Structural and functional study in the rhizosphere of Oryza sativa L. plants growing under biotic and abiotic stress

Journal of Applied Microbiology

Volumn 115, Issue 1, 2013, Pages 218-235

  Lucas, J A ^a   Garcia Villaraco A ^a   Ramos, B ^a   Garcia Cristobal J ^a   Algar, E ^a   Gutierrez Manero J ^a  

^a UNIVERSIDAD SAN PABLO CEU   (Spain)

Author keywords

16S rRNA libraries; Microbial functional diversity; Plant growth promoting rhizobacteria; Rhizobacteria biodiversity; Rice; Stress conditions

Indexed keywords

BACTERIA; CROPS; DNA SEQUENCES; ENVIRONMENTAL IMPACT; LIBRARIES; METABOLISM; PLANTS (BOTANY); RNA; SOILS;

16S RRNA; 16S RRNA LIBRARY; MICROBIAL FUNCTIONAL DIVERSITIES; PARTIAL SEQUENCES; PLANT GROWTH-PROMOTING RHIZOBACTERIA; RHIZOBACTERIA; RHIZOBACTERIUM BIODIVERSITY; RICE; RICE PRODUCTION; STRESS CONDITION;

BIODIVERSITY;

BIOFERTILIZER; FERTILIZER; RNA 16S; UNCLASSIFIED DRUG;

BIODIVERSITY; BIOTIC FACTOR; CROP PLANT; CROP PRODUCTION; ENVIRONMENTAL IMPACT; ENVIRONMENTAL STRESS; GENERALIST; MARSH; PLANT; RHIZOBACTERIUM; RHIZOSPHERE; RICE; RNA; SALINITY;

ABIOTIC STRESS; ARTICLE; BACTERIAL STRAIN; BACTERIUM ISOLATE; BACTERIUM ISOLATION; BIOTIC STRESS; COMMUNITY STRUCTURE; CONTROLLED STUDY; CROP PRODUCTION; ENVIRONMENTAL STRESS; FUNGAL COMMUNITY; MAGNAPORTHE ORYZAE; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENETIC TREE; PLANT METABOLISM; PROTEOBACTERIA; RHIZOSPHERE; RICE; RNA SEQUENCE; SALINITY; SOIL MICROFLORA; SPAIN; SPHINGOBACTERIA; THERMOCOCCUS; VERRUCOMICROBIA;

ANDALUCIA; GUADALQUIVIR RIVER; SPAIN;

BACTERIA (MICROORGANISMS); MAGNAPORTHE; MAGNAPORTHE ORYZAE; ORYZA SATIVA; PROTEOBACTERIA; RHIZOBIALES; SPHINGOBACTERIA; THERMOCOCCI; VERRUCOMICROBIAE;

EID: 84879116254     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/jam.12225     Document Type: Article

References (86)

