Abstract
Background
The root system of a plant is known to host a wide diversity of microbes that can be essential or detrimental to the plant. Microbial ecologists have long struggled to understand what factors structure the composition of these communities. An overlooked part of the microbial community succession in root systems has been the potential for individual variation among plants shaped by early colonisation events such as microbial exposure of the seed inside the parent plant and during dispersal.
Scope
In this review we outline life events of the plant that can affect the composition of its root microbiota and relate ecological theory of community assembly to the formation of the root microbiota.
Conclusion
All plants are exposed to environmental conditions and events throughout their lifetime that shape their phenotype. The microbial community associated with the plant is ultimately an extension of this phenotype. Therefore, only by following a plant from its origin inside the flower to senescence, can we fully understand how the associated microbial community was assembled and what determined its composition.
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References
Agans R, Rigsbee L, Kenche H et al (2011) Distal gut microbiota of adolescent children is different from that of adults. FEMS Microbiol Ecol 1:404–412. doi:10.1111/j.1574-6941.2011.01120.x
Allison SD, Martiny JBH (2008) Colloquium paper: resistance, resilience, and redundancy in microbial communities. P Natl Acad Sci USA 105(Suppl):11512–11519. doi:10.1073/pnas.0801925105
Aulakh MS, Wassmann R, Bueno C et al (2001) Characterization of root exudates at different growth stages of ten rice (Oryza sativa L.) cultivars. Plant Biol 3:139–148. doi:10.1055/s-2001-12905
Bååth E, Anderson T-H (2003) Comparison of soil fungal/bacterial ratios in a pH gradient using physiological and PLFA-based techniques. Soil Biol Biochem 35:955–963
Babich H, Stotzky G (1977) Sensitivity of various bacteria, including actinomycetes, and fungi to cadmium and the influence of pH on sensitivity. Appl Environ Microbiol 33:681–695
Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant Cell Environ 32:666–681. doi:10.1111/j.1365-3040.2009.01926.x
Bailey JK, Deckert R, Schweitzer JA et al (2005) Host plant genetics affect hidden ecological players: links among Populus, condensed tannins, and fungal endophyte infection. Can J Bot 83:356–361. doi:10.1139/B05-008
Bais HP, Weir TL, Perry LG et al (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Ann rev plant biol 57:233–266. doi:10.1146/annurev.arplant.57.032905.105159
Bakker MG, Manter DK, Sheflin AM et al (2012) Harnessing the rhizosphere microbiome through plant breeding and agricultural management. Plant Soil 360:1–13. doi:10.1007/s11104-012-1361-x
Belisle M, Peay KG, Fukami T (2012) Flowers as islands: spatial distribution of nectar-inhabiting microfungi among plants of Mimulus aurantiacus, a hummingbird-pollinated shrub. Microb Ecol 63:711–718. doi:10.1007/s00248-011-9975-8
Belyea LR, Lancaster J (1999) Assembly rules within a contingent ecology. Oikos 86:402–416
Benson AK, Kelly SA, Legge R et al (2010) Individuality in gut microbiota composition is a complex polygenic trait shaped by multiple environmental and host genetic factors. P Natl Acad Sci USA 107:18933–18938. doi:10.1073/pnas.1007028107
Berendsen RL, Pieterse CMJ, Bakker PAHM (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486. doi:10.1016/j.tplants.2012.04.001
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 68:1–13. doi:10.1111/j.1574-6941.2009.00654.x
