The rhizosphere microbiome and plant health
Open accessAbstract
The diversity of microbes associated with plant roots is enormous, in the order of tens of thousands of species. This complex plant-associated microbial community, also referred to as the second genome of the plant, is crucial for plant health. Recent advances in plant-microbe interactions research revealed that plants are able to shape their rhizosphere microbiome, as evidenced by the fact that different plant species host specific microbial communities when grown on the same soil. In this review, we discuss evidence that upon pathogen or insect attack, plants are able to recruit protective microorganisms, and enhance microbial activity to suppress pathogens in the rhizosphere. A comprehensive understanding of the mechanisms that govern selection and activity of microbial communities by plant roots will provide new opportunities to increase crop production.
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The contributions and functions of the large majority of species in plant, rhizosphere, or soil microbiomes are still mostly unknown.
“Microbiomes of plants, rhizosphere, or soil have been elucidated by large-scale, DNA sequencing-based metagenomics approaches [7, 15, 16], but the contributions and functions of the large majority of the species are still mostly unknown.”
From Competition assays and physiological experiments of soil and phyllosphere yeasts identify Candida subhashii as a novel antagonist of filamentous fungi (2017) · cites this paper as [16]
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Going back to the roots: the microbial ecology of the rhizosphere
Philippot, L., Raaijmakers, J. M., Lemanceau, P., & van der Putten, W. H. (2013) · Nature Reviews Microbiology · doi:10.1038/nrmicro3109 · Cited by 3,925 · see citing works
Structure and functions of the bacterial microbiota of plants
Bulgarelli, D., Schlaeppi, K., Spaepen, S., van Themaat, E. V. L., & Schulze-Lefert, P. (2013) · Annual Review of Plant Biology · doi:10.1146/annurev-arplant-050312-120106 · Cited by 3,308 · see citing works
Induced systemic resistance by beneficial microbes
Pieterse, C. M. J., Zamioudis, C., Berendsen, R. L., Weller, D. M., Van Wees, S. C. M., & Bakker, P. A. H. M. (2014) · Annual Review of Phytopathology · doi:10.1146/annurev-phyto-082712-102340 · Cited by 3,272 · see citing works
Self-citationHormonal Modulation of Plant Immunity
Pieterse, C. M. J., van der Does, D., Zamioudis, C., León-Reyes, A., & Wees, S. C. M. V. (2011) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-092910-154055 · Cited by 3,021 · see citing works
Self-citationStructure, variation, and assembly of the root-associated microbiomes of rice
Edwards, J. A., Johnson, C. S., Santos‐Medellín, C., Lurie, E., Podishetty, N. K., Bhatnagar, S., Eisen, J. A., & Sundaresan, V. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1414592112 · Cited by 2,875 · see citing works
Plant biostimulants: Definition, concept, main categories and regulation
du Jardin, P. (2015) · Scientia Horticulturae · doi:10.1016/j.scienta.2015.09.021 · Cited by 2,863 · see citing works
Mendes, R., Garbeva, P., & Raaijmakers, J. M. (2013) · FEMS Microbiology Reviews · doi:10.1111/1574-6976.12028 · Cited by 2,836 · see citing works
Hardoim, P. R., van Overbeek, L. S., Berg, G., Pirttilä, A. M., Compant, S., Campisano, A., Döring, M., & Sessitsch, A. (2015) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00050-14 · Cited by 2,740 · see citing works
The importance of the microbiome of the plant holobiont
Vandenkoornhuyse, P., Quaiser, A., Duhamel, M., Van, A. L., & Dufresne, A. (2015) · New Phytologist · doi:10.1111/nph.13312 · Cited by 2,236 · see citing works
