Plant and Soil

, Volume 360, Issue 1–2, pp 1–13 | Cite as

Harnessing the rhizosphere microbiome through plant breeding and agricultural management

Marschner Review

Abstract

Background

The need to enhance the sustainability of intensive agricultural systems is widely recognized One promising approach is to encourage beneficial services provided by soil microorganisms to decrease the inputs of fertilizers and pesticides. However, limited success of this approach in field applications raises questions as to how this might be best accomplished.

Scope

We highlight connections between root exudates and the rhizosphere microbiome, and discuss the possibility of using plant exudation characteristics to selectively enhance beneficial microbial activities and microbiome characteristics. Gaps in our understanding and areas of research that are vital to our ability to more fully exploit the soil microbiome for agroecosystem productivity and sustainability are also discussed.

Conclusion

This article outlines strategies for more effectively exploiting beneficial microbial services on agricultural systems, and cals attention to topics that require additional research.

Keywords

Rhizosphere Exudates Plant-driven selection Beneficial microbes Plant breeding 

References

  1. Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827PubMedGoogle Scholar
  2. Ayres E, Steltzer H, Berg S, Wall DH (2009) Soil biota accelerate decomposition in high-elevation forests by specializing in the breakdown of litter produced by the plant species above them. J Ecol 97:901–912Google Scholar
  3. Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant Cell Environ 32:666–681PubMedGoogle Scholar
  4. Badri DV, Loyola-Vargas VM, Broeckling CD, De-la-Pena C, Jasinski M, Santelia D et al (2008) Altered profile of secondary metabolites in the root exudates of Arabidopsis ATP-binding cassette transporter mutants. Plant Phys 146:762–771Google Scholar
  5. Badri DV, Quintana N, El Kassis EG, Kim HK, Choi YH, Sugiyama A et al (2009) An ABC transporter mutation alters root exudation of phytochemicals that provoke an overhaul of natural soil microbiota. Plant Phys 151:2006–2017Google Scholar
  6. 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 57:233–266PubMedGoogle Scholar
  7. Baudoin E, Benizri E, Guckert A (2002) Impact of growth stage on the bacterial community structure along maize roots, as determined by metabolic and genetic fingerprinting. Appl Soil Ecol 19:135–145Google Scholar
  8. 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 68:1–13PubMedGoogle Scholar
  9. Besserer A, Puech-Pages V, Kiefer P, Gomez-Roldan V, Jauneau A, Roy S et al (2006) Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biol 4:1239–1247Google Scholar
  10. Bonanomi G, Rietkerk M, Dekker SC, Mazzoleni S (2007) Islands of fertility induce co-occurring negative and positive plant-soil feedbacks promoting coexistence. Plant Ecol 197:207–218Google Scholar
  11. Brandt BW, Kelpin FDL, van Leeuwen IMM, Kooijman SALM (2004) Modelling microbial adaptation to changing availability of substrates. Water Res 38:1003–1013PubMedGoogle Scholar
  12. Bremer C, Braker G, Matthies D, Beierkuhnlein C, Conrad R (2009) Plant presence and species combination, but not diversity, influence denitrifier activity and the composition of nirK-type denitrifier communities in grassland soil. FEMS Microbiol Ecol 70:377–387PubMedGoogle Scholar
  13. Broeckling CD, Broz AK, Bergelson J, Manter DK, Vivanco JM (2008) Root exudates regulate soil fungal community composition and diversity. Appl Environ Microbiol 74:738–744PubMedGoogle Scholar
