Compositional shifts in root-associated bacterial and archaeal microbiota track the plant life cycle in field-grown rice
Bacterial communities associated with roots impact the health and nutrition of the host plant. The dynamics of these microbial assemblies over the plant life cycle are, however, not well understood. Here, we use dense temporal sampling of 1,510 samples from root spatial compartments to characterize...
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description | Bacterial communities associated with roots impact the health and nutrition of the host plant. The dynamics of these microbial assemblies over the plant life cycle are, however, not well understood. Here, we use dense temporal sampling of 1,510 samples from root spatial compartments to characterize the bacterial and archaeal components of the root-associated microbiota of field grown rice (Oryza sativa) over the course of 3 consecutive growing seasons, as well as 2 sites in diverse geographic regions. The root microbiota was found to be highly dynamic during the vegetative phase of plant growth and then stabilized compositionally for the remainder of the life cycle. Bacterial and archaeal taxa conserved between field sites were defined as predictive features of rice plant age by modeling using a random forest approach. The age-prediction models revealed that drought-stressed plants have developmentally immature microbiota compared to unstressed plants. Further, by using genotypes with varying developmental rates, we show that shifts in the microbiome are correlated with rates of developmental transitions rather than age alone, such that different microbiota compositions reflect juvenile and adult life stages. These results suggest a model for successional dynamics of the root-associated microbiota over the plant life cycle. |
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The dynamics of these microbial assemblies over the plant life cycle are, however, not well understood. Here, we use dense temporal sampling of 1,510 samples from root spatial compartments to characterize the bacterial and archaeal components of the root-associated microbiota of field grown rice (Oryza sativa) over the course of 3 consecutive growing seasons, as well as 2 sites in diverse geographic regions. The root microbiota was found to be highly dynamic during the vegetative phase of plant growth and then stabilized compositionally for the remainder of the life cycle. Bacterial and archaeal taxa conserved between field sites were defined as predictive features of rice plant age by modeling using a random forest approach. The age-prediction models revealed that drought-stressed plants have developmentally immature microbiota compared to unstressed plants. Further, by using genotypes with varying developmental rates, we show that shifts in the microbiome are correlated with rates of developmental transitions rather than age alone, such that different microbiota compositions reflect juvenile and adult life stages. These results suggest a model for successional dynamics of the root-associated microbiota over the plant life cycle.</description><identifier>ISSN: 1545-7885</identifier><identifier>ISSN: 1544-9173</identifier><identifier>EISSN: 1545-7885</identifier><identifier>DOI: 10.1371/journal.pbio.2003862</identifier><identifier>PMID: 29474469</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Age ; Archaea - classification ; Archaea - isolation & purification ; Bacteria ; Bacteria - classification ; Bacteria - isolation & purification ; BASIC BIOLOGICAL SCIENCES ; Biology and Life Sciences ; Data collection ; Drought ; Droughts ; Earth Sciences ; Ecology and Environmental Sciences ; Genotypes ; Host plants ; Life cycle engineering ; Life cycles ; Mathematical models ; Microbiomes ; Microbiota ; Microorganisms ; Multivariate analysis ; Nutrition ; Oryza - growth & development ; Oryza - microbiology ; Oryza - physiology ; Oryza sativa ; Phylogeny ; Plant biology ; Plant growth ; Plant resistance ; Plant Roots - microbiology ; Prediction models ; Research and Analysis Methods ; Rice ; Seasons ; Stress, Physiological</subject><ispartof>PLoS biology, 2018-02, Vol.16 (2), p.e2003862-e2003862</ispartof><rights>2018 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Edwards JA, Santos-Medellín CM, Liechty ZS, Nguyen B, Lurie E, Eason S, et al. (2018) Compositional shifts in root-associated bacterial and archaeal microbiota track the plant life cycle in field-grown rice. PLoS Biol 16(2): e2003862. https://doi.org/10.1371/journal.pbio.2003862</rights><rights>2018 Edwards et al 2018 Edwards et al</rights><rights>2018 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Edwards JA, Santos-Medellín CM, Liechty ZS, Nguyen B, Lurie E, Eason S, et al. (2018) Compositional shifts in root-associated bacterial and archaeal microbiota track the plant life cycle in field-grown rice. 