Biology and Fertility of Soils

, Volume 48, Issue 5, pp 489–499 | Cite as

Manipulating the soil microbiome to increase soil health and plant fertility

  • Jacqueline M. Chaparro
  • Amy M. Sheflin
  • Daniel K. Manter
  • Jorge M. Vivanco
Review

Abstract

A variety of soil factors are known to increase nutrient availability and plant productivity. The most influential might be the organisms comprising the soil microbial community of the rhizosphere, which is the soil surrounding the roots of plants where complex interactions occur between the roots, soil, and microorganisms. Root exudates act as substrates and signaling molecules for microbes creating a complex and interwoven relationship between plants and the microbiome. While individual microorganisms such as endophytes, symbionts, pathogens, and plant growth promoting rhizobacteria are increasingly featured in the literature, the larger community of soil microorganisms, or soil microbiome, may have more far-reaching effects. Each microorganism functions in coordination with the overall soil microbiome to influence plant health and crop productivity. Increasing evidence indicates that plants can shape the soil microbiome through the secretion of root exudates. The molecular communication fluctuates according to the plant development stage, proximity to neighboring species, management techniques, and many other factors. This review seeks to summarize the current knowledge on this topic.

Keywords

Microbiome Root exudates Plant growth promoting rhizobacteria (PGPRs) 

References

  1. Adesemoye AO, Torbert HA, Kloepper JW (2009) Plant growth-promoting rhizobacteria allow reduced application rates of chemical fertilizers. Microb Ecol 58:921–929. doi:10.1007/s00248-009-9531-y PubMedCrossRefGoogle Scholar
  2. Ahemad M, Khan MS (2011) Plant growth promoting rhizobacteria: recent advancements. Insight Microbiol 1:39–54. doi:10.5567/IMICRO-IK.2011.39.54 CrossRefGoogle Scholar
  3. Andren O, Balandreau J (1999) Biodiversity and soil functioning—from black box to can of worms? Appl Soil Ecol 13:105–108CrossRefGoogle Scholar
  4. Babalola OO (2010) Beneficial bacteria of agricultural importance. Biotechnol Lett 32:1559–1570PubMedCrossRefGoogle Scholar
  5. Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant Cell Environ 32:666–681PubMedCrossRefGoogle Scholar
  6. Badri DV, Loyola-Vargas VM, Broeckling CD, De-la-Pena C, Jasinski M, Santelia D, Martinoia E, Sumner LW, Banta LM, Stermitz F, Vivanco JM (2008) Altered profile of secondary metabolites in the root exudates of Arabidopsis ATP-binding cassette transporter mutants. Plant Physiol 146:762–771PubMedCrossRefGoogle Scholar
  7. Badri DV, Quintana N, El Kassis EG, Kim HK, Choi YH, Sugiyama A, Verpoorte R, Martinoia E, Manter DK, Vivanco JM (2009a) An ABC transporter mutation alters root exudation of phytochemicals that provoke an overhaul of natural soil microbiota. Plant Physiol 151:2006–2017PubMedCrossRefGoogle Scholar
  8. Badri DV, Weir TL, van der Lelie D, Vivanco JM (2009b) Rhizosphere chemical dialogues: plant–microbe interactions. Curr Opin Biotechnol 20:642–650PubMedCrossRefGoogle Scholar
  9. Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266PubMedCrossRefGoogle Scholar
  10. Balser TC, Kinzig AP, Firestone MK (2002) Linking soil microbial communities and ecosystem functioning. In: Kinzig AP, Pacala SW, Tilman D (eds) The functional consequences of biodiversity: Empirical progress and theoretical extensions. Princeton University Press, Princeton, pp 265–293Google Scholar
  11. Bardgett RD, Shine A (1999) Linkages between plant litter diversity, soil microbial biomass and ecosystem function in temperate grasslands. Soil Biol Biochem 31:317–321CrossRefGoogle Scholar
  12. Barea JM, Azcon R, Azcon-Aguilar C (2002) Mycorrhizosphere interactions to improve plant fitness and soil quality. Anton Leeuw Int J G 81:343–351CrossRefGoogle Scholar
