A widespread plant-fungal-bacterial symbiosis promotes plant biodiversity, plant nutrition and seedling recruitment

ISME Journal

Volumn 10, Issue 2, 2016, Pages 389-399

  Van Der Heijden, Marcel G A ^a,b,c   Bruin, Susanne De ^d   Luckerhoff, Ludo ^d   Van Logtestijn, Richard S P ^d   Schlaeppi, Klaus ^a  

^a Plant Soil Interactions Institute for Sustainability Sciences   (Switzerland)

^b UTRECHT UNIVERSITY   (Netherlands)

^c UNIVERSITY OF ZURICH   (Switzerland)

^d VU UNIVERSITY AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ARBUSCULAR MYCORRHIZA; BIODIVERSITY; FUNGUS; GRASSLAND; LEGUME; NUTRIENT UPTAKE; NUTRITION; RECRUITMENT (POPULATION DYNAMICS); RHIZOBACTERIUM; ROOT COLONIZATION; SEEDLING ESTABLISHMENT; SPECIES DIVERSITY; SYMBIOSIS;

BACTERIA (MICROORGANISMS); FUNGI;

NITROGEN;

BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIUM; BIODIVERSITY; FABACEAE; FUNGUS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; MYCORRHIZA; PHYSIOLOGY; PLANT ROOT; SEEDLING; SYMBIOSIS;

BACTERIA; BACTERIAL PHYSIOLOGICAL PHENOMENA; BIODIVERSITY; FABACEAE; FUNGI; MYCORRHIZAE; NITROGEN; PLANT ROOTS; SEEDLINGS; SYMBIOSIS;

EID: 84955109845     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2015.120     Document Type: Article

References (56)