Bowers RM, Sullivan AP, Costello EK et al. (2011) Sources of bacteria in outdoor air across cities in the midwestern United States. Appl environ microbiol 77:6350–6. doi:10.1128/AEM.05498-11
Broeckling CD, Broz AK, Bergelson J et al (2008) Root exudates regulate soil fungal community composition and diversity. Appl Environ Microbiol 74:738–744. doi:10.1128/AEM.02188-07
Buée M, Boer W, Martin F, Overbeek L and Jurkevitch E (2009) The rhizosphere zoo: An overview of plant-associated communities of microorganisms, including phages, bacteria, archaea, and fungi, and of some of their structuring factors. Plant Soil 321:189–212. doi:10.1007/s11104-009-9991-3
Bulgarelli D, Rott M, Schlaeppi K et al (2012) Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488:91–95. doi:10.1038/nature11336
Chesson P (2000) Mechanisms of maintenance of species diversity. Annu rev Ecol Syst 31:343–366. doi:10.1146/annurev.ecolsys.31.1.343
Claridge AW, Tanton MT, Seebeck JH et al (1992) Establishment of ectomycorrhizae on the roots of two species of Eucalyptus from fungal spores contained in the faeces of the long-nosed potoroo (Potorous tridactylus). Austral Ecol 17:207–217. doi:10.1111/j.1442-9993.1992.tb00799.x
Compant S, Clément C and Sessitsch A (2010) Plant growth-promoting bacteria in the rhizo- and endosphere of plants: Their role, colonization, mechanisms involved and prospects for utilization. Soil Biol Biochem 42:669–678. doi:10.1016/j.soilbio.2009.11.024
Compant S, Mitter B, Colli-Mull JG et al (2011) Endophytes of grapevine flowers, berries, and seeds: identification of cultivable bacteria, comparison with other plant parts, and visualization of niches of colonization. Microb Ecol 62:188–197. doi:10.1007/s00248-011-9883-y
Costello EK, Stagaman K, Dethlefsen L et al (2012) The application of ecological theory toward an understanding of the human microbiome. Sci (N Y, NY) 336:1255–1262. doi:10.1126/science.1224203
De Boer W, Folman LB, Summerbell RC, Boddy L (2005) Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol Rev 29:795–811. doi:10.1016/j.femsre.2004.11.005
Dodd J, Jeffries P (1986) Early development of vesicular-arbuscular mycorrhizas in autumn-sown cereals. Soil Biol Biochem 18:149–154. doi:10.1016/0038-0717(86)90019-2
Doornbos RF, Geraats BPJ, Kuramae EE et al (2011a) Effects of jasmonic acid, ethylene, and salicylic acid signaling on the rhizosphere bacterial community of Arabidopsis thaliana. Mol Plant-Microb: MPMI 24:395–407. doi:10.1094/MPMI-05-10-0115
Doornbos RF, Van Loon LC, Bakker PAHM (2011b) Impact of root exudates and plant defense signaling on bacterial communities in the rhizosphere. A review. Agron Sustain Dev 32:227–243. doi:10.1007/s13593-011-0028-y
Dumbrell AJ, Nelson M, Helgason T et al (2010) Relative roles of niche and neutral processes in structuring a soil microbial community. ISME J 4:337–345. doi:10.1038/ismej.2009.122
Dumbrell AJ, Ashton PD, Aziz N et al (2011) Distinct seasonal assemblages of arbuscular mycorrhizal fungi revealed by massively parallel pyrosequencing. New Phytol 190:794–804. doi:10.1111/j.1469-8137.2010.03636.x
Dunne MJ, Fitter AH (1989) The phosphorus budget of a field-grown strawberry (Fragaria x ananassa cv. Hapil) crop: evidence for a mycorrhizal contribution. Ann Appl Biol 114:185–193. doi:10.1111/j.1744-7348.1989.tb06799.x
Eisenlord SD, Zak DR, Upchurch RA (2012) Dispersal limitation and the assembly of soil Actinobacteria communities in a long-term chronosequence. Ecol Evol 2:538–549. doi:10.1002/ece3.210
