The state of rhizospheric science in the era of multi-omics: A practical guide to omics technologies

White, Richard Allen; Rivas-Ubach, Albert; Borkum, Mark I.; Köberl, Martina; Bilbao, Aivett; Colby, Sean M.; Hoyt, David W.; Bingol, Kerem; Kim, Young-Mo; Wendler, Jason P.; Hixson, Kim K.; Jansson, Christer

doi:10.1016/J.RHISPH.2017.05.003

Title: The state of rhizospheric science in the era of multi-omics: A practical guide to omics technologies

Journal Article · Sat May 06 00:00:00 EDT 2017 · Rhizosphere

DOI:https://doi.org/10.1016/J.RHISPH.2017.05.003· OSTI ID:1355770

White, Richard Allen ^[1]; Rivas-Ubach, Albert ^[1]; Borkum, Mark I. ^[1]; Köberl, Martina ^[2]; Bilbao, Aivett ^[1]; Colby, Sean M. ^[1]; Hoyt, David W. ^[1]; Bingol, Kerem ^[1]; Kim, Young-Mo ^[1]; Wendler, Jason P. ^[1]; Hixson, Kim K. ^[1]; Jansson, Christer ^[1]

Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Earth and Biological Sciences Directorate
Graz Univ. of Technology (Austria). Inst. of Environmental Biotechnology

Over the past century, the significance of the rhizosphere has been increasingly recognized by the scientific community. Furthermore, this complex biological system is comprised of vast interconnected networks of microbial organisms that interact directly with their plant hosts, including archaea, bacteria, fungi, picoeukaryotes, and viruses. The rhizosphere provides a nutritional base to the terrestrial biosphere, and is integral to plant growth, crop production, and ecosystem health. There is little mechanistic understanding of the rhizosphere, but, and that constitutes a critical knowledge gap. It inhibits our ability to predict and control the terrestrial ecosystem to achieve desirable outcomes, such as bioenergy production, crop yield maximization, and soil-based carbon sequestration. Multi-omics have the potential to significantly advance our knowledge of rhizospheric science. Our review covers multi-omic techniques and technologies; methods and protocols for specific rhizospheric science questions; and the challenges to be addressed during this century of rhizospheric science.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC05-76RL01830

OSTI ID:: 1355770

Alternate ID(s):: OSTI ID: 1496481

Report Number(s):: PNNL-SA-124859; PII: S2452219817300666

Journal Information:: Rhizosphere, Vol. 3, Issue 2; ISSN 2452-2198

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 46 works

Citation information provided by
Web of Science

References (95)

