Integrated analysis of root microbiomes of soybean and wheat from agricultural fields

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Rascovan, Nicolás ^a   Carbonetto, Belén ^a   Perrig, Diego ^b   Díaz, Marisa ^b   Canciani, Wilter ^b   Abalo, Matías ^b   Alloati, Julieta ^a   González Anta, Gustavo ^b   Vazquez, Martín P ^a  

^a Instituto de Agrobiotecnología de Rosario INDEAR Predio CCT Rosario   (Argentina)

^b Argentina ^*  (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84975479109     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep28084     Document Type: Article

References (78)

1. Raja, N. Biopesticides and biofertilizers: ecofriendly sources for sustainable agriculture. J Biofertil Biopestici 1000e112, 1000e1112 (2013).
2. Evenson, R. E. & Gollin, D. Assessing the Impact of the Green Revolution, 1960 to 2000. Science 300, 758-762 (2003).
3. Conway, G. R. & Pretty, J. N. Unwelcome Harvest: Agriculture and Pollution. (Taylor & Francis, 2013).
4. McGuinness, H. Living Soils: Sustainable Alternatives to Chemical Fertilizers for Developing Countries. (Consumer Policy Institute, Consumers Union, 1993).
5. Altieri, M. A. & Nicholis, C. I. Agroecology and the Search for a Truly Sustainable Agriculture. (United Nations Environmental Programme, Environmental Training Network for Latin America and the Caribbean, 2005).
6. Bhardwaj, D., Ansari, M., Sahoo, R. & Tuteja, N. Biofertilizers function as key player in sustainable agriculture by improving soil fertility, plant tolerance and crop productivity. Microbial Cell Factories 13, 66 (2014).
7. Berendsen, R. L., Pieterse, C. M. J. & Bakker, P. A. H. M. The rhizosphere microbiome and plant health. Trends in plant science 17, 478-486, doi: http://dx.doi.org/10.1016/j.tplants.2012.04.001 (2012).
8. Turner, T., James, E. & Poole, P. The plant microbiome. Genome biology 14, 1-10, doi: 10.1186/gb-2013-14-6-209 (2013).
9. Bais, H. P., Weir, T. L., Perry, L. G., Gilroy, S. & Vivanco, J. M. The role of root exudates in rhizosphere interactions with plants and other organisms. Annual Review of Plant Biology 57, 233-266, doi: 10.1146/annurev.arplant.57.032905.105159 (2006).
10. Moe, L. A. Amino acids in the rhizosphere: From plants to microbes. American Journal of Botany 100, 1692-1705 (2013).
11. Laksmanan, V., Selvaraj, G. & Bais, H. Functional soil microbiome: Belowground solutions to an aboveground problem. Plant physiology (2014).
12. Tkacz, A. & Poole, P. Role of root microbiota in plant productivity. Journal of experimental botany 66, 2167-2175 (2015).
13. De-la-Pena, C. & Loyola-Vargas, V. M. Biotic interactions in the rhizosphere: a diverse cooperative enterprise for plant productivity. 166, 701-719, doi: 10.1104/pp.114.241810 (2014).
14. Schlaeppi, K., Dombrowski, N., Oter, R. G., Ver Loren van Themaat, E. & Schulze-Lefert, P. Quantitative divergence of the bacterial root microbiota in Arabidopsis thaliana relatives. Proceedings of the National Academy of Sciences 111, 585-592 (2014).
15. Lundberg, D. S. et al. Defining the core Arabidopsis thaliana root microbiome. Nature 488, 86-90, doi: 10.1038/nature11237 (2012).
16. Bulgarelli, D. et al. Structure and function of the bacterial root microbiota in wild and domesticated barley. Cell host & microbe 17, 392-403, doi: 10.1016/j.chom.2015.01.011 (2015).
17. Bulgarelli, D. et al. Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488, 91-95, doi: 10.1038/nature11336 (2012).
18. Mendes, L. W., Kuramae, E. E., Navarrete, A. A., van Veen, J. A. & Tsai, S. M. Taxonomical and functional microbial community selection in soybean rhizosphere. The ISME journal 8, 1577-1587, doi: 10.1038/ismej.2014.17 (2014).
19. Aira, M., Gómez-Brandón, M., Lazcano, C., Bååth, E. & Domínguez, J. Plant genotype strongly modifies the structure and growth of maize rhizosphere microbial communities. Soil Biology and Biochemistry 42, 2276-2281, doi: http://dx.doi.org/10.1016/j. soilbio.2010.08.029 (2010).
