An integrated metagenomic, metabolomic and transcriptomic survey of Populus across genotypes and environments.


Journal

Scientific data
ISSN: 2052-4463
Titre abrégé: Sci Data
Pays: England
ID NLM: 101640192

Informations de publication

Date de publication:
05 Apr 2024
Historique:
received: 14 09 2023
accepted: 13 02 2024
medline: 6 4 2024
pubmed: 6 4 2024
entrez: 5 4 2024
Statut: epublish

Résumé

Bridging molecular information to ecosystem-level processes would provide the capacity to understand system vulnerability and, potentially, a means for assessing ecosystem health. Here, we present an integrated dataset containing environmental and metagenomic information from plant-associated microbial communities, plant transcriptomics, plant and soil metabolomics, and soil chemistry and activity characterization measurements derived from the model tree species Populus trichocarpa. Soil, rhizosphere, root endosphere, and leaf samples were collected from 27 different P. trichocarpa genotypes grown in two different environments leading to an integrated dataset of 318 metagenomes, 98 plant transcriptomes, and 314 metabolomic profiles that are supported by diverse soil measurements. This expansive dataset will provide insights into causal linkages that relate genomic features and molecular level events to system-level properties and their environmental influences.

Identifiants

pubmed: 38580669
doi: 10.1038/s41597-024-03069-7
pii: 10.1038/s41597-024-03069-7
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

339

Informations de copyright

© 2024. UT-Battelle, LLC, Pacific Northwest National Laboratory and The Author(s).