  13. Barret M, Morrissey JP, O'Gara F (2011) Functional genomics analysis of plant growth-promoting rhizobacterial traits involved in rhizosphere competence. Biol Fertil Soils 47:729–743CrossRefGoogle Scholar
  14. Berg G (2009) Plant–microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture. Appl Microbiol Biotechnol 84:11–18PubMedCrossRefGoogle Scholar
  15. Berg G, Smalla K (2009) Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol Ecol 68:1–13PubMedCrossRefGoogle Scholar
  16. Bernard E, Larkin RP, Tavantzis S, Erich MS, Alyokhin A, Sewell G, Lannan A, Gross SD (2012) Compost, rapeseed rotation, and biocontrol agents significantly impact soil microbial communities in organic and conventional potato production systems. App Soil Ecol 52:29CrossRefGoogle Scholar
  17. Bertin C, Yang X, Weston LA (2003) The role of root exudates and allelochemicals in the rhizosphere. Plant Soil 256:67–83CrossRefGoogle Scholar
  18. Bonkowski M, Roy J (2005) Soil microbial diversity and soil functioning affect competition among grasses in experimental microcosms. Oecologia 143:232–240PubMedCrossRefGoogle Scholar
  19. Broeckling CD, Broz AK, Bergelson J, Manter DK, Vivanco JM (2008) Root exudates regulate soil fungal community composition and diversity. Appl Environ Microbiol 74:738–744PubMedCrossRefGoogle Scholar
  20. Broz AK, Manter DK, Vivanco JM (2007) Soil fungal abundance and diversity: another victim of the invasive plant Centaurea maculosa. ISME J 1:763–765PubMedCrossRefGoogle Scholar
  21. Brussaard L, de Ruiter PC, Brown GG (2007) Soil biodiversity for agricultural sustainability. Agr Ecosyst Environ 121:233–244CrossRefGoogle Scholar
  22. Chithrashree UAC, Nayaka SC, Reddy MS, Srinivas C (2011) Plant growth-promoting rhizobacteria mediate induced systemic resistance in rice against bacterial leaf blight caused by Xanthomonas oryzae pv. oryzae. Biol Control 59:114–122CrossRefGoogle Scholar
  23. Conrath U, Loon LCV (2009) Priming of induced plant defense responses. In: Van Loon LC (ed) Advances in botanical research, vol 51. Academic Press, London, pp 361–395Google Scholar
  24. Crowder DW, Northfield TD, Strand MR, Snyder WE (2010) Organic agriculture promotes evenness and natural pest control. Nature 466:109–112PubMedCrossRefGoogle Scholar
  25. Cummings SP (2009) The application of plant growth promoting rhizobacteria (PGPR) in low input and organic cultivation of graminaceous crops; potential and problems. Environ Biotechnol 5:43–50Google Scholar
  26. de Ridder-Duine AS, Kowalchuk GA, Klein Gunnewiek PJA, Smant W, van Veen JA, de Boer W (2005) Rhizosphere bacterial community composition in natural stands of Carex arenaria (sand sedge) is determined by bulk soil community composition. Soil Biol Biochem 37:349–357CrossRefGoogle Scholar
  27. De Vleesschauwer D, Höfte M (2009) Rhizobacteria-induced systemic resistance. In: Van Loon LC (ed) Advances in botanical research, vol 51. Elsevier, Burlington, pp 223–281. doi:10.1016/S0065-2296(09)51006-3 Google Scholar
  28. de Weert S, Vermeiren H, Mulders IHM, Kuiper I, Hendrickx N, Bloemberg GV, Vanderleyden J, De Mot R, Lugtenberg BJJ (2002) Flagella-driven chemotaxis towards exudate components is an important trait for tomato root colonization by Pseudomonas fluorescens. Mol Plant Microbe Interact 15:1173–1180PubMedCrossRefGoogle Scholar
  29. Degens BP, Schipper LA, Sparling GP, Vojvodic-Vukovic M (2000) Decreases in organic C reserves in soils can reduce the catabolic diversity of soil microbial communities. Soil Biol Biochem 32:189–196CrossRefGoogle Scholar
  30. Degens BP, Schipper LA, Sparling GP, Duncan LC (2001) Is the microbial community in a soil with reduced catabolic diversity less resistant to stress or disturbance? Soil Biol Biochem 33:1143–1153CrossRefGoogle Scholar
  31. De-la-Pena C, Badri DV, Lei Z, Watson BS, Brandao MM, Silva-Filho MC, Sumner LW, Vivanco JM (2010) Root secretion of defense-related proteins is development-dependent and correlated with flowering time. J Biol Chem 285:30654–30665PubMedCrossRefGoogle Scholar