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The dynamics of these microbial assemblies over the plant life cycle are, however, not well understood. Here, we use dense temporal sampling of 1,510 samples from root spatial compartments to characterize the bacterial and archaeal components of the root-associated microbiota of field grown rice (Oryza sativa) over the course of 3 consecutive growing seasons, as well as 2 sites in diverse geographic regions. The root microbiota was found to be highly dynamic during the vegetative phase of plant growth and then stabilized compositionally for the remainder of the life cycle. Bacterial and archaeal taxa conserved between field sites were defined as predictive features of rice plant age by modeling using a random forest approach. The age-prediction models revealed that drought-stressed plants have developmentally immature microbiota compared to unstressed plants. Further, by using genotypes with varying developmental rates, we show that shifts in the microbiome are correlated with rates of developmental transitions rather than age alone, such that different microbiota compositions reflect juvenile and adult life stages. These results suggest a model for successional dynamics of the root-associated microbiota over the plant life cycle.</description><subject>Age</subject><subject>Archaea - classification</subject><subject>Archaea - isolation & purification</subject><subject>Bacteria</subject><subject>Bacteria - classification</subject><subject>Bacteria - isolation & purification</subject><subject>BASIC BIOLOGICAL SCIENCES</subject><subject>Biology and Life Sciences</subject><subject>Data collection</subject><subject>Drought</subject><subject>Droughts</subject><subject>Earth Sciences</subject><subject>Ecology and Environmental Sciences</subject><subject>Genotypes</subject><subject>Host plants</subject><subject>Life cycle engineering</subject><subject>Life cycles</subject><subject>Mathematical models</subject><subject>Microbiomes</subject><subject>Microbiota</subject><subject>Microorganisms</subject><subject>Multivariate analysis</subject><subject>Nutrition</subject><subject>Oryza - growth & development</subject><subject>Oryza - microbiology</subject><subject>Oryza - physiology</subject><subject>Oryza sativa</subject><subject>Phylogeny</subject><subject>Plant biology</subject><subject>Plant growth</subject><subject>Plant resistance</subject><subject>Plant Roots - microbiology</subject><subject>Prediction models</subject><subject>Research and Analysis Methods</subject><subject>Rice</subject><subject>Seasons</subject><subject>Stress, Physiological</subject><issn>1545-7885</issn><issn>1544-9173</issn><issn>1545-7885</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNptksluFDEQhlsIRELgDRC04MKlB-_LBQmNWCJF4gJny3ZXz3joaQ-2B8jb42Y6UYI4efvrq_rL1TTPMVphKvHbXTymyY6rgwtxRRCiSpAHzTnmjHdSKf7wzv6seZLzDiFCNFGPmzOimWRM6PPm9zruDzGHEmKFtXkbhpLbMLUpxtLZnKMPtkDfOusLpFA1dupbm_zWQj3sg0-xVlBsW5L139uyhfYw2qm0Yxig9dd-hJk3BBj7bpPir8oOHp42jwY7Zni2rBfNt48fvq4_d1dfPl2u3191XkhUOsx76gbGsOots4qLQVClEHOs7ylgPWiL1SCdY1JiwjUg7jFVnAmhe-8EvWhenriHMWazNC0bgjDjhFdYVVyeFH20O3NIYW_TtYk2mL8XMW2MTSVUH4ZzhqngIAR1zAtn9SC1BOIdIOv4zHq3ZDu6PfQeptqV8R70_ssUtmYTfxquqkUiK-DVCRBzCSb7UMBvfZwm8MVgzjVmqIreLFlS_HGEXMw-ZA9jbTvE42wOSa0klbP09T_S_7eAnVT1M3NOMNxWjJGZp-0myszTZpZpq2Ev7rq9DboZL_oH6cPTzg</recordid><startdate>20180201</startdate><enddate>20180201</enddate><creator>Edwards, Joseph A</creator><creator>Santos-Medellín, Christian M</creator><creator>Liechty, Zachary S</creator><creator>Nguyen, Bao</creator><creator>Lurie, Eugene</creator><creator>Eason, Shane</creator><creator>Phillips, Gregory</creator><creator>Sundaresan, Venkatesan</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>P64</scope><scope>PATMY</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>OIOZB</scope><scope>OTOTI</scope><scope>5PM</scope><scope>DOA</scope><scope>CZG</scope><orcidid>https://orcid.org/0000-0002-4670-0630</orcidid><orcidid>https://orcid.org/0000000246700630</orcidid></search><sort><creationdate>20180201</creationdate><title>Compositional shifts in root-associated bacterial and archaeal microbiota track the plant life cycle in field-grown rice</title><author>Edwards, Joseph A ; Santos-Medellín, Christian M ; Liechty, Zachary S ; Nguyen, Bao ; Lurie, Eugene ; Eason, Shane ; Phillips, Gregory ; Sundaresan, Venkatesan</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c670t-15d3bf4418da4a856f638804b4dd3e19f9a18f7bb4771259e05c13854669dcb63</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>Age</topic><topic>Archaea - classification</topic><topic>Archaea - isolation & purification</topic><topic>Bacteria</topic><topic>Bacteria - classification</topic><topic>Bacteria - isolation & purification</topic><topic>BASIC BIOLOGICAL SCIENCES</topic><topic>Biology and Life Sciences</topic><topic>Data collection</topic><topic>Drought</topic><topic>Droughts</topic><topic>Earth Sciences</topic><topic>Ecology and Environmental Sciences</topic><topic>Genotypes</topic><topic>Host plants</topic><topic>Life cycle engineering</topic><topic>Life cycles</topic><topic>Mathematical models</topic><topic>Microbiomes</topic><topic>Microbiota</topic><topic>Microorganisms</topic><topic>Multivariate analysis</topic><topic>Nutrition</topic><topic>Oryza - growth & development</topic><topic>Oryza - microbiology</topic><topic>Oryza - physiology</topic><topic>Oryza sativa</topic><topic>Phylogeny</topic><topic>Plant biology</topic><topic>Plant growth</topic><topic>Plant resistance</topic><topic>Plant Roots - microbiology</topic><topic>Prediction models</topic><topic>Research and Analysis Methods</topic><topic>Rice</topic><topic>Seasons</topic><topic>Stress, Physiological</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Edwards, Joseph A</creatorcontrib><creatorcontrib>Santos-Medellín, Christian M</creatorcontrib><creatorcontrib>Liechty, Zachary S</creatorcontrib><creatorcontrib>Nguyen, Bao</creatorcontrib><creatorcontrib>Lurie, Eugene</creatorcontrib><creatorcontrib>Eason, Shane</creatorcontrib><creatorcontrib>Phillips, Gregory</creatorcontrib><creatorcontrib>Sundaresan, Venkatesan</creatorcontrib><creatorcontrib>Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environmental Science Database</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Environmental Science Collection</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - 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The dynamics of these microbial assemblies over the plant life cycle are, however, not well understood. Here, we use dense temporal sampling of 1,510 samples from root spatial compartments to characterize the bacterial and archaeal components of the root-associated microbiota of field grown rice (Oryza sativa) over the course of 3 consecutive growing seasons, as well as 2 sites in diverse geographic regions. The root microbiota was found to be highly dynamic during the vegetative phase of plant growth and then stabilized compositionally for the remainder of the life cycle. Bacterial and archaeal taxa conserved between field sites were defined as predictive features of rice plant age by modeling using a random forest approach. The age-prediction models revealed that drought-stressed plants have developmentally immature microbiota compared to unstressed plants. Further, by using genotypes with varying developmental rates, we show that shifts in the microbiome are correlated with rates of developmental transitions rather than age alone, such that different microbiota compositions reflect juvenile and adult life stages. These results suggest a model for successional dynamics of the root-associated microbiota over the plant life cycle.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>29474469</pmid><doi>10.1371/journal.pbio.2003862</doi><orcidid>https://orcid.org/0000-0002-4670-0630</orcidid><orcidid>https://orcid.org/0000000246700630</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Age Archaea - classification Archaea - isolation & purification Bacteria Bacteria - classification Bacteria - isolation & purification BASIC BIOLOGICAL SCIENCES Biology and Life Sciences Data collection Drought Droughts Earth Sciences Ecology and Environmental Sciences Genotypes Host plants Life cycle engineering Life cycles Mathematical models Microbiomes Microbiota Microorganisms Multivariate analysis Nutrition Oryza - growth & development Oryza - microbiology Oryza - physiology Oryza sativa Phylogeny Plant biology Plant growth Plant resistance Plant Roots - microbiology Prediction models Research and Analysis Methods Rice Seasons Stress, Physiological |
title | Compositional shifts in root-associated bacterial and archaeal microbiota track the plant life cycle in field-grown rice |
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