Genomic features of bacterial adaptation to plants

Asaf Levy; Isai Salas Gonzalez; Maximilian Mittelviefhaus; Scott Clingenpeel; Sur Herrera Paredes; Jiamin Miao; Kunru Wang; Giulia Devescovi; Kyra Stillman; Freddy Monteiro; Bryan Rangel Alvarez; Derek S. Lundberg; Tse Yuan Lu; Sarah Lebeis; Zhao Jin; Meredith McDonald; Andrew P. Klein; Meghan E. Feltcher; Tijana Glavina Rio; Sarah R. Grant; Sharon L. Doty; Ruth E. Ley; Bingyu Zhao; Vittorio Venturi; Dale A. Pelletier; Julia A. Vorholt; Susannah G. Tringe; Tanja Woyke; Jeffery L. Dangl

doi:10.1038/s41588-017-0012-9

Genomic features of bacterial adaptation to plants

Asaf Levy, Isai Salas Gonzalez, Maximilian Mittelviefhaus, Scott Clingenpeel, Sur Herrera Paredes, Jiamin Miao, Kunru Wang, Giulia Devescovi, Kyra Stillman, Freddy Monteiro, Bryan Rangel Alvarez, Derek S. Lundberg, Tse Yuan Lu, Sarah Lebeis, Zhao Jin, Meredith McDonald, Andrew P. Klein, Meghan E. Feltcher, Tijana Glavina Rio, Sarah R. GrantSharon L. Doty, Ruth E. Ley, Bingyu Zhao, Vittorio Venturi, Dale A. Pelletier, Julia A. Vorholt, Susannah G. Tringe, Tanja Woyke, Jeffery L. Dangl

Integrative Microbiomics

Research output: Contribution to journal › Article › peer-review

377 Scopus citations

Abstract

Plants intimately associate with diverse bacteria. Plant-associated bacteria have ostensibly evolved genes that enable them to adapt to plant environments. However, the identities of such genes are mostly unknown, and their functions are poorly characterized. We sequenced 484 genomes of bacterial isolates from roots of Brassicaceae, poplar, and maize. We then compared 3,837 bacterial genomes to identify thousands of plant-associated gene clusters. Genomes of plant-associated bacteria encode more carbohydrate metabolism functions and fewer mobile elements than related non-plant-associated genomes do. We experimentally validated candidates from two sets of plant-associated genes: one involved in plant colonization, and the other serving in microbe-microbe competition between plant-associated bacteria. We also identified 64 plant-associated protein domains that potentially mimic plant domains; some are shared with plant-associated fungi and oomycetes. This work expands the genome-based understanding of plant-microbe interactions and provides potential leads for efficient and sustainable agriculture through microbiome engineering.

Original language	English
Pages (from-to)	138-150
Number of pages	13
Journal	Nature Genetics
Volume	50
Issue number	1
DOIs	https://doi.org/10.1038/s41588-017-0012-9
State	Published - Jan 1 2018