  32. Dennis PG, Miller AJ, Hirsch PR (2010) Are root exudates more important than other sources of rhizodeposits in structuring rhizosphere bacterial communities? FEMS Microbiol Ecol 72:313–327PubMedCrossRefGoogle Scholar
  33. Dimkpa C, Weinand T, Asch F (2009) Plant–rhizobacteria interactions alleviate abiotic stress conditions. Plant Cell Environ 32:1682–1694PubMedCrossRefGoogle Scholar
  34. Donnelly A, Craigon J, Black CR, Colls JJ, Landon G (2001) Elevated CO2 increases biomass and tuber yield in potato even at high ozone concentrations. New Phytol 149:265–274CrossRefGoogle Scholar
  35. Doran JW, Safley W (1997) Defining and assessing soil health and sustainable productivity. In: Gupta VVSR, Pankhurst C, Doube BM (eds) Biological indicators of soil health. CAB International, Wallingford, pp 1–28Google Scholar
  36. Elliot LF, Lynch JM (1994) Biodiversity and soil resilience. In: Greenland DJ, Szabolos I (eds) Soil resilience and sustainable land use, vol 31, CAB International. Wallingford, UK, pp 353–364Google Scholar
  37. Esitken A (2011) Use of plant growth promoting rhizobacteria in horticultural plants. In: Maheshwari DK (ed) Bacteria in agrobiology: Crop ecosystems. Springer, Berlin, pp 189–235CrossRefGoogle Scholar
  38. Faoro H, Alves AC, Souza EM, Rigo LU, Cruz LM, Al-Janabi SM, Monteiro RA, Baura VA, Pedrosa FO (2010) Influence of soil characteristics on the diversity of bacteria in the Southern Brazilian Atlantic Forest. App Environ Microb 76:4744–4749CrossRefGoogle Scholar
  39. Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci U S A 103:626–631PubMedCrossRefGoogle Scholar
  40. Fitzsimons MS, Miller RM (2010) The importance of soil microorganisms for maintaining diverse plant communities in tallgrass Prairie. Am J Bot 97:1937–1943PubMedCrossRefGoogle Scholar
  41. Fliessbach A, Winkler M, Lutz MP, Oberholzer HR, Mader P (2009) Soil amendment with Pseudomonas fluorescens CHA0: lasting effects on soil biological properties in soils low in microbial biomass and activity. Microb Ecol 57:611–623PubMedCrossRefGoogle Scholar
  42. Flores HE, Vivanco JM, Loyola-Vargas VM (1999) 'Radicle' biochemistry: the biology of root-specific metabolism. Trends Plant Sci 4:220–226PubMedCrossRefGoogle Scholar
  43. Frey SD, Knorr M, Parrent JL, Simpson RT (2004) Chronic nitrogen enrichment affects the structure and function of the soil microbial community in temperate hardwood and pine forests. For Ecol Manag 196:159–171CrossRefGoogle Scholar
  44. Garbeva P, van Veen JA, van Elsas JD (2004) Microbial diversity in soil: selection microbial populations by plant and soil type and implications for disease suppressiveness. Annu Rev Phytopathol 42:243–270PubMedCrossRefGoogle Scholar
  45. Girvan MS, Bullimore J, Pretty JN, Osborn AM, Ball AS (2003) Soil type is the primary determinant of the composition of the total and active bacterial communities in arable soils. Appl Environ Microbiol 69:1800–1809PubMedCrossRefGoogle Scholar
  46. Godfray HC, Beddington JR, Crute IR, Haddad L, Lawrence D, Muir JF, Pretty J, Robinson S, Thomas SM, Toulmin C (2010) Food security: the challenge of feeding 9 billion people. Science 327:812–818PubMedCrossRefGoogle Scholar
  47. Gold MV (1995) Organic production/organic food: information access tools. USDA National Agricultural LibraryGoogle Scholar
  48. Guiñazú LB, Andrés JA, Del Papa MF, Pistorio M, Rosas SB (2009) Response of alfalfa (Medicago sativa L.) to single and mixed inoculation with phosphate-solubilizing bacteria and Sinorhizobium meliloti. Biol Fertil Soils 46:185–190. doi:10.1007/s00374-009-0408-5 CrossRefGoogle Scholar
  49. Hamilton EW, Frank DA (2001) Can plants stimulate soil microbes and their own nutrient supply? Evidence from a grazing tolerant grass. Ecology 82:2397–2402CrossRefGoogle Scholar
  50. Hayat R, Ali S, Amara U, Khalid R, Ahmed I (2010) Soil beneficial bacteria and their role in plant growth promotion: a review. Ann Microbiol 60:579–598CrossRefGoogle Scholar