Backer, R. G. M., Rokem, J. S., Ilangumaran, G., Lamont, J. R., Praslickova, D., Ricci, E., Subramanian, S., & Smith, D. L. (2018) · Frontiers in Plant Science · doi:10.3389/fpls.2018.01473 · Cited by 2,233 · see citing works
The concept and future prospects of soil health
Lehmann, J. C., Bossio, D., Kögel‐Knabner, I., & Rillig, M. C. (2020) · Nature Reviews Earth & Environment · doi:10.1038/s43017-020-0080-8 · Cited by 1,903 · see citing works
Rhizosphere microbiome assemblage is affected by plant development
Chaparro, J. M., Badri, D. V., & Vivanco, J. M. (2013) · The ISME Journal · doi:10.1038/ismej.2013.196 · Cited by 1,591 · see citing works
Microbial interactions within the plant holobiont
Hassani, M. A., Durán, P., & Hacquard, S. (2018) · Microbiome · doi:10.1186/s40168-018-0445-0 · Cited by 1,416 · see citing works
Functional overlap of the Arabidopsis leaf and root microbiota
Bai, Y., Müller, D. B., Srinivas, G., Garrido‐Oter, R., Potthoff, E., Rott, M., Dombrowski, N., Münch, P. C., Spaepen, S., Remus‐Emsermann, M. N. P., et al. (2015) · Nature · doi:10.1038/nature16192 · Cited by 1,322 · see citing works
Turner, T. R., James, E. K., & Poole, P. S. (2013) · Genome Biology · doi:10.1186/gb-2013-14-6-209 · Cited by 1,349 · see citing works
Host Biology in Light of the Microbiome: Ten Principles of Holobionts and Hologenomes
Bordenstein, S. R., & Theis, K. R. (2015) · PLOS Biology · doi:10.1371/journal.pbio.1002226 · Cited by 1,240 · see citing works
Rhizosphere bacteriome structure and functions
Ling, N., Wang, T., & Kuzyakov, Y. V. (2022) · Nature Communications · doi:10.1038/s41467-022-28448-9 · Cited by 1,180 · see citing works
Pathogen-induced activation of disease-suppressive functions in the endophytic root microbiome
Carrión, V. J., Pérez‐Jaramillo, J. E., Cordovez, V., Tracanna, V., de Hollander, M., Ruiz-Buck, D., Mendes, L. W., van IJcken, W. F. J., Expósito, R. G., Elsayed, S. S., et al. (2019) · Science · doi:10.1126/science.aaw9285 · Cited by 1,171 · see citing works
NRT1.1B is associated with root microbiota composition and nitrogen use in field-grown rice
Zhang, J., Liu, Y., Zhang, N., Hu, B., Jin, T., Xu, H., Qin, Y., Yan, P., Zhang, X., Guo, X., et al. (2019) · Nature Biotechnology · doi:10.1038/s41587-019-0104-4 · Cited by 1,125 · see citing works
Assembly and ecological function of the root microbiome across angiosperm plant species
Fitzpatrick, C. R., Copeland, J. K., Wang, P. W., Guttman, D. S., Kotanen, P. M., & Johnson, M. T. J. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1717617115 · Cited by 1,102 · see citing works
Core microbiomes for sustainable agroecosystems
Toju, H., Peay, K., Yamamichi, M., Narisawa, K., Hiruma, K., Naito, K., Fukuda, S., Ushio, M., Nakaoka, S., Onoda, Y., et al. (2018) · Nature Plants · doi:10.1038/s41477-018-0139-4 · Cited by 1,077 · see citing works
Disease-induced assemblage of a plant-beneficial bacterial consortium
Berendsen, R. L., Vismans, G., Yu, K., Song, Y., de Jonge, R., Burgman, W. P., Burmølle, M., Herschend, J., Bakker, P. A. H. M., & Pieterse, C. M. J. (2018) · The ISME Journal · doi:10.1038/s41396-018-0093-1 · Cited by 1,050 · see citing works
Self-citationBiological control using invertebrates and microorganisms: plenty of new opportunities
LENTEREN, J. C. V., Bolckmans, K., Köhl, J., Ravensberg, W. J., & Urbaneja, A. (2017) · BioControl · doi:10.1007/s10526-017-9801-4 · Cited by 1,047 · see citing works
MYB72-dependent coumarin exudation shapes root microbiome assembly to promote plant health
Stringlis, I. A., Yu, K., Feussner, K., de Jonge, R., van Bentum, S., Verk, M. C. V., Berendsen, R. L., Bakker, P. A. H. M., Feußner, I., & Pieterse, C. M. J. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1722335115 · Cited by 1,011 · see citing works
Self-citationHost genotype and age shape the leaf and root microbiomes of a wild perennial plant