1. Al-Mufti MM, Sydes CL, Furness SB, Grime JP, Band SR. (1977). A quantitative analysis of shoot phenology and dominance in herbaceous vegetation. J Ecol 65: 759-791.
2. Bauer JT, Kleczewski NM, Bever JD, Clay K, Reynolds HL. (2012). Nitrogen-fixing bacteria, arbuscular mycorrhizal fungi, and the productivity and structure of prairie grassland communities. Oecologia 170: 1089-1098.
3. Bécard G, Piché Y. (1992). Establishment of vesiculararbuscular mycorrhiza in root organ culture: review and proposed methodology. In Norris JR, Read DJ, Varma AK (eds), Methods in Microbiology, Vol. 24. Academic Press: London, pp 89-108.
4. Berendsen RL, Pieterse CM, Bakker PA. (2012). The rhizosphere microbiome and plant health. Trends Plant Sci 17: 478-486.
5. Bethlenfalvay GJ, Pacovsky RS, Bayne HG, Stafford AE. (1982). Interactions between nitrogen fixation, mycorrhizal colonization, and host-plant growth in the phaseolus-rhizobium-glomus symbiosis. Plant Physiol 70: 446-450.
6. Bonfante P, Genre A. (2010). Mechanisms underlying beneficial plant-fungus interactions in mycorrhizal symbiosis. Nat Commun 1: 48.
7. Bulgarelli D, Rott M, Schlaeppi K, Ver Loren van Themaat E, Ahmadinejad N, Assenza F et al. (2012). Revealing structure and assembly cues for Arabidopsis rootinhabiting bacterial microbiota. Nature 488: 91-95.
8. Bulgarelli D, Schlaeppi K, Spaepen S, Ver Loren van Themaat E, Schulze-Lefert P. (2013). Structure and functions of the bacterial microbiota of plants. Annu Rev Plant Biol 64: 807-838.
9. Cleveland CC, Townsend AR, Schimel DS, Fisher H, Howarth RW, Hedin LO et al. (1999). Global patterns of terrestrial biological nitrogen (N2) fixation in natural ecosystems. Global Biogeochem Cycles 13: 623-645.
10. Curtis TP, Sloan WT, Scannell JW. (2002). Estimating prokaryotic diversity and its limits. Proc Natl Acad Sci USA 99: 10494-10499.
11. De Bary A (1879). Die Erscheinung der Symbiose. Strassburg, Germany: Verlag von Karl J. Trubner.
12. De Faria SM, Diedhiou AG, de Lima HC, Ribeiro RD, Galiana A, Castilho AF et al. (2010). Evaluating the nodulation status of leguminous species from the Amazonian forest of Brazil. J Exp Bot 61: 3119-3127.
13. Drigo B, Pijl AS, Duyts H, Kielak AM, Gamper HA, Houtekamer MJ et al. (2010). Shifting carbon flow from roots into associated microbial communities in response to elevated atmospheric CO2. Proc Natl Acad Sci USA 107: 10938-10942.
14. Eisenhauer N. (2012). Aboveground-belowground interactions as a source of complementarity effects in biodiversity experiments. Plant Soil 351: 1-22.
15. Elser JJ, Bracken MES, Cleland EE, Gruner DS, Harpole WS, Hillebrand H et al. (2007). Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol Lett 10: 1135-1142.
16. Galloway JN, Dentener FJ, Capone DG, Boyer EW, Howarth RW, Seitzinger SP et al. (2004). Nitrogen cycles: Past, present, and future. Biogeochemistry 70: 153-226.
17. Grime JP, Mackey JML, Hillier SH, Read DJ. (1987). Floristic diversity in a model system using experimental microcosms. Nature 328: 420-422.
18. Hautier Y, Seabloom EW, Borer ET, Adler PB, Harpole WS, Hillebrand H et al. (2014). Eutrophication weakens stabilizing effects of diversity in natural grasslands. Nature 508: 521-525.
19. Herridge DF, Peoples MB, Boddey RM. (2008). Global inputs of biological nitrogen fixation in agricultural systems. Plant Soil 311: 1-18.
20. Högberg P. (1997). Tansley Review NO 95-N-15 Natural abundance in soil - plant systems. New Phytol 137: 179-203.
21. Isbell F, Calcagno V, Hector A, Connolly J, Harpole WS, Reich PB et al. (2011). High plant diversity is needed to maintain ecosystem services. Nature 477: 199-202.
22. Jakobsen I, Abbott LK, Robson AD. (1992). External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum L. New Phytol 120: 371-380.
23. Janssens F, Peeters A, Tallowin JRB, Bakker JP, Bekker RM, Fillat F et al. (1998). Relationship between soil chemical factors and grassland diversity. Plant Soil 202: 69-78.
24. Kooijman AM, Dopheide JCR, Sevink J, Takken I, Verstraten JM. (1998). Nutrient limitations and their implications on the effects of atmospheric deposition in coastal dunes; lime-poor and lime-rich sites in the Netherlands. J Ecol 86: 511-526.
25. Larimer AL, Bever JD, Clay K. (2010). The interactive effects of plant microbial symbionts: A review and meta-analysis. Symbiosis 51: 139-148.
26. Mack KML, Rudgers JA. (2008). Balancing multiple mutualists: Asymmetric interactions among plants, arbuscular mycorrhizal fungi, and fungal endophytes. Oikos 117: 310-320.
27. McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA. (1990). A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytol 115: 495-501.
28. Mendes R, Kruijt M, de Bruijn I, Dekkers E, van der VoortM, JHM Schneider et al. (2011). Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332: 1097-1100.