Mass Spectrometry in Proteomics Aebersold, Ruedi; Goodlett, David R. Chemical Reviews, Vol. 101, Issue 2 https://doi.org/10.1021/cr990076h	journal	February 2001
Mass spectrometry-based proteomics Aebersold, Ruedi; Mann, Matthias Nature, Vol. 422, Issue 6928 https://doi.org/10.1038/nature01511	journal	March 2003
Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system Anantharaman, Karthik; Brown, Christopher T.; Hug, Laura A. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms13219	journal	October 2016
Regulation and function of root exudates Badri, Dayakar V.; Vivanco, Jorge M. Plant, Cell & Environment, Vol. 32, Issue 6 https://doi.org/10.1111/j.1365-3040.2009.01926.x	journal	June 2009
Metaproteomic Identification of Diazotrophic Methanotrophs and Their Localization in Root Tissues of Field-Grown Rice Plants Bao, Zhihua; Okubo, Takashi; Kubota, Kengo Applied and Environmental Microbiology, Vol. 80, Issue 16 https://doi.org/10.1128/AEM.00969-14	journal	August 2014
Accurate whole human genome sequencing using reversible terminator chemistry Bentley, David R.; Balasubramanian, Shankar; Swerdlow, Harold P. Nature, Vol. 456, Issue 7218 https://doi.org/10.1038/nature07517	journal	November 2008
The rhizosphere microbiome and plant health Berendsen, Roeland L.; Pieterse, Corné M. J.; Bakker, Peter A. H. M. Trends in Plant Science, Vol. 17, Issue 8 https://doi.org/10.1016/j.tplants.2012.04.001	journal	August 2012
Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere: Plant species, soil type and rhizosphere communities Berg, Gabriele; Smalla, Kornelia FEMS Microbiology Ecology, Vol. 68, Issue 1 https://doi.org/10.1111/j.1574-6941.2009.00654.x	journal	April 2009
Dynamics of 18O Incorporation from H 2 18O into Soil Microbial DNA Blazewicz, Steven J.; Schwartz, Egbert Microbial Ecology, Vol. 61, Issue 4 https://doi.org/10.1007/s00248-011-9826-7	journal	March 2011
Evaluating rRNA as an indicator of microbial activity in environmental communities: limitations and uses Blazewicz, Steven J.; Barnard, Romain L.; Daly, Rebecca A. The ISME Journal, Vol. 7, Issue 11 https://doi.org/10.1038/ismej.2013.102	journal	July 2013
Sampling for Metabolome Analysis of Microorganisms Bolten, Christoph J.; Kiefer, Patrick; Letisse, Fabien Analytical Chemistry, Vol. 79, Issue 10 https://doi.org/10.1021/ac0623888	journal	May 2007
Unusual biology across a group comprising more than 15% of domain Bacteria Brown, Christopher T.; Hug, Laura A.; Thomas, Brian C. Nature, Vol. 523, Issue 7559 https://doi.org/10.1038/nature14486	journal	June 2015
Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota Bulgarelli, Davide; Rott, Matthias; Schlaeppi, Klaus Nature, Vol. 488, Issue 7409 https://doi.org/10.1038/nature11336	journal	August 2012
Environmental metabolomics: a critical review and future perspectives Bundy, Jacob G.; Davey, Matthew P.; Viant, Mark R. Metabolomics, Vol. 5, Issue 1 https://doi.org/10.1007/s11306-008-0152-0	journal	December 2008
A method for high precision sequencing of near full-length 16S rRNA genes on an Illumina MiSeq Burke, Catherine M.; Darling, Aaron E. PeerJ, Vol. 4 https://doi.org/10.7717/peerj.2492	journal	January 2016
Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms Caporaso, J. Gregory; Lauber, Christian L.; Walters, William A. The ISME Journal, Vol. 6, Issue 8 https://doi.org/10.1038/ismej.2012.8	journal	March 2012
Relic DNA is abundant in soil and obscures estimates of soil microbial diversity Carini, Paul; Marsden, Patrick J.; Leff, Jonathan W. Nature Microbiology, Vol. 2, Issue 3 https://doi.org/10.1038/nmicrobiol.2016.242	journal	December 2016