Fierer N (2008) Microbial biogeography: patterns in microbial diversity across space and time. In: Zengler K (ed) Accessing uncultivated microorganisms: from the environment to organisms and genomes and back. ASM press, Washington DC, pp 95–115
Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. P Natl Acad Sci USA 103:626–631. doi:10.1073/pnas.0507535103
Fierer N, Nemergut D, Knight R, Craine JM (2010) Changes through time: integrating microorganisms into the study of succession. Res Microbiol 161:635–642. doi:10.1016/j.resmic.2010.06.002
Finlay BJ (2002) Global dispersal of free-living microbial eukaryote species. Science 296:1061–1063. doi:10.1126/science.1070710
Friese CF, Allen MF (1991) The spread of VA mycorrhizal fungal hyphae in the soil: inoculum types and external hyphal architecture. Mycologia 83:409–418. doi:10.2307/3760351
Fukami T, Nakajima M (2011) Community assembly: alternative stable states or alternative transient states? Ecol Lett 14:973–984. doi:10.1111/j.1461-0248.2011.01663.x
Fukami T, Martijn Bezemer T, Mortimer SR, Putten WH (2005) Species divergence and trait convergence in experimental plant community assembly. Ecol Lett 8:1283–1290. doi:10.1111/j.1461-0248.2005.00829.x
Fukami T, Dickie IA, Wilkie JP et al (2010) Assembly history dictates ecosystem functioning: evidence from wood decomposer communities. Ecol Lett 13:675–684. doi:10.1111/j.1461-0248.2010.01465.x
Fulthorpe RR, Rhodes AN, Tiedje JM (1998) High levels of endemicity of 3-Chlorobenzoate-degrading soil bacteria. Appl Environ Ecol 64:1620–1627
Fürnkranz M, Lukesch B, Müller H et al (2012) Microbial diversity inside pumpkins: microhabitat-specific communities display a high antagonistic potential against phytopathogens. Microb Ecol 63:418–428. doi:10.1007/s00248-011-9942-4
Gilbert JA, Meyer F (2012) Modeling the earth’s microbiome: a real world deliverable for microbial ecology. ASM Microbe Mag
Gilbert JA, Steele JA, Caporaso JG et al (2012) Defining seasonal marine microbial community dynamics. ISME J 6:298–308. doi:10.1038/ismej.2011.107
Gonzalez A, Clemente JC, Shade A et al (2011) Our microbial selves: what ecology can teach us. EMBO Reports 12:775–784. doi:10.1038/embor.2011.137
Gransee A, Wittenmayer L (2000) Qualitative and quantitative analysis of water-soluble root exudates in relation to plant species and development. J Plant Nutr Soil Sci 163:381–385. doi:10.1002/1522-2624(200008)163:4<381::AID-JPLN381>3.0.CO;2-7
Green J, Bohannan BJM (2006) Spatial scaling of microbial biodiversity. Trends Ecol Evol 21:501–507. doi:10.1016/j.tree.2006.06.012
Green SJ, Inbar E, Michel FC et al (2006) Succession of bacterial communities during early plant development: transition from seed to root and effect of compost amendment. Appl Environ Microbiol 72:3975–3983. doi:10.1128/AEM.02771-05
Gutjahr C, Paszkowski U (2009) Weights in the balance: jasmonic acid and salicylic acid signaling in root-biotroph interactions. Mol Plant-Microb:MPMI 22:763–772. doi:10.1094/MPMI-22-7-0763
Hartmann A, Schmid M, Van Tuinen D, Berg G (2009) Plant-driven selection of microbes. Plant Soil 321:235–257. doi:10.1007/s11104-008-9814-y
Hawkes CV, DeAngelis KM, Firestone MK (2007) Root interactions with soil microbial communitites and processes. In: Cardon Z and Whitbeck J (eds). The Rhizosphere. Elsevier, New York
Hazard C, Gosling P, Van der Gast CJ et al (2012) The role of local environment and geographical distance in determining community composition of arbuscular mycorrhizal fungi at the landscape scale. ISME J 1–11. doi:10.1038/ismej.2012.127
Hodge A, Berta G, Doussan C et al (2009) Plant root growth, architecture and function. Plant Soil 321:153–187. doi:10.1007/s11104-009-9929-9
