Abstract
Aims
The present study provides an insight on physiological parameters and root-associated microbiome of two complementary Arabidopsis thaliana culture systems suitable for physiological studies.
Methods
A. thaliana plants were grown in rhizobox and in classic pot culture. An analysis of plant growth parameters along with the characterization of the bacterial communities of the compost and the rhizosphere, rhizoplane and endosphere compartments were performed.
Results
A. thaliana plants grown in rhizobox exhibited a plant habitus similar to those grown in pots during the first month, but with a delayed leaf initiation and slower rate of growth over the experiment. No nutrient deficiency symptoms were observed in these plants. The rhizobox design permits the migration of bacteria from compost to plant roots and allowed root-bacteria interactions to be established as in traditional pot culture. Some differences into the composition of the rhizobiome were highlighted between the two culture systems. Nevertheless, key bacterial taxa that help to ensure plant growth and health colonized the rhizo- and endosphere compartments in both systems.
Conclusions
This study gives some clues for future research programs and selection of efficient root systems with the use of such specific culture devices.
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References
Adu M, Yawson D, Bennett M, Broadley M, Dupuy L, White P (2017) A scanner-based rhizobox system enabling the quantification of root system development and response of Brassica rapa seedlings to external P availability. Plant Root 11:16–32. https://doi.org/10.3117/plantroot.11.16
Aviani I, Laor Y, Raviv M (2006) Limitations and potential of in situ Rhizobox sampling for assessing microbial activity in fruit tree Rhizosphere. Plant Soil 279(1):327–332. https://doi.org/10.1007/s11104-005-2189-4
Badri DV, Chaparro JM, Zhang R, Shen Q, Vivanco JM (2013) Application of natural blends of phytochemicals derived from the root exudates of Arabidopsis to the soil reveal that phenolic-related compounds predominantly modulate the soil microbiome. J Biol Chem 288(7):4502–4512. https://doi.org/10.1074/jbc.M112.433300
Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annual Review of Plant Biology 57(1):233–266. https://doi.org/10.1146/annurev.arplant.57.032905.105159
Baker GC, Smith JJ, Cowan DA (2003) Review and re-analysis of domain-specific 16S primers. J Microbiol Methods 55(3):541–555
Bakker PAHM, Berendsen RL, Doornbos RF, Wintermans PCA, Pieterse CMJ (2013) The rhizosphere revisited: root microbiomics. Front Plant Sci 4. https://doi.org/10.3389/fpls.2013.00165
Barillot CC, Sarde C-O, Bert V, Tarnaud E, Cochet N (2012) A standardized method for the sampling of rhizosphere and rhizoplan soil bacteria associated to a herbaceous root system. Ann Microbiol 63(2):471–476. https://doi.org/10.1007/s13213-012-0491-y
Berendsen RL, Pieterse CMJ, Bakker PAHM (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17(8):478–486. https://doi.org/10.1016/j.tplants.2012.04.001
Berry D, Ben Mahfoudh K, Wagner M, Loy A (2011) Barcoded primers used in multiplex amplicon pyrosequencing bias amplification. Appl Environ Microbiol 77(21):7846–7849. https://doi.org/10.1128/AEM.05220-11
Blossfeld S, Schreiber CM, Liebsch G, Kuhn AJ, Hinsinger P (2013) Quantitative imaging of rhizosphere pH and CO2 dynamics with planar optodes. Ann Bot 112(2):267–276. https://doi.org/10.1093/aob/mct047
