Genomic features of bacterial adaptation to plants

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

doi:10.1038/s41588-017-0012-9

Title: Genomic features of bacterial adaptation to plants

Journal Article · Mon Dec 18 00:00:00 EST 2017 · Nature Genetics

DOI:https://doi.org/10.1038/s41588-017-0012-9· OSTI ID:1415202

^[1]; Salas Gonzalez, Isai ^[2]; Mittelviefhaus, Maximilian ^[3];

^[1];

^[4]; Miao, Jiamin ^[5]; Wang, Kunru ^[6]; Devescovi, Giulia ^[7]; Stillman, Kyra ^[1]; Monteiro, Freddy ^[2]; Rangel Alvarez, Bryan ^[1]; Lundberg, Derek S. ^[2]; Lu, Tse-Yuan ^[8]; Lebeis, Sarah ^[9]; Jin, Zhao ^[10]; McDonald, Meredith ^[2]; Klein, Andrew P. ^[2]; Feltcher, Meghan E. ^[11]; Rio, Tijana Glavina ^[1];

^[12] more »

USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Univ. of North Carolina, Chapel Hill, NC (United States). Department of Biology; Howard Hughes Medical Institute, Chevy Chase, MD (United States)
Institute of Microbiology, ETH Zurich (Switzerland)
Univ. of North Carolina, Chapel Hill, NC (United States). Department of Biology; Howard Hughes Medical Institute, Chevy Chase, MD (United States); Stanford Univ., CA (United States). Department of Biology
Virginia Tech, Blacksburg, VA (United States). Department of Horticulture; Gansu Agricultural University (China). The Grassland College
Virginia Tech, Blacksburg, VA (United States). Department of Horticulture
International Centre for Genetic Engineering and Biotechnology, Trieste (Italy)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division
Univ. of Tennessee, Knoxville, TN (United States). Department of Microbiology
Cornell Univ., Ithaca, NY (United States). Department of Molecular Biology and Genetics
Univ. of North Carolina, Chapel Hill, NC (United States). Department of Biology; Howard Hughes Medical Institute, Chevy Chase, MD (United States); BD Technologies and Innovation, Research Triangle Park, NC (United States)
Univ. of North Carolina, Chapel Hill, NC (United States). Department of Biology
Univ. of Washington, Seattle, WA (United States). School of Environmental and Forest Sciences
Max Planck Institute for Developmental Biology, Tubingen (Germany)
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); University of California, Merced, CA (United States)
Univ. of North Carolina, Chapel Hill, NC (United States). Department of Biology, The Carolina Center for Genome Sciences and Department of Microbiology and Immunology; Howard Hughes Medical Institute, Chevy Chase, MD (United States)

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.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23), Biological Systems Science Division (SC-23.2 )

Grant/Contract Number:: AC05-00OR22725; AC02-05CH11231; SC0010423; SC0014395

OSTI ID:: 1415202

Alternate ID(s):: OSTI ID: 1529504; OSTI ID: 1571092

Journal Information:: Nature Genetics, Vol. 50, Issue 1; ISSN 1061-4036

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 275 works

Citation information provided by
Web of Science

References (101)

