Coadaptationary Aspects of the Underground Communication Between Plants and Other Organisms

  • Akifumi Sugiyama
  • Daniel K. Manter
  • Jorge M. VivancoEmail author
Part of the Signaling and Communication in Plants book series (SIGCOMM, volume 14)


Soil microbial communities are comprised of a vast array of bacteria, fungi, nematodes, and other organisms. It is becoming increasingly clear that these communities are not passively determined but actively regulated by plants. This chapter discusses the role plant root exudates play in the active regulation of soil microbial communities. In addition, we discuss the potential role coadapted plant-soil microbial communities may play in agricultural sustainability and production. We suggest that minimal disruption in the plant microbial community should be maintained in order to achieve maximum long-term agricultural production by minimizing disease outbreaks and by reducing costly agricultural inputs such as pesticides and fertilizers.


Arbuscular Mycorrhizal Fungus Root Exudate Fungal Community Soil Microbial Community Arbuscular Mycorrhiza 
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.



We thank Mr. Derek Sonderegger for statistical analysis for visual representation of soil microbial evenness (Fig. 1). A.S. was supported by a JSPS Postdoctoral Fellowships for Research Abroad. These studies were supported by the National Science Foundation (MCB-0950857 to JMV).


  1. Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827PubMedCrossRefGoogle Scholar
  2. Akiyama K, Tanigawa F, Kashihara T, Hayashi H (2010) Lupin pyranoisoflavones inhibiting hyphal development in arbuscular mycorrhizal fungi. Phytochemistry 71:1865–1871PubMedCrossRefGoogle Scholar
  3. Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant Cell Environ 32:666–681PubMedCrossRefGoogle Scholar
  4. 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
  5. Badri DV, Weir TL, van der Lelie D, Vivanco JM (2009b) Rhizosphere chemical dialogues: plant–microbe interactions. Curr Opin Biotechnol 20:642–650PubMedCrossRefGoogle Scholar
  6. Badri DV, Loyola-Vargas VM, Broeckling CD, Vivanco JM (2010) Root secretion of phytochemicals in Arabidopsis is predominantly not influenced by diurnal rhythms. Mol Plant 3:491–498PubMedCrossRefGoogle Scholar
  7. Baker KF, Cook RJ (1974) Biological control of plant pathogens. Freeman and Company, San FransciscoGoogle Scholar
  8. Batten K, Scow K, Davies K, Harrison S (2006) Two invasive plants alter soil microbial community composition in serpentine grasslands. Biol Invasions 8:217–230CrossRefGoogle Scholar
  9. 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 19:135–145CrossRefGoogle Scholar
  10. Bird DM (2004) Signaling between nematodes and plants. Curr Opin Plant Biol 7:372–376PubMedCrossRefGoogle Scholar
  11. Bonfante P, Anca IA (2009) Plants, mycorrhizal fungi, and bacteria: a network of interactions. Annu Rev Microbiol 63:363–383PubMedCrossRefGoogle Scholar
  12. Bouwmeester HJ, Matusova R, Zhongkui S, Beale MH (2003) Secondary metabolite signalling in host-parasitic plant interactions. Curr Opin Plant Biol 6:358–364PubMedCrossRefGoogle 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 74:738–744PubMedCrossRefGoogle Scholar
  14. Broz AK, Manter DK, Vivanco JM (2007) Soil fungal abundance and diversity: another victim of the invasive plant Centaurea maculosa. ISME J 1:763–765PubMedCrossRefGoogle Scholar
  15. Buee M, Rossignol M, Jauneau A, Ranjeva R, Becard G (2000) The pre-symbiotic growth of arbuscular mycorrhizal fungi is induced by a branching factor partially purified from plant root exudates. Mol Plant–Microbe Interact 13:693–698PubMedCrossRefGoogle Scholar
  16. Cai T, Cai W, Zhang J, Zheng H, Tsou AM, Xiao L, Zhong Z, Zhu J (2009) Host legume-exuded antimetabolites optimize the symbiotic rhizosphere. Mol Microbiol 73:507–517PubMedCrossRefGoogle Scholar
  17. Cook RJ, Baker KF (1983) The nature and practice of biological control of plant pathogens. APS Press, St. PaulGoogle Scholar
