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Plant function and evolutionary biology
RESEARCH ARTICLE (Open Access)

The microbiomes on the roots of wheat (Triticum aestivum L.) and rice (Oryza sativa L.) exhibit significant differences in structure between root types and along root axes

Akitomo Kawasaki A F , Paul G. Dennis B , Christian Forstner B , Anil K. H. Raghavendra B F , Alan E. Richardson A , Michelle Watt C , Ulrike Mathesius D , Matthew Gilliham E and Peter R. Ryan https://orcid.org/0000-0002-1376-9543 A G
+ Author Affiliations
- Author Affiliations

A CSIRO Agriculture and Food, PO Box 1700, Canberra, ACT 2601, Australia.

B School of Earth and Environmental Sciences, Faculty of Sciences, The University of Queensland, St Lucia, Qld 4072, Australia.

C School of BioSciences, University of Melbourne, Parkville, Vic. 3010, Australia.

D Division of Plant Sciences, Research School of Biology, Australian National University, Canberra, ACT 2601, Australia.

E ARC Centre of Excellence in Plant Energy Biology, School of Agriculture, Food and Wine, Waite Research Institute, University of Adelaide, Glen Osmond, SA 5064, Australia.

F Present address: NSW Department of Primary Industries, Elizabeth Macarthur Agricultural Institute, Menangle, NSW 2568, Australia.

G Corresponding author. Email: peter.ryan@csiro.au

Functional Plant Biology 48(9) 871-888 https://doi.org/10.1071/FP20351
Submitted: 12 November 2020  Accepted: 22 March 2021   Published: 3 May 2021

Journal Compilation © CSIRO 2021 Open Access CC BY

Abstract

There is increasing interest in understanding how the microbial communities on roots can be manipulated to improve plant productivity. Root systems are not homogeneous organs but are comprised of different root types of various ages and anatomies that perform different functions. Relatively little is known about how this variation influences the distribution and abundance of microorganisms on roots and in the rhizosphere. Such information is important for understanding how root–microbe interactions might affect root function and prevent diseases. This study tested specific hypotheses related to the spatial variation of bacterial and fungal communities on wheat (Triticum aestivum L.) and rice (Oryza sativa L.) roots grown in contrasting soils. We demonstrate that microbial communities differed significantly between soil type, between host species, between root types, and with position along the root axes. The magnitude of variation between different root types and along individual roots was comparable with the variation detected between different plant species. We discuss the general patterns that emerged in this variation and identify bacterial and fungal taxa that were consistently more abundant on specific regions of the root system. We argue that these patterns should be measured more routinely so that localised root–microbe interactions can be better linked with root system design, plant health and performance.

Keywords: rhizosphere, root–microbe interactions, soil microorganisms, Triticum aestivum L., Oryza sativa L., bacterial colonies, fungal colonies, root type, root axes.


References

Aguirre-von-Wobeser E, Rocha-Estrada J, Shapiro LR, de la Torre M (2018) Enrichment of Verrucomicrobia, Actinobacteria and Burkholderiales drives selection of bacterial community from soil by maize roots in a traditional milpa agroecosystem. PLoS One 13, e0208852
Enrichment of Verrucomicrobia, Actinobacteria and Burkholderiales drives selection of bacterial community from soil by maize roots in a traditional milpa agroecosystem.Crossref | GoogleScholarGoogle Scholar | 30571782PubMed |

Ahmed MA, Zarebanadkouki M, Kaestner A, Carminati A (2016) Measurements of water uptake of maize roots: the key function of lateral roots. Plant and Soil 398, 59–77.
Measurements of water uptake of maize roots: the key function of lateral roots.Crossref | GoogleScholarGoogle Scholar |

Ahmed MA, Zarebanadkouki M, Meunier F, Javaux M, Kaestner A, Carminati A (2018) Root type matters: measurement of water uptake by seminal, crown, and lateral roots in maize. Journal of Experimental Botany 69, 1199–1206.
Root type matters: measurement of water uptake by seminal, crown, and lateral roots in maize.Crossref | GoogleScholarGoogle Scholar | 29304205PubMed |

Bakker PAHM, Berendsen RL, Doornbos RF, Wintermans PCA, Pieterse CMJ (2013) The rhizosphere revisited: root microbiomics. Frontiers in Plant Science 4, 165
The rhizosphere revisited: root microbiomics.Crossref | GoogleScholarGoogle Scholar |

Beckers B, De Beeck MO, Thijs S, Truyens S, Weyens N, Boerjan W, Vangronsveld J (2016) Performance of 16s rDNA primer pairs in the study of rhizosphere and endosphere bacterial microbiomes in metabarcoding studies. Frontiers in Microbiology 7, 650
Performance of 16s rDNA primer pairs in the study of rhizosphere and endosphere bacterial microbiomes in metabarcoding studies.Crossref | GoogleScholarGoogle Scholar | 27242686PubMed |

Bei Q, Moser G, Wu X, Müller C, Liesack W (2019) Metatranscriptomics reveals climate change effects on the rhizosphere microbiomes in European grassland. Soil Biology & Biochemistry 138, 107604
Metatranscriptomics reveals climate change effects on the rhizosphere microbiomes in European grassland.Crossref | GoogleScholarGoogle Scholar |