  51. Hernandez M, Chailloux M (2004) Las micorrizas arbusculares y las bacterias rizosfericas como alternativa a la nutricion mineral del tomate. Cultivos Tropicales 25:5–16Google Scholar
  52. Hierro JL, Maron JL, Callaway RM (2005) A biogeographical approach to plant invasions: the importance of studying exotics in their introduced and native range. J Ecol 93:5–15CrossRefGoogle Scholar
  53. Hillebrand H, Bennett DM, Cadotte MW (2008) Consequences of dominance: a review of evenness effects on local and regional ecosystem processes. Ecology 89:1510–1520PubMedCrossRefGoogle Scholar
  54. Horiuchi J, Prithiviraj B, Bais HP, Kimball BA, Vivanco JM (2005) Soil nematodes mediate positive interactions between legume plants and rhizobium bacteria. Planta 222:848–857PubMedCrossRefGoogle Scholar
  55. Janvier C, Villeneuve F, Alabouvette C, Edel-Hermann V, Mateille T, Steinberg C (2007) Soil health through soil disease suppression: which strategy from descriptors to indicators? Soil Biol Biochem 39:1CrossRefGoogle Scholar
  56. Jetiyanon K, Kloepper JW (2002) Mixtures of plant growth-promoting rhizobacteria for induction of systemic resistance against multiple plant diseases. Biol Control 24:285–291CrossRefGoogle Scholar
  57. Jonsson LM, Nilsson M-C, Wardle DA, Zackrisson O (2001) Context dependent effects of Ectomycorrhizal species richness on tree seedling productivity. Oikos 93:353–364CrossRefGoogle Scholar
  58. Karlen DL, Mausbach MJ, Doran JW, Cline RG, Harris RF, Schuman GE (1997) Soil quality: a concept, definition, and framework for evaluation (A Guest Editorial). Soil Sci Soc Am J 61:4–10. doi:10.2136/sssaj1997.03615995006100010001x CrossRefGoogle Scholar
  59. Kaymak HC (2011) Plant growth and health promoting bacteria. In: Maheshwari DK (ed) Microbiology Monographs, vol 18. Springer-Verlag, Berlin, pp 45–79. doi:10.1007/978-3-642-13612-2_3 Google Scholar
  60. Kinsella K, Schulthess CP, Morris TF, Stuart JD (2009) Rapid quantification of Bacillus subtilis antibiotics in the rhizosphere. Soil Biol Biochem 41:374–379CrossRefGoogle Scholar
  61. Kirankumar R, Jagadeesh KS, Krishnaraj PU, Patil MS (2008) Enhanced growth promotion of tomato and nutrient uptake by plant growth promoting rhizobacterial isolates in presence of tobacco mosaic virus pathogen. Karnataka J Agric Sci 21:309–311Google Scholar
  62. Klironomos JN (2002) Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417:67–70PubMedCrossRefGoogle Scholar
  63. Knops JMH, Tilman D, Haddad NM, Naeem S, Mitchell CE, Haarstad J, Ritchie ME, Howe KM, Reich PB, Siemann E, Groth J (1999) Effects of plant species richness on invasion dynamics, disease outbreaks, insect abundances and diversity. Ecol Lett 2:286–293CrossRefGoogle Scholar
  64. Krauss J, Gallenberger I, Steffan-Dewenter I (2011) Decreased functional diversity and biological pest control in conventional compared to organic crop fields. PLoS One 6:e19502PubMedCrossRefGoogle Scholar
  65. Lamb E, Kennedy N, Siciliano S (2011) Effects of plant species richness and evenness on soil microbial community diversity and function. Plant Soil 338:483–495CrossRefGoogle Scholar
  66. Lambers H, Mougel C, Jaillard B, Hinsinger P (2009) Plant–microbe–soil interactions in the rhizosphere: an evolutionary perspective. Plant Soil 321:83–115CrossRefGoogle Scholar
  67. Lau JA, Lennon JT (2011) Evolutionary ecology of plant–microbe interactions: soil microbial structure alters selection on plant traits. New Phytol 192:215–224PubMedCrossRefGoogle Scholar
  68. Lauber CL, Strickland MS, Bradford MA, Fierer N (2008) The influence of soil properties on the structure of bacterial and fungal communities across land-use types. Soil Biol Biochem 40:2407–2415CrossRefGoogle Scholar
  69. Lim JH, Kim SD (2009) Synergistic plant growth promotion by the indigenous auxins-producing PGPR Bacillus subtilis AH18 and Bacillus licheniforims K11. J Korean Soc Appl Bi 52:531–538CrossRefGoogle Scholar