20. De-la-Peña, C. & Loyola-Vargas, V. M. Biotic Interactions in the Rhizosphere: A Diverse Cooperative Enterprise for Plant Productivity. Plant physiology 166, 701-719 (2014).
21. Blee, K., Hein, J. & Wolfe, G. V. In Molecular Microbial Ecology of the Rhizosphere 265-270 (John Wiley & Sons, Inc, 2013).
22. Food and Agriculture Organization of the United Nations. Statistic Division (FAOSTAT), (2015). Available at: http://faostat3.fao.org/. (Accessed: May 2016).
23. Food and Agriculture Organization of the United Nations. World Food Situation - FAO Cereal Supply and Demand Brief, (2016). Available at: http://www.fao.org/worldfoodsituation/csdb/en/. (Accessed: May 2016).
24. Global Soybean Production. Global Soybean Production, (2016). Available at: http://www.globalsoybeanproduction.com/. (Accessed: May 2016).
25. Peoples, M. B., Herridge, D. F. & Ladha, J. K. Biological nitrogen fixation: An efficient source of nitrogen for sustainable agricultural production? Plant and Soil 174, 3-28, doi: 10.1007/BF00032239.
26. Franche, C., Lindström, K. & Elmerich, C. Nitrogen-fixing bacteria associated with leguminous and non-leguminous plants. Plant and Soil 321, 35-59, doi: 10.1007/s11104-008-9833-8 (2008).
27. Kuzyakov, Y. & Domanski, G. Carbon input by plants into the soil. Review. Journal of Plant Nutrition and Soil Science 163, 421-431, doi: 10.1002/1522-2624(200008)163:4< 421::AID-JPLN421> 3.0.CO;2-R (2000).
28. Coleman-Derr, D. & Tringe, S. G. Building the crops of tomorrow: advantages of symbiont-based approaches to improving abiotic stress tolerance. Frontiers in microbiology 5 (2014).
29. Herrmann, L. & Lesueur, D. Challenges of formulation and quality of biofertilizers for successful inoculation. Applied microbiology and biotechnology 97, 8859-8873, doi: 10.1007/s00253-013-5228-8 (2013).
30. Kloepper, J. W., Lifshitz, R. & Zablotowicz, R. M. Free-living bacterial inocula for enhancing crop productivity. Trends in Biotechnology 7, 39-44, doi: http://dx.doi.org/10.1016/0167-7799(89)90057-7 (1989).
31. Nelson, D. W. et al. In Methods of Soil Analysis. Part 3-Chemical Methods SSSA Book Series 961-1010 (Soil Science Society of America, American Society of Agronomy, 1996).
32. Bremner, J. M. E., Sparks, D. L. E., Page, A. L. E., Helmke, P. A. E. & Loeppert, R. H. In Methods of Soil Analysis. Part 3-Chemical Methods SSSA Book Series 1085-1121 (Soil Science Society of America, American Society of Agronomy, 1996).
33. Kuo, S. E., Sparks, D. L. E., Page, A. L. E., Helmke, P. A. E. & H, L. R. In Methods of Soil Analysis. Part 3-Chemical Methods SSSA Book Series 869-919 (Soil Science Society of America, American Society of Agronomy, 1996).
34. Rhoades, J. D. E., Sparks, D. L. E., Page, A. L. E., Helmke, P. A. E. & H, L. R. In Methods of Soil Analysis. Part 3-Chemical Methods SSSA Book Series 417-435 (Soil Science Society of America, American Society of Agronomy, 1996).
35. Gee, G. W. & Bauder, J. W. E. K. A. In Methods of Soil Analysis: Part 1-Physical and Mineralogical Methods SSSA Book Series 383-411 (Soil Science Society of America, American Society of Agronomy, 1986).
36. Vaerewijck, M. J. M. et al. Occurrence of Bacillus sporothermodurans and other aerobic spore-forming species in feed concentrate for dairy cattle. J. Appl. Microbiol 91, 1074-1084 (2001).
37. Cho, J.-C. & Tiedje, J. M. Biogeography and Degree of Endemicity of Fluorescent Pseudomonas Strains in Soil. Applied and environmental microbiology 66, 5448-5456 (2000).
38. Döbereiner, J. In Methods in Applied Soil Microbiology and Biochemistry (eds K. Alef & P. Nannipieri) 134-141 (Academic Press, 1995).
39. Bric, J. M., Bostock, R. M. & Silverstone, S. E. Rapid in situ assay for indoleacetic Acid production by bacteria immobilized on a nitrocellulose membrane. Applied and environmental microbiology 57, 535-538 (1991).