Boyes DC, Zayed AM, Ascenzi R, McCaskill AJ, Hoffman NE, Davis KR, Görlach J (2001) Growth stage–based phenotypic analysis of Arabidopsis. A Model for High Throughput Functional Genomics in Plants 13(7):1499–1510. https://doi.org/10.1105/tpc.010011
Bulgarelli D, Rott M, Schlaeppi K, Ver Loren van Themaat E, 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(7409):91–95
Bulgarelli D, Schlaeppi K, Spaepen S, van Themaat EVL, Schulze-Lefert P (2013) Structure and functions of the bacterial microbiota of plants. Annu Rev Plant Biol 64 (1):807–838. https://doi.org/10.1146/annurev-arplant-050312-120106
Chaparro JM, Badri DV, Vivanco JM (2013) Rhizosphere microbiome assemblage is affected by plant development. The Isme Journal 8:790. https://doi.org/10.1038/ismej.2013.196https://www.nature.com/articles/ismej2013196#supplementary-information
Ciampitti IA, Camberato JJ, Murrell ST, Vyn TJ (2013) Maize nutrient accumulation and partitioning in response to plant density and nitrogen rate: I. macronutrients. Agron J 105(3):783–795. https://doi.org/10.2134/agronj2012.0467
Den Herder G, Van Isterdael G, Beeckman T, De Smet I (2010) The roots of a new green revolution. Trends Plant Sci 15(11):600–607. https://doi.org/10.1016/j.tplants.2010.08.009
Drake T, Keating M, Summers R, Yochikawa A, Pitman T, Dodd AN (2016) The cultivation of Arabidopsis for experimental research using commercially available peat-based and peat-free growing media. PLoS One 11(4):e0153625. https://doi.org/10.1371/journal.pone.0153625
Durand M, Porcheron B, Hennion N, Maurousset L, Lemoine R, Pourtau N (2016) Water deficit enhances C export to the roots in Arabidopsis thaliana plants with contribution of sucrose transporters in both shoot and roots. Plant Physiol 170(3):1460–1479. https://doi.org/10.1104/pp.15.01926
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. Proc Natl Acad Sci 112(8):E911–E920. https://doi.org/10.1073/pnas.1414592112
Faure D, Vereecke D, Leveau JHJ (2009) Molecular communication in the rhizosphere. Plant Soil 321(1):279–303. https://doi.org/10.1007/s11104-008-9839-2
Finkel OM, Salas-González I, Castrillo G, Law TF, Conway JM, Jones CD, Dangl JL (2019) Root development is maintained by specific bacteria-bacteria interactions within a complex microbiome. bioRxiv:645655. https://doi.org/10.1101/645655
Gaiero JR, McCall CA, Thompson KA, Day NJ, Best AS, Dunfield KE (2013) Inside the root microbiome: bacterial root endophytes and plant growth promotion. American journal of botany 100 (9):1738–1750. https://doi.org/10.3732/ajb.1200572
Gruber BD, Giehl RFH, Friedel S, von Wirén N (2013) Plasticity of the Arabidopsis root system under nutrient deficiencies. Plant Physiol 163(1):161–179. https://doi.org/10.1104/pp.113.218453
Hänsch R, Mendel RR (2009) Physiological functions of mineral micronutrients (cu, Zn, Mn, Fe, Ni, Mo, B, cl). Curr Opin Plant Biol 12(3):259–266. https://doi.org/10.1016/j.pbi.2009.05.006
Himelblau E, Amasino RM (2001) Nutrients mobilized from leaves of Arabidopsis thaliana during leaf senescence. J Plant Physiol 158(10):1317–1323. https://doi.org/10.1078/0176-1617-00608
Hinsinger P, Plassard C, Tang C, Jaillard B (2003) Origins of root-mediated pH changes in the rhizosphere and their responses to environmental constraints: a review. Plant Soil 248(1):43–59. https://doi.org/10.1023/a:1022371130939