Direct Cellular Lysis/Protein Extraction Protocol for Soil Metaproteomics Chourey, Karuna; Jansson, Janet; VerBerkmoes, Nathan Journal of Proteome Research, Vol. 9, Issue 12 https://doi.org/10.1021/pr100787q	journal	December 2010
The number of known plants species in the world and its annual increase Christenhusz, Maarten J. M.; Byng, James W. Phytotaxa, Vol. 261, Issue 3 https://doi.org/10.11646/phytotaxa.261.3.1	journal	May 2016
Untargeted large-scale plant metabolomics using liquid chromatography coupled to mass spectrometry De Vos, Ric CH; Moco, Sofia; Lommen, Arjen Nature Protocols, Vol. 2, Issue 4 https://doi.org/10.1038/nprot.2007.95	journal	April 2007
Impact of root exudates and plant defense signaling on bacterial communities in the rhizosphere. A review Doornbos, Rogier F.; van Loon, Leendert Cornelis; Bakker, Peter A. H. M. Agronomy for Sustainable Development, Vol. 32, Issue 1 https://doi.org/10.1007/s13593-011-0028-y	journal	April 2011
Towards long-read metagenomics: complete assembly of three novel genomes from bacteria dependent on a diazotrophic cyanobacterium in a freshwater lake co-culture Driscoll, Connor B.; Otten, Timothy G.; Brown, Nathan M. Standards in Genomic Sciences, Vol. 12, Issue 1 https://doi.org/10.1186/s40793-017-0224-8	journal	January 2017
Metabolic profiling by ion mobility mass spectrometry (IMMS) Dwivedi, Prabha; Wu, Peiying; Klopsch, Steve J. Metabolomics, Vol. 4, Issue 1 https://doi.org/10.1007/s11306-007-0093-z	journal	December 2007
Real-Time DNA Sequencing from Single Polymerase Molecules Eid, John; Fehr, Adrian; Gray, Jeremy Science, Vol. 323, Issue 5910, p. 133-138 https://doi.org/10.1126/science.1162986	journal	January 2009
Peptide Separations by On-Line MudPIT Compared to Isoelectric Focusing in an Off-Gel Format: Application to a Membrane-Enriched Fraction from C2C12 Mouse Skeletal Muscle Cells Elschenbroich, Sarah; Ignatchenko, Vladimir; Sharma, Parveen Journal of Proteome Research, Vol. 8, Issue 10 https://doi.org/10.1021/pr900318k	journal	August 2009
Metabolomics – the link between genotypes and phenotypes Fiehn, Oliver Plant Molecular Biology, Vol. 48, Issue 1/2, p. 155-171 https://doi.org/10.1023/A:1013713905833	journal	January 2002
Applications of Fourier Transform Ion Cyclotron Resonance (FT-ICR) and Orbitrap Based High Resolution Mass Spectrometry in Metabolomics and Lipidomics Ghaste, Manoj; Mistrik, Robert; Shulaev, Vladimir International Journal of Molecular Sciences, Vol. 17, Issue 6 https://doi.org/10.3390/ijms17060816	journal	May 2016
Design of experiments: an efficient strategy to identify factors influencing extraction and derivatization of Arabidopsis thaliana samples in metabolomic studies with gas chromatography/mass spectrometry Gullberg, Jonas; Jonsson, Pär; Nordström, Anders Analytical Biochemistry, Vol. 331, Issue 2 https://doi.org/10.1016/j.ab.2004.04.037	journal	August 2004
Molecular biological access to the chemistry of unknown soil microbes: a new frontier for natural products Handelsman, Jo; Rondon, Michelle R.; Brady, Sean F. Chemistry & Biology, Vol. 5, Issue 10 https://doi.org/10.1016/S1074-5521(98)90108-9	journal	October 1998
Quorum Sensing of Bacteria and Trans-Kingdom Interactions of N-Acyl Homoserine Lactones with Eukaryotes Hartmann, Anton; Schikora, Adam Journal of Chemical Ecology, Vol. 38, Issue 6 https://doi.org/10.1007/s10886-012-0141-7	journal	May 2012
Lorenz Hiltner, a pioneer in rhizosphere microbial ecology and soil bacteriology research Hartmann, Anton; Rothballer, Michael; Schmid, Michael Plant and Soil, Vol. 312, Issue 1-2 https://doi.org/10.1007/s11104-007-9514-z	journal	December 2007