Bengtsson-Palme J, Ryberg M, Hartmann M, Branco S, Wang Z, Godhe A, De Wit P, Sánchez-García M, Ebersberger I, de Sousa F, Amend A, Jumpponen A, Unterseher M, Kristiansson E, Abarenkov K, Bertrand YJK, Sanli K, Eriksson KM, Vik U, Veldre V, Nilsson RH (2013) Improved software detection and extraction of ITS1 and ITS2 from ribosomal ITS sequences of fungi and other eukaryotes for analysis of environmental sequencing data. Methods in Ecology and Evolution 4, 914–919.
Improved software detection and extraction of ITS1 and ITS2 from ribosomal ITS sequences of fungi and other eukaryotes for analysis of environmental sequencing data.Crossref | GoogleScholarGoogle Scholar |

Berg G, Smalla K (2009) Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiology Ecology 68, 1–13.
Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere.Crossref | GoogleScholarGoogle Scholar | 19243436PubMed |

Bianciotto V, Bandi C, Minerdi D, Sironi M, Tichy HV, Bonfante P (1996) An obligately endosymbiotic mycorrhizal fungus itself harbors obligately intracellular bacteria. Applied and Environmental Microbiology 62, 3005–3010.
An obligately endosymbiotic mycorrhizal fungus itself harbors obligately intracellular bacteria.Crossref | GoogleScholarGoogle Scholar | 8702293PubMed |

Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F, et al (2019) Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nature Biotechnology 37, 852–857.
Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2.Crossref | GoogleScholarGoogle Scholar | 31341288PubMed |

Bouam A, Armstrong N, Levasseur A, Drancourt M (2018) Mycobacterium terramassiliense, Mycobacterium rhizamassiliense and Mycobacterium numidiamassiliense sp. nov., three new Mycobacterium simiae complex species cultured from plant roots. Scientific Reports 8, 9309
Mycobacterium terramassiliense, Mycobacterium rhizamassiliense and Mycobacterium numidiamassiliense sp. nov., three new Mycobacterium simiae complex species cultured from plant roots.Crossref | GoogleScholarGoogle Scholar | 29915369PubMed |

Bulgarelli D, Rott M, Schlaeppi K, van Themaat EVL, Ahmadinejad N, Assenza F, Rauf P, Huettel B, Reinhardt R, Schmelzer E, Peplies J, Gloeckner FO, Amann R, Eickhorst T, Schulze-Lefert P (2012) Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488, 91–95.
Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota.Crossref | GoogleScholarGoogle Scholar | 22859207PubMed |

Bulgarelli D, Garrido-Oter R, Munch PC, Weiman A, Droge J, Pan Y, McHardy AC, Schulze-Lefert P (2015) Structure and function of the bacterial root microbiota in wild and domesticated barley. Cell Host & Microbe 17, 392–403.
Structure and function of the bacterial root microbiota in wild and domesticated barley.Crossref | GoogleScholarGoogle Scholar |

Chaluvadi S, Bennetzen JL (2018) Species-associated differences in the below-ground microbiomes of wild and domesticated Setaria. Frontiers in Plant Science 9, 1183
Species-associated differences in the below-ground microbiomes of wild and domesticated Setaria.Crossref | GoogleScholarGoogle Scholar | 30186294PubMed |

Chaparro JM, Badri DV, Vivanco JM (2014) Rhizosphere microbiome assemblage is affected by plant development. The ISME Journal 8, 790–803.
Rhizosphere microbiome assemblage is affected by plant development.Crossref | GoogleScholarGoogle Scholar | 24196324PubMed |

Chelius MK, Triplett EW (2001) The diversity of archaea and bacteria in association with the roots of Zea mays L. Microbial Ecology 41, 252–263.
The diversity of archaea and bacteria in association with the roots of Zea mays L.Crossref | GoogleScholarGoogle Scholar | 11391463PubMed |

Chen S, Waghmode TR, Sun R, Kuramae EE, Hu C, Liu B (2019) Root-associated microbiomes of wheat under the combined effect of plant development and nitrogen fertilization. Microbiome 7, 136
Root-associated microbiomes of wheat under the combined effect of plant development and nitrogen fertilization.Crossref | GoogleScholarGoogle Scholar | 31640813PubMed |

Chin-A-Woeng T, Priester W, Bij A, Lugtenberg B (1997) Description of the colonization of a gnotobiotic tomato rhizosphere by Pseudomonas fluorescens biocontrol strain WCS365, using scanning electron microscopy. Molecular Plant-Microbe Interactions 10, 79–86.
Description of the colonization of a gnotobiotic tomato rhizosphere by Pseudomonas fluorescens biocontrol strain WCS365, using scanning electron microscopy.Crossref | GoogleScholarGoogle Scholar |

Coenye T, Vandamme P (2003) Diversity and significance of Burkholderia species occupying diverse ecological niches. Environmental Microbiology 5, 719–729.
Diversity and significance of Burkholderia species occupying diverse ecological niches.Crossref | GoogleScholarGoogle Scholar | 12919407PubMed |

Cole JR, Wang Q, Fish JA, Chai B, McGarrell DM, Sun Y, Brown CT, Porras-Alfaro A, Kuske CR, Tiedje JM (2014) Ribosomal Database Project: data and tools for high throughput rRNA analysis. Nucleic Acids Research 42, D633–D642.
Ribosomal Database Project: data and tools for high throughput rRNA analysis.Crossref | GoogleScholarGoogle Scholar | 24288368PubMed |

de Vries FT, Griffiths RI, Knight CG, Nicolitch O, Williams A (2020) Harnessing rhizosphere microbiomes for drought-resilient crop production. Science 368, 270–274.
Harnessing rhizosphere microbiomes for drought-resilient crop production.Crossref | GoogleScholarGoogle Scholar | 32299947PubMed |