Huang AC, Jiang T, Liu Y-X, Bai Y-C, Reed J, Qu B, Goossens A, Nützmann H-W, Bai Y, Osbourn A (2019) A specialized metabolic network selectively modulates <em>Arabidopsis</em> root microbiota. Science 364 (6440):eaau6389. https://doi.org/10.1126/science.aau6389
Jeudy C, Adrian M, Baussard C, Bernard C, Bernaud E, Bourion V, Busset H, Cabrera-Bosquet L, Cointault F, Han S, Lamboeuf M, Moreau D, Pivato B, Prudent M, Trouvelot S, Truong HN, Vernoud V, Voisin A-S, Wipf D, Salon C (2016) RhizoTubes as a new tool for high throughput imaging of plant root development and architecture: test, comparison with pot grown plants and validation. Plant Methods 12(1):31. https://doi.org/10.1186/s13007-016-0131-9
Kong Z, Hart M, Liu H (2018) Paving the way from the lab to the field: using synthetic microbial consortia to produce high-quality crops. Front Plant Sci 9(1467). https://doi.org/10.3389/fpls.2018.01467
Leadbetter JR, Greenberg EP (2000) Metabolism of acyl-Homoserine lactone quorum-sensing signals by <em>Variovorax paradoxus</em>. J Bacteriol 182(24):6921–6926. https://doi.org/10.1128/jb.182.24.6921-6926.2000
Lemanceau P, Blouin M, Muller D, Moënne-Loccoz Y (2017) Let the Core microbiota be functional. Trends Plant Sci 22(7):583–595. https://doi.org/10.1016/j.tplants.2017.04.008
Lemonnier P, Gaillard C, Veillet F, Verbeke J, Lemoine R, Coutos-Thévenot P, La Camera S (2014) Expression of Arabidopsis sugar transport protein STP13 differentially affects glucose transport activity and basal resistance to Botrytis cinerea. Plant Mol Biol 85(4–5):473–484. https://doi.org/10.1007/s11103-014-0198-5
Liñero O, Cornu J-Y, de Diego A, Bussière S, Coriou C, Thunot S, Robert T, Nguyen C (2018) Source of Ca, cd, cu, Fe, K, mg, Mn, Mo and Zn in grains of sunflower (Helianthus annuus) grown in nutrient solution: root uptake or remobilization from vegetative organs? Plant Soil 424(1):435–450. https://doi.org/10.1007/s11104-017-3552-y
Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S, Tremblay J, Engelbrektson A, Kunin V, Rio TG, Edgar RC, Eickhorst T, Ley RE, Hugenholtz P, Tringe SG, Dangl JL (2012) Defining the core Arabidopsis thaliana root microbiome. Nature 488(7409):86–90
Maathuis FJM (2007) Monovalent cation transporters; establishing a link between bioinformatics and physiology. Plant Soil 301(1–2):1–15. https://doi.org/10.1007/s11104-007-9429-8
Maathuis FJM (2009) Physiological functions of mineral macronutrients. Curr Opin Plant Biol 12(3):250–258. https://doi.org/10.1016/j.pbi.2009.04.003
Maillard A, Diquélou S, Billard V, Laîné P, Garnica M, Prudent M, Garcia-Mina J-M, Yvin J-C, Ourry A (2015) Leaf mineral nutrient remobilization during leaf senescence and modulation by nutrient deficiency. Front Plant Sci 6(317). https://doi.org/10.3389/fpls.2015.00317
Mauchline TH, Malone JG (2017) Life in earth – the root microbiome to the rescue? Curr Opin Microbiol 37:23–28. https://doi.org/10.1016/j.mib.2017.03.005
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(6033):1097–1100. https://doi.org/10.1126/science.1203980
Nawrocki EP, Eddy SR (2013) Infernal 1.1: 100-fold faster RNA homology searches. Bioinformatics 29(22):2933–2935. https://doi.org/10.1093/bioinformatics/btt509
Neumann G, George TS, Plassard C (2009) Strategies and methods for studying the rhizosphere—the plant science toolbox. Plant Soil 321(1):431–456. https://doi.org/10.1007/s11104-009-9953-9
Philippot L, M Raaijmakers J, Lemanceau P, H van der Putten W (2013a) Going back to the roots: The microbial ecology of the rhizosphere, vol 11. https://doi.org/10.1038/nrmicro3109