Integrated multi-omics of the human gut microbiome in a case study of familial type 1 diabetes Heintz-Buschart, Anna; May, Patrick; Laczny, Cédric C. Nature Microbiology, Vol. 2, Issue 1 https://doi.org/10.1038/nmicrobiol.2016.180	journal	October 2016
Tackling soil diversity with the assembly of large, complex metagenomes Howe, Adina Chuang; Jansson, Janet K.; Malfatti, Stephanie A. Proceedings of the National Academy of Sciences, Vol. 111, Issue 13 https://doi.org/10.1073/pnas.1402564111	journal	March 2014
Multi-omics of permafrost, active layer and thermokarst bog soil microbiomes Hultman, Jenni; Waldrop, Mark P.; Mackelprang, Rachel Nature, Vol. 521, Issue 7551 https://doi.org/10.1038/nature14238	journal	March 2015
Development of an Ion Mobility Spectrometry-Orbitrap Mass Spectrometer Platform Ibrahim, Yehia M.; Garimella, Sandilya V. B.; Prost, Spencer A. Analytical Chemistry, Vol. 88, Issue 24 https://doi.org/10.1021/acs.analchem.6b03027	journal	December 2016
The Oxford Nanopore MinION: delivery of nanopore sequencing to the genomics community Jain, Miten; Olsen, Hugh E.; Paten, Benedict Genome Biology, Vol. 17, Issue 1 https://doi.org/10.1186/s13059-016-1103-0	journal	November 2016
Protein-based stable isotope probing Jehmlich, Nico; Schmidt, Frank; Taubert, Martin Nature Protocols, Vol. 5, Issue 12 https://doi.org/10.1038/nprot.2010.166	journal	November 2010
Metatranscriptomic analysis of diverse microbial communities reveals core metabolic pathways and microbiome-specific functionality Jiang, Yue; Xiong, Xuejian; Danska, Jayne Microbiome, Vol. 4, Issue 1 https://doi.org/10.1186/s40168-015-0146-x	journal	January 2016
Metabolomic analysis of soil communities can be used for pollution assessment: Metabolomics of soil communities Jones, Oliver A. H.; Sdepanian, Stephanie; Lofts, Steven Environmental Toxicology and Chemistry, Vol. 33, Issue 1 https://doi.org/10.1002/etc.2418	journal	November 2013
Simultaneous Extraction of Viral and Bacterial Nucleic Acids for Molecular Diagnostic Applications Kajiura, Lauren N.; Stewart, Scott D.; Dresios, John Journal of Biomolecular Techniques : JBT, Vol. 26, Issue 4 https://doi.org/10.7171/jbt.15-2604-002	journal	December 2015
Metaproteogenomic analysis of microbial communities in the phyllosphere and rhizosphere of rice Knief, Claudia; Delmotte, Nathanaël; Chaffron, Samuel The ISME Journal, Vol. 6, Issue 7 https://doi.org/10.1038/ismej.2011.192	journal	December 2011
Microbial Metabolomics with Gas Chromatography/Mass Spectrometry Koek, Maud M.; Muilwijk, Bas; van der Werf, Mariët J. Analytical Chemistry, Vol. 78, Issue 4 https://doi.org/10.1021/ac051683+	journal	January 2006
One chromosome, one contig: complete microbial genomes from long-read sequencing and assembly Koren, Sergey; Phillippy, Adam M. Current Opinion in Microbiology, Vol. 23 https://doi.org/10.1016/j.mib.2014.11.014	journal	February 2015
Synthetic long-read sequencing reveals intraspecies diversity in the human microbiome Kuleshov, Volodymyr; Jiang, Chao; Zhou, Wenyu Nature Biotechnology, Vol. 34, Issue 1 https://doi.org/10.1038/nbt.3416	journal	January 2016
A Bioinformatician's Guide to Metagenomics Kunin, V.; Copeland, A.; Lapidus, A. Microbiology and Molecular Biology Reviews, Vol. 72, Issue 4 https://doi.org/10.1128/MMBR.00009-08	journal	December 2008
Zero-Mode Waveguides for Single-Molecule Analysis at High Concentrations Levene, M. J. Science, Vol. 299, Issue 5607 https://doi.org/10.1126/science.1079700	journal	January 2003
Method for Determining Molar Concentrations of Metabolites in Complex Solutions from Two-Dimensional ¹ H− ¹³ C NMR Spectra Lewis, Ian A.; Schommer, Seth C.; Hodis, Brendan Analytical Chemistry, Vol. 79, Issue 24 https://doi.org/10.1021/ac071583z	journal	December 2007