Hodge A, Helgason T, Fitter AH (2010) Nutritional ecology of arbuscular mycorrhizal fungi. Fungal Ecol 3:267–273. doi:10.1016/j.funeco.2010.02.002
Hoeksema JD, Chaudhary VB, Gehring CA et al (2010) A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecol Lett 13:394–407. doi:10.1111/j.1461-0248.2009.01430.x
Horner-Devine MC, Carney KM, Bohannan BJM (2004) An ecological perspective on bacterial biodiversity. P Roy Soc Biol Sci 271:113–122. doi:10.1098/rspb.2003.2549
Houlden A, Timms-Wilson TM, Day MJ, Bailey MJ (2008) Influence of plant developmental stage on microbial community structure and activity in the rhizosphere of three field crops. FEMS Microbiol Ecol 65:193–201. doi:10.1111/j.1574-6941.2008.00535.x
Hubbell S (2001) The unified neutral theory of biodiversity and biogeography, Monogr pop biol, vol 32. Princeton University Press, Princeton
Jenkins DG, Brescacin CR, Duxbury CV et al (2007) Does size matter for dispersal distance? Global Ecol Biogeogr 16:415–425. doi:10.1111/j.1466-8238.2007.00312.x
Johnson NC (2010) Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales. New Phytol 185:631–647. doi:10.1111/j.1469-8137.2009.03110.x
Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329. doi:10.1038/nature05286
Jones DL, Hodge A, Kuzyakov Y (2004) Plant and mycorrhizal regulation of rhizodeposition. New Phytol 163:459–480. doi:10.1111/j.1469-8137.2004.01130.x
Kardol P, Cornips NJ, Van Kempen MML et al (2007) Microbe-mediated plant–soil feedback causes historical contingency effects in plant community assembly. Ecol Monogr 77:147–162. doi:10.1890/06-0502
Kennedy PG, Bruns TD (2005) Priority effects determine the outcome of ectomycorrhizal competition between two Rhizopogon species colonizing Pinus muricata seedlings. New Phytol 166:631–638. doi:10.1111/j.1469-8137.2005.01355.x
Kennedy PG, Peay KG, Bruns TD (2009) Root tip competition among ectomycorrhizal fungi: Are priority effects a rule or an exception? Ecology 90:2098–2107. doi:10.1890/08-1291.1
Koenig JE, Spor A, Scalfone N et al (2011) Succession of microbial consortia in the developing infant gut microbiome. P Natl Acad Sci USA 108(Suppl):4578–4585. doi:10.1073/pnas.1000081107
Koide RT (2010) Mycorrhizal symbiosis and plant reproduction. In: Koltai H, Kapulnik Y (eds) Arbuscular mycorrhizas: physiology and function. Springer Netherlands, Dordrecht, pp 297–320
Kotter MM, Farentinos RC (1984) Tassel-eared squirrels as spore dispersal agents of hypogeous mycorrhizal fungi. J Mammal 65:684. doi:10.2307/1380853
Larsen PE, Gibbons SM, Gilbert JA (2012) Modeling microbial community structure and functional diversity across time and space. FEMS Microbiol Lett 332:91–98. doi:10.1111/j.1574-6968.2012.02588.x
Latch GCM (1993) Physiological interactions of endophytic fungi and their hosts. Biotic stress tolerance imparted to grasses by endophytes. Agr Ecosyst Environ 44:143–156. doi:10.1016/0167-8809(93)90043-O
Lau JA, Lennon JT (2011) Evolutionary ecology of plant-microbe interactions: soil microbial structure alters selection on plant traits. New Phytol 192:215–224. doi:10.1111/j.1469-8137.2011.03790.x
Lauber CL, Hamady M, Knight R, Fierer N (2009) Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol 75:5111–5120. doi:10.1128/AEM.00335-09
Leibold MA, McPeek MA (2006) Coexistence of the niche and neutral perspectives in community ecology. Ecology 87:1399–1410. doi:10.1890/0012-9658(2006)87[1399:COTNAN]2.0.CO;2
Lekberg Y, Koide RT, Rohr JR et al (2007) Role of niche restrictions and dispersal in the composition of arbuscular mycorrhizal fungal communities. J Ecol 95:95–105. doi:10.1111/j.1365-2745.2006.01193.x