Philippot L, Spor A, Henault C, Bru D, Bizouard F, Jones CM, Sarr A, Maron P-A (2013b) Loss in microbial diversity affects nitrogen cycling in soil. ISME J 7(8):1609–1619. https://doi.org/10.1038/ismej.2013.34
Plassart P, Terrat S, Thomson B, Griffiths R, Dequiedt S, Lelievre M, Regnier T, Nowak V, Bailey M, Lemanceau P, Bispo A, Chabbi A, Maron P-A, Mougel C, Ranjard L (2012) Evaluation of the ISO standard 11063 DNA extraction procedure for assessing soil microbial abundance and community structure. PLoS One 7(9):e44279. https://doi.org/10.1371/journal.pone.0044279
Pourtau N, Jennings R, Pelzer E, Pallas J, Wingler A (2006) Effect of sugar-induced senescence on gene expression and implications for the regulation of senescence in Arabidopsis. Planta 224(3):556–568. https://doi.org/10.1007/s00425-006-0243-y
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41(D1):D590–D596. https://doi.org/10.1093/nar/gks1219
R Development Core Team (2018) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. Available online at https://www.R-project.org/. Accessed 2 Sept 2019
Ranjard L, Lejon DPH, Mougel C, Schehrer L, Merdinoglu D, Chaussod R (2003) Sampling strategy in molecular microbial ecology: influence of soil sample size on DNA fingerprinting analysis of fungal and bacterial communities. Environ Microbiol 5(11):1111–1120. https://doi.org/10.1046/j.1462-2920.2003.00521.x
Rellán-Álvarez R, Lobet G, Lindner H, Pradier P-L, Sebastian J, Yee M-C, Geng Y, Trontin C, LaRue T, Schrager-Lavelle A, Haney CH, Nieu R, Maloof J, Vogel JP, Dinneny JR (2015) GLO-roots: an imaging platform enabling multidimensional characterization of soil-grown root systems. eLife 4:e07597. doi:https://doi.org/10.7554/eLife.07597
Sasse J, Martinoia E, Northen T (2017) Feed your friends: do Plant exudates shape the root microbiome? Trends Plant Sci 23(1):25–41. https://doi.org/10.1016/j.tplants.2017.09.003
Slafer GA (2003) Genetic basis of yield as viewed from a crop physiologist's perspective. Ann Appl Biol 142(2):117–128. https://doi.org/10.1111/j.1744-7348.2003.tb00237.x
Terrat S, Christen R, Dequiedt S, Lelièvre M, Nowak V, Regnier T, Bachar D, Plassart P, Wincker P, Jolivet C, Bispo A, Lemanceau P, Maron PA, Mougel C, Ranjard L (2012) Molecular biomass and MetaTaxogenomic assessment of soil microbial communities as influenced by soil DNA extraction procedure. Microb Biotechnol 5(1):135–141. https://doi.org/10.1111/j.1751-7915.2011.00307.x
Terrat S, Plassart P, Bourgeois E, Ferreira S, Dequiedt S, Adele-Dit-De-Renseville N, Lemanceau P, Bispo A, Chabbi A, Maron P-A, Ranjard L (2015) Meta-barcoded evaluation of the ISO standard 11063 DNA extraction procedure to characterize soil bacterial and fungal community diversity and composition. Microb Biotechnol 8(1):131–142. https://doi.org/10.1111/1751-7915.12162
Toussaint J-P, Pham TTM, Barriault D, Sylvestre M (2012) Plant exudates promote PCB degradation by a rhodococcal rhizobacteria. Appl Microbiol Biotechnol 95(6):1589–1603. https://doi.org/10.1007/s00253-011-3824-z
Vacheron J, Desbrosses G, Bouffaud M-L, Touraine B, MoÎnne-Loccoz Y, Muller D, Legendre L, Wisniewski-DyÈ F, Prigent-Combaret C (2013) Plant growth-promoting rhizobacteria and root system functioning. Front Plant Sci 4. https://doi.org/10.3389/fpls.2013.00356
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(3):296–310. https://doi.org/10.1111/j.1461-0248.2007.01139.x