Wagner, M. R., Lundberg, D. S., del Rio, T. G., Tringe, S. G., Dangl, J. L., & Mitchell‐Olds, T. (2016) · Nature Communications · doi:10.1038/ncomms12151 · Cited by 976 · see citing works
Soil microbiomes and one health
Banerjee, S., & van der Heijden, M. G. A. (2022) · Nature Reviews Microbiology · doi:10.1038/s41579-022-00779-w · Cited by 948 · see citing works
Harnessing rhizosphere microbiomes for drought-resilient crop production
de Vries, F. T., Griffiths, R. I., Cg, K., Nicolitch, O., & Williams, A. (2020) · Science · doi:10.1126/science.aaz5192 · Cited by 924 · see citing works
The Plant Microbiota: Systems-Level Insights and Perspectives
Müller, D. B., Vogel, C., Bai, Y., & Vorholt, J. A. (2016) · Annual Review of Genetics · doi:10.1146/annurev-genet-120215-034952 · Cited by 849 · see citing works
Rhizosphere interactions: root exudates, microbes, and microbial communities
Huang, X.-F., Chaparro, J. M., Reardon, K. F., Zhang, R., Shen, Q., & Vivanco, J. M. (2014) · Botany · doi:10.1139/cjb-2013-0225 · Cited by 824 · see citing works
Roots Shaping Their Microbiome: Global Hotspots for Microbial Activity
Reinhold‐Hurek, B., Bünger, W., Burbano, C. S., Sabale, M., & Hurek, T. (2015) · Annual Review of Phytopathology · doi:10.1146/annurev-phyto-082712-102342 · Cited by 781 · see citing works
Microbiota and Host Nutrition across Plant and Animal Kingdoms
Hacquard, S., Garrido-Oter, R., González, A., Spaepen, S., Ackermann, G., Lebeis, S., McHardy, A. C., Dangl, J. L., Knight, R., Ley, R., et al. (2015) · Cell Host & Microbe · doi:10.1016/j.chom.2015.04.009 · Cited by 779 · see citing works
Simplified and representative bacterial community of maize roots
Niu, B., Paulson, J. N., Zheng, X., & Kolter, R. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1616148114 · Cited by 767 · see citing works
Drought Stress and Root-Associated Bacterial Communities
Naylor, D., & Coleman‐Derr, D. (2018) · Frontiers in Plant Science · doi:10.3389/fpls.2017.02223 · Cited by 765 · see citing works
Rook, G. A. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1313731110 · Cited by 760 · see citing works
Hartman, K., van der Heijden, M. G. A., Wittwer, R., Banerjee, S., Walser, J., & Schlaeppi, K. (2018) · Microbiome · doi:10.1186/s40168-017-0389-9 · Cited by 758 · see citing works
Emerging microbial biocontrol strategies for plant pathogens
Syed-Ab-Rahman, S. F., Singh, E., Pieterse, C. M. J., & Schenk, P. M. (2017) · Plant Science · doi:10.1016/j.plantsci.2017.11.012 · Cited by 748 · see citing works
Self-citationA specialized metabolic network selectively modulates Arabidopsis root microbiota
Huang, A. C., Jiang, T., Liu, Y., Bai, Y., Reed, J., Qu, B., Goossens, A., Nützmann, H., Bai, Y., & Osbourn, A. (2019) · Science · doi:10.1126/science.aau6389 · Cited by 740 · see citing works
Microbiome-Mediated Stress Resistance in Plants
Liu, H., Brettell, L. E., Qiu, Z. G., & Singh, B. K. (2020) · Trends in Plant Science · doi:10.1016/j.tplants.2020.03.014 · Cited by 744 · see citing works
Impact of plant domestication on rhizosphere microbiome assembly and functions
Pérez‐Jaramillo, J. E., Mendes, R., & Raaijmakers, J. M. (2015) · Plant Molecular Biology · doi:10.1007/s11103-015-0337-7 · Cited by 735 · see citing works
Soil Health and Sustainable Agriculture
Tahat, M. M., Alananbeh, K. M., Othman, Y. A., & Leskovar, D. I. (2020) · Sustainability · doi:10.3390/su12124859 · Cited by 772 · see citing works
Chaparro, J. M., Badri, D. V., Bakker, M. G., Sugiyama, A., Manter, D. K., & Vivanco, J. M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0055731 · Cited by 706 · see citing works
Biochar Amendment Improves Crop Production in Problem Soils: A Review
