Evaluation of Strategies to Separate Root-Associated Microbial Communities: A Crucial Choice in Rhizobiome Research
Plants shape distinct, species-specific microbiomes in their rhizospheres. A main premise for evaluating microbial communities associated with root-soil compartments is their successful separation into the rhizosphere (soil-root interface), the rhizoplane (root surface), and the endosphere (inside r...
Saved in:
| Published in | Frontiers in microbiology Vol. 7; p. 773 |
|---|---|
| Main Authors | , , , , |
| Format | Journal Article |
| Language | English |
| Published |
Switzerland
Frontiers Media S.A
24.05.2016
|
| Subjects | |
| Online Access | Get full text |
Cover
Loading…
| Abstract | Plants shape distinct, species-specific microbiomes in their rhizospheres. A main premise for evaluating microbial communities associated with root-soil compartments is their successful separation into the rhizosphere (soil-root interface), the rhizoplane (root surface), and the endosphere (inside roots). We evaluated different approaches (washing, sonication, and bleaching) regarding their efficiency to separate microbial cells associated with different root compartments of soil-grown rice using fluorescence microscopy and community fingerprinting of 16S rRNA genes. Vigorous washing detached 45% of the rhizoplane population compared to untreated roots. Additional sonication reduced rhizoplane-attached microorganisms by up to 78% but caused various degrees of root tissue destruction at all sonication intensities tested. Treatment with sodium hypochlorite almost completely (98%) removed rhizoplane-associated microbial cells. Community fingerprinting revealed that microbial communities obtained from untreated, washed, and sonicated roots were not statistically distinguishable. Hypochlorite-treated roots harbored communities significantly different from all other samples, likely representing true endospheric populations. Applying these procedures to other root samples (bean and clover) revealed that treatment efficiencies were strongly affected by root morphological parameters such as root hair density and rigidity of epidermis. Our findings suggest that a careful evaluation of separation strategies prior to molecular community analysis is indispensable, especially when endophytes are the subject of interest. |
|---|---|
| AbstractList | Plants shape distinct, species-specific microbiomes in their rhizospheres. A main premise for evaluating microbial communities associated with root-soil compartments is their successful separation into the rhizosphere (soil-root interface), the rhizoplane (root surface), and the endosphere (inside roots). We evaluated different approaches (washing, sonication, bleaching) regarding their efficiency to separate microbial cells associated with different root compartments of soil-grown rice using fluorescence microscopy and community fingerprinting of 16S rRNA genes. Vigorous washing detached 45% of the rhizoplane population compared to untreated roots. Additional sonication reduced rhizoplane-attached microorganisms by up to 78% but caused various degrees of root tissue destruction at all sonication intensities tested. Treatment with sodium hypochlorite almost completely (98%) removed rhizoplane-associated microbial cells. Community fingerprinting revealed that microbial communities obtained from untreated, washed, and sonicated roots were not statistically distinguishable. Hypochlorite-treated roots harbored communities significantly different from all other samples, likely representing true endospheric populations. Applying these procedures to other root samples (bean, clover) revealed that treatment efficiencies were strongly affected by root morphological parameters such as root hair density and rigidity of epidermis. Our findings suggest that a careful evaluation of separation strategies prior to molecular community analysis is indispensable, especially when endophytes are the subject of interest. Plants shape distinct, species-specific microbiomes in their rhizospheres. A main premise for evaluating microbial communities associated with root-soil compartments is their successful separation into the rhizosphere (soil-root interface), the rhizoplane (root surface), and the endosphere (inside roots). We evaluated different approaches (washing, sonication, and bleaching) regarding their efficiency to separate microbial