  18. Crowder DW, Northfield TD, Strand MR, Snyder WE (2010) Organic agriculture promotes evenness and natural pest control. Nature 466:109–112PubMedCrossRefGoogle Scholar
  19. D’Haeze W, Holsters M (2004) Surface polysaccharides enable bacteria to evade plant immunity. Trends Microbiol 12:555–561PubMedCrossRefGoogle Scholar
  20. Djordjevic MA, Redmond JW, Batley M, Rolfe BG (1987) Clovers secrete specific phenolic compounds which either stimulate or repress nod gene expression in Rhizobium trifolii. EMBO J 6:1173–1179PubMedGoogle Scholar
  21. Doyle JJ, Luckow MA (2003) The rest of the iceberg. Legume diversity and evolution in a phylogenetic context. Plant Physiol 131:900–910PubMedCrossRefGoogle Scholar
  22. Esperschutz J, Gattinger A, Mader P, Schloter M, Fliessbach A (2007) Response of soil microbial biomass and community structures to conventional and organic farming systems under identical crop rotations. FEMS Microbiol Ecol 61:26–37PubMedCrossRefGoogle Scholar
  23. Gagnon H, Ibrahim RK (1998) Aldonic acids: a novel family of nod gene inducers of Mesorhizobium loti, Rhizobium lupini, and Sinorhizobium meliloti. Mol Plant–Microbe Interact 11:988–998CrossRefGoogle Scholar
  24. Garcia-Garrido JM, Lendzemo V, Castellanos-Morales V, Steinkellner S, Vierheilig H (2009) Strigolactones, signals for parasitic plants and arbuscular mycorrhizal fungi. Mycorrhiza 19:449–459PubMedCrossRefGoogle Scholar
  25. Goldwasser Y, Yoneyama K, Xie X, Yoneyama K (2008) Production of Strigolactones by Arabidopsis thaliana responsible for Orobanche aegyptiaca seed germination. Plant Growth Regul 55:21–28CrossRefGoogle Scholar
  26. Hartmann A, Schmid M, van Tuinen D, Berg G (2009) Plant-driven selection of microbes. Plant Soil 321:235–257CrossRefGoogle Scholar
  27. Helga W, Lukas KE (2009) The world of organic agriculture—statistics and emerging trends 2009. Bonn, GermanyGoogle Scholar
  28. Hirsch AM, Dietz Bauer W, Bird DM, Cullimore J, Tyler B, Yoder JI (2003) Molecular signals and receptors: controlling rhizosphere interactions between plants and other organisms. Ecology 84:858–868CrossRefGoogle Scholar
  29. 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
  30. Hungria M, Joseph CM, Phillips DA (1991) Anthocyanidins and flavonols, major nod gene Inducers from seeds of a black-seeded common bean (Phaseolus vulgaris L.). Plant Physiol 97:751–758PubMedCrossRefGoogle Scholar
  31. Innes L, Hobbs PJ, Bardgett RD (2004) The impacts of individual plant species on rhizosphere microbial communities in soils of different fertility. Biol Fertil Soils 40:7–13CrossRefGoogle Scholar
  32. Kaplan F, Badri DV, Zachariah C, Ajredini R, Sandoval FJ, Roje S, Levine LH, Zhang F, Robinette SL, Alborn HT, Zhao W, Stadler M, Nimalendran R, Dossey AT, Bruschweiler R, Vivanco JM, Edison AS (2009) Bacterial attraction and quorum sensing inhibition in Caenorhabditis elegans exudates. J Chem Ecol 35:878–892PubMedCrossRefGoogle Scholar
  33. Kaufman DG, Franz CM (1993) Biosphere 2000: protecting our global environment. HarperCollins College Publishers, New YorkGoogle Scholar
  34. Kirk JL, Beaudette LA, Hart M, Moutoglis P, Klironomos JN, Lee H, Trevors JT (2004) Methods of studying soil microbial diversity. J Microbiol Methods 58:169–188PubMedCrossRefGoogle Scholar
  35. Klironomos JN (2003) Variation in plant response to native and exotic arbuscular mycorrhizal fungi: underground processes in plant communities. Ecology 84:2292–2301CrossRefGoogle Scholar
  36. Kobae Y, Sekino T, Yoshioka H, Nakagawa T, Martinoia E, Maeshima M (2006) Loss of AtPDR8, a plasma membrane ABC transporter of Arabidopsis thaliana, causes hypersensitive cell death upon pathogen infection. Plant Cell Physiol 47:309–318PubMedCrossRefGoogle Scholar
  37. Kobae Y, Hata S (2010) Dynamics of periarbuscular membranes visualized with a fluorescent phosphate transporter in arbuscular mycorrhizal roots of rice. Plant Cell Physiol 51:341-353Google Scholar