Yu, H., Zou, W., Chen, J., Chen, H., Yu, Z., Huang, J., Tang, H., Wei, X., & Gao, B. (2019) · Journal of Environmental Management · doi:10.1016/j.jenvman.2018.10.117 · Cited by 675 · see citing works
Plant root-microbe communication in shaping root microbiomes
Lareen, A., Burton, F., & Schäfer, P. (2016) · Plant Molecular Biology · doi:10.1007/s11103-015-0417-8 · Cited by 664 · see citing works
Kembel, S. W., O’Connor, T. K., Arnold, H. K., Hubbell, S. P., Wright, S. J., & Green, J. L. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1216057111 · Cited by 667 · see citing works
Root exudates drive the soil-borne legacy of aboveground pathogen infection
Yuan, J. J., Jun, Z., Wen, T., Zhao, M., Li, R., Goossens, P., Huang, Q., Bai, Y., Vivanco, J. M., Kowalchuk, G. A., et al. (2018) · Microbiome · doi:10.1186/s40168-018-0537-x · Cited by 666 · see citing works
Self-citationDrought and host selection influence bacterial community dynamics in the grass root microbiome
Naylor, D., DeGraaf, S., Purdom, E. A., & Coleman‐Derr, D. (2017) · The ISME Journal · doi:10.1038/ismej.2017.118 · Cited by 664 · see citing works
Pascale, A., Proietti, S., Pantelides, I. S., & Stringlis, I. A. (2020) · Frontiers in Plant Science · doi:10.3389/fpls.2019.01741 · Cited by 521 · see citing works
Inside the root microbiome: Bacterial root endophytes and plant growth promotion
Gaiero, J. R., McCall, C. A., Thompson, K. A., Day, N. J., Best, A., & Dunfield, K. E. (2013) · American Journal of Botany · doi:10.3732/ajb.1200572 · Cited by 650 · see citing works
Yu, P., He, X., Baer, M., Beirinckx, S., Tian, T., Moya, Y. A. T., Zhang, X., Deichmann, M., Frey, F. P., Bresgen, V., et al. (2021) · Nature Plants · doi:10.1038/s41477-021-00897-y · Cited by 626 · see citing works
Unraveling the plant microbiome: looking back and future perspectives
Berg, G., Grube, M., Schloter, M., & Smalla, K. (2014) · Frontiers in Microbiology · doi:10.3389/fmicb.2014.00148 · Cited by 630 · see citing works
Developing climate‐resilient crops: improving plant tolerance to stress combination
Rivero, R. M., Mittler, R., Blumwald, E., & Zandalinas, S. I. (2021) · The Plant Journal · doi:10.1111/tpj.15483 · Cited by 630 · see citing works
Initial soil microbiome composition and functioning predetermine future plant health
Wei, Z., Gu, Y., Friman, V., Kowalchuk, G., Xu, Y.-C., Shen, Q., & Jousset, A. (2019) · Science Advances · doi:10.1126/sciadv.aaw0759 · Cited by 544 · see citing works
Wei, Z., Yang, T., Friman, V., Xu, Y., Shen, Q., & Jousset, A. (2015) · Nature Communications · doi:10.1038/ncomms9413 · Cited by 601 · see citing works
A plant perspective on nitrogen cycling in the rhizosphere
Moreau, D., Bardgett, R. D., Finlay, R. D., Jones, D. L., & Philippot, L. (2019) · Functional Ecology · doi:10.1111/1365-2435.13303 · Cited by 592 · see citing works
Colla, G., Hoagland, L., Ruzzi, M., Cardarelli, M., Bonini, P., Canaguier, R., & Rouphael, Y. (2017) · Frontiers in Plant Science · doi:10.3389/fpls.2017.02202 · Cited by 586 · see citing works
Badri, D. V., Chaparro, J. M., Zhang, R., Shen, Q., & Vivanco, J. M. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.433300 · Cited by 579 · see citing works
A plant genetic network for preventing dysbiosis in the phyllosphere
Chen, T., Nomura, K., Wang, X., Sohrabi, R., Xu, J. H., Yao, L., Paasch, B. C., Ma, L. M., Kremer, J. M., Cheng, Y., et al. (2020) · Nature · doi:10.1038/s41586-020-2185-0 · Cited by 560 · see citing works
Rolfe, S. A., Griffiths, J., & Ton, J. (2019) · Current Opinion in Microbiology · doi:10.1016/j.mib.2019.10.003 · Cited by 575 · see citing works
The seed microbiome: Origins, interactions, and impacts
Nelson, E. B. (2017) · Plant and Soil · doi:10.1007/s11104-017-3289-7 · Cited by 563 · see citing works
Mycorrhiza-induced resistance: more than the sum of its parts?