1. Aguilar, M. (2001) Cultivo del arroz en el sur de España. Caja de Ahorros El Monte. Sevilla. Spain..
2. Alexander, D.B. and Zuberer, D.A. (1991) Use of chrome azurol S reagents to evaluate siderophore production by rhizosphere bacteria. Biol Fertil Soils 12, 39-45.
3. Ali, B., Sabri, A.N., Ljun, K. and Hasnain, S. (2009) Auxin production by plant associated bacteria: impact on endogenous IAA content and growth of Triticum aestivum (L.). Lett Appl Microbiol 48, 542-547.
4. Alisi, C., Lasinio, G.F., Dalmastri, C., Sprocati, A., Tabacchioni, S., Bevivino, A. and Chiarini, L. (2005) Metabolic profiling of Burkholderia cenocepacia, Burkholderia ambifaria and Burkholderia pyrrocinia isolates from maize rhizosphere. Microb Ecol 50, 385-395.
5. Arjun, J.K. and Harikrishnan, K. (2011) Metagenomic analysis of bacterial diversity in the rice rhizosphere soil microbiome. Biotechnol Bioinform Bioeng 1, 361-367.
6. Barriuso, J., Pereyra, M.T., Lucas-García, J.A., Megias, M., Gutierrez Mañero, F.J. and Ramos, B. (2005) Screening for putative PGPR to improve establishment of the symbiosis Lactarius deliciosus-Pinus sp. Microb Ecol 50, 82-89.
7. Barriuso, J., Ramos Solano, B. and Gutierrez Mañero, F.J. (2008) Protection against pathogen and salt stress by four plant growth-promoting rhizobacteria isolated from Pinus sp. on Arabidopsis thaliana. Phytopathol 98, 666-672.
8. Baudoin, E., Benizri, E. and Guckert, A. (2001) Metabolic fingerprint of microbial communities from distinct rhizosphere compartments. Eur J Soil Biol 37, 85-93.
9. Benizri, E., Courtade, A., Picard, C. and Guckert, A. (1998) Role of maize root exudates in the production of auxins by Pseudomonas fluorescens M.3.1. Soil Biol Biochem 30, 1481-1484.
10. Berendsen, R.L., Pieterse, C.M.J. and Bakke, P.A.H.M. (2012) The rhizosphere microbiome and plant health. Trends in Plant Sci 17, 478-486.
11. Brusetti, L., Francia, P., Bertolini, C., Pagliuca, A., Borin, S., Sorlini, C., Abruzzese, A., Sacchi, G. et al. (2005) Bacterial communities associated with the rhizosphere of transgenic Bt 176 maize (Zea mays) and its non transgenic counterpart. Plant Soil 266, 11-21.
12. Cattelan, A.J., Hartel, P.G. and Fuhrmann, J.J. (1999) Screening for plant growth-promoting rhizobacteria to promote early soybean growth. Soil Sci Soc Am J 63, 1670-1680.
13. Cheng, Z., Park, E. and Glick, B.R. (2007) 1-Aminocyclopropane-1-carboxylate deaminase from Pseudomonas putida UW4 facilitates the growth of canola in the presence of salt. Can J Microbiol 53, 912-918.
14. Chowdhury, S.P., Schmid, M., Hartmann, A. and Tripathi, A.K. (2009) Diversity of 16S-rRNA and nifH genes derived from rhizosphere soil and roots of an endemic drought tolerant grass, Lasiurus sindicus. Eur J Soil Biol 45, 114-122.
15. Collavino, M.M., Sansberro, P.A., Mroginski, L.A. and Aguilar, O.M. (2010) Comparison of in vitro solubilization activity of diverse phosphate-solubilizing bacteria native to acid soil and their ability to promote Phaseolus vulgaris growth. Biol Fertil Soils 46, 727-738.
16. Crecchio, C., Gelsomino, A., Ambrosoli, R., Minati, J.L. and Ruggiero, P. (2004) Functional and molecular responses of soil microbial communities under differing soil management practices. Soil Biol Biochem 36, 1873-1883.
17. Dakora, F.D. and Phillips, D.A. (2002) Root exudates as mediators of mineral acquisition in low-nutrient environments. Plant Soil 245, 35-47.
18. Domenech, J., Ramos, B., Probanza, A., Lucas, J.A. and Gutierrez Mañero, F.J. (2007) Elicitation of systemic resistance and growth promotion of Arabidopsis thaliana by PGPRs from Nicotiana glauca: a study of the putative induction pathway. Plant Soil 290, 43-50.