cells associated with different root compartments of soil-grown rice using fluorescence microscopy and community fingerprinting of 16S rRNA genes. Vigorous washing detached 45% of the rhizoplane population compared to untreated roots. Additional sonication reduced rhizoplane-attached microorganisms by up to 78% but caused various degrees of root tissue destruction at all sonication intensities tested. Treatment with sodium hypochlorite almost completely (98%) removed rhizoplane-associated microbial cells. Community fingerprinting revealed that microbial communities obtained from untreated, washed, and sonicated roots were not statistically distinguishable. Hypochlorite-treated roots harbored communities significantly different from all other samples, likely representing true endospheric populations. Applying these procedures to other root samples (bean and clover) revealed that treatment efficiencies were strongly affected by root morphological parameters such as root hair density and rigidity of epidermis. Our findings suggest that a careful evaluation of separation strategies prior to molecular community analysis is indispensable, especially when endophytes are the subject of interest. |
| Author | Eickhorst, Thilo Friedrich, Michael W. Richter-Heitmann, Tim Knauth, Stefan Schmidt, Hannes |
| AuthorAffiliation | 1 Microbial Ecophysiology, Faculty of Biology/Chemistry, University of Bremen Bremen, Germany 2 International Max Planck Research School for Marine Microbiology, Max Planck Institute for Marine Microbiology Bremen, Germany 3 Soil Microbial Ecology, Faculty of Biology/Chemistry, University of Bremen Bremen, Germany |
| AuthorAffiliation_xml | – name: 1 Microbial Ecophysiology, Faculty of Biology/Chemistry, University of Bremen Bremen, Germany – name: 2 International Max Planck Research School for Marine Microbiology, Max Planck Institute for Marine Microbiology Bremen, Germany – name: 3 Soil Microbial Ecology, Faculty of Biology/Chemistry, University of Bremen Bremen, Germany |
| Author_xml | – sequence: 1 givenname: Tim surname: Richter-Heitmann fullname: Richter-Heitmann, Tim – sequence: 2 givenname: Thilo surname: Eickhorst fullname: Eickhorst, Thilo – sequence: 3 givenname: Stefan surname: Knauth fullname: Knauth, Stefan – sequence: 4 givenname: Michael W. surname: Friedrich fullname: Friedrich, Michael W. – sequence: 5 givenname: Hannes surname: Schmidt fullname: Schmidt, Hannes |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/27252690$$D View this record in MEDLINE/PubMed |
| BookMark | eNp1Uk1r3DAUFCWhSdPceyo69uKNrC_bPRSWJW0CKYEkhd6E_CztKtjWVpID7a-v1puUpBAdJL2nmXmgmXfoYPSjQehDSRaM1c2ZHRy0C0pKuSCkqtgbdFxKyQtG6M-DZ_cjdBrjPcmLE5r3t-iIVlRQ2ZBjFM8fdD_p5PyIvcW3Kehk1s5EnDy-NVu9q_GN96lYxujB5bLD3x0E3zrd45Ufhml0KTM-4yVehQnm9sY7MNiN-Gbj_mSoH7KKiUYH2LxHh1b30Zw-nifox9fzu9VFcXX97XK1vCqAS5qKutKcC6ob1jJiBWWkqknZWkY7SkFyXUMjGZGSgG25JbxkrdSZwTiQFkp2gi73up3X92ob3KDDb-W1U3PDh7XSITnojaLMGsO0EDXUXGjZdK0QoqMdQG2ttFnry15rO7WD6cCM-af6F6IvX0a3UWv_oHhdVYLwLPDpUSD4X5OJSQ0ugul7PRo_RVVWDWvKbCbL0I_PZ_0b8uRaBsg9ILsQYzBWgUuzh3m061VJ1C4hak6I2iVEzQnJRPIf8Un7VcpfK5K_-w |
| CitedBy_id | crossref_primary_10_3389_fmicb_2017_02667 crossref_primary_10_1016_j_funeco_2020_100993 crossref_primary_10_1007_s11274_019_2761_3 crossref_primary_10_3389_fmicb_2020_01677 crossref_primary_10_1186_s40168_018_0413_8 crossref_primary_10_1111_mec_17652 crossref_primary_10_3389_fenvs_2018_00061 crossref_primary_10_3389_fmicb_2023_1163488 crossref_primary_10_1128_msystems_00367_22 crossref_primary_10_1007_s00128_018_2426_1 crossref_primary_10_3354_ame01937 crossref_primary_10_3389_fmicb_2019_02694 crossref_primary_10_1094_PBIOMES_08_20_0058_R crossref_primary_10_1186_s40793_022_00445_x crossref_primary_10_3389_fpls_2017_00284 crossref_primary_10_1007_s10530_021_02692_4 crossref_primary_10_3389_fpls_2020_00006 crossref_primary_10_1128_msystems_00651_21 crossref_primary_10_1094_PBIOMES_03_19_0016_R crossref_primary_10_1128_AEM_01765_18 crossref_primary_10_1094_PBIOMES_04_22_0021_FI crossref_primary_10_1016_j_fcr_2024_109641 crossref_primary_10_2903_sp_efsa_2024_EN_8602 crossref_primary_10_1016_j_soilbio_2019_03_007 crossref_primary_10_1080_07060661_2023_2290041 crossref_primary_10_3389_fmicb_2020_00034 crossref_primary_10_1016_j_jhazmat_2020_123253 crossref_primary_10_1016_j_scitotenv_2019_05_220 crossref_primary_10_1186_s12866_021_02393_x crossref_primary_10_3389_ffgc_2024_1336037 