Metatranscriptomic Study of Common and Host-Specific Patterns of Gene Expression between Pines and Their Symbiotic Ectomycorrhizal Fungi in the Genus Suillus Liao, Hui-Ling; Chen, Yuan; Vilgalys, Rytas PLOS Genetics, Vol. 12, Issue 10 https://doi.org/10.1371/journal.pgen.1006348	journal	October 2016
Collisional effects on the charge distribution of ions from large molecules, formed by electrospray-ionization mass spectrometry Loo, Joseph A.; Udseth, Harold R.; Smith, Richard D. Rapid Communications in Mass Spectrometry, Vol. 2, Issue 10 https://doi.org/10.1002/rcm.1290021006	journal	December 1988
Analytical strategies for LC–MS-based targeted metabolomics Lu, Wenyun; Bennett, Bryson D.; Rabinowitz, Joshua D. Journal of Chromatography B, Vol. 871, Issue 2 https://doi.org/10.1016/j.jchromb.2008.04.031	journal	August 2008
Defining the core Arabidopsis thaliana root microbiome Lundberg, Derek S.; Lebeis, Sarah L.; Paredes, Sur Herrera Nature, Vol. 488, Issue 7409 https://doi.org/10.1038/nature11237	journal	August 2012
Deciphering the Rhizosphere Microbiome for Disease-Suppressive Bacteria Mendes, R.; Kruijt, M.; de Bruijn, I. Science, Vol. 332, Issue 6033 https://doi.org/10.1126/science.1203980	journal	May 2011
Taxonomical and functional microbial community selection in soybean rhizosphere Mendes, Lucas W.; Kuramae, Eiko E.; Navarrete, Acácio A. The ISME Journal, Vol. 8, Issue 8 https://doi.org/10.1038/ismej.2014.17	journal	February 2014
Nanoelectromechanics of Methylated DNA in a Synthetic Nanopore Mirsaidov, U.; Timp, W.; Zou, X. Biophysical Journal, Vol. 96, Issue 4 https://doi.org/10.1016/j.bpj.2008.12.3760	journal	February 2009
Amino acids in the rhizosphere: From plants to microbes Moe, Luke A. American Journal of Botany, Vol. 100, Issue 9 https://doi.org/10.3732/ajb.1300033	journal	September 2013
The methylomes of six bacteria Murray, Iain A.; Clark, Tyson A.; Morgan, Richard D. Nucleic Acids Research, Vol. 40, Issue 22 https://doi.org/10.1093/nar/gks891	journal	October 2012
MPLEx: a Robust and Universal Protocol for Single-Sample Integrative Proteomic, Metabolomic, and Lipidomic Analyses Nakayasu, Ernesto S.; Nicora, Carrie D.; Sims, Amy C. mSystems, Vol. 1, Issue 3 https://doi.org/10.1128/mSystems.00043-16	journal	May 2016
A survey of computational methods and error rate estimation procedures for peptide and protein identification in shotgun proteomics Nesvizhskii, Alexey I. Journal of Proteomics, Vol. 73, Issue 11 https://doi.org/10.1016/j.jprot.2010.08.009	journal	October 2010
Changes in rhizosphere bacterial gene expression following glyphosate treatment Newman, Molli M.; Lorenz, Nicola; Hoilett, Nigel Science of The Total Environment, Vol. 553 https://doi.org/10.1016/j.scitotenv.2016.02.078	journal	May 2016
Metagenomics: Tools and Insights for Analyzing Next-Generation Sequencing Data Derived from Biodiversity Studies Oulas, Anastasis; Pavloudi, Christina; Polymenakou, Paraskevi Bioinformatics and Biology Insights, Vol. 9 https://doi.org/10.4137/BBI.S12462	journal	January 2015
Proteomics to study genes and genomes Pandey, Akhilesh; Mann, Matthias Nature, Vol. 405, Issue 6788 https://doi.org/10.1038/35015709	journal	June 2000
Ecological metabolomics Peñuelas, Josep; Sardans, Jordi Chemistry and Ecology, Vol. 25, Issue 4 https://doi.org/10.1080/02757540903062517	journal	August 2009
Going back to the roots: the microbial ecology of the rhizosphere Philippot, Laurent; Raaijmakers, Jos M.; Lemanceau, Philippe Nature Reviews Microbiology, Vol. 11, Issue 11 https://doi.org/10.1038/nrmicro3109	journal	September 2013