19. Doornbos, R.F., Loon, L.C. and Bakker, P.A.H.M. (2011) Impact of root exudates and plant defense signaling on bacterial communities in the rhizosphere. A review. Agron Sustainable Dev 32, 227-243.
20. Drogue, B., Doré, H., Borland, S., Wisniewski-Dyé, F. and Prigent-Combaret, C. (2012) Which specificity in cooperation between phytostimulating rhizobacteria and plants? Res Microbiol 163, 500-510.
21. Elazegui, F.A. (1997) Cultivo del arroz en clima mediterráneo. Junta de Andalucía, Consejería de Agricultura y Pesca (Eds). Sevilla, Spain.
22. FAO (2008) The State of Food and Agriculture 2008. Biofuels: Prospects, Risks and Opportunities. Rome: Food and Agriculture Organization of the United Nations.
23. Fierer, N., Bradford, M.A. and Jackson, R.B. (2007) Toward an ecological classification of soil bacteria. Ecology 88, 1354-1364.
24. Friesen, M.L., Porter, S.S., Stark, S.C., von Wettberg, E.J., Sachs, J.L. and Martinez-Romero, E. (2011) Microbially mediated plant functional traits. Annu Rev Ecol Evol Syst 42, 23-46.
25. Galimany, G., Almacellas, J., Marin, J.P., Catala, M.M., Llorach, T., Matamoros, E., Tomas, A. and Montes, F. (2006) Estrategias para la optimización del control de las enferemedades del arroz en el Delta del Ebro. Phytoma 178, 34-48.
26. Gao, J.P., Chao, D.Y. and Lin, H.X. (2007) Understanding abiotic stress tolerance mechanisms: recent studies on stress response in rice. J Integr Plant Biol 49, 742-750.
27. García-Villaraco Velasco, A., Probanza, A., Gutierrez Mañero, F.J., Ramos, B. and Lucas García, J.A. (2009) Functional diversity of rhizosphere microorganisms from different genotypes of Arabidopsis thaliana. Comm Ecol 10, 111-119.
28. Garland, J.L. and Mills, A.L. (1991) Classification and characterization of heterotrophic microbial communities on the basis of patterns of community-level sole-carbon-source utilization. Appl Environ Microbiol 57, 2351-2359.
29. Glick, B.R., Karaturovic, D.M. and Newell, P.C. (1995) A novel procedure for rapid isolation of plant growth promoting pseudomonads. Can J Microbiol 41, 533-536.
30. 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.
31. Glickmann, E. and Dessaux, Y. (1995) A critical examination of the specificity of the salkowski reagent for indolic compounds produced by phytopathogenic bacteria. Appl Environ Microbiol 61, 793-796.
32. Graham, M.H. and Haynes, R.J. (2005) Catabolic diversity of soil microbial communities under sugarcane and other land uses estimated by Biolog and substrate-induced respiration methods. Appl Soil Ecol 29, 155-164.
33. Grayston, S.J., Griffith, G.S., Mawdsley, J.L., Campbell, C.D. and Bardgett, R.D. (2001) Accounting for variability in soil microbial communities of temperate upland grassland ecosystems. Soil Biol Biochem 33, 533-551.
34. Griffiths, B.S., Caul, S., Thompson, J., Birch, A.N.E., Scrimgeour, C., Andersen, M.N., Cortet, J., Messe, A. et al. (2005) A comparison of soil microbial community structure, protozoa and nematodes in field plots of conventional and genetically modified maize expressing the Bacillus thuringiensis CryIAb toxin. Plant Soil 275, 135-146.
35. Griffiths, B.S., Thompson, S.C.J., Birch, A.N.E., Scrimgeour, C., Cortet, J., Foggo, A., Hackett, C.A. and Krogh, P.H. (2006) Soil microbial and faunal community responses to Bt maize and insecticide in two soils. J Environ Qual 35, 734-741.