  14. Broz AK, Manter DK, Vivanco JM (2007) Soil fungal abundance and diversity: another victim of the invasive plant Centaurea maculosa. ISME J 1:763–765PubMedGoogle Scholar
  15. Bruinsma M, Kowalchuk GA, van Veen JA (2003) Effects of genetically modified plants on microbial communities and processes in soil. Biol Fertil Soils 37:329–337Google Scholar
  16. Buchanan RL, Bagi LK (1999) Microbial competition: effect of Pseudomonas fluorescens on the growth of Listeria monocytogenes. Food Microbiol 16:523–529Google Scholar
  17. Cairney JWG (2011) Ectomycorrhizal fungi: the symbiotic route to the root for phosphorus in forest soils. Plant Soil 344:51–71Google Scholar
  18. Callaway RM, Thelen GC, Rodriguez A, Holben WE (2004) Soil biota and exotic plant invasion. Nature 427:731–733PubMedGoogle Scholar
  19. Carney KM, Matson PA (2006) The influence of tropical plant diversity and composition on soil microbial communities. Microb Ecol 52:226–238PubMedGoogle Scholar
  20. Chiang PN, Chiu C-Y, Wang MK, Chen B-T (2011) Low-molecular-weight organic acids exuded by millet (Setaria italica (L.) Beauv.) roots and their effect on the remediation of cadmium-contaminated soil. Soil Sci 176:33–38Google Scholar
  21. Crowder DW, Northfield TD, Strand MR, Snyder WE (2010) Organic agriculture promotes evenness and natural pest control. Nature 466:109–112PubMedGoogle Scholar
  22. Delalande L, Faure D, Raffoux A, Uroz S, D’Angelo-Picard C, Elasri M et al (2005) N-hexanoyl-L-homoserine lactone, a mediator of bacterial quorum-sensing regulation, exhibits plant-dependent stability and may be inactivated by germinating Lotus corniculatus seedlings. FEMS Microbiol Ecol 52:13–20PubMedGoogle Scholar
  23. Elliot LF, Lynch JM (1994) Biodiversity and soil resilience. In: Greenland DJ, Szabolc I (eds) Soil resilience and sustainable land use. CAB International pp 353–364Google Scholar
  24. Erlich Y, Chang K, Gordon A, Ronen R, Navon O, Rooks M et al (2009) DNA sudoku - Harnessing high-throughput sequencing for multiplexed specimen analysis. Genome Res 19:1243–1253PubMedGoogle Scholar
  25. Fliessbach A, Winkler M, Lutz MP, Oberholzer H-R, Mäder P (2009) Soil amendment with Pseudomonas fluorescens CHA0: Lasting effects on soil biological properties in soils low in microbial biomass and activity. Microb Ecol 57:611–623PubMedGoogle Scholar
  26. Friesen ML, Porter SS, Stark SC, von Wettberg EJ, Sachs JL, Martinez-Romero E (2011) Microbially mediated plant functional traits. Annu Rev Ecol Evol Syst 42:23–46Google Scholar
  27. Fussmann GF, Heber G (2002) Food web complexity and chaotic population dynamics. Ecol Lett 5:394–401Google Scholar
  28. Gao MS, Teplitski M, Robinson JB, Bauer WD (2003) Production of substances by Medicago truncatula that affect bacterial quorum sensing. Mol Plant Microbe Interact 16:827–834PubMedGoogle Scholar
  29. Gaur R, Khare SK (2011) Solvent tolerant Pseudomonads as a source of novel lipases for applications in non-aqueous systems. Biocat Biotransform 29:161–171Google Scholar
  30. Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pages V, Dun EA, Pillot J-P et al (2008) Strigolactone inhibition of shoot branching. Nature 455:189–194PubMedGoogle Scholar
  31. Gosling P, Hodge A, Goodlass G, Bending GD (2006) Arbuscular mycorrhizal fungi and organic farming. Agr Ecosyst Environ 113:17–35Google Scholar
  32. Grayston SJ, Wang SQ, Campbell CD, Edwards AC (1998) Selective influence of plant species on microbial diversity in the rhizosphere. Soil Biol Biochem 30:369–378Google Scholar
  33. Grunsven RHA, Putten WH, Bezemer TM, Veenendaal EM (2009) Plant–soil feedback of native and range-expanding plant species is insensitive to temperature. Oecologia 162:1059–1069PubMedGoogle Scholar