Storage of environmental samples for guaranteeing nucleic acid yields for molecular microbiological studies Rissanen, Antti Juhani; Kurhela, Emilia; Aho, Tommi Applied Microbiology and Biotechnology, Vol. 88, Issue 4 https://doi.org/10.1007/s00253-010-2838-2	journal	August 2010
Strong relationship between elemental stoichiometry and metabolome in plants Rivas-Ubach, A.; Sardans, J.; Perez-Trujillo, M. Proceedings of the National Academy of Sciences, Vol. 109, Issue 11 https://doi.org/10.1073/pnas.1116092109	journal	February 2012
Ecometabolomics: optimized NMR-based method Rivas-Ubach, Albert; Pérez-Trujillo, Miriam; Sardans, Jordi Methods in Ecology and Evolution, Vol. 4, Issue 5 https://doi.org/10.1111/2041-210X.12028	journal	February 2013
Bacterial volatiles promote growth in Arabidopsis Ryu, C. -M.; Farag, M. A.; Hu, C. -H. Proceedings of the National Academy of Sciences, Vol. 100, Issue 8 https://doi.org/10.1073/pnas.0730845100	journal	April 2003
Ecological metabolomics: overview of current developments and future challenges Sardans, Jordi; Peñuelas, Josep; Rivas-Ubach, Albert Chemoecology, Vol. 21, Issue 4 https://doi.org/10.1007/s00049-011-0083-5	journal	June 2011
Who is who in litter decomposition? Metaproteomics reveals major microbial players and their biogeochemical functions Schneider, Thomas; Keiblinger, Katharina M.; Schmid, Emanuel The ISME Journal, Vol. 6, Issue 9 https://doi.org/10.1038/ismej.2012.11	journal	March 2012
Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi Schoch, C. L.; Seifert, K. A.; Huhndorf, S. Proceedings of the National Academy of Sciences, Vol. 109, Issue 16 https://doi.org/10.1073/pnas.1117018109	journal	March 2012
Characterization of Growing Microorganisms in Soil by Stable Isotope Probing with H218O Schwartz, E. Applied and Environmental Microbiology, Vol. 73, Issue 8 https://doi.org/10.1128/AEM.02021-06	journal	February 2007
Accurate, multi-kb reads resolve complex populations and detect rare microorganisms Sharon, Itai; Kertesz, Michael; Hug, Laura A. Genome Research, Vol. 25, Issue 4 https://doi.org/10.1101/gr.183012.114	journal	February 2015
Metabolomics for plant stress response Shulaev, Vladimir; Cortes, Diego; Miller, Gad Physiologia Plantarum, Vol. 132, Issue 2 https://doi.org/10.1111/j.1399-3054.2007.01025.x	journal	January 2008
High-resolution phylogenetic microbial community profiling Singer, Esther; Bushnell, Brian; Coleman-Derr, Devin The ISME Journal, Vol. 10, Issue 8 https://doi.org/10.1038/ismej.2015.249	journal	February 2016
Proposed minimum reporting standards for chemical analysis: Chemical Analysis Working Group (CAWG) Metabolomics Standards Initiative (MSI) Sumner, Lloyd W.; Amberg, Alexander; Barrett, Dave Metabolomics, Vol. 3, Issue 3 https://doi.org/10.1007/s11306-007-0082-2	journal	September 2007
Challenges and developments in protein identification using mass spectrometry Szabo, Zoltan; Janaky, Tamas TrAC Trends in Analytical Chemistry, Vol. 69 https://doi.org/10.1016/j.trac.2015.03.007	journal	June 2015
An accelerated workflow for untargeted metabolomics using the METLIN database Tautenhahn, Ralf; Cho, Kevin; Uritboonthai, Winnie Nature Biotechnology, Vol. 30, Issue 9 https://doi.org/10.1038/nbt.2348	journal	September 2012
Investigating dissolved organic matter decomposition in northern peatlands using complimentary analytical techniques Tfaily, Malak M.; Hamdan, Rasha; Corbett, Jane E. Geochimica et Cosmochimica Acta, Vol. 112 https://doi.org/10.1016/j.gca.2013.03.002	journal	July 2013
Metagenomics - a guide from sampling to data analysis Thomas, Torsten; Gilbert, Jack; Meyer, Folker Microbial Informatics and Experimentation, Vol. 2, Issue 1 https://doi.org/10.1186/2042-5783-2-3	journal	February 2012