DeAngelis KM, Brodie EL, DeSantis TZ, Andersen GL, Lindow SE, Firestone MK (2009) Selective progressive response of soil microbial community to wild oat roots. The ISME Journal 3, 168–178.
Selective progressive response of soil microbial community to wild oat roots.Crossref | GoogleScholarGoogle Scholar | 19005498PubMed |

Delhaize E, Ryan PR, Randall PJ (1993) Aluminum tolerance in wheat (Triticum aestivum L.) (II. Aluminum-stimulated excretion of malic acid from root apices). Plant Physiology 103, 695–702.
Aluminum tolerance in wheat (Triticum aestivum L.) (II. Aluminum-stimulated excretion of malic acid from root apices).Crossref | GoogleScholarGoogle Scholar | 12231973PubMed |

Dennis PG, Miller AJ, Clark IM, Taylor RG, Valsami-Jones E, Hirsch PR (2008) A novel method for sampling bacteria on plant root and soil surfaces at the microhabitat scale. Journal of Microbiological Methods 75, 12–18.
A novel method for sampling bacteria on plant root and soil surfaces at the microhabitat scale.Crossref | GoogleScholarGoogle Scholar | 18558444PubMed |

Dennis PG, Hirsch PR, Smith SJ, Taylor RG, Valsami-Jones E, Miller AJ (2009) Linking rhizoplane pH and bacterial density at the microhabitat scale. Journal of Microbiological Methods 76, 101–104.
Linking rhizoplane pH and bacterial density at the microhabitat scale.Crossref | GoogleScholarGoogle Scholar | 18926861PubMed |

Dennis PG, Miller AJ, Hirsch PR (2010) Are root exudates more important than other sources of rhizodeposits in structuring rhizosphere bacterial communities? FEMS Microbiology Ecology 72, 313–327.
Are root exudates more important than other sources of rhizodeposits in structuring rhizosphere bacterial communities?Crossref | GoogleScholarGoogle Scholar | 20370828PubMed |

Donn S, Kirkegaard JA, Perera G, Richardson AE, Watt M (2015) Evolution of bacterial communities in the wheat crop rhizosphere. Environmental Microbiology 17, 610–621.
Evolution of bacterial communities in the wheat crop rhizosphere.Crossref | GoogleScholarGoogle Scholar | 24628845PubMed |

Donn S, Kawasaki A, Delroy B, Chochois V, Watt M, Powell JR (2017) Root type is not an important driver of mycorrhizal colonisation in Brachypodium distachyon. Pedobiologia 65, 5–15.
Root type is not an important driver of mycorrhizal colonisation in Brachypodium distachyon.Crossref | GoogleScholarGoogle Scholar |

Dupuy LX, Silk WK (2016) Mechanisms of early microbial establishment on growing root surfaces. Vadose Zone Journal 15, 1–13.
Mechanisms of early microbial establishment on growing root surfaces.Crossref | GoogleScholarGoogle Scholar |

Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461.
Search and clustering orders of magnitude faster than BLAST.Crossref | GoogleScholarGoogle Scholar | 20709691PubMed |

Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nature Methods 10, 996–998.
UPARSE: highly accurate OTU sequences from microbial amplicon reads.Crossref | GoogleScholarGoogle Scholar | 23955772PubMed |

Edwards J, Johnson C, Santos-Medellín C, Lurie E, Podishetty NK, Bhatnagar S, Eisen JA, Sundaresan V (2015) Structure, variation, and assembly of the root-associated microbiomes of rice. Proceedings of the National Academy of Sciences of the United States of America 112, E911–E920.
Structure, variation, and assembly of the root-associated microbiomes of rice.Crossref | GoogleScholarGoogle Scholar | 25605935PubMed |

Farrar J, Hawes M, Jones D, Lindow S (2003) How roots control the flux of carbon to the rhizosphere. Ecology 84, 827–837.
How roots control the flux of carbon to the rhizosphere.Crossref | GoogleScholarGoogle Scholar |

Fernández-González AJ, Villadas PJ, Gómez-Lama Cabanás C, Valverde-Corredor A, Belaj A, Mercado-Blanco J, Fernández-López M (2019) Defining the root endosphere and rhizosphere microbiomes from the world olive germplasm collection. Scientific Reports 9, 20423
Defining the root endosphere and rhizosphere microbiomes from the world olive germplasm collection.Crossref | GoogleScholarGoogle Scholar | 31892747PubMed |

Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88, 1354–1364.
Toward an ecological classification of soil bacteria.Crossref | GoogleScholarGoogle Scholar | 17601128PubMed |

Forstner C, Orton TG, Skarshewski A, Wang P, Kopittke PM, Dennis PG (2019) Effects of graphene oxide and graphite on soil bacterial and fungal diversity. The Science of the Total Environment 671, 140–148.
Effects of graphene oxide and graphite on soil bacterial and fungal diversity.Crossref | GoogleScholarGoogle Scholar | 30928743PubMed |

Gamuyao R, Chin JH, Pariasca-Tanaka J, Pesaresi P, Catausan S, Dalid C, Slamet-Loedin I, Tecson-Mendoza EM, Wissuwa M, Heuer S (2012) The protein kinase Pstol1 from traditional rice confers tolerance of phosphorus deficiency. Nature 488, 535
The protein kinase Pstol1 from traditional rice confers tolerance of phosphorus deficiency.Crossref | GoogleScholarGoogle Scholar | 22914168PubMed |