  38. Kosslak RM, Bookland R, Barkei J, Paaren HE, Appelbaum ER (1987) Induction of Bradyrhizobium japonicum common nod genes by isoflavones isolated from Glycine max. Proc Natl Acad Sci USA 84:7428–7432PubMedCrossRefGoogle Scholar
  39. Kowalchuka GA, Hola WHG, Van Veen JA (2006) Rhizosphere fungal communities are influenced by Senecio jacobaea pyrrolizidine alkaloid content and composition. Soil Biol Biochem 38:2852–2859CrossRefGoogle Scholar
  40. Liljeroth E, Burgers SLGE, van Veen VA (1991) Changes in bacterial populations along roots of wheat (Triticum aestivum L.) seedlings. Biol Fertil Soils 10:276–280CrossRefGoogle Scholar
  41. Liu Z, Lozupone C, Hamady M, Bushman FD, Knight R (2007) Short pyrosequencing reads suffice for accurate microbial community analysis. Nucleic Acids Res 35:e120PubMedCrossRefGoogle Scholar
  42. Mader P, Fliessbach A, Dubois D, Gunst L, Fried P, Niggli U (2002) Soil fertility and biodiversity in organic farming. Science 296:1694–1697PubMedCrossRefGoogle Scholar
  43. Maillet F, Poinsot V, Andre O, Puech-Pages V, Haouy A, Gueunier M, Cromer L, Giraudet D, Formey D, Niebel A, Martinez EA, Driguez H, Becard G, Denarie J (2011) Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469:58–63PubMedCrossRefGoogle Scholar
  44. Maxwell CA, Hartwig UA, Joseph CM, Phillips DA (1989) A chalcone and two related flavonoids released from alfalfa roots induce nod genes of Rhizobium meliloti. Plant Physiol 91:842–847PubMedCrossRefGoogle Scholar
  45. Mazzola M, Funnell DL, Raaijmakers JM (2004) Wheat cultivar-specific selection of 2,4-diacetylphloroglucinol-producing fluorescent Pseudomonas species from resident soil populations. Microb Ecol 48:338–348PubMedCrossRefGoogle Scholar
  46. 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 60:1729–1742PubMedCrossRefGoogle Scholar
  47. Miller RM, Reinhardt DR, Jastrow JD (1995) External hyphal production of vesicular-arbuscular mycorrhizal fungi in pasture and tallgrass prairie communities. Oecologia 103:17–23CrossRefGoogle Scholar
  48. Morgan JA, Bending GD, White PJ (2005) Biological costs and benefits to plant–microbe interactions in the rhizosphere. J Exp Bot 56:1729–1739PubMedCrossRefGoogle Scholar
  49. Mougel C, Offre P, Ranjard L, Corberand T, Gamalero E, Robin C, Lemanceau P (2006) Dynamic of the genetic structure of bacterial and fungal communities at different developmental stages of Medicago truncatula Gaertn. cv. Jemalong line J5. New Phytologist 170:165–175PubMedCrossRefGoogle Scholar
  50. 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 132:146–153PubMedCrossRefGoogle Scholar
  51. Oehl F, Sieverding E, Mader P, Dubois D, Ineichen K, Boller T, Wiemken A (2004) Impact of long-term conventional and organic farming on the diversity of arbuscular mycorrhizal fungi. Oecologia 138:574–583PubMedCrossRefGoogle Scholar
  52. Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6:763–775PubMedCrossRefGoogle Scholar
  53. Perry JN, Moens M (2006) Plant nematology. CABI, CambridgeCrossRefGoogle Scholar
  54. Peters NK, Frost JW, Long SR (1986) A plant flavone, luteolin, induces expression of Rhizobium meliloti nodulation genes. Science 233:977–980PubMedCrossRefGoogle Scholar
  55. Phillips DA, Joseph CM, Maxwell CA (1992) Trigonelline and stachydrine released from alfalfa seeds activate nodD2 protein in Rhizobium meliloti. Plant Physiol 99:1526–1531PubMedCrossRefGoogle Scholar
  56. Postma-Blaauw MB, de Goede RG, Bloem J, Faber JH, Brussaard L (2010) Soil biota community structure and abundance under agricultural intensification and extensification. Ecology 91:460–473PubMedCrossRefGoogle Scholar
  57. Priha O, Grayston SJ, Pennanen T, Smolander A (1999) Microbial activities related to C and N cycling and microbial community structure in the rhizospheres of Pinus sylvestris, Picea abies and Betula pendula seedlings in an organic and mineral soil. FEMS Microbiol Ecol 30:187–199PubMedCrossRefGoogle Scholar