Cameron, D. D., Neal, A. L., Wees, S. C. M. V., & Ton, J. (2013) · Trends in Plant Science · doi:10.1016/j.tplants.2013.06.004 · Cited by 562 · see citing works
Community Structure Follows Simple Assembly Rules in Microbial Microcosms
Friedman, J., Higgins, L. M., & Gore, J. (2017) · Nature Ecology & Evolution · doi:10.1038/s41559-017-0109 · Cited by 557 · see citing works
The plant microbiome explored: implications for experimental botany
Berg, G., Rybakova, D., Grube, M., & Köberl, M. (2015) · Journal of Experimental Botany · doi:10.1093/jxb/erv466 · Cited by 557 · see citing works
Zia, R., Nawaz, M. S., Siddique, M. J., Hakim, S., & Imran, A. (2020) · Microbiological Research · doi:10.1016/j.micres.2020.126626 · Cited by 567 · see citing works
Schlaeppi, K., & Bulgarelli, D. (2014) · Molecular Plant-Microbe Interactions · doi:10.1094/mpmi-10-14-0334-fi · Cited by 551 · see citing works
Competition for iron drives phytopathogen control by natural rhizosphere microbiomes
Gu, S., Wei, Z., Shao, Z., Friman, V., Cao, K., Yang, T., Kramer, J., Wang, X., Li, M., Mei, X., et al. (2020) · Nature Microbiology · doi:10.1038/s41564-020-0719-8 · Cited by 549 · see citing works
Plant microbial diversity is suggested as the key to future biocontrol and health trends
Berg, G., Köberl, M., Rybakova, D., Müller, H., Grosch, R., & Smalla, K. (2017) · FEMS Microbiology Ecology · doi:10.1093/femsec/fix050 · Cited by 546 · see citing works
Microbial indicators for soil quality
Schloter, M., Nannipieri, P., Sørensen, S. J., & van Elsas, J. D. (2018) · Biology and Fertility of Soils · doi:10.1007/s00374-017-1248-3 · Cited by 540 · see citing works
In Posidonia oceanica cadmium induces changes in DNA methylation and chromatin patterning
Greco, M., Chiappetta, A. A. C., Bruno, L., & Bitonti, M. B. (2011) · Journal of Experimental Botany · doi:10.1093/jxb/err313 · Cited by 533 · see citing works
Beckers, B., Beeck, M. O. D., Weyens, N., Boerjan, W., & Vangronsveld, J. (2017) · Microbiome · doi:10.1186/s40168-017-0241-2 · Cited by 527 · see citing works
Root exudates impact plant performance under abiotic stress
Chai, Y. N., & Schachtman, D. P. (2021) · Trends in Plant Science · doi:10.1016/j.tplants.2021.08.003 · Cited by 523 · see citing works
Chen, S., Waghmode, T. R., Sun, R., Kuramae, E. E., Hu, C., & Liu, B. (2019) · Microbiome · doi:10.1186/s40168-019-0750-2 · Cited by 517 · see citing works
Plant microbiome–an account of the factors that shape community composition and diversity
Dastogeer, K. M. G., Tumpa, F. H., Sultana, A., Akter, M. A., & Chakraborty, A. (2020) · Current Plant Biology · doi:10.1016/j.cpb.2020.100161 · Cited by 507 · see citing works
Phytopathogen Effectors Subverting Host Immunity: Different Foes, Similar Battleground
Dou, D., & Zhou, J. (2012) · Cell Host & Microbe · doi:10.1016/j.chom.2012.09.003 · Cited by 497 · see citing works
Microbes Drive Evolution of Animals and Plants: the Hologenome Concept
ROSENBERG, E. B., & Zilber‐Rosenberg, I. (2016) · mBio · doi:10.1128/mbio.01395-15 · Cited by 499 · see citing works
Etesami, H., & Beattie, G. A. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.00148 · Cited by 496 · see citing works
Plant-derived coumarins shape the composition of an Arabidopsis synthetic root microbiome
Voges, M. J., Bai, Y., Schulze‐Lefert, P., & Sattely, E. S. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1820691116 · Cited by 494 · see citing works
Systems Biology of Plant-Microbiome Interactions
Rodriguez, P. A., Rothballer, M., Chowdhury, S. P., Nußbaumer, T., Gutjahr, C., & Falter‐Braun, P. (2019) · Molecular Plant · doi:10.1016/j.molp.2019.05.006 · Cited by 493 · see citing works