Gilligan CA (1980) Colonization of lateral, seminal and adventitious roots of wheat by the take-all fungus, Gaeumannomyces graminis var. tritici. The Journal of Agricultural Science 94, 325–329.
Colonization of lateral, seminal and adventitious roots of wheat by the take-all fungus, Gaeumannomyces graminis var. tritici.Crossref | GoogleScholarGoogle Scholar |

Gkarmiri K, Mahmood S, Ekblad A, Alström S, Högberg N, Finlay R (2017) Identifying the active microbiome associated with roots and rhizosphere soil of oilseed rape. Applied and Environmental Microbiology 83, e01938-17
Identifying the active microbiome associated with roots and rhizosphere soil of oilseed rape.Crossref | GoogleScholarGoogle Scholar | 28887416PubMed |

Gupta S, Schillaci M, Walker R, Smith PMC, Watt M, Roessner U (2020) Alleviation of salinity stress in plants by endophytic plant-fungal symbiosis: Current knowledge, perspectives and future directions. Plant and Soil
Alleviation of salinity stress in plants by endophytic plant-fungal symbiosis: Current knowledge, perspectives and future directions.Crossref | GoogleScholarGoogle Scholar |

Ho A, Di Lonardo DP, Bodelier PLE (2017) Revisiting life strategy concepts in environmental microbial ecology. FEMS Microbiology Ecology 93, fix006
Revisiting life strategy concepts in environmental microbial ecology.Crossref | GoogleScholarGoogle Scholar | 28115400PubMed |

Hochholdinger F, Zimmermann R (2018) Molecular and genetic dissection of cereal root system development. In ‘Annual Plant Reviews online.’ (Ed. JA Roberts.) pp. 175–191. (Blackwell Publishing Ltd)

Ihrmark K, Bodeker ITM, Cruz-Martinez K, Friberg H, Kubartova A, Schenck J, Strid Y, Stenlid J, Brandstrom-Durling M, Clemmensen KE, Lindahl BD (2012) New primers to amplify the fungal ITS2 region - evaluation by 454-sequencing of artificial and natural communities. FEMS Microbiology Ecology 82, 666–677.
New primers to amplify the fungal ITS2 region - evaluation by 454-sequencing of artificial and natural communities.Crossref | GoogleScholarGoogle Scholar | 22738186PubMed |

İnceoğlu Ö, Salles JF, van Overbeek L, van Elsas JD (2010) Effects of plant genotype and growth stage on the Betaproteobacterial communities associated with different potato cultivars in two fields. Applied and Environmental Microbiology 76, 3675–3684.
Effects of plant genotype and growth stage on the Betaproteobacterial communities associated with different potato cultivars in two fields.Crossref | GoogleScholarGoogle Scholar | 20363788PubMed |

Kandel SL, Joubert PM, Doty SL (2017) Bacterial endophyte colonization and distribution within plants. Microorganisms 5, 77
Bacterial endophyte colonization and distribution within plants.Crossref | GoogleScholarGoogle Scholar |

Kawasaki A, Ryan PR (2021) Peptide nucleic acid (PNA) clamps to reduce co-amplification of plant DNA during PCR amplification of 16S rRNA genes from endophytic bacteria. In ‘The Plant Microbiome: Methods and Protocols.’ (Eds LC Carvalhais, PG Dennis.) pp. 123–134. (Springer US: New York, NY)

Kawasaki A, Donn S, Ryan PR, Mathesius U, Devilla R, Jones A, Watt M (2016) Microbiome and exudates of the root and rhizosphere of Brachypodium distachyon, a model for wheat. PLoS One 11, e0164533
Microbiome and exudates of the root and rhizosphere of Brachypodium distachyon, a model for wheat.Crossref | GoogleScholarGoogle Scholar | 27727301PubMed |

Kuhlmann H, Barraclough PB (1987) Comparison between the seminal and nodal root systems of winter-wheat in their activity for N and K uptake. Zeitschrift für Pflanzenernährung und Bodenkunde 150, 24–30.
Comparison between the seminal and nodal root systems of winter-wheat in their activity for N and K uptake.Crossref | GoogleScholarGoogle Scholar |

Lakshmanan V, Ray P, Craven KD (2017) Rhizosphere Sampling Protocols for Microbiome (16S/18S/ITS rRNA) Library Preparation and Enrichment for the Isolation of Drought Tolerance-Promoting Microbes. In ‘Plant Stress Tolerance: Methods and Protocols.’ (Ed. R Sunkar.) pp. 349–362. (Springer New York: New York, NY)

Lareen A, Burton F, Schafer P (2016) Plant root-microbe communication in shaping root microbiomes. Plant Molecular Biology 90, 575–587.
Plant root-microbe communication in shaping root microbiomes.Crossref | GoogleScholarGoogle Scholar | 26729479PubMed |

Lay C-Y, Bell TH, Hamel C, Harker KN, Mohr R, Greer CW, Yergeau É, St-Arnaud M (2018) Canola root–associated microbiomes in the Canadian prairies. Frontiers in Microbiology 9, 1188
Canola root–associated microbiomes in the Canadian prairies.Crossref | GoogleScholarGoogle Scholar | 29937756PubMed |