40. Glick, B. R., Karaturovíc, D. M. & Newell, P. C. A novel procedure for rapid isolation of plant growth promoting pseudomonads. Canadian journal of microbiology 41, 533-536, doi: 10.1139/m95-070 (1995).
41. Dell'Amico, E., Cavalca, L. & Andreoni, V. Analysis of rhizobacterial communities in perennial Graminaceae from polluted water meadow soil, and screening of metal-resistant, potentially plant growth-promoting bacteria. FEMS Microbiol Ecol 52, 153-162, doi: 10.1016/j.femsec.2004.11.005 (2005).
42. Döbereiner, J. Isolation and identification of root associated diazotrophs. Plant and Soil 110, 207-212, doi: 10.1007/BF02226800 (1988).
43. Baldani, J. I., Reis, V. M., Videira, S. S., Boddey, L. H. & Baldani, V. L. D. The art of isolating nitrogen-fixing bacteria from nonleguminous plants using N-free semi-solid media: a practical guide for microbiologists. Plant Soil 384, 413-431, doi: 10.1007/s11104-014-2186-6 (2014).
44. Katznelson, H., Peterson, E. A. & Rouatt, J. W. Phosphate-dissolving microorganisms on seed and in the root zone of plants. Canadian Journal of Botany 40, 1181-1186, doi: 10.1139/b62-108 (1962).
45. Caporaso, J. G. et al. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proceedings of the National Academy of Sciences of the United States of America 108 Suppl 1, 4516-4522, doi: 10.1073/pnas.1000080107 (2011).
46. Rascovan, N. et al. The PAMPA datasets: a metagenomic survey of microbial communities in Argentinean pampean soils. Microbiome 1, 21 (2013).
47. Caporaso, G. J., Kuczynski, J., Stombaugh, J., Bittinger, K. & Bushman, F. D. QIIME allows analysis of high-throughput community sequencing data. Nature methods, 335-336 (2010).
48. Caporaso, J. G., Lauber, C. L., Walters, W. A., Berg Lyons, D. & Huntley, J. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. The ISME journal, 1621-1624 (2012).
49. Kuczynski, J. et al. Microbial community resemblance methods differ in their ability to detect biologically relevant patterns. Nature methods 7, 813-819, doi: 10.1038/nmeth.1499 (2010).
50. Clarke, K. R. & Ainsworth, M. A method of linking multivariate community structure to environmental variables. Marine Ecologyprogress Series 92, 205-219, doi: 10.3354/meps092205 (1993).
51. Li, X. et al. Shifts of functional gene representation in wheat rhizosphere microbial communities under elevated ozone. The ISME journal 7, 660-671, doi: 10.1038/ismej.2012.120 (2013).
52. Lauber, C. L., Hamady, M., Knight, R. & Fierer, N. Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Applied and environmental microbiology, 11-20 (2009).
53. Schloss, P. D. & Handelsman, J. Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Applied and environmental microbiology 71, 1501-1506, doi: 10.1128/AEM.71.3.1501-1506.2005 (2005).
54. Glick, B. R. Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiological Research 169, 30-39, doi: http://dx.doi.org/10.1016/j.micres.2013.09.009 (2014).
55. Gaiero, J. R. et al. Inside the root microbiome: Bacterial root endophytes and plant growth promotion. American journal of botany 100, 1738-1750 (2013).
56. Glick, B. R. Plant Growth-Promoting Bacteria: Mechanisms and Applications. Scientifica 2012, 15, doi: 10.6064/2012/963401 (2012).
57. Pérez-Montaño, F. et al. Plant growth promotion in cereal and leguminous agricultural important plants: From microorganism capacities to crop production. Microbiological research 169, 325-336, doi: http://dx.doi.org/10.1016/j.micres.2013.09.011 (2014).
58. Sachdev, D. P., Chaudhari, H. G., Kasture, V. M., Dhavale, D. D. & Chopade, B. A. Isolation and characterization of indole acetic acid (IAA) producing Klebsiella pneumoniae strains from rhizosphere of wheat (Triticum aestivum) and their effect on plant growth. Indian journal of experimental biology 47, 993-1000 (2009).
59. Bergey, D. H. et al. Bergey's manual of systematic bacteriology. 2nd edn, (Springer, 2001).
60. Rich, S. M. & Watt, M. Soil conditions and cereal root system architecture: review and considerations for linking Darwin and Weaver. Journal of experimental botany 64, 1193-1208, doi: 10.1093/jxb/ert043 (2013).