Liu Y, Zuo S, Zou Y et al (2012) Investigation on diversity and population succession dynamics of indigenous bacteria of the maize spermosphere. World J Microb Biot 28:391–396. doi:10.1007/s11274-011-0822-3
Lundberg DS, Lebeis SL, Paredes SH et al (2012) Defining the core Arabidopsis thaliana root microbiome. Nature 488:86–90. doi:10.1038/nature11237
Marschner P, Neumann G, Kania A (2002) Spatial and temporal dynamics of the microbial community structure in the rhizosphere of cluster roots of white lupin (Lupinus albus L.). Plant Soil 246:167–174
Marschner P, Crowley D, Rengel Z (2011) Rhizosphere interactions between microorganisms and plants govern iron and phosphorus acquisition along the root axis – model and research methods. Soil Biol Biochem 43:883–894. doi:10.1016/j.soilbio.2011.01.005
Martiny JBH, Bohannan BJM, Brown JH et al (2006) Microbial biogeography: putting microorganisms on the map. Nat Rev Microbiol 4:102–112. doi:10.1038/nrmicro1341
Maser C, Trappe JM, Nussbaum RA (1978) Fungal-small mammal interrelationships with emphasis on Oregon coniferous forests. Ecology 59:799. doi:10.2307/1938784
McIlveen WD, Cole HJ (1976) Spore dispersal of Endogonaceae by worms, ants, wasps, and birds. Can J Bot 54:1486–1489. doi:10.1139/b76-161
Mendes R, Kruijt M, De Bruijn I et al (2011) Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Sci (N Y, NY) 332:1097–1100. doi:10.1126/science.1203980
Merryweather J, Fitter A (1998) The arbuscular mycorrhizal fungi of Hyacinthoides non-scripta: seasonal and spatial patterns of fungal populations. New Phytol 138:131–142. doi:10.1046/j.1469-8137.1998.00889.x
Micallef SA, Channer S, Shiaris MP, Colón-Carmona A (2009) Plant age and genotype impact the progression of bacterial community succession in the Arabidopsis rhizosphere. Plant Signal Behav 4:777–780. doi:10.1093/jxb/erp053
Mougel C, Offre P, Ranjard L 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 170:165–175. doi:10.1111/j.1469-8137.2006.01650.x
Nelson EB (2004) Microbial dynamics and interactions in the spermosphere. Ann Rev Phytopathol 42:271–309. doi:10.1146/annurev.phyto.42.121603.131041
Normander B, Prosser JI (2000) Bacterial origin and community composition in the barley phytosphere as a function of habitat and presowing conditions. Appl Environ Microbiol 66:4372–4377. doi:10.1128/AEM.66.10.4372-4377.2000
Norros V, Penttilä R, Suominen M, Ovaskainen O (2012) Dispersal may limit the occurrence of specialist wood decay fungi already at small spatial scales. Oikos 121:961–974. doi:10.1111/j.1600-0706.2012.20052.x
Oehl F, Laczko E, Bogenrieder A et al (2010) Soil type and land use intensity determine the composition of arbuscular mycorrhizal fungal communities. Soil Biol Biochem 42:724–738. doi:10.1016/j.soilbio.2010.01.006
Packer A, Clay K (2000) Soil pathogens and spatial patterns of seedling mortality in a temperate tree. Nature 404:278–281. doi:10.1038/35005072
Pivato B, Mazurier S, Lemanceau P et al (2007) Medicago species affect the community composition of arbuscular mycorrhizal fungi associated with roots. New Phytol 176:197–210. doi:10.1111/j.1469-8137.2007.02151.x
Pivato B, Offre P, Marchelli S et al (2009) Bacterial effects on arbuscular mycorrhizal fungi and mycorrhiza development as influenced by the bacteria, fungi, and host plant. Mycorrhiza 19:81–90. doi:10.1007/s00572-008-0205-2
Porras-Alfaro A, Bayman P (2011) Hidden fungi, emergent properties: endophytes and microbiomes. Ann Rev Phytopathol 49:291–315. doi:10.1146/annurev-phyto-080508-081831