The rhizosphere revisited: root microbiomics
Bakker, P. A. H. M., Berendsen, R. L., Doornbos, R. F., Wintermans, P. C. A., & Pieterse, C. M. J. (2013) · Frontiers in Plant Science · doi:10.3389/fpls.2013.00165 · Cited by 492 · see citing works
Self-citationNetworking in the Plant Microbiome
van der Heijden, M. G. A., & Hartmann, M. (2016) · PLoS Biology · doi:10.1371/journal.pbio.1002378 · Cited by 492 · see citing works
Edwards, J. A., Santos‐Medellín, C., Liechty, Z., Nguyen, B., Lurie, E., Eason, S., Phillips, G. C., & Sundaresan, V. (2018) · PLoS Biology · doi:10.1371/journal.pbio.2003862 · Cited by 488 · see citing works
Revisiting fertilisers and fertilisation strategies for improved nutrient uptake by plants
Bindraban, P. S., Dimkpa, C. O., Nagarajan, L., Roy, A. A., & Rabbinge, R. (2015) · Biology and Fertility of Soils · doi:10.1007/s00374-015-1039-7 · Cited by 485 · see citing works
Transmission of Bacterial Endophytes
Frank, A. C., Guzmán, J. P. S., & Shay, J. E. (2017) · Microorganisms · doi:10.3390/microorganisms5040070 · Cited by 485 · see citing works
Ecology and Genomic Insights into Plant-Pathogenic and Plant-Nonpathogenic Endophytes
Brader, G., Compant, S., Vescio, K., Mitter, B., Trognitz, F., Ma, L., & Sessitsch, A. (2017) · Annual Review of Phytopathology · doi:10.1146/annurev-phyto-080516-035641 · Cited by 484 · see citing works
Systemic propagation of immunity in plants
Vlot, A. C., Sales, J. H., Lenk, M., Bauer, K., Brambilla, A., Sommer, A. K., Chen, Y., Wenig, M., & Nayem, S. (2020) · New Phytologist · doi:10.1111/nph.16953 · Cited by 467 · see citing works
A Synthetic Community Approach Reveals Plant Genotypes Affecting the Phyllosphere Microbiota
Bodenhausen, N., Bortfeld‐Miller, M., Ackermann, M., & Vorholt, J. A. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004283 · Cited by 477 · see citing works
Rhizosphere Microbiome Assembly and Its Impact on Plant Growth
Qu, Q., Zhang, Z., Peijnenburg, W. J. G. M., Liu, W., Lu, T., Hu, B., Chen, J., Chen, J., Lin, Z., & Qian, H. (2020) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.0c00073 · Cited by 467 · see citing works
Tao, C., Li, R., Xiong, W., Shen, Z., Liu, S., Wang, B., Ruan, Y., Geisen, S., Shen, Q., & Kowalchuk, G. A. (2020) · Microbiome · doi:10.1186/s40168-020-00892-z · Cited by 465 · see citing works
Zhao, Z.-B., He, J., Geisen, S., Han, L.-L., Wang, J., Shen, J., Wei, W.-X., Fang, Y., Li, P.-P., & Zhang, L. (2019) · Microbiome · doi:10.1186/s40168-019-0647-0 · Cited by 465 · see citing works
Rhizosphere Colonization Determinants by Plant Growth-Promoting Rhizobacteria (PGPR)
Santoyo, G., Urtis-Flores, C. A., Loeza-Lara, P. D., Orozco-Mosqueda, M. D. C., & Glick, B. R. (2021) · Biology · doi:10.3390/biology10060475 · Cited by 463 · see citing works
Associations with rhizosphere bacteria can confer an adaptive advantage to plants
Haney, C. H., Samuel, B. S., Bush, J., & Ausubel, F. M. (2015) · Nature Plants · doi:10.1038/nplants.2015.51 · Cited by 462 · see citing works
Root exudates drive soil‐microbe‐nutrient feedbacks in response to plant growth
Zhao, M., Zhao, J., Yuan, J. J., Hale, L. E., Wen, T., Huang, Q., Vivanco, J. M., Zhou, J. Z., Kowalchuk, G. A., & Shen, Q. (2020) · Plant Cell & Environment · doi:10.1111/pce.13928 · Cited by 459 · see citing works
van der Heijden, M. G. A., de Bruin, S. J., Luckerhoff, L. L. P., van Logtestijn, R. S. P., & Schlaeppi, K. (2015) · The ISME Journal · doi:10.1038/ismej.2015.120 · Cited by 443 · see citing works