  34. Hetrick BAD, Wilson GWT, Cox TS (1993) Mycorrhizal dependence of modern wheat cultivars and ancestors: a synthesis. Can J Bot 71:512–518Google Scholar
  35. Högberg MN, Högberg P, Myrold DD (2006) Is microbial community composition in boreal forest soils determined by pH, C-to-N ratio, the trees, or all three? Oecologia 150:590–601PubMedGoogle Scholar
  36. Hwang SF, Ahmed HU, Gossen BD, Kutcher HR, Brandt SA, Strelkov SE et al (2009) Effect of crop rotation on the soil pathogen population dynamics and canola seedling establishment. Plant Pathol J 8:106–112Google Scholar
  37. Iavicoli A, Boutet E, Buchala A, Métraux JP (2003) Induced systemic resistance in Arabidopsis thaliana in response to root inoculation with Pseudomonas fluorescens CHA0. Mol Plant-Micro Int 16:851–858Google Scholar
  38. Jain A, Singh S, Sarma BK, Singh HB (2011) Microbial consortium mediated reprogramming of defense network in pea to enhance tolerance against Sclerotinia sclerotiorum. J App Microbiol 112:537–550Google Scholar
  39. Janos DP (2007) Plant responsiveness to mycorrhizas differs from dependence upon mycorrhizas. Mycorrhiza 17:75–91PubMedGoogle Scholar
  40. Jones DL, Hodge A, Kuzyakov Y (2004) Plant and mycorrhizal regulation of rhizodeposition. New Phytol 163:459–480Google Scholar
  41. Jousset A, Rochat L, Lanoue A, Bonkowski M, Keel C, Scheu S (2011) Plants respond to pathogen infection by enhancing the antifungal gene expression of root-associated bacteria. Mol Plant Microbe Interact 24:352–358PubMedGoogle Scholar
  42. Kamilova F, Kravchenko LV, Shaposhnikov AI, Azarova T, Makarova N, Lugtenberg B (2006) Organic acids, sugars, and L-tryptophane in exudates of vegetables growing on stonewool and their effects on activities of rhizosphere bacteria. Mol Plant Microbe Interact 19:250–256PubMedGoogle Scholar
  43. Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O, Verbruggen E et al (2011) Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333:880–882PubMedGoogle Scholar
  44. Knops JMH, Tilman D, Haddad NM, Naeem S, Mitchell CE, Haarstad J et al (1999) Effects of plant species richness on invasion dynamics, disease outbreaks, insect abundances and diversity. Ecol Lett 2:286–293Google Scholar
  45. Kowalchuk GA, Buma DS, de Boer W, Klinkhamer PGL, van Veen JA (2002) Effects of above-ground plant species composition and diversity on the diversity of soil-borne microorganisms. Ant van Leeuw Int J Gen Mol Microbiol 81:509–520Google Scholar
  46. Kuklinsky-Sobral J, Araujo WL, Mendes R, Geraldi IO, Pizzirani-Kleiner AA, Azevedo JL (2004) Isolation and characterization of soybean-associated bacteria and their potential for plant growth promotion. Environ Microbiol 6:1244–1251PubMedGoogle Scholar
  47. Lambers H, Mougel C, Jaillard B, Hinsinger P (2009) Plant-microbe-soil interactions in the rhizosphere: an evolutionary perspective. Plant Soil 321:83–115Google Scholar
  48. Landa BB, Mavrodi OV, Schroeder KL, Allende-Molar R, Weller DM (2006) Enrichment and genotypic diversity of phlD-containing fluorescent Pseudomonas spp. in two soils after a century of wheat and flax monoculture. FEMS Microbiol Ecol 55:351–68PubMedGoogle Scholar
  49. Larkin RP, Honeycutt CW (2006) Effects of different 3-year cropping systems on soil microbial communities and Rhizoctonia diseases of potato. Phytopathology 96:68–79PubMedGoogle Scholar
  50. Larsen EH, Lobinski R, Burger-Meÿer K, Hansen M, Ruzik R, Mazurowska L et al (2006) Uptake and speciation of selenium in garlic cultivated in soil amended with symbiotic fungi (mycorrhiza) and selenate. Anal Bioanal Chem 385:1098–1108PubMedGoogle Scholar