36. Gutierrez Mañero, F.J., Acero, N., Lucas, J.A. and Probanza, A. (1996) The influence of native rhizobacteria on European alder [Alnus glutinosa (L.) Gaertn.] growth. II. Characterization of growth promoting and growth inhibiting strains. Plant Soil 182, 67-74.
37. Hinsinger, P., Plassard, C., Jaillard, B. and Tang, C.X. (2003) Origins of root-mediated pH changes in the rhizosphere and their responses to environmental constraints: a review. Plant Soil 248, 43-59.
38. Hjort, K., Bergstrã, M., Adesina, M.F., Jansson, J.K., Smalla, K. and Ling, S. (2010) Chitinase genes revealed and compared in bacterial isolates, DNA extracts and a metagenomic library from a phytopathogen-suppressive soil. FEMS Microbiol Ecol 71, 197-207.
39. Holguin, G. and Glick, B.R. (2003) Transformation of Azospirillum brasilense Cd with an ACC deaminase gene from Enterobacter cloacae UW4 fused to the Tetr gene promoter improves its fitness and plant growth promoting ability. Microb Ecol 46, 122-133.
40. Hoshino, Y.T., Morimoto, S., Hayatsu, M., Nagaoka, K., Suzuki, C., Karasawa, T., Takenaka, M. and Akiyama, H. (2011) Effect of soil type and fertilizer management on archaeal community in upland field soils. Microbes Environ 26, 307-316.
41. Jalili, F., Khavazi, K., Pazira, E., Nejati, A., Rahmani, H.A., Sadaghiani, H.R. and Miransari, M. (2009) Isolation and characterization of ACC deaminase- producing fluorescent pseudomonads, to alleviate salinity stress on canola (Brassica napus L.) growth. J Plant Physiol 166, 667-674.
42. Janssen, P.H. (2006) Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes. Appl Environ Microbiol 72, 1719-1728.
43. Kloepper, J.W., Scrhoth, M.N. and Miller, T.D. (1980) Effects of rhizosphere colonization by plant growth-promoting rhizobacteria on potato plant development and yield. Phytopathology 70, 1078-1082.
44. Kuzyakov, Y., Hill, P.W. and Jones, D.L. (2007) Root exudate components change litter decomposition in a simulated rhizosphere depending on temperature. Plant Soil 290, 293-305.
45. Legendre, P. and Anderson, M.J. (1999) Distance-based redundancy analysis: testing multispecies responses in multifactorial ecological experiments. Ecol Monographs 69, 1-24.
46. Li, X.-G., Zhang, T.-L., Wang, X.-X., Hua, K., Zhao, L. and Han, Z.-M. (2012) The composition of root exudates from two different resistant peanut cultivars and their effects on the growth of soil-borne pathogen. Int J Biol Sci 9, 164-173.
47. Liao, H., Wan, H.Y., Shaff, J., Wang, X.R., Yan, X.L. and Kochian, L.V. (2006) Phosphorus and aluminum interactions in soybean in relation to aluminum tolerance, exudation of specific organic acids from different regions of the intact root system. Plant Physiol 141, 674-684.
48. Lippi, D., Paolis, M.R., Mattia, E.D., Pietrosanti, T. and Cacciari, I. (2004) Influence of substrate composition and flow rate on growth of Azospirillum brasilensis Cd in a co-culture with 3 sorghum rhizobacteria. Can J Microbiol 50, 861-867.
49. Liu, B., Zeng, Q., Yan, F., Xu, H. and Xu, C. (2005) Effects of transgenic plants on soil microorganisms. Plant Soil 271, 1-13.
50. van Loon, L.C., Bakker, P.A.H.M. and Pieterse, C.M.J. (1998) Systemic resistance induced by rhizosphere bacteria. Ann Rev Phytopathol 36, 453-483.
51. Lucas Garcia, J.A., Barbas, C., Probanza, A., Barrientos, M.L. and Gutierrez Mañero, F.J. (2001) Low molecular weight organic acids and fatty acids in root exudates of two Lupinus cultivars at flowering and fruiting stages. Phytochem Anal 12, 305-311.