  70. Liu B, Tu C, Hu S, Gumpertz M, Ristaino JB (2007) Effect of organic, sustainable, and conventional management strategies in grower fields on soil physical, chemical, and biological factors and the incidence of Southern blight. Appl Soil Ecol 37:202–214CrossRefGoogle Scholar
  71. Lucas JA (2011) Advances in plant disease and pest management. J Agr Sci 149:91–114. doi:10.1017/S0021859610000997 CrossRefGoogle Scholar
  72. Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Annu Rev Microbiol 63:541–556PubMedCrossRefGoogle Scholar
  73. Lumini E, Vallino M, Alguacil MM, Romani M, Bianciotto V (2011) Different farming and water regimes in Italian rice fields affect arbuscular mycorrhizal fungal soil communities. Ecol Appl 21:1696–1707PubMedCrossRefGoogle Scholar
  74. Maherali H, Klironomos JN (2007) Influence of phylogeny on fungal community assembly and ecosystem functioning. Science 316:1746–1748PubMedCrossRefGoogle Scholar
  75. Maheshwari DK (ed) (2011) Plant growth and health promoting bacteria, vol 18. Microbiology monographs. Springer, MunsterGoogle Scholar
  76. Malajczuk N (1983) Microbial antagonism to Phytophthora. In: Erwin DC, Bartnicki-Garcia S, Tsao PH (eds) Phytophthora its biology, taxonomy, ecology, and pathology. American Phytopathological Society, St. Paul, pp 197–218Google Scholar
  77. Mangla S, Callaway RM (2008) Exotic invasive plant accumulates native soil pathogens which inhibit native plants. J Ecol 96:58. doi:10.1111/j.1365-2745.2007.01312.x Google Scholar
  78. Mark G, Morrissey JP, Higgins P, O'Gara F (2006) Molecular-based strategies to exploit Pseudomonas biocontrol strains for environmental biotechnology applications. FEMS Microbiol Ecol 56:167–177PubMedCrossRefGoogle Scholar
  79. Markowitz VM, Ivanova NN, Szeto E, Palaniappan K, Chu K, Dalevi D, Chen IM, Grechkin Y, Dubchak I, Anderson I, Lykidis A, Mavromatis K, Hugenholtz P, Kyrpides NC (2008) IMG/M: a data management and analysis system for metagenomes. Nucleic Acids Res 36:D534–538PubMedCrossRefGoogle Scholar
  80. Maron JL, Marler M, Klironomos JN, Cleveland CC (2010) Soil fungal pathogens and the relationship between plant diversity and productivity. Ecol Lett 14:36–41PubMedCrossRefGoogle Scholar
  81. Mendes R, Kruijt M, de Bruijn I, Dekkers E, van der Voort M, Schneider JHM, Piceno YM, DeSantis TZ, Andersen GL, Bakker PAHM, Raaijmakers JM (2011) Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332:1097–1100. doi:10.1126/science.1203980 PubMedCrossRefGoogle Scholar
  82. Micallef SA, Shiaris MP, Colon-Carmona A (2009) Influence of Arabidopsis thaliana accessions on rhizobacterial communities and natural variation in root exudates. J Exp Bot 60:1729–1742. doi:10.1093/jxb/erp053 PubMedCrossRefGoogle Scholar
  83. Morales SE, Holben WE (2011) Linking bacterial identities and ecosystem processes: can ‘omic’ analyses be more than the sum of their parts? FEMS Microbiol Ecol 75:2PubMedCrossRefGoogle Scholar
  84. Morrissey JP, Dow JM, Mark GL, O'Gara F (2004) Are microbes at the root of a solution to world food production? Rational exploitation of interactions between microbes and plants can help to transform agriculture. EMBO Rep 5:922–926PubMedCrossRefGoogle Scholar
  85. Naeem S, Knops JMH, Tilman D, Howe KM, Kennedy T, Gale S (2000) Plant diversity increases resistance to invasion in the absence of covarying extrinsic factors. Oikos 91:97–108CrossRefGoogle Scholar
  86. Nannipieri P, Ascher J, Ceccherini MT, Landi L, Pietramellara G, Renella G (2003) Microbial diversity and soil functions. Eur J Soil Sci 54:655–670CrossRefGoogle Scholar
  87. Nannipieri P, Ascher J, Ceccherini MT, Landi L, Pietramellara G, Renella G, Valori F (2008) Effects of root exudates in microbial diversity and activity in rhizosphere soils. In: Nautiyal CS, Dion P (eds) Molecular mechanisms of plant and microbe coexistence, vol 15, Soil Biology. Springer-Verlag, Berlin, pp 339–365CrossRefGoogle Scholar