Tandem Mass Tags: A Novel Quantification Strategy for Comparative Analysis of Complex Protein Mixtures by MS/MS Thompson, Andrew; Schäfer, Jürgen; Kuhn, Karsten Analytical Chemistry, Vol. 75, Issue 8 https://doi.org/10.1021/ac0262560	journal	April 2003
Comparative metatranscriptomics reveals kingdom level changes in the rhizosphere microbiome of plants Turner, Thomas R.; Ramakrishnan, Karunakaran; Walshaw, John The ISME Journal, Vol. 7, Issue 12 https://doi.org/10.1038/ismej.2013.119	journal	July 2013
Community structure and metabolism through reconstruction of microbial genomes from the environment Tyson, Gene W.; Chapman, Jarrod; Hugenholtz, Philip Nature, Vol. 428, Issue 6978 https://doi.org/10.1038/nature02340	journal	February 2004
Metabolomics in the Rhizosphere: Tapping into Belowground Chemical Communication van Dam, Nicole M.; Bouwmeester, Harro J. Trends in Plant Science, Vol. 21, Issue 3 https://doi.org/10.1016/j.tplants.2016.01.008	journal	March 2016
Mass spectrometry based environmental metabolomics: a primer and review Viant, Mark R.; Sommer, Ulf Metabolomics, Vol. 9, Issue S1 https://doi.org/10.1007/s11306-012-0412-x	journal	March 2012
Unambiguous metabolite identification in high-throughput metabolomics by hybrid 1D ¹ H NMR/ESI MS ¹ approach : Hybrid 1D Walker, Lawrence R.; Hoyt, David W.; Walker, S. Michael Magnetic Resonance in Chemistry, Vol. 54, Issue 12 https://doi.org/10.1002/mrc.4503	journal	September 2016
Characterization of Metaproteomics in Crop Rhizospheric Soil Wang, Hai-Bin; Zhang, Zhi-Xing; Li, Hui Journal of Proteome Research, Vol. 10, Issue 3 https://doi.org/10.1021/pr100981r	journal	March 2011
Targeted Profiling: Quantitative Analysis of ¹ H NMR Metabolomics Data Weljie, Aalim M.; Newton, Jack; Mercier, Pascal Analytical Chemistry, Vol. 78, Issue 13 https://doi.org/10.1021/ac060209g	journal	July 2006
Flavonoids: Their Structure, Biosynthesis and Role in the Rhizosphere, Including Allelopathy Weston, Leslie A.; Mathesius, Ulrike Journal of Chemical Ecology, Vol. 39, Issue 2 https://doi.org/10.1007/s10886-013-0248-5	journal	February 2013
From data to knowledge: The future of multi-omics data analysis for the rhizosphere Allen White, Richard; Borkum, Mark I.; Rivas-Ubach, Albert Rhizosphere, Vol. 3 https://doi.org/10.1016/j.rhisph.2017.05.001	journal	June 2017
Moleculo Long-Read Sequencing Facilitates Assembly and Genomic Binning from Complex Soil Metagenomes White, Richard Allen; Bottos, Eric M.; Roy Chowdhury, Taniya mSystems, Vol. 1, Issue 3 https://doi.org/10.1128/mSystems.00045-16	journal	June 2016
The past, present and future of microbiome analyses White, Richard Allen; Callister, Stephen J.; Moore, Ronald J. Nature Protocols, Vol. 11, Issue 11 https://doi.org/10.1038/nprot.2016.148	journal	September 2016
Protein labeling by iTRAQ: A new tool for quantitative mass spectrometry in proteome research Wiese, Sebastian; Reidegeld, Kai A.; Meyer, Helmut E. PROTEOMICS, Vol. 7, Issue 3 https://doi.org/10.1002/pmic.200600422	journal	February 2007
A decade of metaproteomics: Where we stand and what the future holds: PROTEOMICS Wilmes, Paul; Heintz-Buschart, Anna; Bond, Philip L. PROTEOMICS, Vol. 15, Issue 20 https://doi.org/10.1002/pmic.201500183	journal	September 2015
High-pH reversed-phase chromatography with fraction concatenation for 2D proteomic analysis Yang, Feng; Shen, Yufeng; Camp, David G. Expert Review of Proteomics, Vol. 9, Issue 2 https://doi.org/10.1586/epr.12.15	journal	April 2012
Soil metaproteomics reveals an inter-kingdom stress response to the presence of black truffles Zampieri, Elisa; Chiapello, Marco; Daghino, Stefania Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep25773	journal	May 2016