crossref_primary_10_1016_j_soilbio_2021_108208 crossref_primary_10_3389_frmbi_2024_1335791 crossref_primary_10_3389_fpls_2023_1136418 crossref_primary_10_1007_s11104_024_06512_1 crossref_primary_10_1038_s41467_023_37188_3 crossref_primary_10_1094_PBIOMES_3_4 crossref_primary_10_1094_PBIOMES_5_2 crossref_primary_10_1038_s41396_021_01094_7 crossref_primary_10_1094_PBIOMES_06_23_0049_R crossref_primary_10_7717_peerj_6162 crossref_primary_10_1007_s00374_020_01528_y crossref_primary_10_1007_s00248_019_01357_z crossref_primary_10_3389_fmicb_2021_665999 crossref_primary_10_3389_fpls_2019_01313 crossref_primary_10_5194_soil_9_609_2023 crossref_primary_10_1016_j_envpol_2024_123909 |
| Cites_doi | 10.1073/pnas.1302837110 10.1111/1462-2920.12452 10.1038/ismej.2011.192 10.1038/nature11336 10.3389/fpls.2014.00216 10.1111/nph.13312 10.3389/fmicb.2014.00148 10.1126/science.aaa8764 10.1073/pnas.1414592112 10.3354/ame027029 10.1186/s12866-014-0332-1 10.1023/B:PLSO.0000035569.80747.c5 10.1007/s13213-012-0491-y 10.1890/13-0133.1 10.1007/s00726-003-0016-x 10.1073/pnas.1321597111 10.1111/1462-2920.12228 10.1128/AEM.67.12.5849-5854.2001 10.1038/nature11237 10.1890/ES13-00136.1 10.1016/j.mimet.2008.04.011 10.1038/ismej.2013.196 10.1007/s00248-012-0082-2 10.1038/ismej.2013.119 10.1371/journal.pone.0023321 10.1007/s11104-010-0613-x 10.1128/AEM.52.3.520-526.1986 10.1111/1574-6941.12308 10.1128/AEM.05255-11 10.1111/1574-6941.12232 10.1016/j.chom.2015.01.011 10.1016/j.soilbio.2008.10.027 10.1111/j.1574-6941.2011.01092.x 10.1094/mpmi-08-11-0204 10.1016/j.tplants.2012.04.001 10.1371/journal.pone.0009788 10.1111/j.1462-2920.2005.00959.x 10.1128/AEM.71.11.6784-6792.2005 10.1016/j.soilbio.2009.11.024 10.1007/s11104-008-9885-9 10.1038/nature16192 10.1016/j.ejsobi.2008.06.007 10.1371/journal.pone.0056329 10.1007/s002480000121 10.1007/s11104-010-0637-2 10.1038/nbt.2387 10.1016/j.cropro.2007.07.010 10.1016/j.envexpbot.2009.04.010 10.1038/nrmicro3109 10.1146/annurev-phyto-082712-102342 |
| ContentType | Journal Article |
| Copyright | Copyright © 2016 Richter-Heitmann, Eickhorst, Knauth, Friedrich and Schmidt. 2016 Richter-Heitmann, Eickhorst, Knauth, Friedrich and Schmidt |
| Copyright_xml | – notice: Copyright © 2016 Richter-Heitmann, Eickhorst, Knauth, Friedrich and Schmidt. 2016 Richter-Heitmann, Eickhorst, Knauth, Friedrich and Schmidt |
| DBID | AAYXX CITATION NPM 7X8 5PM DOA |
| DOI | 10.3389/fmicb.2016.00773 |
| DatabaseName | CrossRef PubMed MEDLINE - Academic PubMed Central (Full Participant titles) DOAJ - Directory of Open Access Journals |
| DatabaseTitle | CrossRef PubMed MEDLINE - Academic |
| DatabaseTitleList | MEDLINE - Academic PubMed |
| Database_xml | – sequence: 1 dbid: DOA name: DOAJ Directory of Open Access Journals url: https://www.doaj.org/ sourceTypes: Open Website – sequence: 2 dbid: NPM name: PubMed url: https://proxy.k.utb.cz/login?url=http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed sourceTypes: Index Database |
| DeliveryMethod | fulltext_linktorsrc |
| Discipline | Biology |
| EISSN | 1664-302X |
| EndPage | 773 |
| ExternalDocumentID | oai_doaj_org_article_23fee3a558c845a69db555d2dcc8ff6f PMC4877504 27252690 10_3389_fmicb_2016_00773 |
| Genre | Journal Article |
| GroupedDBID | 53G 5VS 9T4 AAFWJ AAKDD AAYXX ACGFO ACGFS ACXDI ADBBV ADRAZ AENEX AFPKN ALMA_UNASSIGNED_HOLDINGS AOIJS BAWUL BCNDV CITATION DIK ECGQY GROUPED_DOAJ GX1 HYE IPNFZ KQ8 M48 M~E O5R O5S OK1 PGMZT RIG RNS RPM NPM 7X8 5PM |
| ID | FETCH-LOGICAL-c462t-87a4452a93b30f52307801bf32d22c64a8c9630660cfb4f0413b6a45234c0bc13 |
| IEDL.DBID | M48 |
| ISSN | 1664-302X |
| IngestDate | Wed Aug 27 01:29:14 EDT 2025 Thu Aug 21 18:41:28 EDT 2025 Fri Jul 11 00:51:25 EDT 2025 Mon Jul 21 05:38:28 EDT 2025 Tue Jul 01 03:55:00 EDT 2025 Thu Apr 24 23:02:17 EDT 2025 |
| IsDoiOpenAccess | true |
| IsOpenAccess | true |
| IsPeerReviewed | true |
| IsScholarly | true |
| Keywords | microbial abundance endosphere root microbiome rhizoplane rhizosphere sonication |
| Language | English |
| License | This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
| LinkModel | DirectLink |
| MergedId | FETCHMERGED-LOGICAL-c462t-87a4452a93b30f52307801bf32d22c64a8c9630660cfb4f0413b6a45234c0bc13 |
| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Edited by: Pierre-Emmanuel Courty, University of Fribourg, Switzerland Reviewed by: Claudia Knief, University of Bonn, Germany; Biswapriya Biswavas Misra, University of Florida, USA; Samuel Abiven, University of Zurich, Switzerland This article was submitted to Plant Biotic Interactions, a section of the journal Frontiers in Microbiology |