  88. Nee S (2004) More than meets the eye. Nature 429:804–805PubMedCrossRefGoogle Scholar
  89. Neuman G, Romheld V (2007) The release of root exudates as affected by the plant plysiological status. In: Pinton R, Varanini Z, Nannipieri P (eds) The rhizosphere biochemistry and organic substances at the soil-plant interface. CRC, Boca Raton, pp 23–72CrossRefGoogle Scholar
  90. Nihorimbere V, Ongena M, Smargiassi M, Thonart P (2011) Beneficial effect of the rhizosphere microbial community for plant growth and health. Biotechnol Agron Soc 15:327–337Google Scholar
  91. Ochiai N, Powelson M, Crowe F, Dick R (2008) Green manure effects on soil quality in relation to suppression of Verticillium wilt of potatoes. Biol Fertil Soils 44:1013–1023CrossRefGoogle Scholar
  92. Okubara PA, Bonsall RF (2008) Accumulation of Pseudomonas-derived 2,4-diacetylphloroglucinol on wheat seedling roots is influenced by host cultivar. Biol Control 46:322–331CrossRefGoogle Scholar
  93. Pérez-Piqueres A, Edel-Hermann V, Alabouvette C, Steinberg C (2006) Response of soil microbial communities to compost amendments. Soil Biol Biochem 38:460–470CrossRefGoogle Scholar
  94. Perry LG, Alfored ER, Horiuchi J, Paschke MW, Vivanco JM (2007) Chemical signals in the rhizosphere: root-root and root-microbe communication. In: Pinton R, Varanini Z, Nannipieri P (eds) The rhizosphere biochemistry and organic substances at the soil–plant interface, 2nd edn. CRC Press, Boca Raton, pp 297–330Google Scholar
  95. Postma J, Schilder MT, Bloem J, van Leeuwen-Haagsma WK (2008) Soil suppressiveness and functional diversity of the soil microflora in organic farming systems. Soil Biol Biochem 40:2394–2406CrossRefGoogle Scholar
  96. Pugliese M, Liu BP, Gullino ML, Garibaldi A (2011) Microbial enrichment of compost with biological control agents to enhance suppressiveness to four soil-borne diseases in greenhouse. J Plant Dis Protect 118:45–50Google Scholar
  97. Raaijmakers JM, Weller DM (1998) Natural plant protection by 2,4-diacetylphloroglucinol-producing Pseudomonas spp. in take-all decline soils. Mol Plant Microbe Interact 11:144–152CrossRefGoogle Scholar
  98. Raaijmakers JM, Weller DM, Thomashow LS (1997) Frequency of antibiotic-producing Pseudomonas spp. in natural environments. Appl Environ Microbiol 63:881–887PubMedGoogle Scholar
  99. Ramos Solano B, Barriuso Maicas J, Pereyra de la Iglesia MT, Domenech J, Gutierrez Manero FJ (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. doi:doi:10.1094/PHYTO-98-4-0451 PubMedCrossRefGoogle Scholar
  100. Reeve JR, Schadt CW, Carpenter-Boggs L, Kang S, Zhou J, Reganold JP (2010) Effects of soil type and farm management on soil ecological functional genes and microbial activities. ISME J 4:1099–1107PubMedCrossRefGoogle Scholar
  101. Rousk J, Baath E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG, Knight R, Fierer N (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 4:1340–1351PubMedCrossRefGoogle Scholar
  102. Rovira AD (1969) Plant root exudates. Bot Rev 35:35–57CrossRefGoogle Scholar
  103. Rudrappa T, Czymmek KJ, Pare PW, Bais HP (2008) Root-secreted malic acid recruits beneficial soil bacteria. Plant Physiol 148:1547–1556PubMedCrossRefGoogle Scholar
  104. Ryan PR, Dessaux Y, Thomashow LS, Weller DM (2009) Rhizosphere engineering and management for sustainable agriculture. Plant Soil 321:363–383CrossRefGoogle Scholar
  105. Schloss PD, Handelsman J (2006) Toward a census of bacteria in soil. PLoS Comput Biol 2:e92PubMedCrossRefGoogle Scholar
  106. Schnitzer SA, Klironomos JN, Hillerislambers J, Kinkel LL, Reich PB, Xiao K, Rillig MC, Sikes BA, Callaway RM, Mangan SA, van Nes EH, Scheffer M (2011) Soil microbes drive the classic plant diversity-productivity pattern. Ecology 92:296–303PubMedCrossRefGoogle Scholar
  107. Selvakumar G, Panneerselvam P, Ganeshamurthy AN, Maheshwari DK (2012) Bacterial mediated alleviation of abiotic stress in crops. In: Maheshwari DK (ed) Bacteria in agrobiology: Stress management. Springer, New York, pp 205–224CrossRefGoogle Scholar