  58. Raaijmakers JM, Paulitz TC, Steinberg C, Alabouvette C, Moënne-Loccoz Y (2009) The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant Soil 321:341–361CrossRefGoogle Scholar
  59. Rangarajan S, Saleena LM, Nair S (2002) Diversity of Pseudomonas spp. isolated from rice rhizosphere populations grown along a salinity gradient. Microb Ecol 43:280–289PubMedCrossRefGoogle Scholar
  60. Redecker D, Kodner R, Graham LE (2000) Glomalean fungi from the Ordovician. Science 289:1920–1921PubMedCrossRefGoogle Scholar
  61. Redmond J, Batley M, Djordjevic M, Innes R, Kuempel P, Rolfe B (1986) Flavones induce expression of nodulation genes in Rhizobium. Nature 323:632–635CrossRefGoogle Scholar
  62. Reganold J, Elliott L, Unger Y (1987) Long-term effects of organic and conventional farming on soil erosion. Nature 330:370–372CrossRefGoogle Scholar
  63. Reinhart KO, Callaway RM (2006) Soil biota and invasive plants. New Phytologist 170:445–457PubMedCrossRefGoogle Scholar
  64. Remy W, Taylor TN, Hass H, Kerp H (1994) Four hundred-million-year-old vesicular arbuscular mycorrhizae. Proc Natl Acad Sci USA 91:11841–11843PubMedCrossRefGoogle Scholar
  65. Rengel Z (2002) Breeding for better symbiosis. Plant Soil 245:147–162CrossRefGoogle Scholar
  66. Rotem J (1994) The genus Alternaria: biology, epidemiology and pathogenicity. American Phytopathological Society Press, St PaulGoogle Scholar
  67. Ryan PR, Dessaux Y, Thomashow LS, Weller DM (2009) Rhizosphere engineering and management for sustainable agriculture. Plant Soil 321:363–383CrossRefGoogle Scholar
  68. Simon L, Bousquet J, Levesque RC, Lalonde M (1993) Origin and diversification of endomycorrhizal fungi and coincidence with vascular land plants. Nature 363:67–69CrossRefGoogle Scholar
  69. Sprent JI (2007) Evolving ideas of legume evolution and diversity: a taxonomic perspective on the occurrence of nodulation. New Phytologist 174:11–25PubMedCrossRefGoogle Scholar
  70. Stein M, Dittgen J, Sanchez-Rodriguez C, Hou BH, Molina A, Schulze-Lefert P, Lipka V, Somerville S (2006) Arabidopsis PEN3/PDR8, an ATP binding cassette transporter, contributes to nonhost resistance to inappropriate pathogens that enter by direct penetration. Plant Cell 18:731–746PubMedCrossRefGoogle Scholar
  71. Sugiyama A, Vivanco JM, Jayanty SS, Manter DK (2010) Pyrosequencing assessment of soil microbial communities in organic and conventional potato farms. Plant Dis 94:1329–1335CrossRefGoogle Scholar
  72. Takagi S (1976) Naturally occurring iron-chelating compounds in oat and rice root-washings. Soil Sci Plant Nutr 22:423–433CrossRefGoogle Scholar
  73. Trevors JT (2010) One gram of soil: a microbial biochemical gene library. Antonie Van Leeuwenhoek 97:99–106Google Scholar
  74. Wissuwa M, Mazzola M, Picard C (2009) Novel approaches in plant breeding for rhizosphere-related traits. Plant Soil 321:409–430CrossRefGoogle Scholar
  75. Wu T, Chellemi DO, Graham JH, Martin KJ, Rosskopf EN (2008) Comparison of soil bacterial communities under diverse agricultural land management and crop production practices. Microb Ecol 55:293–310PubMedCrossRefGoogle Scholar
  76. Yang CH, Crowley DE (2000) Rhizosphere microbial community structure in relation to root location and plant iron nutritional status. Appl Environ Microbiol 66:345–351PubMedCrossRefGoogle Scholar
  77. Yoneyama K, Xie X, Sekimoto H, Takeuchi Y, Ogasawara S, Akiyama K, Hayashi H, Yoneyama K (2008) Strigolactones, host recognition signals for root parasitic plants and arbuscular mycorrhizal fungi, from Fabaceae plants. New Phytologist 179:484–494PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Akifumi Sugiyama
    • 1
    • 2
  • Daniel K. Manter
    • 3
  • Jorge M. Vivanco
    • 1
    Email author
  1. 1.Center for Rhizosphere Biology, Department of Horticulture and Landscape ArchitectureColorado State UniversityFort CollinsUSA
  2. 2.Research Institute for Sustainable HumanosphereKyoto UniversityGokashoJapan
  3. 3.USDA-ARS, Soil, Plant Nutrient Research UnitFort CollinsUSA

Personalised recommendations