Santhanam, R., Schepler‐Luu, V., Weinhold, A., Goldberg, J. K., Oh, Y., & Baldwin, I. T. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1505765112 · Cited by 443 · see citing works
Saleem, M., Hu, J., & Jousset, A. (2019) · Annual Review of Ecology, Evolution, and Systematics · doi:10.1146/annurev-ecolsys-110617-062605 · Cited by 437 · see citing works
The Populus holobiont: dissecting the effects of plant niches and genotype on the microbiome
Cregger, M. A., Veach, A. M., Yang, Z. K., Crouch, M. J., Vilgalys, R. J., Tuskan, G. A., & Schadt, C. W. (2018) · Microbiome · doi:10.1186/s40168-018-0413-8 · Cited by 437 · see citing works
Rhizosphere microorganisms can influence the timing of plant flowering
Lu, T., Ke, M., Lavoie, M., Jin, Y., Fan, X., Zhang, Z., Fu, Z., Sun, L., Gillings, M. R., Peñuelas, J., et al. (2018) · Microbiome · doi:10.1186/s40168-018-0615-0 · Cited by 435 · see citing works
Root-Secreted Coumarins and the Microbiota Interact to Improve Iron Nutrition in Arabidopsis
Harbort, C. J., Hashimoto, M., Inoue, H., Niu, Y., Guan, R., Rombolà, A. D., Kopřiva, S., Voges, M. J., Sattely, E. S., Garrido‐Oter, R., et al. (2020) · Cell Host & Microbe · doi:10.1016/j.chom.2020.09.006 · Cited by 413 · see citing works
Barnawal, D., Bharti, N., Pandey, S. S., Pandey, A., Chanotiya, C. S., & Kalra, A. (2017) · Physiologia Plantarum · doi:10.1111/ppl.12614 · Cited by 424 · see citing works
Plant health: feedback effect of root exudates-rhizobiome interactions
Olanrewaju, O. S., Ayangbenro, A. S., Glick, B. R., & Babalola, O. O. (2018) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-018-9556-6 · Cited by 423 · see citing works
The Age of Coumarins in Plant–Microbe Interactions
Stringlis, I. A., de Jonge, R., & Pieterse, C. M. J. (2019) · Plant and Cell Physiology · doi:10.1093/pcp/pcz076 · Cited by 421 · see citing works
Self-citation
- Authors
- Berendsen, R. L., Pieterse, C. M. J., & Bakker, P. A. H. M.
- Affiliations
- Utrecht University (NL)
- Venue
- Trends in Plant Science
- Publisher
- Elsevier BV
- Published
- 2012-08
- Volume
- 17
- Issue
- 8
- Pages
- 478-486
- ISSN
- 1360-1385 (ISSN-L)
- OpenAlex
- W2017387862
- Cited by
- 5,347
- References
- 96
- Citations by year
- 2026: 587 · 2025: 545 · 2024: 570 · 2023: 546 · 2022: 565 · 2021: 573 · 2020: 509 · 2019: 395 · 2018: 289 · 2017: 240 · 2016: 173 · 2015: 147 · 2014: 114 · 2013: 79 · 2012: 7
- FWCI
- 11.84
- Type
- journal article
- Language
- en
- Open access
- green
- dspace.library.uu.nl
- Licence
- Locations
- Trends in Plant Science (publishedVersion)
- PubMed (publishedVersion)
- Utrecht University Repository (Utrecht University) (submittedVersion)
- Utrecht University Repository (Utrecht University) (submittedVersion, other-oa)
- Funders
- FP7 Ideas: European Research Council (269072)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant-Microbe Interactions and Immunity
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Mycorrhizal Fungi and Plant Interactions
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Legume Nitrogen Fixing Symbiosis
- Keywords
- rhizosphere microbiome, plant health, plant-microbe interactions, root-associated microorganisms, plant defense against pathogens, plant defense against insects, plant-associated microbial communities, crop production
- MeSH terms
- Anti-Infective Agents, Fungi, Plant Diseases, Plants, Pseudomonas, Rhizobiaceae, Soil Microbiology, Species Specificity, Plant Roots, Host-Pathogen Interactions, Metagenome, Microbial Interactions, Rhizosphere, Biota
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