Vandenkoornhuyse P, Quaiser A, Duhamel M, Le Van A, Dufresne A (2015) The importance of the microbiome of the plant holobiont. New Phytol 206(4):1196–1206. https://doi.org/10.1111/nph.13312
Veillet F, Gaillard C, Coutos-Thévenot P, La Camera S (2016) Targeting the AtCWIN1 gene to explore the role of Invertases in sucrose transport in roots and during Botrytis cinerea infection. Front Plant Sci 7(1899). https://doi.org/10.3389/fpls.2016.01899
Venturi V, Keel C (2016) Signaling in the Rhizosphere. Trends Plant Sci 21(3):187–198. https://doi.org/10.1016/j.tplants.2016.01.005
Verbon EH, Liberman LM (2016) Beneficial microbes affect endogenous mechanisms controlling root development. Trends Plant Sci 21(3):218–229. https://doi.org/10.1016/j.tplants.2016.01.013
Vereecke D, Burssens S, Simón-Mateo C, Inzé D, Van Montagu M, Goethals K, Jaziri M (2000) The Rhodococcus fascians-plant interaction: morphological traits and biotechnological applications. Planta 210(2):241–251. https://doi.org/10.1007/PL00008131
Větrovský T, Baldrian P (2013) The variability of the 16S rRNA gene in bacterial genomes and its consequences for bacterial community analyses. PLoS One 8(2):e57923. https://doi.org/10.1371/journal.pone.0057923
Warnes GR, Bolker B, Bonebakker L, Gentleman R, Liaw WHA, Lumley T, Maechler M, Magnusson A, Moeller S, Schwartz M (2015) gplots: various R programming tools for plotting data. R package version 2.17. 0. Computer software]. Available online at: https://cran.r-project.org/web/packages/gplots/index.html
Wenzel WW, Wieshammer G, Fitz WJ, Puschenreiter M (2001) Novel rhizobox design to assess rhizosphere characteristics at high spatial resolution. Plant Soil 237(1):37–45. https://doi.org/10.1023/a:1013395122730
Xiong L, Wang R-G, Mao G, Koczan JM (2006) Identification of drought tolerance determinants by genetic analysis of root response to drought stress and Abscisic acid. Plant Physiol 142(3):1065–1074. https://doi.org/10.1104/pp.106.084632
Xu J, Zhang Y, Zhang P, Trivedi P, Riera N, Wang Y, Liu X, Fan G, Tang J, Coletta-Filho HD, Cubero J, Deng X, Ancona V, Lu Z, Zhong B, Roper MC, Capote N, Catara V, Pietersen G, Vernière C, Al-Sadi AM, Li L, Yang F, Xu X, Wang J, Yang H, Jin T, Wang N (2018) The structure and function of the global citrus rhizosphere microbiome. Nat Commun 9(1):4894. https://doi.org/10.1038/s41467-018-07343-2
Yan Y, Kuramae EE, de Hollander M, Klinkhamer PGL, van Veen JA (2017) Functional traits dominate the diversity-related selection of bacterial communities in the rhizosphere. The Isme Journal 11:56–66. https://doi.org/10.1038/ismej.2016.108. https://www.nature.com/articles/ismej2016108#supplementary-information
Acknowledgements
The authors are grateful to Dr. Cécile Vriet for comprehensive review of the manuscript. The results presented here were obtained through the EBI program “AAP”. The authors are sincerely thankful for the scientific support and helpful discussions provided by S. Terrat and the GenoSol platform (INRA Dijon, France; www2.dijon.inra.fr/plateforme_genosol/) for the development of the pyrosequencing and data analysis.
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Mercier, A., Mignerot, L., Hennion, N. et al. Growth of Arabidopsis thaliana in rhizobox culture system evaluated through the lens of root microbiome. Plant Soil 455, 467–487 (2020). https://doi.org/10.1007/s11104-020-04650-w
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DOI: https://doi.org/10.1007/s11104-020-04650-w