Bacterial activity in the rhizosphere analyzed at the single-cell level by monitoring ribosome contents and synthesis rates. Appl Environ Microbiol 66: 801–809CrossRefPubMedGoogle Scholar
  49. 49.
    Ramos, HJ, Roncato-Maccari, LD, Souza, EM, Soares-Ramos, JR, Hungria, M, Pedrosa, FO (2002) Monitoring Azospirillum–wheat interactions using the gfp and gusA genes constitutively expressed from a new broad-host range vector. J Biotechnol 97: 243–252CrossRefPubMedGoogle Scholar
  50. 50.
    Scheideler, M, Schlaich, NL, Fellenberg, K, Beissbarth, T, Hauser, NC, Vingron, M, Slusarenko, AJ, Hoheisel, JD (2002) Monitoring the switch from housekeeping to pathogen defense metabolism in Arabidopsis thaliana using cDNA arrays. J Biol Chem 277: 10555–10561CrossRefPubMedGoogle Scholar
  51. 51.
    Schena, M, Heller, RA, Theriault, TP, Konrad, K, Lachenmeier, E, Davis, RW (1998) Microarrays: biotechnology's discovery platform for functional genomics. Trends Biotechnol 16: 301–306CrossRefPubMedGoogle Scholar
  52. 52.
    Schenk, PM, Kazan, K, Wilson, I, Anderson, JP, Richmond, T, Somerville, SC, Manners, JM (2000) Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc Natl Acad Sci USA 97: 11655–11660CrossRefPubMedGoogle Scholar
  53. 53.
    Schuster, M, Lostroh, CP, Ogi, T, Greenberg, EP (2003) Identification, timing, and signal specificity of Pseudomonas aeruginosa quorum-controlled genes: a transcriptome analysis. J Bacteriol 185: 2066–2079CrossRefPubMedGoogle Scholar
  54. 54.
    Silby, MW, Levy, SB (2004) Use of in vivo expression technology to identify genes important in growth and survival of Pseudomonas fluorescens Pf0-1 in soil: discovery of expressed sequences with novel genetic organization. J Bacteriol 186: 7411–7419CrossRefPubMedGoogle Scholar
  55. 55.
    Smalla, K, Wieland, G, Buchner, A, Zock, A, Parzy, J, Kaiser, S, Roskot, N, Heuer, H, Berg, G (2001) Bulk and rhizosphere soil bacterial communities studied by denaturing gradient gel electrophoresis: plant-dependent enrichment and seasonal shifts revealed. Appl Environ Microbiol 67: 4742–4751CrossRefPubMedGoogle Scholar
  56. 56.
    Stover, CK, Pham, XQ, Erwin, AL, Mizoguchi, SD, Warrener, P, Hickey, MJ, Brinkman, FS, Hufnagle, WO, Kowalik, DJ, Lagrou, M, Garber, RL, Goltry, L, Tolentino, E, Westbrock-Wadman, S, Yuan, Y, Brody, LL, Coulter, SN, Folger, KR, Kas, A, Larbig, K, Lim, R, Smith, K, Spencer, D, Wong, GK, Wu, Z, Paulsen, IT, Reizer, J, Saier, MH, Hancock, RE, Lory, S, Olson, MV (2000) Complete genome sequence of Pseudomonas aeruginosa PA01, an opportunistic pathogen. Nature 406: 959–964CrossRefPubMedGoogle Scholar
  57. 57.
    Sweeney P (2005) The influence of plant varieties and P. fluorescens F113, on the diversity of ecologically significant bacterial communities in the rhizosphere. MSc thesis, University College Cork, IrelandGoogle Scholar
  58. 58.
    Thomas MAaK, R (2004) Genomics for the ecological toolbox. Trends Ecol Evol 19: 439–445CrossRefGoogle Scholar
  59. 59.
    Tombolini, R, Unge, A, Davy, ME, de Bruijn, FJ, Jansson, J (1997) Flow cytometric and microscopic analysis of GFP-tagged Pseudomonas fluorescens bacteria. FEMS Microbiol Ecol 22: 17–28CrossRefGoogle Scholar
  60. 60.
    Tombolini, R, van der Gaag, DJ, Gerhardson, B, Jansson, JK (1999) Colonization pattern of the biocontrol strain Pseudomonas chlororaphis MA 342 on barley seeds visualized by using green fluorescent protein. Appl Environ Microbiol 65: 3674–3680PubMedGoogle Scholar
  61. 61.