29. Mosse B, Powell C, Hayman D. (1976). Plant growth responses to vesicular-arbuscular mycorrhiza. New Phytol 76: 331-342.
30. Munkvold L, Kjoller R, Vestberg M, Rosendahl S, Jakobsen I. (2004). High functional diversity within species of arbuscular mycorrhizal fungi. New Phytol 164: 357-364.
31. Murphy J, Riley JP. (1962). A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27: 31-36.
32. Nasto MK, Alvarez-Clare S, Lekberg Y, Sullivan BW, Townsend AR, Cleveland CC. (2014). Interactions among nitrogen fixation and soil phosphorus acquisition strategies in lowland tropical rain forests. Ecol Lett 17: 1282-1289.
33. Oksanen J, Blanchet F, Kindt R, Legendre P, Minchin P, O'Hara R et al. (2013). vegan: Community Ecology Package. R package version 2. 0-10. R Packag version 1: 10. 4135/9781412971874. N145.
34. Olde Venterink H, WassenMJ, Verkroost AWM, De Ruiter PC. (2003). Species richness-productivity patterns differ between N-, P-, and K-limited wetlands. Ecology 84: 2191-2199.
35. Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team. (2009). Nlme: Linear and Nonlinear Mixed Effects Models. R package version 3. 1-120. Available at http://CRAN. R-project. org/package=nlme.
36. R Core Team. (2014). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing: Vienna, Austria. http://www. R-project. org/.
37. Read DJ. (2002). Towards ecological relevance - progress and pitfalls in the path towards an understanding of mycorrhizal functions in nature. In: Van der Heijden MGA, Sanders IR (eds). Ecological Studies: Mycorrhizal Ecology, Vol. 157. Springer: Berlin, Heidelberg, pp 3-29.
38. Requena N, Jimenez I, Toro M, Barea JM. (1997). Interactions between plant-growth-promoting rhizobacteria (PGPR), arbuscular mycorrhizal fungi and Rhizobium spp. in the rhizosphere of Anthyllis cytisoides, a model legume for revegetation in mediterranean semi-arid ecosystems. New Phytol 136: 667-677.
39. Scherber C, Eisenhauer N, WeisserWW, Schmid B, VoigtW, Fischer M et al. (2010). Bottom-up effects of plant diversity on multitrophic interactions in a biodiversity experiment. Nature 468: 553-556.
40. Scheublin TR, Ridgway KP, Young JPW, Van Der Heijden MGA. (2004). Nonlegumes, legumes, and root nodules harbor different arbuscular mycorrhizal fungal communities. Appl Environ Microbiol 70: 6240-6246.
41. Scheublin TR, van der Heijden MGA. (2006). Arbuscular mycorrhizal fungi colonize nonfixing root nodules of several legume species. New Phytol 172: 732-738.
42. Sessitsch A, Hardoim P, Döring J, Weilharter A, Krause A, Woyke T et al. (2012). Functional characteristics of an endophyte community colonizing rice roots as revealed by metagenomic analysis. Mol Plant Microbe Interact 25: 28-36.
43. Sieverding E, da Silva GA, Berndt R, Oehl F. (2014). Rhizoglomus, a new genus of the Glomeraceae. Mycotaxon 129: 373-386.
44. Siviero MA, Motta AM, Lima D, dos S, Birolli RR, Huh SY, Santinoni IA et al. (2008). Interaction among N-fixing bacteria and AM fungi in Amazonian legume tree (Schizolobium amazonicum) in field conditions. Appl Soil Ecol 39: 144-152.
45. Smith SE, Read D. (2008). Mycorrhizal Symbiosis3rd edn. Academic PressLondon, UK.
46. Tilman D, Knops J, Wedin D, Reich P, Ritchie M, Siemann E. (1997). The influence of functional diversity and composition on ecosystem processes. Science 277: 1300-1302.
47. Van der Heijden MGA, Bakker R, Verwaal J, Scheublin TR, Rutten M, van Logtestijn R et al. (2006). Symbiotic bacteria as a determinant of plant community structure and plant productivity in dune grassland. FEMS Microbiol Ecol 56: 178-187.
48. 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: 296-310.
49. Van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T et al. (1998). Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396: 69-72.
50. Van der Heijden MGA, Martin FM, Selosse M-A, Sanders IR. (2015). Mycorrhizal ecology and evolution: The past, the present, and the future. New Phytol 205: 1406-1423.
51. 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. Proc Natl Acad Sci 109: 1159-1164.
52. Vandenkoornhuyse P, Ridgway KP, Watson IJ, Fitter AH, Young JPW. (2003). Co-existing grass species have distinctive arbuscular mycorrhizal communities. Mol Ecol 12: 3085-3095.
53. Wagg C, Bender SF, Widmer F, van der Heijden MGA. (2014). Soil biodiversity and soil community composition determine ecosystem multifunctionality. Proc Natl Acad Sci USA 111: 5266-5270.
54. Wang B, Qiu YL. (2006). Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16: 299-363.
55. Wardle DA, Bardgett RD, Klironomos JN, Setälä H, van der Putten WH, Wall DH. (2004). Ecological linkages between aboveground and belowground biota. Science 304: 1629-1633.
56. Willems JH, Peet RK, Bik L. (1993). Changes in chalkgrassland structure and species richness resulting from selective nutrient additions. J Veg Sci 4: 203-212.