| OpenAccessLink | http://journals.scholarsportal.info/openUrl.xqy?doi=10.3389/fmicb.2016.00773 |
| PMID | 27252690 |
| PQID | 1793910163 |
| PQPubID | 23479 |
| PageCount | 1 |
| ParticipantIDs | doaj_primary_oai_doaj_org_article_23fee3a558c845a69db555d2dcc8ff6f pubmedcentral_primary_oai_pubmedcentral_nih_gov_4877504 proquest_miscellaneous_1793910163 pubmed_primary_27252690 crossref_citationtrail_10_3389_fmicb_2016_00773 crossref_primary_10_3389_fmicb_2016_00773 |
| ProviderPackageCode | CITATION AAYXX |
| PublicationCentury | 2000 |
| PublicationDate | 2016-05-24 |
| PublicationDateYYYYMMDD | 2016-05-24 |
| PublicationDate_xml | – month: 05 year: 2016 text: 2016-05-24 day: 24 |
| PublicationDecade | 2010 |
| PublicationPlace | Switzerland |
| PublicationPlace_xml | – name: Switzerland |
| PublicationTitle | Frontiers in microbiology |
| PublicationTitleAlternate | Front Microbiol |
| PublicationYear | 2016 |
| Publisher | Frontiers Media S.A |
| Publisher_xml | – name: Frontiers Media S.A |
| References | Knief (B28) 2014; 5 Reinhold (B44) 1986; 52 van Dorst (B52) 2014; 89 R Development Core Team (B43) 2015 Lebeis (B31) 2015; 349 Buesing (B8) 2002; 27 Bai (B2) 2015; 528 Gottel (B19) 2011; 77 Hinsinger (B23) 2009; 321 Puente (B42) 2009; 66 Berg (B6) 2014; 5 Chaparro (B12) 2014; 8 Knief (B29) 2012; 6 Philippot (B40) 2013; 11 Becerra-Castro (B4) 2011; 340 McNear (B34) 2013; 4 Ofek (B36) 2014; 16 Vandenkoornhuyse (B53) 2015; 206 Wieland (B54) 2001; 67 Schlaeppi (B46) 2014; 111 Donn (B17) 2015; 17 Lane (B30) 1991 Oh (B37) 2012; 64 Sokol (B50) 2013; 4 Herberich (B22) 2010; 5 Reinhold-Hurek (B45) 2015; 53 da Silva (B16) 2014; 14 Abdo (B1) 2006; 8 Berendsen (B5) 2012; 17 Kaiser (B27) 2001; 42 Culman (B15) 2008; 75 Xu (B55) 2009; 41 Chave (B13) 2008; 27 Marschner (B33) 2004; 261 Bulgarelli (B9) 2015; 17 Sessitsch (B49) 2012; 25 Hirsch (B24) 2012; 30 Lundberg (B32) 2012; 488 Inceoglu (B25) 2011; 6 Prince (B41) 1992; 12 Edwards (B18) 2015; 112 Schmidt (B48) 2011; 341 Barillot (B3) 2013; 63 Jha (B26) 2009; 45 Peiffer (B39) 2013; 110 Schmidt (B47) 2014; 87 Hawkins (B21) 2003; 25 Chao (B11) 2013; 84 Hardoim (B20) 2011; 77 Nunan (B35) 2005; 71 Oksanen (B38) 2015 Bodenhausen (B7) 2013; 8 Turner (B51) 2013; 7 Compant (B14) 2010; 42 Bulgarelli (B10) 2012; 488 25732064 - Cell Host Microbe. 2015 Mar 11;17(3):392-403 24379374 - Proc Natl Acad Sci U S A. 2014 Jan 14;111(2):585-92 24628845 - Environ Microbiol. 2015 Mar;17(3):610-21 14661089 - Amino Acids. 2003 Dec;25(3-4):259-74 26243728 - Annu Rev Phytopathol. 2015;53:403-24 21764952 - Appl Environ Microbiol. 2011 Sep;77(17):5934-44 21886785 - PLoS One. 2011;6(8):e23321 16347149 - Appl Environ Microbiol. 1986 Sep;52(3):520-6 22564542 - Trends Plant Sci. 2012 Aug;17(8):478-86 20360960 - PLoS One. 2010 Mar 29;5(3):e9788 23864127 - ISME J. 2013 Dec;7(12):2248-58 24580036 - FEMS Microbiol Ecol. 2014 Aug;89(2):316-30 24118011 - FEMS Microbiol Ecol. 2014 Feb;87(2):390-402 24196324 - ISME J. 2014 Apr;8(4):790-803 21426364 - FEMS Microbiol Ecol. 2011 Jul;77(1):154-64 25655016 - New Phytol. 2015 Jun;206(4):1196-206 26633631 - Nature. 2015 Dec 17;528(7582):364-9 23457551 - PLoS One. 2013;8(2):e56329 22859207 - Nature. 2012 Aug 2;488(7409):91-5 22767122 - Microb Ecol. 2012 Nov;64(4):1018-27 12024277 - Microb Ecol. 2001 Aug;42(2):136-149 24056930 - Nat Rev Microbiol. 2013 Nov;11(11):789-99 25540019 - BMC Microbiol. 2014 Dec 24;14:332 11722945 - Appl Environ Microbiol. 2001 Dec;67(12):5849-54 21970692 - Mol Plant Microbe Interact. 2012 Jan;25(1):28-36 23051815 - Nat Biotechnol. 2012 Oct;30(10):961-2 22189496 - ISME J. 2012 Jul;6(7):1378-90 25605935 - Proc Natl Acad Sci U S A. 2015 Feb 24;112(8):E911-20 23576752 - Proc Natl Acad Sci U S A. 2013 Apr 16;110(16):6548-53 24926286 - Front Microbiol. 2014 Jun 04;5:148 1571142 - Biotechniques. 1992 Mar;12(3):358-60 26184915 - Science. 2015 Aug 21;349(6250):860-4 24904612 - Front Plant Sci. 2014 May 21;5:216 22859206 - Nature. 2012 Aug 2;488(7409):86-90 16623749 - Environ Microbiol. 2006 May;8(5):929-38 23962203 - Environ Microbiol. 2014 Jul;16(7):2157-67 16269710 - Appl Environ Microbiol. 2005 Nov;71(11):6784-92 18584903 - J Microbiol Methods. 2008 Sep;75(1):55-63 |