Références

Bar-On, Y. M., Phillips, R. & Milo, R. The biomass distribution on Earth. Proceedings of the National Academy of Sciences 115, 6506–6511 (2018).
doi: 10.1073/pnas.1711842115
Iversen, C. M. & Norby, R. J. Nitrogen limitation in a sweetgum plantation: implications for carbon allocation and storage. Canadian Journal of Forest Research 38, 1021–1032 (2008).
doi: 10.1139/X07-213
Thornton, P. E., Lamarque, J. F., Rosenbloom, N. A. & Mahowald, N. M. Influence of Carbon‐Nitrogen Cycle Coupling on Land Model Response to CO
doi: 10.1029/2006GB002868
Van Der Heijden, M. G. & Bardgett, R. D. & Van Straalen, N. M. The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecology letters 11, 296–310 (2008).
doi: 10.1111/j.1461-0248.2007.01139.x pubmed: 18047587
Luo, J. & Zhou, J.-J. Growth performance, photosynthesis, and root characteristics are associated with nitrogen use efficiency in six poplar species. Environmental and Experimental Botany 164, 40–51 (2019).
doi: 10.1016/j.envexpbot.2019.04.013
Soolanayakanahally, R. Y., Guy, R. D., Silim, S. N., Drewes, E. C. & Schroeder, W. R. Enhanced assimilation rate and water use efficiency with latitude through increased photosynthetic capacity and internal conductance in balsam poplar (Populus balsamifera L.). Plant, Cell & Environment 32, 1821–1832 (2009).
doi: 10.1111/j.1365-3040.2009.02042.x
Bardon, C. et al. Evidence for biological denitrification inhibition (BDI) by plant secondary metabolites. New Phytol 204, 620–630 (2014).
doi: 10.1111/nph.12944 pubmed: 25059468
Laffite, A. et al. Biological inhibition of soil nitrification by forest tree species affects Nitrobacter populations. Environmental microbiology 22, 1141–1153 (2020).
doi: 10.1111/1462-2920.14905 pubmed: 31867821
Subbarao, G. et al. Evidence for biological nitrification inhibition in Brachiaria pastures. Proceedings of the National Academy of Sciences 106, 17302–17307 (2009).
doi: 10.1073/pnas.0903694106
Subbarao, G. et al. Biological nitrification inhibition—a novel strategy to regulate nitrification in agricultural systems. Advances in agronomy 114, 249–302 (2012).
doi: 10.1016/B978-0-12-394275-3.00001-8
Ghatak, A., Chaturvedi, P., Waldherr, S., Subbarao, G. V. & Weckwerth, W. PANOMICS at the Interface of Root–Soil Microbiome and BNI. Trends in Plant Science 28, 106–122 (2023).
doi: 10.1016/j.tplants.2022.08.016 pubmed: 36229336
Cregger, M. A. et al. Plant–microbe interactions: from genes to ecosystems using populus as a model system. Phytobiomes Journal 5, 29–38 (2021).
doi: 10.1094/PBIOMES-01-20-0009-FI
Evans, L. M. et al. Population genomics of Populus trichocarpa identifies signatures of selection and adaptive trait associations. Nature genetics 46, 1089–1096 (2014).
doi: 10.1038/ng.3075 pubmed: 25151358
Tuskan, G. A. et al. The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313, 1596–1604 (2006).
doi: 10.1126/science.1128691 pubmed: 16973872
Chhetri, H. B. et al. Genome-Wide Association Study of Wood Anatomical and Morphological Traits in Populus trichocarpa. Front Plant Sci 11, 545748 (2020).
doi: 10.3389/fpls.2020.545748 pubmed: 33013968 pmcid: 7509168
Soil Survey Staff, Natural Resources Conservation Service, United States Department of Agriculture. Web Soil Survey http://websoilsurvey.sc.egov.usda.gov/ (2023).
Gopalakrishnan, S. et al. Nitrification inhibitors from the root tissues of Brachiaria humidicola, a tropical grass. Journal of agricultural and food chemistry 55, 1385–1388 (2007).
doi: 10.1021/jf062593o pubmed: 17243702
Subbarao, G. V. et al. Free fatty acids from the pasture grass Brachiaria humidicola and one of their methyl esters as inhibitors of nitrification. Plant and Soil 313, 89–99 (2008).
doi: 10.1007/s11104-008-9682-5
Gee, G. W. & Or, D. in Methods of soil analysis, Part 4: Physical methods (eds Dane, J. H. & Topp, C. G.) Ch 2.4 (Soil Science Society of America, 2002).
Hart, S. C., Stark, J. M., Davidson, E. A. & Firestone, M. K. in Methods of soil analysis: Part 2 microbiological and biochemical properties (eds. Weaver, R. W., Angle, S., Bottomley, P., Bezdicek, D., Smith, S., Tabatabai, A., Wollum, A.) Ch. 42 (1994).
Tiedje, J. M. in Methods of soil analysis, Part 2: Microbiological and Biochemical Properties (eds. et al Ch 14 (Soil Society of America, 1994).
Cregger, M. et al. The Populus holobiont: dissecting the effects of plant niches and genotype on the microbiome. Microbiome 6, 1–14 (2018).
doi: 10.1186/s40168-018-0413-8
Utturkar, S. M. et al. Enrichment of root endophytic bacteria from Populus deltoides and single-cell-genomics analysis. Applied and environmental microbiology 82, 5698–5708 (2016).
doi: 10.1128/AEM.01285-16 pubmed: 27422831 pmcid: 5007785
McCormack, M. L. et al. Redefining fine roots improves understanding of below-ground contributions to terrestrial biosphere processes. New Phytol 207, 505–518 (2015).
doi: 10.1111/nph.13363 pubmed: 25756288
Zhang, J. et al. Genome‐wide association studies and expression‐based quantitative trait loci analyses reveal roles of HCT 2 in caffeoylquinic acid biosynthesis and its regulation by defense‐responsive transcription factors in Populus. New Phytol 220, 502–516 (2018).
doi: 10.1111/nph.15297 pubmed: 29992670
Nurk, S., Meleshko, D., Korobeynikov, A. & Pevzner, P. A. metaSPAdes: a new versatile metagenomic assembler. Genome research 27, 824–834 (2017).
doi: 10.1101/gr.213959.116 pubmed: 28298430 pmcid: 5411777
Bushnell, B., Rood, J. & Singer, E. BBMerge - Accurate paired shotgun read merging via overlap. PLoS ONE 12, e0185056 (2017).
doi: 10.1371/journal.pone.0185056 pubmed: 29073143 pmcid: 5657622
Clum, A. et al. DOE JGI metagenome workflow. mSystems 6, e00804–00820 (2021).
doi: 10.1128/mSystems.00804-20 pubmed: 34006627 pmcid: 8269246
Kim, D., Langmead, B. & Salzberg, S. L. HISAT: a fast spliced aligner with low memory requirements. Nature methods 12, 357–360 (2015).
doi: 10.1038/nmeth.3317 pubmed: 25751142 pmcid: 4655817
Ramírez, F., Dündar, F., Diehl, S., Grüning, B. A. & Manke, T. deepTools: a flexible platform for exploring deep-sequencing data. Nucleic acids research 42, W187–W191 (2014).
doi: 10.1093/nar/gku365 pubmed: 24799436 pmcid: 4086134
Liao, Y., Smyth, G. K. & Shi, W. FeatureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30, 923–930 (2014).
doi: 10.1093/bioinformatics/btt656 pubmed: 24227677
Doktycz, M. J. & Bowen, B. P. GNPS - Metabolomics study of root, rhizosphere and leaf samples from a Populus Trichocarpa common garden. MassIVE Data Repository https://doi.org/10.25345/C58K7520G (2023).
Doktycz, M., Eloe-Fadrosh, E., Schadt, C. & BioScales, - Defining plant gene function and its connection to ecosystem nitrogen and carbon cycling. Joint Genome Institute Genome Data Portal https://doi.org/10.46936/10.25585/60000017 (2020).
National Center for Biotechnology Information https://identifiers.org/ncbi/bioproject:PRJNA1034652 (2023).
National Microbiome Data Collaborative https://data.microbiomedata.org/details/study/nmdc:sty-11-r2h77870 (2023).
Mayes, M. et al. 2020 Soil Characterization measurements at Clatskanie and Corvallis, Oregon Populus Trichocarpa GWAS Populations, DOE Oak Ridge National Laboratory (ORNL) Repository, https://doi.org/10.25983/2205588 (2023).
Carper, D. L. et al. Cultivating the Bacterial Microbiota of Populus Roots. mSystems 6, e01306-20 (2021).
doi: 10.1128/mSystems.01306-20 pubmed: 34156297 pmcid: 8269261
Bushnell B. BBTools software package. (BBMap) http://bbtools.jgi.doe.gov . 2014.
Yao, Y. et al. Analysis of Metabolomics Datasets with High-Performance Computing and Metabolite Atlases. Metabolites 5, 431–442 (2015).
doi: 10.3390/metabo5030431 pubmed: 26287255 pmcid: 4588804
Holtz, W. et al Metabolite Atlas. https://github.com/biorack/metatlas (2023).