    Unge, A, Jansson, J (2001) Monitoring population size, activity, and distribution of gfp-luxAB-tagged Pseudomonas fluorescens SBW25 during colonization of wheat. Microb Ecol 41: 290–300PubMedGoogle Scholar
  62. 62.
    Urbanczyk-Wochniak, E, Luedemann, A, Kopka, J, Selbig, J, Roessner-Tunali, U, Willmitzer, L, Fernie, AR (2003) Parallel analysis of transcript and metabolic profiles: a new approach in systems biology. EMBO Rep 4: 989–993CrossRefPubMedGoogle Scholar
  63. 63.
    van Loon, LC, Bakker, PA, Pieterse, CM (1998) Systemic resistance induced by rhizosphere bacteria. Annu Rev Phytopathol 36: 453–483CrossRefPubMedGoogle Scholar
  64. 64.
    van Mispelaar, VG, Tas, AC, Smilde, AK, Schoenmakers, PJ, van Asten, AC (2003) Quantitative analysis of target components by comprehensive two-dimensional gas chromatography. J Chromatogr A 1019: 15–29CrossRefPubMedGoogle Scholar
  65. 65.
    Villacieros, M, Power, B, Sanchez-Contreras, M, Lloret, J, Oruezabal, RI, Martin, M, Fernandez-Piñas, F, Bonilla, I, Whelan, C, Dowling, DN, Rivilla, R (2003) Colonization behaviour of Pseudomonas fluorescens and Sinorhizobium meliloti in the alfalfa (Medicago sativa) rhizosphere. Plant Soil 251(1): 47–54CrossRefGoogle Scholar
  66. 66.
    Walsh, UF, Morrissey, JP, O'Gara, F (2001) Pseudomonas for biocontrol of phytopathogens: from functional genomics to commercial exploitation. Curr Opin Biotechnol 12: 289–295CrossRefPubMedGoogle Scholar
  67. 67.
    Weckwerth, W (2003) Metabolomics in systems biology. Annu Rev Plant Biol 54: 669–689CrossRefPubMedGoogle Scholar
  68. 68.
    Wilkins, MR, Sanchez, JC, Gooley, AA, Appel, RD, Humphery-Smith, I, Hochstrasser, DF, Williams, KL (1996) Progress with proteome projects: why all proteins expressed by a genome should be identified and how to do it. Biotechnol Genet Eng Rev 13: 19–50PubMedGoogle Scholar
  69. 69.
    Yu, J, Hu, S, Wang, J, Wong, GK, Li, S, Liu, B, Deng, Y, Dai, L, Zhou, Y, Zhang, X, Cao, M, Liu, J, Sun, J, Tang, J, Chen, Y, Huang, X, Lin, W, Ye, C, Tong, W, Cong, L, Geng, J, Han, Y, Li, L, Li, W, Hu, G, Li, J, Liu, Z, Qi, Q, Li, T, Wang, X, Lu, H, Wu, T, Zhu, M, Ni, P, Han, H, Dong, W, Ren, X, Feng, X, Cui, P, Li, X, Wang, H, Xu, X, Zhai, W, Xu, Z, Zhang, J, He, S, Xu, J, Zhang, K, Zheng, X, Dong, J, Zeng, W, Tao, L, Ye, J, Tan, J, Chen, X, He, J, Liu, D, Tian, W, Tian, C, Xia, H, Bao, Q, Li, G, Gao, H, Cao, T, Zhao, W, Li, P, Chen, W, Zhang, Y, Hu, J, Liu, S, Yang, J, Zhang, G, Xiong, Y, Li, Z, Mao, L, Zhou, C, Zhu, Z, Chen, R, Hao, B, Zheng, W, Chen, S, Guo, W, Tao, M, Zhu, L, Yuan, L, Yang, H (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science 296: 79–92CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  • P. D. Kiely
    • 1
  • J. M. Haynes
    • 1
  • C. H. Higgins
    • 1
  • A. Franks
    • 1
  • G. L. Mark
    • 1
  • J. P. Morrissey
    • 1
  • F. O'Gara
    • 1
    Email author
  1. 1.Biomerit Research Centre, Department of MicrobiologyNational University of Ireland (UCC)CorkIreland

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