Cited By (3)

Atmo-ecometabolomics: a novel atmospheric particle chemical characterization methodology for ecological research Rivas-Ubach, Albert; Liu, Yina; Steiner, Allison L. Environmental Monitoring and Assessment, Vol. 191, Issue 2 https://doi.org/10.1007/s10661-019-7205-x	journal	January 2019
Recent Advances in Targeted and Untargeted Metabolomics by NMR and MS/NMR Methods Bingol, Kerem High-Throughput, Vol. 7, Issue 2 https://doi.org/10.3390/ht7020009	journal	April 2018
Microbial Group Dynamics in Plant Rhizospheres and Their Implications on Nutrient Cycling Garcia, Joshua; Kao-Kniffin, Jenny Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.01516	journal	July 2018

Similar Records

The state of rhizospheric science in the era of multi-omics: A practical guide to omics technologies

Journal Article · Thu Jun 01 00:00:00 EDT 2017 · Rhizosphere · OSTI ID:1355770

White, Richard Allen; Rivas-Ubach, Albert; Borkum, Mark I.; +9 more

From data to knowledge: The future of multi-omics data analysis for the rhizosphere

Journal Article · Thu May 04 00:00:00 EDT 2017 · Rhizosphere · OSTI ID:1355770

Allen White III, Richard; Borkum, Mark I.; Rivas-Ubach, Albert; +5 more

Rhizosphere engineering: Enhancing sustainable plant ecosystem productivity

Journal Article · Thu Jun 01 00:00:00 EDT 2017 · Rhizosphere · OSTI ID:1355770

Ahkami, Amir H.; Allen White, III, Richard; Handakumbura, Pubudu P.; +1 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
60 APPLIED LIFE SCIENCES
rhizosphere
multi-omics
next-generation sequencing
metagenomics
metatranscriptomics
metabolomics
metaproteomics

Title: The state of rhizospheric science in the era of multi-omics: A practical guide to omics technologies

Citation Formats

References (95)

Cited By (3)

Similar Records

Related Subjects