Auteurs

Christopher Schadt (C)

Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, USA. schadtcw@ornl.gov.

Stanton Martin (S)

Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, USA. martins@ornl.gov.

Alyssa Carrell (A)

Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, USA.

Allison Fortner (A)

Environmental Sciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, USA.

Dan Hopp (D)

Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, USA.

Dan Jacobson (D)

Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, USA.

Dawn Klingeman (D)

Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, USA.

Brandon Kristy (B)

Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, USA.

Jana Phillips (J)

Environmental Sciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, USA.

Bryan Piatkowski (B)

Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, USA.
Division of Computational Biology, Mayo Clinic, Rochester, MN, 55905, USA.

Mark A Miller (MA)

Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA.

Montana Smith (M)

Pacific Northwest National Laboratory, Richland, WA, 99354, USA.

Sujay Patil (S)

Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA.

Mark Flynn (M)

Bioscience Division, Los Alamos National Laboratory, Los Alamos, NM, 87545, USA.

Shane Canon (S)

Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA.

Alicia Clum (A)

Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA.

Christopher J Mungall (CJ)

Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA.

Christa Pennacchio (C)

DOE Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, USA.

Benjamin Bowen (B)

DOE Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, USA.

Katherine Louie (K)

DOE Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, USA.

Trent Northen (T)

DOE Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, USA.

Emiley A Eloe-Fadrosh (EA)

Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA.
DOE Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, USA.

Melanie A Mayes (MA)

Environmental Sciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, USA.

Wellington Muchero (W)

Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, USA.

David J Weston (DJ)

Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, USA.

Julie Mitchell (J)

Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, USA.

Mitchel Doktycz (M)

Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, USA. doktyczmj@ornl.gov.

Classifications MeSH