Lee DW, Lee SY, Yoon JH, Lee SD (2011) Nocardioides ultimimeridianus sp nov. and Nocardioides maradonensis sp nov., isolated from rhizosphere soil. International Journal of Systematic and Evolutionary Microbiology 61, 1933–1937.
Nocardioides ultimimeridianus sp nov. and Nocardioides maradonensis sp nov., isolated from rhizosphere soil.Crossref | GoogleScholarGoogle Scholar | 20833879PubMed |

Legendre P, Gallagher ED (2001) Ecologically meaningful transformations for ordination of species data. Oecologia 129, 271–280.
Ecologically meaningful transformations for ordination of species data.Crossref | GoogleScholarGoogle Scholar | 28547606PubMed |

Liljeroth E, Burgers S, Vanveen JA (1991) Changes in bacterial populations along roots of wheat (Triticum aestivum L.) seedlings. Biology and Fertility of Soils 10, 276–280.
Changes in bacterial populations along roots of wheat (Triticum aestivum L.) seedlings.Crossref | GoogleScholarGoogle Scholar |

Liu Z, Giehl RFH, Hartmann A, Hajirezaei MR, Carpentier S, von Wirén N (2020) Seminal and nodal roots of barley differ in anatomy, proteome and nitrate uptake capacity. Plant & Cell Physiology 61, 1297–1308.
Seminal and nodal roots of barley differ in anatomy, proteome and nitrate uptake capacity.Crossref | GoogleScholarGoogle Scholar |

Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology 15, 550
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2.Crossref | GoogleScholarGoogle Scholar | 25516281PubMed |

Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S, Tremblay J, Engelbrektson A, Kunin V, del Rio TG, Edgar RC, Eickhorst T, Ley RE, Hugenholtz P, Tringe SG, Dangl JL (2012) Defining the core Arabidopsis thaliana root microbiome. Nature 488, 86–90.
Defining the core Arabidopsis thaliana root microbiome.Crossref | GoogleScholarGoogle Scholar | 22859206PubMed |

Maharachchikumbura SSN, Hyde KD, Jones EBG, McKenzie EHC, Bhat JD, Dayarathne MC, Huang SK, Norphanphoun C, Senanayake IC, Perera RH, et al (2016) Families of Sordariomycetes. Fungal Diversity 79, 1–317.
Families of Sordariomycetes.Crossref | GoogleScholarGoogle Scholar |

Maloney PE, van Bruggen AHC, Hu S (1997) Bacterial community structure in relation to the carbon environments in lettuce and tomato rhizospheres and in bulk soil. Microbial Ecology 34, 109–117.
Bacterial community structure in relation to the carbon environments in lettuce and tomato rhizospheres and in bulk soil.Crossref | GoogleScholarGoogle Scholar | 9230098PubMed |

Marschner H, Römheld V, Kissel M (1987) Localization of phytosiderophore release and of iron uptake along intact barley roots. Physiologia Plantarum 71, 157–162.
Localization of phytosiderophore release and of iron uptake along intact barley roots.Crossref | GoogleScholarGoogle Scholar |

Massalha H, Korenblum E, Malitsky S, Shapiro OH, Aharoni A (2017) Live imaging of root–bacteria interactions in a microfluidics setup. Proceedings of the National Academy of Sciences of the United States of America 114, 4549–4554.
Live imaging of root–bacteria interactions in a microfluidics setup.Crossref | GoogleScholarGoogle Scholar | 28348235PubMed |

McDonald D, Clemente JC, Kuczynski J, Rideout JR, Stombaugh J, Wendel D, Wilke A, Huse S, Hufnagle J, Meyer F, Knight R, Caporaso JG (2012) The Biological Observation Matrix (BIOM) format or: how I learned to stop worrying and love the ome-ome. GigaScience 1, 7
The Biological Observation Matrix (BIOM) format or: how I learned to stop worrying and love the ome-ome.Crossref | GoogleScholarGoogle Scholar | 23587224PubMed |

McMurdie PJ, Holmes S (2013) phyloseq: An R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8, e61217
phyloseq: An R package for reproducible interactive analysis and graphics of microbiome census data.Crossref | GoogleScholarGoogle Scholar | 23630581PubMed |

McMurdie PJ, Holmes S (2014) Waste not, want not: Why rarefying microbiome data is inadmissible. PLoS Computational Biology 10, e1003531
Waste not, want not: Why rarefying microbiome data is inadmissible.Crossref | GoogleScholarGoogle Scholar | 24699258PubMed |

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.
Deciphering the rhizosphere microbiome for disease-suppressive bacteria.Crossref | GoogleScholarGoogle Scholar | 21551032PubMed |

Mitter B, Brader G, Pfaffenbichler N, Sessitsch A (2019) Next generation microbiome applications for crop production — limitations and the need of knowledge-based solutions. Current Opinion in Microbiology 49, 59–65.
Next generation microbiome applications for crop production — limitations and the need of knowledge-based solutions.Crossref | GoogleScholarGoogle Scholar | 31731227PubMed |

Naylor D, DeGraaf S, Purdom E, Coleman-Derr D (2017) Drought and host selection influence bacterial community dynamics in the grass root microbiome. The ISME Journal 11, 2691
Drought and host selection influence bacterial community dynamics in the grass root microbiome.Crossref | GoogleScholarGoogle Scholar | 28753209PubMed |