61. Gaiero, J. R. et al. Inside the root microbiome: bacterial root endophytes and plant growth promotion. American journal of botany 100, 1738-1750, doi: 10.3732/ajb.1200572 (2013).
62. Berg, G. & Smalla, K. Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS microbiology ecology 68, 1-13, doi: 10.1111/j.1574-6941.2009.00654.x (2009).
63. Santos-Gonzalez, J. C., Nallanchakravarthula, S., Alstrom, S. & Finlay, R. D. Soil, but not cultivar, shapes the structure of arbuscular mycorrhizal fungal assemblages associated with strawberry. Microbial ecology 62, 25-35, doi: 10.1007/s00248-011-9834-7 (2011).
64. Bala, A., Murphy, P. & Giller, K. E. Distribution and diversity of rhizobia nodulating agroforestry legumes in soils from three continents in the tropics. Molecular ecology 12, 917-929 (2003).
65. Long, H. H., Sonntag, D. G., Schmidt, D. D. & Baldwin, I. T. The structure of the culturable root bacterial endophyte community of Nicotiana attenuata is organized by soil composition and host plant ethylene production and perception. The New phytologist 185, 554-567, doi: 10.1111/j.1469-8137.2009.03079.x (2010).
66. Peiffer, J. A. et al. Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proceedings of the National Academy of Sciences of the United States of America 110, 6548-6553, doi: 10.1073/pnas.1302837110 (2013).
67. Chen, L., Dodd, I. C., Theobald, J. C., Belimov, A. A. & Davies, W. J. The rhizobacterium Variovorax paradoxus 5C-2, containing ACC deaminase, promotes growth and development of Arabidopsis thaliana via an ethylene-dependent pathway. Journal of experimental botany 64, 1565-1573, doi: 10.1093/jxb/ert031 (2013).
68. Vacheron, J. et al. Plant growth-promoting rhizobacteria and root system functioning. Frontiers in plant science 4, 356, doi: 10.3389/fpls.2013.00356 (2013).
69. Wang, H., Wang, S. D., Jiang, Y., Zhao, S. J. & Chen, W. X. Diversity of rhizosphere bacteria associated with different soybean cultivars in two soil conditions. Soil Science and Plant Nutrition 60, 630-639, doi: 10.1080/00380768.2014.942212 (2014).
70. Carbonetto, B., Rascovan, N., Alvarez, R., Mentaberry, A. & Vazquez, M. P. Structure, composition and metagenomic profile of soil microbiomes associated to agricultural land use and tillage systems in Argentine Pampas. PloS one 9, e99949, doi: 10.1371/journal. pone.0099949 (2014).
71. Hinsinger, P., Plassard, C., Tang, C. & Jaillard, B. Origins of root-mediated pH changes in the rhizosphere and their responses to environmental constraints: A review. Plant and Soil 248, 43-59, doi: 10.1023/A:1022371130939.
72. Mantelin, S. & Touraine, B. Plant growth-promoting bacteria and nitrate availability: impacts on root development and nitrate uptake. Journal of experimental botany 55, 27-34, doi: 10.1093/jxb/erh010 (2004).
73. Zhang, H., Jennings, A., Barlow, P. W. & Forde, B. G. Dual pathways for regulation of root branching by nitrate. Proceedings of the National Academy of Sciences of the United States of America 96, 6529-6534 (1999).
74. Zhang, H. & Forde, B. G. An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279, 407-409 (1998).
75. Robinson, D., Linehan, D. J. & Gordon, D. C. Capture of nitrate from soil by wheat in relation to root length, nitrogen inflow and availability. New Phytologist 128, 297-305, doi: 10.1111/j.1469-8137.1994.tb04013.x (1994).
76. Brown, T. N., Kulasiri, D. & Gaunt, R. E. A root-morphology based simulation for plant/soil microbial ecosystem modelling. Ecological Modelling 99, 275-287, doi: http://dx.doi.org/10.1016/S0304-3800(97)01961-3 (1997).
77. Szoboszlay, M. et al. Comparison of root system architecture and rhizosphere microbial communities of Balsas teosinte and domesticated corn cultivars. Soil Biology and Biochemistry 80, 34-44, doi: http://dx.doi.org/10.1016/j.soilbio.2014.09.001 (2015).
78. Cheng, Y., Jiang, Y., Wu, Y., Valentine, T. A. & Li, H. Soil Nitrogen Status Modifies Rice Root Response to Nematode-Bacteria Interactions in the Rhizosphere. PloS one 11, e0148021, doi: 10.1371/journal.pone.0148021 (2016).