  108. Shaharoona B, Naveed M, Arshad M, Zahir ZA (2008) Fertilizer-dependent efficiency of Pseudomonads for improving growth, yield, and nutrient use efficiency of wheat (Triticum aestivum L.). Appl Microbiol Biot 79:147–155CrossRefGoogle Scholar
  109. Sharma SK, Ramesh A, Sharma MP, Joshi OP, Govaerts B, Steenwerth KL, Karlen DL (2010) Microbial community structure and diversity as indicators for evaluating soil quality. In: Lichtfouse E (ed) Biodiversity, biofuels, agroforestry and conservation agriculture, vol 5. Sustainable Agriculture Reviews, Springer Netherlands, pp 317–358CrossRefGoogle Scholar
  110. Shennan C (2008) Biotic interactions, ecological knowledge and agriculture. Philos T Roy Soc B 363:717–739CrossRefGoogle Scholar
  111. Somers E, Vanderleyden J, Srinivasan M (2004) Rhizosphere bacterial signalling: a love parade beneath our feet. Crit Rev Microbiol 30:205–240. doi:doi:10.1080/10408410490468786 PubMedCrossRefGoogle Scholar
  112. Stinson KA, Campbell SA, Powell JR, Wolfe BE, Callaway RM, Thelen GC, Hallett SG, Prati D, Klironomos JN (2006) Invasive plant suppresses the growth of native tree seedlings by disrupting belowground mutualisms. PLoS Biol 4:e140PubMedCrossRefGoogle Scholar
  113. Sugiyama A, Vivanco JM, Jayanty SS, Manter DK (2010) Pyrosequencing assessment of soil microbial communities in organic and conventional potato farms. Plant Dis 94:1329–1335. doi:10.1094/PDIS-02-10-0090 CrossRefGoogle Scholar
  114. Tang CS, Cai WF, Kohl K, Nishimoto RK (1995) Plant stress and allelopathy. In: Inderjit KMMD, Einhellig FA (eds) Allelopathy: organisms, processes, and applications, vol 582, Acs Symposium Series. Amer Chemical Soc, Washington, pp 142–157CrossRefGoogle Scholar
  115. Tilman D, Socolow R, Foley JA, Hill J, Larson E, Lynd L, Pacala S, Reilly J, Searchinger T, Somerville C, Williams R (2009) Energy. Beneficial biofuels—the food, energy, and environment trilemma. Science 325:270–271PubMedCrossRefGoogle Scholar
  116. Uren NC (2007) Types, amounts, and possible functions of compounds released into the rhizosphere by soil-grown plants. In: Pinton R, Varanini Z, Nannipieri P (eds) The rhizosphere biochemistry and organic substances at the soil-plant interface, 2nd edn. CRC, Boca Raton, pp 1–21CrossRefGoogle Scholar
  117. van Bruggen AHC, Semenov AM (2000) In search of biological indicators for soil health and disease suppression. Appl Soil Ecol 15:13–24CrossRefGoogle Scholar
  118. van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72CrossRefGoogle Scholar
  119. van der Heijden MGA, Bakker R, Verwaal J, Scheublin TR, Rutten M, Van Logtestijn R, Staehelin C (2006) Symbiotic bacteria as a determinant of plant community structure and plant productivity in dune grassland. FEMS Microbiol Ecol 56:178–187PubMedCrossRefGoogle Scholar
  120. van der Heijden MGA, Bardgett RD, Van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310PubMedCrossRefGoogle Scholar
  121. van der Putten W, Bardgett R, de Ruiter P, Hol W, Meyer K, Bezemer T, Bradford M, Christensen S, Eppinga M, Fukami T, Hemerik L, Molofsky J, Schädler M, Scherber C, Strauss S, Vos M, Wardle D (2009) Empirical and theoretical challenges in aboveground-belowground ecology. Oecologia 161:1–14PubMedCrossRefGoogle Scholar
  122. van Overbeek L, van Elsas JD (2008) Effects of plant genotype and growth stage on the structure of bacterial communities associated with potato (Solanum tuberosum L.). FEMS Microbiol Ecol 64:283–296PubMedCrossRefGoogle Scholar
  123. Vandenkoornhuyse P, Mahe S, Ineson P, Staddon P, Ostle N, Cliquet JB, Francez AJ, Fitter AH, Young JP (2007) Active root-inhabiting microbes identified by rapid incorporation of plant-derived carbon into RNA. Proc Natl Acad Sci U S A 104:16970–16975PubMedCrossRefGoogle Scholar
  124. von Braun J (2007) The world food situation: new driving forces and required actions. doi:10.2499/0896295303