Nguyen C (2003) Rhizodeposition of organic C by plants: mechanisms and controls. Agronomie 23, 375–396.
Rhizodeposition of organic C by plants: mechanisms and controls.Crossref | GoogleScholarGoogle Scholar |

Nilsson RH, Glöckner FO, Saar I, Tedersoo L, Kõljalg U, Abarenkov K, Larsson K-H, Taylor AFS, Bengtsson-Palme J, Schigel D, Jeppesen TS, Kennedy P, Picard K (2019) The UNITE database for molecular identification of fungi: handling dark taxa and parallel taxonomic classifications. Nucleic Acids Research 47, D259–D264.
The UNITE database for molecular identification of fungi: handling dark taxa and parallel taxonomic classifications.Crossref | GoogleScholarGoogle Scholar | 30371820PubMed |

Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2019) vegan: Community Ecology Package. R package version 2.5-6. https://CRAN.R-project.org/package=vegan

Palaniyandi SA, Yang SH, Zhang L, Suh J-W (2013) Effects of actinobacteria on plant disease suppression and growth promotion. Applied Microbiology and Biotechnology 97, 9621–9636.
Effects of actinobacteria on plant disease suppression and growth promotion.Crossref | GoogleScholarGoogle Scholar | 24092003PubMed |

Paterson E, Gebbing T, Abel C, Sim A, Telfer G (2007) Rhizodeposition shapes rhizosphere microbial community structure in organic soil. New Phytologist 173, 600–610.
Rhizodeposition shapes rhizosphere microbial community structure in organic soil.Crossref | GoogleScholarGoogle Scholar |

Peiffer JA, Spor A, Koren O, Jin Z, Tringe SG, Dangl JL, Buckler ES, Ley RE (2013) Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proceedings of the National Academy of Sciences of the United States of America 110, 6548–6553.
Diversity and heritability of the maize rhizosphere microbiome under field conditions.Crossref | GoogleScholarGoogle Scholar | 23576752PubMed |

Pieterse CMJ, Zamioudis C, Berendsen RL, Weller DM, Van Wees SCM, Bakker PAHM (2014) Induced systemic resistance by beneficial microbes. In ‘Annu. Rev. Phytopathol.’ (Ed. NK VanAlfen.) Vol. 52 pp. 347–375.

Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Gloeckner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Research 41, D590–D596.
The SILVA ribosomal RNA gene database project: improved data processing and web-based tools.Crossref | GoogleScholarGoogle Scholar | 23193283PubMed |

R Core Team (2019) ‘R: A language and environment for statistical computing.’ (R Foundation for Statistical Computing: Vienna, Austria)

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 and Soil 321, 341–361.
The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms.Crossref | GoogleScholarGoogle Scholar |

Rascovan N, Carbonetto B, Perrig D, Díaz M, Canciani W, Abalo M, Alloati J, González-Anta G, Vazquez MP (2016) Integrated analysis of root microbiomes of soybean and wheat from agricultural fields. Scientific Reports 6, 28084
Integrated analysis of root microbiomes of soybean and wheat from agricultural fields.Crossref | GoogleScholarGoogle Scholar | 27312589PubMed |

Reinhold-Hurek B, Bunger W, Burbano CS, Sabale M, Hurek T (2015) Roots shaping their microbiome: Global hotspots for microbial activity. Annual Review of Phytopathology 53, 403
Roots shaping their microbiome: Global hotspots for microbial activity.Crossref | GoogleScholarGoogle Scholar | 26243728PubMed |

Richardson AE, Kawasaki A, Condron LM, Ryan PR, Gupta VVSR (2021) Root microbiome structure and microbial succession in the rhizosphere. In ‘Rhizosphere Biology: Interactions Between Microbes and Plants.’ (Eds VVSR Gupta, AK Sharma.) pp. 109–128. (Springer Singapore: Singapore)

Rodriguez RJ, White JF, Arnold AE, Redman RS (2009) Fungal endophytes: diversity and functional roles. New Phytologist 182, 314–330.
Fungal endophytes: diversity and functional roles.Crossref | GoogleScholarGoogle Scholar |

Ryan PR, Raman H, Gupta S, Horst WJ, Delhaize E (2009) A second mechanism for aluminum resistance in wheat relies on the constitutive efflux of citrate from roots. Plant Physiology 149, 340–351.
A second mechanism for aluminum resistance in wheat relies on the constitutive efflux of citrate from roots.Crossref | GoogleScholarGoogle Scholar | 19005085PubMed |

Sasse J, Martinoia E, Northen T (2018) Feed your friends: Do plant exudates shape the root microbiome? Trends in Plant Science 23, 25–41.
Feed your friends: Do plant exudates shape the root microbiome?Crossref | GoogleScholarGoogle Scholar | 29050989PubMed |

Schlaeppi K, Dombrowski N, Oter RG, Ver Loren van Themaat E, Schulze-Lefert P (2014) Quantitative divergence of the bacterial root microbiota in Arabidopsis thaliana relatives. Proceedings of the National Academy of Sciences of the United States of America 111, 585–592.
Quantitative divergence of the bacterial root microbiota in Arabidopsis thaliana relatives.Crossref | GoogleScholarGoogle Scholar | 24379374PubMed |

Schrey SD, Tarkka MT (2008) Friends and foes: streptomycetes as modulators of plant disease and symbiosis. Antonie Van Leeuwenhoek 94, 11–19.
Friends and foes: streptomycetes as modulators of plant disease and symbiosis.Crossref | GoogleScholarGoogle Scholar | 18418729PubMed |