Funding

The work conducted by the US Department of Energy Joint Genome Institute, a DOE Office of Science User Facility, is supported by the Office of Science of the US Department of Energy under contract no. DE-AC02-05CH11231. J.L.D. and S.G.T. were supported by NSF INSPIRE grant IOS-1343020, and J.L.D. was also supported by DOE–USDA Feedstock Award DE-SC001043 and by the Office of Science (BER), US Department of Energy, grant no. DE-SC0014395. S.H.P. was supported by NIH Training Grant T32 GM067553-06 and was a Howard Hughes Medical Institute (HHMI) International Student Research Fellow. D.S.L. was supported by NIH Training Grant T32 GM07092-34. J.L.D. is an Investigator of the HHMI, supported by the HHMI and the Gordon and Betty Moore Foundation (GBMF3030). M.E.F. was supported by NIH Dr. Ruth L. Kirschstein NRSA Fellowship F32-GM112345. D.A.P. and T.-Y.L. were supported by the Genomic Science Program, US Department of Energy, Office of Science, Biological and Environmental Research as part of the Oak Ridge National Laboratory Plant Microbe Interfaces Scientific Focus Area (http://pmi.ornl.gov) and Plant Feedstock Genomics Award DE-SC001043. Oak Ridge National Laboratory is managed by UT-Battelle, LLC, for the US Department of Energy under contract DE-AC05-00OR22725. J.A.V. was supported by a SystemsX.ch grant (Micro2X) and a European Research Council (ERC) advanced grant (PhyMo). We thank I. Bertani, C. Bez, R. Bowers, D. Burstein, A. Chun Chen, D. Chiniquy, B. Cole, O. Cohen, A. Copeland, J. Eisen, E. Eloe-Fadrosh, M. Hadjithomas, O. Finkel, H. Schnitzel Meule Fux, N. Ivanova, J. Knelman, R. Malmstrom, R. Perez-Torres, D. Salomon, R. Sorek, T. Mucyn, R. Seshadri, T.K. Reddy, L. Ryan, and H. Sberro Livnat for general help, text editing, and ideas for this work. We thank R. Walcott (University of Georgia, Athens, GA, USA) for providing the Acidovorax citrulli VasD mutant strain.

UN SDGs

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Levy, A., Salas Gonzalez, I., Mittelviefhaus, M., Clingenpeel, S., Herrera Paredes, S., Miao, J., Wang, K., Devescovi, G., Stillman, K., Monteiro, F., Rangel Alvarez, B., Lundberg, D. S., Lu, T. Y., Lebeis, S., Jin, Z., McDonald, M., Klein, A. P., Feltcher, M. E., Rio, T. G., ... Dangl, J. L. (2018). Genomic features of bacterial adaptation to plants. Nature Genetics, 50(1), 138-150. https://doi.org/10.1038/s41588-017-0012-9

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title = "Genomic features of bacterial adaptation to plants",

abstract = "Plants intimately associate with diverse bacteria. Plant-associated bacteria have ostensibly evolved genes that enable them to adapt to plant environments. However, the identities of such genes are mostly unknown, and their functions are poorly characterized. We sequenced 484 genomes of bacterial isolates from roots of Brassicaceae, poplar, and maize. We then compared 3,837 bacterial genomes to identify thousands of plant-associated gene clusters. Genomes of plant-associated bacteria encode more carbohydrate metabolism functions and fewer mobile elements than related non-plant-associated genomes do. We experimentally validated candidates from two sets of plant-associated genes: one involved in plant colonization, and the other serving in microbe-microbe competition between plant-associated bacteria. We also identified 64 plant-associated protein domains that potentially mimic plant domains; some are shared with plant-associated fungi and oomycetes. This work expands the genome-based understanding of plant-microbe interactions and provides potential leads for efficient and sustainable agriculture through microbiome engineering.",

author = "Asaf Levy and {Salas Gonzalez}, Isai and Maximilian Mittelviefhaus and Scott Clingenpeel and {Herrera Paredes}, Sur and Jiamin Miao and Kunru Wang and Giulia Devescovi and Kyra Stillman and Freddy Monteiro and {Rangel Alvarez}, Bryan and Lundberg, {Derek S.} and Lu, {Tse Yuan} and Sarah Lebeis and Zhao Jin and Meredith McDonald and Klein, {Andrew P.} and Feltcher, {Meghan E.} and Rio, {Tijana Glavina} and Grant, {Sarah R.} and Doty, {Sharon L.} and Ley, {Ruth E.} and Bingyu Zhao and Vittorio Venturi and Pelletier, {Dale A.} and Vorholt, {Julia A.} and Tringe, {Susannah G.} and Tanja Woyke and Dangl, {Jeffery L.}",

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doi = "10.1038/s41588-017-0012-9",