  125. Wagg C, Jansa J, Schmid B, van der Heijden MG (2011) Belowground biodiversity effects of plant symbionts support aboveground productivity. Ecol Lett 14:1001–1009PubMedCrossRefGoogle Scholar
  126. Wardle DA (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633. doi:10.1126/science.1094875 PubMedCrossRefGoogle Scholar
  127. Weisskopf L, Abou-Mansour E, Fromin N, Tomasi N, Santelia D, Edelkott I, Neumann G, Aragno M, Tabacchi R, Martinoia E (2006) White lupin has developed a complex strategy to limit microbial degradation of secreted citrate required for phosphate acquisition. Plant Cell Environ 29:919–927. doi:10.1111/j.1365-3040.2005.01473.x PubMedCrossRefGoogle Scholar
  128. Weller DM, Raaijmakers JM, Gardener BB, Thomashow LS (2002) Microbial populations responsible for specific soil suppressiveness to plant pathogens. Annu Rev Phytopathol 40:309–348PubMedCrossRefGoogle Scholar
  129. Whipps JM (1990) Carbon economy. In: Lynch JM (ed) The rhizosphere, Wiley series in ecological and applied microbiology. J Wiley, Chichester, pp 59–97Google Scholar
  130. Wilsey BJ, Potvin C (2000) Biodiversity and ecosystem functioning: importance of species evenness in an old field. Ecology 81:887–892CrossRefGoogle Scholar
  131. Wittebolle L, Marzorati M, Clement L, Balloi A, Daffonchio D, Heylen K, De Vos P, Verstraete W, Boon N (2009) Initial community evenness favours functionality under selective stress. Nature 458:623–626PubMedCrossRefGoogle Scholar
  132. Xie X, Zhang H, Paré PW (2009) Sustained growth promotion in arabidopsis with long-term exposure to the beneficial soil bacterium Bacillus subtilis (GB03). Plant Signal Behav 4:948–953PubMedCrossRefGoogle Scholar
  133. Yang X, Chen L, Yong X, Shen Q (2011) Formulations can affect rhizosphere colonization and biocontrol efficiency of Trichoderma harzianum SQR-T037 against Fusarium wilt of cucumbers. Biol Fertil Soils 47:239–248CrossRefGoogle Scholar
  134. Yin B, Crowley D, Sparovek G, De Melo WJ, Borneman J (2000) Bacterial functional redundancy along a soil reclamation gradient. Appl Environ Microbiol 66:4361–4365PubMedCrossRefGoogle Scholar
  135. Zak DR, Holmes WE, White DC, Peacock AD, Tilman D (2003) Plant diversity, soil microbial communities, and ecosystem function: are there any links? Ecology 84:2042–2050CrossRefGoogle Scholar
  136. Zhang H, Kim MS, Sun Y, Dowd SE, Shi H, Pare PW (2008a) Soil bacteria confer plant salt tolerance by tissue-specific regulation of the sodium transporter HKT1. Mol Plant Microbe In 21:737–744CrossRefGoogle Scholar
  137. Zhang H, Xie X, Kim MS, Kornyeyev DA, Holaday S, Pare PW (2008b) Soil bacteria augment Arabidopsis photosynthesis by decreasing glucose sensing and abscisic acid levels in planta. Plant J 56:264–273PubMedCrossRefGoogle Scholar
  138. Zhang H, Sun Y, Xie X, Kim M-S, Dowd SE, Paré PW (2009a) A soil bacterium regulates plant acquisition of iron via deficiency-inducible mechanisms. Plant J 58:568–577. doi:10.1111/j.1365-313X.2009.03803.x PubMedCrossRefGoogle Scholar
  139. Zhang J, Subramanian S, Stacey G, Yu O (2009b) Flavones and flavonols play distinct critical roles during nodulation of Medicago truncatula by Sinorhizobium meliloti. Plant J 57:171–183PubMedCrossRefGoogle Scholar
  140. Zhang H, Murzello C, Sun Y, Kim M-S, Xie X, Jeter RM, Zak JC, Dowd SE, Paré PW (2010) Choline and osmotic-stress tolerance induced in Arabidopsis by the soil microbe Bacillus subtilis (GB03). Mol Plant Microbe In 23:1097–1104. doi:10.1094/MPMI-23-8-1097 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Jacqueline M. Chaparro
    • 1
  • Amy M. Sheflin
    • 1
  • Daniel K. Manter
    • 2
  • Jorge M. Vivanco
    • 1
  1. 1.Center for Rhizosphere Biology and Department of Horticulture and Landscape ArchitectureColorado State UniversityFort CollinsUSA
  2. 2.Agricultural Research Service, Soil-Plant-Research UnitUnited States Department of AgricultureFort CollinsUSA

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