52. Lucas García, J.A., Schloter, M., Durkaya, T. and Hartmann, A. (2003) Colonization of pepper roots by a plant growth promoting Pseudomonas fluorescens strain. Biol Fertil Soils 37, 381-385.
53. Lucas García, J.A., Domenech, J., Santamaria, C., Camacho, M., Daza, A. and Gutierrez Mañero, F.J. (2004a) Growth of forest plants (pine and holm-oak) inoculated with rhizobacteria: relationship with microbial community structure and biological activity of its rhizosphere. Environ Exp Bot 52, 239-251.
54. Lucas García, J.A., Probanza, A., Ramos, B., Colon Flores, J.J. and Gutierrez Mañero, F.J. (2004b) Effects of plant growth promoting rhizobacteria (PGPRs) on the biological nitrogen fixation, nodulation, and growth of Lupinus albus L. cv. Multolupa. Eng Life Sci 4, 71-77.
55. Lucas García, J.A., Probanza, A., Ramos, B., Ruiz Palomino, M. and Gutiérrez Mañero, F.J. (2004c) Effect of inoculation of Bacillus licheniformis on tomato and pepper. Agronomie 24, 169-176.
56. Lucas, J.A., Ramos Solano, B., Montes, F., Ojeda, J., Megias, M. and Gutierrez Mañero, J. (2009) Use of two PGPR strains in the integrated management of blast disease in rice (Oryza sativa) in Southern Spain. Field Crops Res 114, 404-410.
57. Lydell, C., Dowell, L., Sikaroodi, M., Gillevet, P. and Emerson, D. (2004) A population survey of members of the phylum Bacteroidetes isolated from salt marsh sediments along the East Coast of the United States. Microb Ecol 48, 263-273.
58. Lynch, J.M. (1990) The Rhizosphere. Chichester: Wiley-Interscience.
59. Marilley, L. and Aragno, M. (1999) Phylogenetic diversity of bacterial communities differing in degree of proximity of Lolium perenne and Trifolium repens roots. Appl Soil Ecol 13, 127-136.
60. Nannipieri, P., Ascher, J., Ceccherini, M.T., Landi, L., Pietramellara, G. and Renella, G. (2003) Microbial diversity and soil functions. Eur J Soil Sci 54, 655-670.
61. Nautiyal, C.S., Rehman, A. and Chauhan, P.S. (2010) Environmental Escherichia coli occur as natural plant growth-promoting soil bacterium. Arch Microbiol 192, 185-193.
62. Nihorimbere, V., Ongena, M., Smargiassi, M. and Thonart, P. (2011) Beneficial effect of the rhizosphere microbial community for plant growth and health. Biotechnol Agron Soc Environ 15, 327-337.
63. Patten, C.L. and Glick, B.R. (2002) Role of Pseudomonas putida indoleacetic acid in development of the host plant root system. Appl Environ Microbiol 68, 3795-3801.
64. Paul, D. and Nair, S. (2008) Stress adaptations in a plant growth promoting Rhizobacterium (PGPR) with increasing salinity in the coastal agricultural soils. J Basic Microbiol 48, 378-384.
65. Philippot, L., Andersson, S.G.E., Battin, T.J., Prosser, J.I., Schimel, J.P., Whitman, W.B. and Hallin, S. (2010) The ecological coherence of high bacterial taxonomic ranks. Nat Rev Microbiol 8, 523-529.
66. Preston-Mafham, J., Boddy, L. and Randerson, P.F. (2002) Analysis of microbial community functional diversity using a sole-carbon-source utilisation profiles - a critique. FEMS Microbiol Ecol 42, 1-14.
67. Ramos Solano, B., Pereyra de la Iglesia, M.T., Probanza, A., Lucas García, J.A., Megias, M. and Gutierrez Mañero, F.J. (2007) Screening for PGPR to improve growth of Cistus ladanifer seedlings for reforestation of degraded mediterranean ecosystems. Plant Soil 287, 59-68.
68. Ramos Solano, B., Barriuso Maicas, J., Pereyra de la Iglesia, M.T., Domenech, J. and Gutierrez Mañero, F.J. (2008) Systemic disease protection elicited by plant growth promoting rhizobacteria strains: relationship between metabolic responses, systemic disease protection, and biotic elicitors. Phytopathology 98, 451-457.