  51. Lesuffleur F, Paynel F, Bataillé MP, Deunff E, Cliquet JB (2007) Root amino acid exudation: measurement of high efflux rates of glycine and serine from six different plant species. Plant Soil 294:235–246Google Scholar
  52. Loreau M, Naeem S, Inchausti P, Bengtsson J, Grime JP, Hector A et al (2001) Biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294:804–808PubMedGoogle Scholar
  53. Lu Y, Abraham WR, Conrad R (2007) Spatial variation of active microbiota in the rice rhizosphere revealed by in situ stable isotope probing of phospholipid fatty acids. Environ Microbiol 9:474–481PubMedGoogle Scholar
  54. Madritch MD, Lindroth RL (2011) Soil microbial communities adapt to genetic variation in leaf litter inputs. Oikos 120:1696–1704Google Scholar
  55. Mahmood S, Paton GI, Prosser JI (2005) Cultivation-independent in situ molecular analysis of bacteria involved in degradation of pentachlorophenol in soil. Environ Microbiol 7:1349–1360PubMedGoogle Scholar
  56. Mathesius U, Mulders S, Gao MS, Teplitski M, Caetano-Anolles G, Rolfe BG et al (2003) Extensive and specific responses of a eukaryote to bacterial quorum-sensing signals. PNAS 100:1444–1449PubMedGoogle Scholar
  57. Mendes R, Kruijt M, de Bruijn I, Dekkers E, van der Voort M, Schneider JHM et al (2011) Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332:1097–1100PubMedGoogle Scholar
  58. Meng Q, Yin J, Rosenzweig N, Douches D, Hao JJ (2012) Culture-based assessment of microbial communities in soil suppressive to potato common scab. Plant Dis 96:712–717Google Scholar
  59. 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 60:1729–1742PubMedGoogle Scholar
  60. 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 75:2–16PubMedGoogle Scholar
  61. Mougel C, Offre P, Ranjard L, Corberand T, Gamalero E, Robin C et al (2006) Dynamic of the genetic structure of bacterial and fungal communities at different developmental stages of Medicago truncatula Gaertn. cv. Jemalong line J5. New Phytol 170:165–175PubMedGoogle Scholar
  62. Naeem S, Knops J, Tilman D, Howe K, Kennedy T, Gale S (2000) Plant diversity increases resistance to invasion in the absence of covarying extrinsic factors. Oikos 91:97–108Google Scholar
  63. Ochiai N, Powelson ML, Crowe FJ, Dick RP (2008) Green manure effects on soil quality in relation to suppression of Verticillium wilt of potatoes. Biol Fertil Soil 44:1013–1023Google Scholar
  64. Oger P, Mansouri H, Nesme X, Dessaux Y (2004) Engineering root exudation of lotus toward the production of two novel carbon compounds leads to the selection of distinct microbial populations in the rhizosphere. Microb Ecol 47:96–103PubMedGoogle Scholar
  65. Oldroyd GED, Downie JA (2008) Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu Rev Plant Biol 59:519–546PubMedGoogle Scholar
  66. Orwin KH, Wardle DA, Greenfield LG (2006) Ecological consequences of carbon substrate identity and diversity in a laboratory study. Ecology 87:580–593PubMedGoogle Scholar
  67. Paterson E, Gebbing T, Abel C, Sim A, Telfer G (2006) Rhizodeposition shapes rhizosphere microbial community structure in organic soil. New Phytol 173:600–610Google Scholar
  68. Paungfoo-Lonhienne C, Rentsch D, Robatzek S, Webb RI, Sagulenko E, Näsholm T et al (2010) Turning the table: plants consume microbes as a source of nutrients. PLoS One 5:e11915PubMedGoogle Scholar
  69. Pennanen T, Caul S, Daniell TJ, Griffiths BS, Ritz K, Wheatley RE (2004) Community-level responses of metabolically-active soil microorganisms to the quantity and quality of substrate inputs. Soil Biol Biochem 36:841–848Google Scholar