Semenov AM, van Bruggen AHC, Zelenev VV (1999) Moving waves of bacterial populations and total organic carbon along roots of wheat. Microbial Ecology 37, 116–128.
Moving waves of bacterial populations and total organic carbon along roots of wheat.Crossref | GoogleScholarGoogle Scholar | 9929400PubMed |

Simmons T, Caddell DF, Deng S, Coleman-Derr D (2018) Exploring the root microbiome: Extracting bacterial community data from the soil, rhizosphere, and root endosphere. Journal of Visualized Experiments (135), e57561
Exploring the root microbiome: Extracting bacterial community data from the soil, rhizosphere, and root endosphere.Crossref | GoogleScholarGoogle Scholar |

Sivasithamparam K, Parker CA (1978) Effect of infection of seminal and nodal roots by take-all fungus on tiller numbers and shoot weight of wheat. Soil Biology & Biochemistry 10, 365–368.
Effect of infection of seminal and nodal roots by take-all fungus on tiller numbers and shoot weight of wheat.Crossref | GoogleScholarGoogle Scholar |

Sivasithamparam K, Parker CA, Edwards CS (1979a) Bacterial antagonists to the take-all fungus and fluorescent pseudomonads in the rhizosphere of wheat. Soil Biology & Biochemistry 11, 161–165.
Bacterial antagonists to the take-all fungus and fluorescent pseudomonads in the rhizosphere of wheat.Crossref | GoogleScholarGoogle Scholar |

Sivasithamparam K, Parker CA, Edwards CS (1979b) Rhizosphere microorganisms of seminal and nodal roots of wheat grown in pots. Soil Biology & Biochemistry 11, 155–160.
Rhizosphere microorganisms of seminal and nodal roots of wheat grown in pots.Crossref | GoogleScholarGoogle Scholar |

Suárez-Moreno ZR, Vinchira-Villarraga DM, Vergara-Morales DI, Castellanos L, Ramos FA, Guarnaccia C, Degrassi G, Venturi V, Moreno-Sarmiento N (2019) Plant-growth promotion and biocontrol properties of three Streptomyces spp. isolates to control bacterial rice pathogens. Frontiers in Microbiology 10, 290
Plant-growth promotion and biocontrol properties of three Streptomyces spp. isolates to control bacterial rice pathogens.Crossref | GoogleScholarGoogle Scholar | 30858835PubMed |

Sun B, Gao Y, Lynch J (2018) Large crown root number improves topsoil foraging and phosphorus acquisition. Plant Physiology 177, 90–104.
Large crown root number improves topsoil foraging and phosphorus acquisition.Crossref | GoogleScholarGoogle Scholar | 29618638PubMed |

Tai H, Lu X, Opitz N, Marcon C, Paschold A, Lithio A, Nettleton D, Hochholdinger F (2016) Transcriptomic and anatomical complexity of primary, seminal, and crown roots highlight root type-specific functional diversity in maize (Zea mays L.). Journal of Experimental Botany 67, 1123–1135.
Transcriptomic and anatomical complexity of primary, seminal, and crown roots highlight root type-specific functional diversity in maize (Zea mays L.).Crossref | GoogleScholarGoogle Scholar | 26628518PubMed |

Tian B, Zhang C, Ye Y, Wen J, Wu Y, Wang H, Li H, Cai S, Cai W, Cheng Z, Lei S, Ma R, Lu C, Cao Y, Xu X, Zhang K (2017) Beneficial traits of bacterial endophytes belonging to the core communities of the tomato root microbiome. Agriculture, Ecosystems & Environment 247, 149–156.
Beneficial traits of bacterial endophytes belonging to the core communities of the tomato root microbiome.Crossref | GoogleScholarGoogle Scholar |

Toju H, Tanabe AS, Yamamoto S, Sato H (2012) High-coverage ITS primers for the DNA-based identification of ascomycetes and basidiomycetes in environmental samples. PLoS One 7, e40863
High-coverage ITS primers for the DNA-based identification of ascomycetes and basidiomycetes in environmental samples.Crossref | GoogleScholarGoogle Scholar | 22808280PubMed |

Volkmar KM (1997) Water stressed nodal roots of wheat: Effects on leaf growth. Australian Journal of Plant Physiology 24, 49–56.

Vurukonda SSKP, Giovanardi D, Stefani E (2018) Plant growth promoting and biocontrol activity of Streptomyces spp. as endophytes. International Journal of Molecular Sciences 19, 952
Plant growth promoting and biocontrol activity of Streptomyces spp. as endophytes.Crossref | GoogleScholarGoogle Scholar |

Wagner MR, Lundberg DS, del Rio TG, Tringe SG, Dangl JL, Mitchell-Olds T (2016) Host genotype and age shape the leaf and root microbiomes of a wild perennial plant. Nature Communications 7, 12151
Host genotype and age shape the leaf and root microbiomes of a wild perennial plant.Crossref | GoogleScholarGoogle Scholar | 27402057PubMed |

Wang Z, Binder M, Schoch CL, Johnston PR, Spatafora JW, Hibbett DS (2006) Evolution of helotialean fungi (Leotiomycetes, Pezizomycotina): A nuclear rDNA phylogeny. Molecular Phylogenetics and Evolution 41, 295–312.
Evolution of helotialean fungi (Leotiomycetes, Pezizomycotina): A nuclear rDNA phylogeny.Crossref | GoogleScholarGoogle Scholar | 16837216PubMed |