69. Ramos-Solano, B., Lucas Garcia, J.A., Garcia-Villaraco, A., Algar, E., Garcia-Cristobal, J. and Gutierrez Manero, F.J. (2010) Siderophore and chitinase producing isolates from the rhizosphere of Nicotiana glauca Graham enhance growth and induce systemic resistance in Solanum lycopersicum L. Plant Soil 334, 189-197.
70. Rincon, A., Valladares, F., Gimeno, T.E. and Pueyo, J.J. (2008) Water stress responses of two Mediterranean tree species influenced by native soil microorganisms and inoculation with a plant growth promoting rhizobacterium. Tree Physiol 28, 1693-1701.
71. Saravanakumar, D. and Samiyappan, R. (2007) ACC deaminase from Pseudomonas fluorescens mediated saline resistance in groundnut (Arachis hypogea) plants. J Appl Microbiol 102, 1283-1292.
72. Schloss, P.D. and Handelsman, J. (2005) Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol 71, 1501-1506.
73. Schloss, P.D. and Handelsman, J. (2006) Introducing SONS, a tool for operational taxonomic unit-based comparisons of microbial community memberships and structures. Appl Environ Microbiol 72, 6773-6779.
74. Schloss, P.D., Larget, B.R. and Handelsman, J. (2004) Integration of microbial ecology and statistics: a test to compare gene libraries. Appl Environ Microbiol 70, 5485-5492.
75. Schutter, M. and Dick, R. (2001) Shifts in substrate utilization potential and structure of soil microbial communities in response to carbon substrates. Soil Biol Biochem 33, 1481-1491.
76. Selvakumar, G., Joshi, P., Nazim, S., Mishra, P.K., Kundu, S. and Gupta, H.S. (2009) Exiguobacterium acetylicum strain 1P (MTCC 8707) a novel bacterial antagonist from the North Western Indian Himalayas. World J Microbiol Biotechol 25, 131-137.
77. Sessitsch, A.A., Hardoim, P.P., Döring, J.J., Weilharter, A.A., Krause, A.A. and Woyke, T.T. (2011) Functional characteristics of an endophyte community colonizing rice roots as revealed by metagenomic analysis. Mol Plant Microbe Interact 25, 28-36.
78. Sokal, R.R. and Rohlf, F.J. (1979) Biometría. Barcelona: Editorial Blume.
79. Spain, A.M., Krumholz, L.R. and Elshahed, M.S. (2009) Abundance, composition, diversity and novelty of soil Proteobacteria. ISME J 3, 992-1000.
80. Tamura, K., Dudley, J., Nei, M. and Kumar, S. (2007) MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24, 1596-1599.
81. TerBraak, C.F.J. and Smilauer, P. (1998) CANOCO Reference Manual and User's Guide to Canoco for Windows. Software for Canonical Community Ordination (Version 4). Wageningen: Centre for Biometry.
82. Tripathi, A.K., Verma, S.C. and Ron, E.Z. (2002) Molecular characterization of a salt-tolerant bacterial community in the rice rhizosphere. Res Microbiol 153, 579-584.
83. Tuchman, N.C., Schollett, M.A., Rier, S.T. and Geddes, P. (2006) Differential heterotrophic utilization of organic compounds by diatoms and bacteria under light and dark conditions. Hydrobiologia 561, 167-177.
84. Ulrike, E., Rogall, T., Blocker, H., Emde, M. and Bottger, E.G. (1989) Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA. Nucleic Acids Res 17, 7843-7853.
85. Wang, A.Y., Chen, J. and Crowley, D.E. (2004) Changes in metabolic and structural diversity of a soil bacterial community in response to cadmium toxicity. Biol Fertil Soils 39, 452-456.
86. de Weert, S., Vermeiren, H., Mulders, I.H.M., Kuiper, I., Hendrickx, N., Bloemberg, G.V., Vanderleyden, J., De Mot, R. et al. (2002) Flagella driven chemotaxis towards exudate components is an important trait for tomato root colonization by Pseudomonas fluorescens. Mol Plant Microbe Interact 15, 1173-1180.