| References_xml | – start-page: 115 year: 1991 ident: B30 article-title: “16S/23S rRNA sequencing,” in publication-title: Nucleic Acid Techniques in Bacterial Systematics – volume: 110 start-page: 6548 year: 2013 ident: B39 article-title: Diversity and heritability of the maize rhizosphere microbiome under field conditions. publication-title: Proc. Natl. Acad. Sci. U.S.A. doi: 10.1073/pnas.1302837110 – volume: 17 start-page: 610 year: 2015 ident: B17 article-title: Evolution of bacterial communities in the wheat crop rhizosphere. publication-title: Environ. Microbiol. doi: 10.1111/1462-2920.12452 – volume: 6 start-page: 1378 year: 2012 ident: B29 article-title: Metaproteogenomic analysis of microbial communities in the phyllosphere and rhizosphere of rice. publication-title: ISME J. doi: 10.1038/ismej.2011.192 – volume: 12 start-page: 358 year: 1992 ident: B41 article-title: PCR: how to kill unwanted DNA. publication-title: Biotechniques – volume: 488 start-page: 91 year: 2012 ident: B10 article-title: Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. publication-title: Nature doi: 10.1038/nature11336 – volume: 5 issue: 216 year: 2014 ident: B28 article-title: Analysis of plant microbe interactions in the era of next generation sequencing technologies. publication-title: Front. Plant Sci. doi: 10.3389/fpls.2014.00216 – volume: 206 start-page: 1196 year: 2015 ident: B53 article-title: The importance of the microbiome of the plant holobiont. publication-title: New Phytol. doi: 10.1111/nph.13312 – volume: 5 issue: 148 year: 2014 ident: B6 article-title: Unraveling the plant microbiome: looking back and future perspectives. publication-title: Front. Microbiol. doi: 10.3389/fmicb.2014.00148 – volume: 349 start-page: 860 year: 2015 ident: B31 article-title: Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa. publication-title: Science doi: 10.1126/science.aaa8764 – volume: 112 start-page: E911 year: 2015 ident: B18 article-title: Structure, variation, and assembly of the root-associated microbiomes of rice. publication-title: Proc. Natl. Acad. Sci. U.S.A. doi: 10.1073/pnas.1414592112 – volume: 27 start-page: 29 year: 2002 ident: B8 article-title: Comparison of detachment procedures for direct counts of bacteria associated with sediment particles, plant litter and epiphytic biofilms. publication-title: Aquat. Microb. Ecol. doi: 10.3354/ame027029 – volume: 14 issue: 332 year: 2014 ident: B16 article-title: Endophytic microbial community in two transgenic maize genotypes and in their near-isogenic non-transgenic maize genotype. publication-title: BMC Microbiol. doi: 10.1186/s12866-014-0332-1 – volume: 261 start-page: 199 year: 2004 ident: B33 article-title: Development of specific rhizosphere bacterial communities in relation to plant species, nutrition and soil type. publication-title: Plant Soil doi: 10.1023/B:PLSO.0000035569.80747.c5 – volume: 63 start-page: 471 year: 2013 ident: B3 article-title: A standardized method for the sampling of rhizosphere and rhizoplan soil bacteria associated to a herbaceous root system. publication-title: Ann. Microbiol. doi: 10.1007/s13213-012-0491-y – volume: 84 start-page: 45 year: 2013 ident: B11 article-title: Rarefaction and extrapolation with Hill numbers: a framework for sampling and estimation in species diversity studies. publication-title: Ecol. Monogr. doi: 10.1890/13-0133.1 – volume: 25 start-page: 259 year: 2003 ident: B21 article-title: Hypochlorite-induced oxidation of amino acids, peptides and proteins. publication-title: Amino Acids doi: 10.1007/s00726-003-0016-x – volume: 4 issue: 1 year: 2013 ident: B34 article-title: The rhizosphere-roots, soil and everything in between. publication-title: Nat. Educ. Knowl. – volume: 111 start-page: 585 year: 2014 ident: B46 article-title: Quantitative divergence of the bacterial root microbiota in Arabidopsis thaliana relatives. publication-title: Proc. Natl. Acad. Sci. U.S.A. doi: 10.1073/pnas.1321597111 – volume: 16 start-page: 2157 year: 2014 ident: B36 article-title: Host signature effect on plant root-associated microbiomes revealed through analyses of resident vs. active communities. publication-title: Environ. Microbiol. doi: 10.1111/1462-2920.12228 – volume: 67 start-page: 5849 year: 2001 ident: B54 article-title: Variation of microbial communities in soil, rhizosphere, and rhizoplane in response to crop species, soil type, and crop development. publication-title: Appl. Environ. Microbiol. doi: 10.1128/AEM.67.12.5849-5854.2001 – volume: 488 start-page: 86 year: 2012 ident: B32 article-title: Defining the core Arabidopsis thaliana root microbiome. publication-title: Nature doi: 10.1038/nature11237 – volume: 4 issue: 136 year: 2013 ident: B50 article-title: Local and regional influences over soil microbial metacommunities in the Transantarctic Mountains. publication-title: Ecosphere doi: 10.1890/ES13-00136.1 – volume: 75 start-page: 55 year: 2008 ident: B15 article-title: Analysis of T-RFLP data using analysis of variance and ordination methods: a comparative study. publication-title: J. Microbiol. Methods doi: 10.1016/j.mimet.2008.04.011 – volume: 8 start-page: 790 year: 2014 ident: B12 article-title: Rhizosphere microbiome assemblage is affected by plant development. publication-title: ISME J. doi: 10.1038/ismej.2013.196 – volume: 64 start-page: 1018 year: 2012 ident: B37 article-title: Distinctive bacterial communities in the rhizoplane of four tropical tree species. publication-title: Microb. Ecol. doi: 10.1007/s00248-012-0082-2 – volume: 7 start-page: 2248 year: 2013 ident: B51 article-title: Comparative metatranscriptomics reveals kingdom level changes in the rhizosphere microbiome of plants. publication-title: ISME J. doi: 10.1038/ismej.2013.119 – volume: 6 issue: e23321 year: 2011 ident: B25 article-title: Comparative analysis of bacterial communities in a potato field as determined by pyrosequencing. publication-title: PLoS ONE doi: 10.1371/journal.pone.0023321 – volume: 340 start-page: 413 year: 2011 ident: B4 article-title: Endophytic and rhizoplane bacteria associated with Cytisus striatus growing on hexachlorocyclohexane-contaminated soil: isolation and characterisation. publication-title: Plant Soil doi: 10.1007/s11104-010-0613-x – volume: 52 start-page: 520 year: 1986 ident: B44 article-title: Close association of Azospirillum and diazotrophic rods with different root zones of kallar grass. publication-title: Appl. Environ. Microbiol. doi: 10.1128/AEM.52.3.520-526.1986 – volume: 89 start-page: 316 year: 2014 ident: B52 article-title: Community fingerprinting in a sequencing world. publication-title: FEMS Microbiol. Ecol. doi: 10.1111/1574-6941.12308 – volume: 77 start-page: 5934 year: 2011 ident: B19 article-title: Distinct microbial communities within the endosphere and rhizosphere of Populus deltoides roots across contrasting soil types. publication-title: Appl. Environ. Microbiol. doi: 10.1128/AEM.05255-11 – volume: 87 start-page: 390 year: 2014 ident: B47 article-title: Detection and quantification of native microbial populations on soil-grown rice roots by catalyzed reporter deposition-fluorescence in situ hybridization. publication-title: FEMS Microbiol. Ecol. doi: 10.1111/1574-6941.12232 – volume: 17 start-page: 392 year: 2015 ident: B9 article-title: Structure and function of the bacterial root microbiota in wild and domesticated barley. publication-title: Cell Host Microbe doi: 10.1016/j.chom.2015.01.011 – volume: 41 start-page: 919 year: 2009 ident: B55 article-title: Bacterial communities in soybean rhizosphere in response to soil type, soybean genotype, and their growth stage. publication-title: Soil Biol. Biochem. doi: 10.1016/j.soilbio.2008.10.027 – volume: 77 start-page: 154 year: 2011 ident: B20 article-title: Rice root-associated bacteria: insights into community structures across 10 cultivars. publication-title: FEMS Microbiol. Ecol. doi: 10.1111/j.1574-6941.2011.01092.x – volume: 25 start-page: 28 year: 2012 ident: B49 article-title: Functional characteristics of an endophyte community colonizing rice roots as revealed by metagenomic analysis. publication-title: Mol. Plant Microbe Interact. doi: 10.1094/mpmi-08-11-0204 – volume: 17 start-page: 478 year: 2012 ident: B5 article-title: The rhizosphere microbiome and plant health. publication-title: Trends Plant Sci. doi: 10.1016/j.tplants.2012.04.001 – year: 2015 ident: B38 publication-title: vegan: Community Ecology Package. – volume: 5 issue: e9788 year: 2010 ident: B22 article-title: A robust procedure for comparing multiple means under heteroscedasticity in unbalanced designs. publication-title: PLoS ONE doi: 10.1371/journal.pone.0009788 – volume: 8 start-page: 929 year: 2006 ident: B1 article-title: Statistical methods for characterizing diversity of microbial communities by analysis of terminal restriction fragment length polymorphisms of 16S rRNA genes. publication-title: Environ. Microbiol. doi: 10.1111/j.1462-2920.2005.00959.x – volume: 71 start-page: 6784 year: 2005 ident: B35 article-title: Links between plant and rhizoplane bacterial communities in grassland soils, characterized using molecular techniques. publication-title: Appl. Environ. Microbiol. doi: 10.1128/AEM.71.11.6784-6792.2005 – volume: 42 start-page: 669 year: 2010 ident: B14 article-title: Plant growth-promoting bacteria in the rhizo- and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. publication-title: Soil Biol. Biochem. doi: 10.1016/j.soilbio.2009.11.024 – volume: 321 start-page: 117 year: 2009 ident: B23 article-title: Rhizosphere: biophysics, biogeochemistry and ecological relevance. publication-title: Plant Soil doi: 10.1007/s11104-008-9885-9 – volume: 528 start-page: 364 year: 2015 ident: B2 article-title: Functional overlap of the Arabidopsis leaf and root microbiota. publication-title: Nature doi: 10.1038/nature16192 – volume: 45 start-page: 62 year: 2009 ident: B26 article-title: Isolation, partial identification and application of diazotrophic rhizobacteria from traditional Indian rice cultivars. publication-title: Eur. J. Soil Biol. doi: 10.1016/j.ejsobi.2008.06.007 – volume: 8 issue: e56329 year: 2013 ident: B7 article-title: Bacterial communities associated with the leaves and the roots of Arabidopsis thaliana. publication-title: PLoS ONE doi: 10.1371/journal.pone.0056329 – volume: 42 start-page: 136 year: 2001 ident: B27 article-title: Phylogenetic analysis of microbial diversity in the rhizoplane of oilseed rape (Brassica napus cv. Westar) employing cultivation-dependent and cultivation-independent approaches. publication-title: Microb. Ecol. doi: 10.1007/s002480000121 – year: 2015 ident: B43 publication-title: R: A Language and Environment for Statistical Computing. – volume: 341 start-page: 221 year: 2011 ident: B48 article-title: Monitoring of root growth and redox conditions in paddy soil rhizotrons by redox electrodes and image analysis. publication-title: Plant Soil doi: 10.1007/s11104-010-0637-2 – volume: 30 start-page: 961 year: 2012 ident: B24 article-title: Who’s who in the plant root microbiome? publication-title: Nat. Biotechnol. doi: 10.1038/nbt.2387 – volume: 27 start-page: 418 year: 2008 ident: B13 article-title: Dynamics of rhizoplane bacterial communities subjected to physicochemical treatments in hydroponic crops. publication-title: Crop Prot. doi: 10.1016/j.cropro.2007.07.010 – volume: 66 start-page: 389 year: 2009 ident: B42 article-title: Rock-degrading endophytic bacteria in cacti. publication-title: Environ. Exp. Bot. doi: 10.1016/j.envexpbot.2009.04.010 – volume: 11 start-page: 789 year: 2013 ident: B40 article-title: Going back to the roots: the microbial ecology of the rhizosphere. publication-title: Nat. Rev. Microbiol. doi: 10.1038/nrmicro3109 – volume: 53 start-page: 403 year: 2015 ident: B45 article-title: Roots shaping their microbiome: global hotspots for microbial activity. publication-title: Annu. Rev. Phytopathol. doi: 10.1146/annurev-phyto-082712-102342 – reference: 25655016 - New Phytol. 2015 Jun;206(4):1196-206 – reference: 24628845 - Environ Microbiol. 2015 Mar;17(3):610-21 – reference: 21426364 - FEMS Microbiol Ecol. 2011 Jul;77(1):154-64 – reference: 25732064 - Cell Host Microbe. 2015 Mar 11;17(3):392-403 – reference: 14661089 - Amino Acids. 2003 Dec;25(3-4):259-74 – reference: 24379374 - Proc Natl Acad Sci U S A. 2014 Jan 14;111(2):585-92 – reference: 22767122 - Microb Ecol. 2012 Nov;64(4):1018-27 – reference: 20360960 - PLoS One. 2010 Mar 29;5(3):e9788 – reference: 24196324 - ISME J. 2014 Apr;8(4):790-803 – reference: 23457551 - PLoS One. 2013;8(2):e56329 – reference: 24056930 - Nat Rev Microbiol. 2013 Nov;11(11):789-99 – reference: 23962203 - Environ Microbiol. 2014 Jul;16(7):2157-67 – reference: 12024277 - Microb Ecol. 2001 Aug;42(2):136-149 – reference: 24580036 - FEMS Microbiol Ecol. 2014 Aug;89(2):316-30 – reference: 23576752 - Proc Natl Acad Sci U S A. 2013 Apr 16;110(16):6548-53 – reference: 25540019 - BMC Microbiol. 2014 Dec 24;14:332 – reference: 23864127 - ISME J. 2013 Dec;7(12):2248-58 – reference: 24926286 - Front Microbiol. 2014 Jun 04;5:148 – reference: 16623749 - Environ Microbiol. 2006 May;8(5):929-38 – reference: 11722945 - Appl Environ Microbiol. 2001 Dec;67(12):5849-54 – reference: 16269710 - Appl Environ Microbiol. 2005 Nov;71(11):6784-92 – reference: 22189496 - ISME J. 2012 Jul;6(7):1378-90 – reference: 26243728 - Annu Rev Phytopathol. 