  70. Pérez-Piqueres A, Edel-Hermann V, Alabouvette C, Steinberg C (2006) Response of soil microbial communities to compost amendments. Soil Biol Biochem 38:460–470Google Scholar
  71. Phillips RP, Erlitz Y, Bier R, Bernhardt ES (2008) New approach for capturing soluble root exudates in forest soils. Funct Ecol 22:990–999Google Scholar
  72. Ping LY, Boland W (2004) Signals from the underground: bacterial volatiles promote growth in Arabidopsis. Trends Plant Sci 9:263–266PubMedGoogle Scholar
  73. 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 40:2394–2406Google Scholar
  74. Powell M, Schlosser W, Ebel E (2004) Considering the complexity of microbial community dynamics in food safety risk assessment. Int J Food Microbiol 90:171–179PubMedGoogle Scholar
  75. Prosser JI, Rangel-Castro JI, Killham K (2006) Studying plant–microbe interactions using stable isotope technologies. Curr Opin Biotechnol 17:98–102PubMedGoogle Scholar
  76. Redman RS, Sheehan KB, Stout RG, Rodriguez RJ, Henson JM (2002) Thermotolerance generated by plant/fungal symbiosis. Science 298:1581–1581PubMedGoogle Scholar
  77. Rengel Z (2002) Breeding for better symbiosis. Plant Soil 245:147–162Google Scholar
  78. Reynolds HL, Packer A, Bever JD, Clay K (2003) Grassroots ecology: plant-microbe-soil interactions as drivers of plant community structure and dynamics. Ecology 84:2281–2291Google Scholar
  79. Roesch LF, Fulthorpe RR, Riva A, Casella G, Hadwin AKM, Kent AD et al (2007) Pyrosequencing enumerates and contrasts soil microbial diversity. ISME J 1:283–290PubMedGoogle Scholar
  80. Rudrappa T, Czymmek KJ, Pare PW, Bais HP (2008) Root-secreted malic acid recruits beneficial soil bacteria. Plant Phys 148:1547–1556Google Scholar
  81. Ryan PR, Dessaux Y, Thomashow LS, Weller DM (2009) Rhizosphere engineering and management for sustainable agriculture. Plant Soil 321:363–383Google Scholar
  82. Salles JF, van Veen JA, van Elsas JD (2004) Multivariate analyses of Burkholderia species in soil: effect of crop and land use history. Appl Environ Microbiol 70:4012–4020PubMedGoogle Scholar
  83. Savka MA, Farrand SK (1997) Modification of rhizobacterial populations by engineering bacterium utilization of a novel plant-produced resource. Nat Biotech 15:363–368Google Scholar
  84. Savka MA, Dessaux Y, Oger P, Rossbach S (2002) Engineering bacterial competitiveness and persistence in the phytosphere. Mol Plant Microbe Interact 15:866–874PubMedGoogle Scholar
  85. Schweitzer JA, Bailey JK, Fischer DG, LeRoy CJ, Lonsdorf EV, Whitham TG et al (2008) Plant-soil-microorganism interactions: heritable relationship between plant genotype and associated soil microorganisms. Ecology 89:773–781PubMedGoogle Scholar
  86. Shaharoona B, Imran M, Arshad M, Khalid A (2011) Manipulation of ethylene synthesis in roots through bacterial ACC deaminase for improving nodulation in legumes. Crit Rev Plant Sci 30:279–291Google Scholar
  87. Shen H, Wang XC, Shi WM, Cao ZH, Yan XL (2001) Isolation and identification of specific root exudates in elephantgrass in response to mobilization of iron- and aluminum-phosphates. J Plant Nutr 24:1117–1130Google Scholar
  88. Shi S, Condron L, Larsen S, Richardson AE, Jones E, Jiao J et al (2011) In situ sampling of low molecular weight organic anions from rhizosphere of radiata pine (Pinus radiata) grown in a rhizotron system. Environ Exp Bot 70:131–142Google Scholar
  89. Smith KP, Goodman RM (1999) Host variation for interactions with beneficial plant-associated microbes. Annu Rev Phytopathology 37:473–491Google Scholar