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Levy, A, Salas Gonzalez, I, Mittelviefhaus, M, Clingenpeel, S, Herrera Paredes, S, Miao, J, Wang, K, Devescovi, G, Stillman, K, Monteiro, F, Rangel Alvarez, B, Lundberg, DS, Lu, TY, Lebeis, S, Jin, Z, McDonald, M, Klein, AP, Feltcher, ME, Rio, TG, Grant, SR, Doty, SL, Ley, RE, Zhao, B, Venturi, V, Pelletier, DA, Vorholt, JA, Tringe, SG, Woyke, T & Dangl, JL 2018, 'Genomic features of bacterial adaptation to plants', Nature Genetics, vol. 50, no. 1, pp. 138-150. https://doi.org/10.1038/s41588-017-0012-9

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T1 - Genomic features of bacterial adaptation to plants

AU - Levy, Asaf

AU - Salas Gonzalez, Isai

AU - Mittelviefhaus, Maximilian

AU - Clingenpeel, Scott

AU - Herrera Paredes, Sur

AU - Miao, Jiamin

AU - Wang, Kunru

AU - Devescovi, Giulia

AU - Stillman, Kyra

AU - Monteiro, Freddy

AU - Rangel Alvarez, Bryan

AU - Lundberg, Derek S.

AU - Lu, Tse Yuan

AU - Lebeis, Sarah

AU - Jin, Zhao

AU - McDonald, Meredith

AU - Klein, Andrew P.

AU - Feltcher, Meghan E.

AU - Rio, Tijana Glavina

AU - Grant, Sarah R.

AU - Doty, Sharon L.

AU - Ley, Ruth E.

AU - Zhao, Bingyu

AU - Venturi, Vittorio

AU - Pelletier, Dale A.

AU - Vorholt, Julia A.

AU - Tringe, Susannah G.

AU - Woyke, Tanja

AU - Dangl, Jeffery L.

PY - 2018/1/1

Y1 - 2018/1/1

N2 - Plants intimately associate with diverse bacteria. Plant-associated bacteria have ostensibly evolved genes that enable them to adapt to plant environments. However, the identities of such genes are mostly unknown, and their functions are poorly characterized. We sequenced 484 genomes of bacterial isolates from roots of Brassicaceae, poplar, and maize. We then compared 3,837 bacterial genomes to identify thousands of plant-associated gene clusters. Genomes of plant-associated bacteria encode more carbohydrate metabolism functions and fewer mobile elements than related non-plant-associated genomes do. We experimentally validated candidates from two sets of plant-associated genes: one involved in plant colonization, and the other serving in microbe-microbe competition between plant-associated bacteria. We also identified 64 plant-associated protein domains that potentially mimic plant domains; some are shared with plant-associated fungi and oomycetes. This work expands the genome-based understanding of plant-microbe interactions and provides potential leads for efficient and sustainable agriculture through microbiome engineering.

AB - Plants intimately associate with diverse bacteria. Plant-associated bacteria have ostensibly evolved genes that enable them to adapt to plant environments. However, the identities of such genes are mostly unknown, and their functions are poorly characterized. We sequenced 484 genomes of bacterial isolates from roots of Brassicaceae, poplar, and maize. We then compared 3,837 bacterial genomes to identify thousands of plant-associated gene clusters. Genomes of plant-associated bacteria encode more carbohydrate metabolism functions and fewer mobile elements than related non-plant-associated genomes do. We experimentally validated candidates from two sets of plant-associated genes: one involved in plant colonization, and the other serving in microbe-microbe competition between plant-associated bacteria. We also identified 64 plant-associated protein domains that potentially mimic plant domains; some are shared with plant-associated fungi and oomycetes. This work expands the genome-based understanding of plant-microbe interactions and provides potential leads for efficient and sustainable agriculture through microbiome engineering.

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U2 - 10.1038/s41588-017-0012-9

DO - 10.1038/s41588-017-0012-9

M3 - Article

C2 - 29255260

AN - SCOPUS:85038392797

SN - 1061-4036

VL - 50

SP - 138

EP - 150

JO - Nature Genetics

JF - Nature Genetics

IS - 1

ER -

Genomic features of bacterial adaptation to plants

Abstract

Funding

UN SDGs

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