2015;53:403-24 – reference: 21970692 - Mol Plant Microbe Interact. 2012 Jan;25(1):28-36 – reference: 24118011 - FEMS Microbiol Ecol. 2014 Feb;87(2):390-402 – reference: 16347149 - Appl Environ Microbiol. 1986 Sep;52(3):520-6 – reference: 25605935 - Proc Natl Acad Sci U S A. 2015 Feb 24;112(8):E911-20 – reference: 18584903 - J Microbiol Methods. 2008 Sep;75(1):55-63 – reference: 21764952 - Appl Environ Microbiol. 2011 Sep;77(17):5934-44 – reference: 22859207 - Nature. 2012 Aug 2;488(7409):91-5 – reference: 23051815 - Nat Biotechnol. 2012 Oct;30(10):961-2 – reference: 1571142 - Biotechniques. 1992 Mar;12(3):358-60 – reference: 21886785 - PLoS One. 2011;6(8):e23321 – reference: 24904612 - Front Plant Sci. 2014 May 21;5:216 – reference: 22564542 - Trends Plant Sci. 2012 Aug;17(8):478-86 – reference: 26633631 - Nature. 2015 Dec 17;528(7582):364-9 – reference: 26184915 - Science. 2015 Aug 21;349(6250):860-4 – reference: 22859206 - Nature. 2012 Aug 2;488(7409):86-90 |
| SSID | ssj0000402000 |
| Score | 2.341808 |
| Snippet | Plants shape distinct, species-specific microbiomes in their rhizospheres. A main premise for evaluating microbial communities associated with root-soil... |
| SourceID | doaj pubmedcentral proquest pubmed crossref |
| SourceType | Open Website Open Access Repository Aggregation Database Index Database Enrichment Source |
| StartPage | 773 |
| SubjectTerms | endosphere Microbiology rhizobiome rhizoplane rhizosphere root microbiome |
| SummonAdditionalLinks | – databaseName: DOAJ - Directory of Open Access Journals dbid: DOA link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwrV1JS8QwFA4iCF7E3XEjghcPxU6WLt5UHAZBTwreQlZmQFuZqQf_ve-lnWFGRC-eCm2ahHzJW5KX7xFyDjqGFyZzSS6dT4QpRKK97Ccul8ZLaeCBt5EfHrPhs7h_kS8Lqb4wJqylB24H7pLx4D3XUha2EFJnpTNSSsectUUIWUDpCzpvwZmKMhjdojRtzyXBCysBprE1GMqFhw95zpf0UKTr_8nG_B4quaB7BptkozMa6XXb2S2y4qttstamkfzcIdO7OWU3rQOdNjP6B9rUdOoju7enYCI3ie7Q8I6-jSMHE9Rr20siSK16Ra-pBbjj61ENUoSOKzrBwLx4UZ925ECjXfI8uHu6HSZdMoXEiow1IPW0EJLpkhueBtwLzkE5mcCZY8xmQhcW1iIYIKkNRoQUlJvJNPzBhU2N7fM9slrVlT8glDvbR-Yy13cCrDFX5ExA7VyDL-hTW_bI5Wxole2YxjHhxasCjwPBUBEMhWCoCEaPXMz_eG9ZNn4pe4NozcshP3Z8AbNGdbNG_TVreuRshrWC9YSHJLry9cdUocAqcUsDGtpvsZ83xXKGCdnTHsmXZsVSX5a_VONR5OwGvxCJ9A__o_NHZB2HA2MYmDgmq83kw5-AadSY07gKvgCBMw_E priority: 102 providerName: Directory of Open Access Journals |
| Title | Evaluation of Strategies to Separate Root-Associated Microbial Communities: A Crucial Choice in Rhizobiome Research |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/27252690 https://www.proquest.com/docview/1793910163 https://pubmed.ncbi.nlm.nih.gov/PMC4877504 https://doaj.org/article/23fee3a558c845a69db555d2dcc8ff6f |
| Volume | 7 |
| hasFullText | 1 |
| inHoldings | 1 |
| isFullTextHit | |
| isPrint | |
| link | http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwrV1ba9RAFB5qi-CL2HrpaltG8MWHaDKXTFYopUovCPXJhX0b5uoutEndpGD_vedMsmtXFp98SSCZG_PNmXPOXL5DyDvQMbyypc-U9CETthKZCbLIvJI2SGnhhbeRr76VlxPxdSqnf65HDx3YbnTtMJ7UZHH94dfP-xMQ-GP0OEHfAgJzZ_GUFu4rKMUfkR3QSwrjGVwNxn6al9FVyvN-r3JjxjXdlCj8N9mdfx-ffKCPzp-Rp4MhSU975HfJVqj3yOM-tOT9c9KerWi8aRNp2y0pIWjX0DYkxu9AwWzuMjMgFDy9mSdeJijX9RdHkG71Ez2lDoZA-jxrYGah85ou8LBeurxPB8Kg2QsyOT_7_uUyGwIsZE6UrIOZ0AghmRlzy_OI68MKFJaNnHnGXClM5UA-wSjJXbQi5qDwbGkgBxcut67gL8l23dRhn1DuXYFsZr7wAiw0XykmoHRuwD8MuRuPyMdl12o3sI9jEIxrDV4IgqETGBrB0AmMEXm_ynHbM2_8I-1nRGuVDjmz04dm8UMPIqgZjyFwI2XlKiFNOfZWSumZd66KsYwj8naJtQYZw40TU4fmrtU4iY1xmQMqetVjv6qKKYZB2vMRUWujYq0t63_q-SzxeIOviOT6r_9H49-QJ9gdeK6BiQOy3S3uwiGYS509SssM8LyYFkdJIn4D4r0ZDg |
| linkProvider | Scholars Portal |
| openUrl | ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Evaluation+of+strategies+to+separate+root-associated+microbial+communities%3A+A+crucial+choice+in+rhizobiome+research&rft.jtitle=Frontiers+in+microbiology&rft.au=Tim+eRichter-Heitmann&rft.au=Tim+eRichter-Heitmann&rft.au=Thilo+eEickhorst&rft.au=Stefan+eKnauth&rft.date=2016-05-24&rft.pub=Frontiers+Media+S.A&rft.eissn=1664-302X&rft.volume=7&rft_id=info:doi/10.3389%2Ffmicb.2016.00773&rft.externalDBID=DOA&rft.externalDocID=oai_doaj_org_article_23fee3a558c845a69db555d2dcc8ff6f |
| thumbnail_l | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1664-302X&client=summon |
| thumbnail_m | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1664-302X&client=summon |
| thumbnail_s | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1664-302X&client=summon |