  90. Smith KP, Handelsman J, Goodman RM (1999) Genetic basis in plants for interactions with disease-suppressive bacteria. PNAS 96:4786–4790PubMedGoogle Scholar
  91. Sneh B, Pozniak D, Salomon D (1987) Soil suppressiveness to Fusarium Wilt of melon, induced by repeated croppings of resistant varieties of melons. J Phytopathology 120:347–354Google Scholar
  92. Sugiyama A, Vivanco JM, Jayanty SS, Manter DK (2010) Pyrosequencing assessment of soil microbial communities in organic and conventional potato farms. Plant Dis 94:1329–1335Google Scholar
  93. Taiz L, Zeiger E (2006) Plant physiology, 4th edn. Sinauer Associates, Inc., SunderlandGoogle Scholar
  94. Teplitski M, Robinson JB, Bauer WD (2000) Plants secrete substances that mimic bacterial N-acyl homoserine lactone signal activities and affect population density-dependent behaviors in associated bacteria. Mol Plant Microbe Interact 13:637–648PubMedGoogle Scholar
  95. Tikhonovich IA, Provorov NA (2011) Microbiology is the basis of sustainable agriculture: an opinion. Ann Appl Biol 159:155–168Google Scholar
  96. Torsvik V, Goksoyr J, Daae F (1990) High diversity in DNA of soil bacteria. Appl Environ Microbiol 56:782–787PubMedGoogle Scholar
  97. Tracy BF, Sanderson MA (2004) Forage productivity, species evenness and weed invasion in pasture communities. Agr Ecosyst Environ 102:175–183Google Scholar
  98. Ulrich A, Becker R (2006) Soil parent material is a key determinant of the bacterial community structure in arable soils. FEMS Microbiol Ecol 56:430–443PubMedGoogle Scholar
  99. Umehara M, Hanada A, Yoshida S, Akiyama K, Arite T, Takeda-Kamiya N et al (2008) Inhibition of shoot branching by new terpenoid plant hormones. Nature 455:195–200PubMedGoogle Scholar
  100. van Elsas JD, Costa R, Jansson J, Sjoling S, Bailey M, Nalin R et al (2008) The metagenomics of disease-suppressive soils – Experiences from the METACONTROL project. Trends Biotechnol 26:591–601PubMedGoogle Scholar
  101. van Elsas JD, Chiurazzi M, Mallon CA, Elhottova D, Kristufek V, Salles JF (2012) Microbial diversity determines the invasion of soil by a bacterial pathogen. PNAS 109:1159–1164PubMedGoogle Scholar
  102. Wakelin SA, Macdonald LM, Rogers SL, Gregg AL, Bolger TP, Baldock JA (2008) Habitat selective factors influencing the structural composition and functional capacity of microbial communities in agricultural soils. Soil Biol Biochem 40:803–813Google Scholar
  103. Weisskopf L, Fromin N, Tomasi N, Aragno M, Martinoia E (2005) Secretion activity of white lupin’s cluster roots influences bacterial abundance, function and community structure. Plant Soil 268:181–194Google Scholar
  104. West S, Kiers E, Pen I, Denison R (2002) Sanctions and mutualism stability: when should less beneficial mutualists be tolerated? J Evol Biol 15:830–837Google Scholar
  105. Wilsey BJ, Potvin C (2000) Biodiversity and ecosystem functioning: Importance of species evenness in an old field. Ecology 81:887–892Google Scholar
  106. Wissuwa M, Mazzola M, Picard C (2009) Novel approaches in plant breeding for rhizosphere-related traits. Plant Soil 321:409–430Google Scholar
  107. Wittebolle L, Marzorati M, Clement L, Balloi A, Daffonchio D, Heylen K et al (2009) Initial community evenness favours functionality under selective stress. Nature 458:623–626PubMedGoogle Scholar
  108. Xie X, Yoneyama K, Yoneyama K (2010) The strigolactone story. Annu Rev Phytopathology 48:93–117Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  1. 1.Center for Rhizosphere BiologyColorado State UniversityFort CollinsUSA
  2. 2.Soil-Plant-Nutrient Research, USDA-ARSFort CollinsUSA

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