Raaijmakers JM, Paulitz TC, Steinberg C et al (2008) The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant Soil 321:341–361. doi:10.1007/s11104-008-9568-6
Ramette A, Tiedje JM (2007) Multiscale responses of microbial life to spatial distance and environmental heterogeneity in a patchy ecosystem. P Natl Acad Sci USA 104:2761–2766. doi:10.1073/pnas.0610671104
Rillig MC, Mummey DL, Ramsey PW et al (2006) Phylogeny of arbuscular mycorrhizal fungi predicts community composition of symbiosis-associated bacteria. FEMS Microbiol Ecol 57:389–395. doi:10.1111/j.1574-6941.2006.00129.x
Rodriguez R, Redman R (2008) More than 400 million years of evolution and some plants still can’t make it on their own: plant stress tolerance via fungal symbiosis. J Exp Bot 59:1109–1114. doi:10.1093/jxb/erm342
Rousk J, Demoling LA, Bahr A, Bååth E (2008) Examining the fungal and bacterial niche overlap using selective inhibitors in soil. FEMS Microbiol Ecol 63:350–358. doi:10.1111/j.1574-6941.2008.00440.x
Rousk J, Bååth E, Brookes PC et al (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 4:1340–1351. doi:10.1038/ismej.2010.58
Rousk J, Brookes PC, Bååth E (2011) Fungal and bacterial growth responses to N fertilization and pH in the 150-year “Park Grass” UK grassland experiment. FEMS Microbiol Ecol 76:89–99. doi:10.1111/j.1574-6941.2010.01032.x
Schnitzer SA, Klironomos JN, HilleRisLambers J et al (2011) Soil microbes drive the classic plant diversity–productivity pattern. Ecology 92:296–303. doi:10.1890/10-0773.1
Schweitzer JA, Bailey JK, Fischer DG et al (2008) Plant–soil–microorganism interactions: heritable relationship between plant genotype and associated soil microorganisms. Ecology 89:773–781. doi:10.1890/07-0337.1
Sekirov I, Russell SL, Antunes LCM, Finlay BB (2010) Gut microbiota in health and disease. Physiol Rev 90:859–904. doi:10.1152/physrev.00045.2009
Shade A, McManus PS, Handelsman J (2013) Unexpected diversity during community succession in the apple flower microbiome. mBio In press
Shuster SM, Lonsdorf EV, Wimp GM et al (2006) Community heritability measures the evolutionary consequences of indirect genetic effects on community structure. Evolution 60:991–1003. doi:10.1111/j.0014-3820.2006.tb01177.x
Singh BK, Munro S, Potts JM, Millard P (2007) Influence of grass species and soil type on rhizosphere microbial community structure in grassland soils. Appl Soil Ecol 36:147–155. doi:10.1016/j.apsoil.2007.01.004
Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic, London
Smith DJ, Timonen H, Jaffe D et al (2012) Intercontinental dispersal of bacteria and archaea in transpacific winds. Appl Environ Microbiol. doi:10.1128/AEM.03029-12
Spor A, Koren O, Ley R (2011) Unravelling the effects of the environment and host genotype on the gut microbiome. Nat Rev Microbiol 9:279–290. doi:10.1038/nrmicro2540
Stockwell VO, McLaughlin RJ, Henkels MD et al. (1999) Epiphytic colonization of pear stigmas and hypanthia by bacteria during primary bloom. Phytopathology 89:1162–8. doi:10.1094/PHYTO.1999.89.12.1162
The Human Microbiome Project Consortium (2012) Structure, function and diversity of the healthy human microbiome. Nature 486:207–214. doi:10.1038/nature11234
Theimer T, Gehring C (2007) Mycorrhizal plants and vertebrate seed and spore dispersal: incorporating mycorrhizas into the seed dispersal paradigm. In: Dennis AJ, Green RJ, Schupp EW, Westcott DA (eds) Seed Dispersal: Theory and its Application in a Changing World. CAB International 2007 pp 463–478
Thomas H (2012) Senescence, ageing and death of the whole plant. New Phytol. doi:10.1111/nph.12047