Wang Y, Naumann U, Wright ST, Warton DI (2012) mvabund– an R package for model-based analysis of multivariate abundance data. Methods in Ecology and Evolution 3, 471–474.
mvabund– an R package for model-based analysis of multivariate abundance data.Crossref | GoogleScholarGoogle Scholar |

Watt M, McCully ME, Kirkegaard JA (2003) Soil strength and rate of root elongation alter the accumulation of Pseudomonas spp. and other bacteria in the rhizosphere of wheat. Functional Plant Biology 30, 483–491.
Soil strength and rate of root elongation alter the accumulation of Pseudomonas spp. and other bacteria in the rhizosphere of wheat.Crossref | GoogleScholarGoogle Scholar | 32689033PubMed |

Watt M, Hugenholtz P, White R, Vinall K (2006a) Numbers and locations of native bacteria on field-grown wheat roots quantified by fluorescence in situ hybridization (FISH). Environmental Microbiology 8, 871–884.
Numbers and locations of native bacteria on field-grown wheat roots quantified by fluorescence in situ hybridization (FISH).Crossref | GoogleScholarGoogle Scholar | 16623744PubMed |

Watt M, Silk WK, Passioura JB (2006b) Rates of root and organism growth, soil conditions, and temporal and spatial development of the rhizosphere. Annals of Botany 97, 839–855.
Rates of root and organism growth, soil conditions, and temporal and spatial development of the rhizosphere.Crossref | GoogleScholarGoogle Scholar | 16551700PubMed |

Watt M, Schneebeli K, Dong P, Wilson IW (2009) The shoot and root growth of Brachypodium and its potential as a model for wheat and other cereal crops. Functional Plant Biology 36, 960–969.
The shoot and root growth of Brachypodium and its potential as a model for wheat and other cereal crops.Crossref | GoogleScholarGoogle Scholar | 32688707PubMed |

White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In ‘PCR protocols: a guide to methods and applications.’ (Eds MA Innis, DH Gelfand, JJ Sninsky, TJ White.) pp. 315–322. (Academic Press: San Diego)

Wiengweera A, Greenway H (2004) Performance of seminal and nodal roots of wheat in stagnant solution: K+ and P uptake and effects of increasing O2 partial pressures around the shoot on nodal root elongation. Journal of Experimental Botany 55, 2121–2129.
Performance of seminal and nodal roots of wheat in stagnant solution: K+ and P uptake and effects of increasing O2 partial pressures around the shoot on nodal root elongation.Crossref | GoogleScholarGoogle Scholar | 15310817PubMed |

Xu L, Ravnskov S, Larsen J, Nicolaisen M (2012) Linking fungal communities in roots, rhizosphere, and soil to the health status of Pisum sativum. FEMS Microbiology Ecology 82, 736–745.
Linking fungal communities in roots, rhizosphere, and soil to the health status of Pisum sativum.Crossref | GoogleScholarGoogle Scholar | 22775574PubMed |

Yang CH, Crowley DE (2000) Rhizosphere microbial community structure in relation to root location and plant iron nutritional status. Applied and Environmental Microbiology 66, 345–351.
Rhizosphere microbial community structure in relation to root location and plant iron nutritional status.Crossref | GoogleScholarGoogle Scholar | 10618246PubMed |

Yu P, Wang C, Baldauf JA, Tai HH, Gutjahr C, Hochholdinger F, Li CJ (2018) Root type and soil phosphate determine the taxonomic landscape of colonizing fungi and the transcriptome of field-grown maize roots. New Phytologist 217, 1240–1253.
Root type and soil phosphate determine the taxonomic landscape of colonizing fungi and the transcriptome of field-grown maize roots.Crossref | GoogleScholarGoogle Scholar |

Zamioudis C, Mastranesti P, Dhonukshe P, Blilou I, Pieterse CMJ (2013) Unraveling root developmental programs initiated by beneficial Pseudomonas spp. bacteria. Plant Physiology 162, 304–318.
Unraveling root developmental programs initiated by beneficial Pseudomonas spp. bacteria.Crossref | GoogleScholarGoogle Scholar | 23542149PubMed |

Zelenev VV, van Bruggen AHC, Semenov AM (2000) “BACWAVE,” a spatial–temporal model for traveling waves of bacterial populations in response to a moving carbon source in soil. Microbial Ecology 40, 260–272.
“BACWAVE,” a spatial–temporal model for traveling waves of bacterial populations in response to a moving carbon source in soil.Crossref | GoogleScholarGoogle Scholar | 11080383PubMed |

Zhang Z, Schwartz S, Wagner L, Miller W (2000) A greedy algorithm for aligning DNA sequences. Journal of Computational Biology 7, 203–214.
A greedy algorithm for aligning DNA sequences.Crossref | GoogleScholarGoogle Scholar | 10890397PubMed |

Zhang H, Wu X, Li G, Qin P (2011) Interactions between arbuscular mycorrhizal fungi and phosphate-solubilizing fungus (Mortierella sp.) and their effects on Kostelelzkya virginica growth and enzyme activities of rhizosphere and bulk soils at different salinities. Biology and Fertility of Soils 47, 543
Interactions between arbuscular mycorrhizal fungi and phosphate-solubilizing fungus (Mortierella sp.) and their effects on Kostelelzkya virginica growth and enzyme activities of rhizosphere and bulk soils at different salinities.Crossref | GoogleScholarGoogle Scholar |