Toljander JF, Santos-González JC, Tehler A, Finlay RD (2008) Community analysis of arbuscular mycorrhizal fungi and bacteria in the maize mycorrhizosphere in a long-term fertilization trial. FEMS Microbiol Ecol 65:323–338. doi:10.1111/j.1574-6941.2008.00512.x
Torsvik V, Øvreås L (2002) Microbial diversity and function in soil: from genes to ecosystems. Curr Opin Microbiol 5:240–245. doi:10.1016/S1369-5274(02)00324-7
Traveset A (1998) Effect of seed passage through vertebrate frugivores’ guts on germination: a review. Perspect Plant Ecol 1:151–190. doi:10.1078/1433-8319-00057
Traveset A, Verdú M (2002) A meta-analysis of the seed germination. In: Levey DJ, Silva WR, Galetti M (eds) Seed dispersal and frugivory: ecology, evolution and conservation. CABI pp 339–350
Treseder KK, Allen MF (2002) Direct nitrogen and phosphorus limitation of arbuscular mycorrhizal fungi: a model and field test. New Phytol 155:507–515. doi:10.1046/j.1469-8137.2002.00470.x
Turnbaugh PJ, Hamady M, Yatsunenko T et al (2009) A core gut microbiome in obese and lean twins. Nature 457:480–484. doi:10.1038/nature07540
Van der Heijden MGA, Streitwolf-Engel R, Riedl R et al (2006) The mycorrhizal contribution to plant productivity, plant nutrition and soil structure in experimental grassland. New Phytol 172:739–752. doi:10.1111/j.1469-8137.2006.01862.x
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. doi:10.1111/j.1461-0248.2007.01139.x
Van Overbeek LS, Franke AC, Nijhuis EHM et al (2011) Bacterial communities associated with Chenopodium album and Stellaria media seeds from arable soils. Microb Ecol 62:257–264. doi:10.1007/s00248-011-9845-4
Wang B, Qiu Y-L (2006) Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16:299–363. doi:10.1007/s00572-005-0033-6
Warner NJ, Allen MF, MacMahon JA (1987) Dispersal agents of Vesicular-Arbuscular mycorrhizal fungi in a disturbed arid ecosystem. Mycologia 79:721. doi:10.2307/3807824
Whitaker RJ, Grogan DW, Taylor JW (2003) Geographic barriers isolate endemic populations of hyperthermophilic archaea. Science 301:976–978. doi:10.1126/science.1086909
Whitham TG, Bailey JK, Schweitzer JA et al (2006) A framework for community and ecosystem genetics: from genes to ecosystems. Nat Rev Genet 7:510–523. doi:10.1038/nrg1877
Wieland G, Neumann R, Backhaus H (2001) Variation of microbial communities in soil, rhizosphere, and rhizoplane in response to crop species, soil type, and crop development. Appl Environ Microbiol 67:5849–5854. doi:10.1128/AEM.67.12.5849-5854.2001
Wilson GWT, Hartnett DC (1998) Interspecific variation in plant responses to mycorrhizal colonization in tallgrass prairie. Am J Bot 85:1732. doi:10.2307/2446507
Zamioudis C, Pieterse CMJ (2012) Modulation of host immunity by beneficial microbes. Mol Plant-Microb: MPMI 25:139–150. doi:10.1094/MPMI-06-11-0179
Zinger L, Shahnavaz B, Baptist F et al (2009) Microbial diversity in alpine tundra soils correlates with snow cover dynamics. ISME J 3:850–859. doi:10.1038/ismej.2009.20
Acknowledgments
We would like to thank our reviewers for good inputs and ideas on how to present our model in a clear and informative way as well as help with editing and inspiration from colleagues and friends such as David Kadish, Monika Gorzelak and Megan Rúa.
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Responsible Editor: Jorge Vivanco.
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Kristin, A., Miranda, H. The root microbiota—a fingerprint in the soil?. Plant Soil 370, 671–686 (2013). https://doi.org/10.1007/s11104-013-1647-7
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DOI: https://doi.org/10.1007/s11104-013-1647-7