Conserved Fungal LysM Effector Ecp6 Prevents Chitin-Triggered Immunity in Plants de Jonge, R.; Peter van Esse, H.; Kombrink, A. Science, Vol. 329, Issue 5994 https://doi.org/10.1126/science.1190859	journal	August 2010
60Ma of legume nodulation. What's new? What's changing? Sprent, J. I. Journal of Experimental Botany, Vol. 59, Issue 5 https://doi.org/10.1093/jxb/erm286	journal	February 2008
Structural mimicry in bacterial virulence Stebbins, C. Erec; Galán, Jorge E. Nature, Vol. 412, Issue 6848 https://doi.org/10.1038/35089000	journal	August 2001
The standard operating procedure of the DOE-JGI Microbial Genome Annotation Pipeline (MGAP v.4) Huntemann, Marcel; Ivanova, Natalia N.; Mavromatis, Konstantinos Standards in Genomic Sciences, Vol. 10, Issue 1 https://doi.org/10.1186/s40793-015-0077-y	journal	October 2015
Genome-Wide RNA Sequencing Analysis of Quorum Sensing-Controlled Regulons in the Plant-Associated Burkholderia glumae PG1 Strain Gao, Rong; Krysciak, Dagmar; Petersen, Katrin Applied and Environmental Microbiology, Vol. 81, Issue 23 https://doi.org/10.1128/AEM.01043-15	journal	September 2015
AvrACXcc8004, a Type III Effector with a Leucine-Rich Repeat Domain from Xanthomonas campestris Pathovar campestris Confers Avirulence in Vascular Tissues of Arabidopsis thaliana Ecotype Col-0 Xu, R. -Q.; Blanvillain, S.; Feng, J. -X. Journal of Bacteriology, Vol. 190, Issue 1 https://doi.org/10.1128/JB.00978-07	journal	October 2007
Structure, variation, and assembly of the root-associated microbiomes of rice Edwards, Joseph; Johnson, Cameron; Santos-Medellín, Christian Proceedings of the National Academy of Sciences, Vol. 112, Issue 8 https://doi.org/10.1073/pnas.1414592112	journal	January 2015
Key physiological properties contributing to rhizosphere adaptation and plant growth promotion abilities of Azospirillum brasilense Fibach-Paldi, Sharon; Burdman, Saul; Okon, Yaacov FEMS Microbiology Letters, Vol. 326, Issue 2 https://doi.org/10.1111/j.1574-6968.2011.02407.x	journal	October 2011
Lectin-Mediated Resistance Impairs Plant Virus Infection at the Cellular Level Yamaji, Yasuyuki; Maejima, Kensaku; Komatsu, Ken The Plant Cell, Vol. 24, Issue 2 https://doi.org/10.1105/tpc.111.093658	journal	February 2012
Evolution of Mammals and Their Gut Microbes Ley, R. E.; Hamady, M.; Lozupone, C. Science, Vol. 320, Issue 5883 https://doi.org/10.1126/science.1155725	journal	June 2008
Surfactant Protein D Binds Selectively to Klebsiella pneumoniae Lipopolysaccharides Containing Mannose-Rich O-Antigens Sahly, Hany; Ofek, Itzhak; Podschun, Rainer The Journal of Immunology, Vol. 169, Issue 6 https://doi.org/10.4049/jimmunol.169.6.3267	journal	September 2002
Pseudomonas fluorescens Induces Strain-Dependent and Strain-Independent Host Plant Responses in Defense Networks, Primary Metabolism, Photosynthesis, and Fitness Weston, David J.; Pelletier, Dale A.; Morrell-Falvey, Jennifer L. Molecular Plant-Microbe Interactions, Vol. 25, Issue 6 https://doi.org/10.1094/MPMI-09-11-0253	journal	June 2012
Elucidation of gibberellin biosynthesis in bacteria reveals convergent evolution Nett, Ryan S.; Montanares, Mariana; Marcassa, Ariana Nature Chemical Biology, Vol. 13, Issue 1 https://doi.org/10.1038/nchembio.2232	journal	November 2016
Type III Protein Secretion Systems in Bacterial Pathogens of Animals and Plants Hueck, Christoph J. Microbiology and Molecular Biology Reviews, Vol. 62, Issue 2 https://doi.org/10.1128/MMBR.62.2.379-433.1998	journal	June 1998
Rhizobium-legume nodulation: Life together in the underground Long, Sharon R. Cell, Vol. 56, Issue 2 https://doi.org/10.1016/0092-8674(89)90893-3	journal	January 1989
A jacalin-related lectin-like gene in wheat is a component of the plant defence system Xiang, Yang; Song, Min; Wei, Zhaoyan Journal of Experimental Botany, Vol. 62, Issue 15 https://doi.org/10.1093/jxb/err226	journal	August 2011
Polarized Defense Against Fungal Pathogens Is Mediated by the Jacalin-Related Lectin Domain of Modular Poaceae -Specific Proteins Weidenbach, Denise; Esch, Lara; Möller, Claudia Molecular Plant, Vol. 9, Issue 4 https://doi.org/10.1016/j.molp.2015.12.009	journal	April 2016
Mannan-binding lectin?a soluble pattern recognition molecule Gadjeva, M. Molecular Immunology, Vol. 41, Issue 2-3 https://doi.org/10.1016/j.molimm.2004.03.015	journal	June 2004
AmphoraNet: The webserver implementation of the AMPHORA2 metagenomic workflow suite Kerepesi, Csaba; Bánky, Dániel; Grolmusz, Vince Gene, Vol. 533, Issue 2 https://doi.org/10.1016/j.gene.2013.10.015	journal	January 2014
Integration of decoy domains derived from protein targets of pathogen effectors into plant immune receptors is widespread Kroj, Thomas; Chanclud, Emilie; Michel-Romiti, Corinne New Phytologist, Vol. 210, Issue 2 https://doi.org/10.1111/nph.13869	journal	February 2016
Microbial species delineation using whole genome sequences Varghese, Neha J.; Mukherjee, Supratim; Ivanova, Natalia Nucleic Acids Research, Vol. 43, Issue 14 https://doi.org/10.1093/nar/gkv657	journal	July 2015
Functional domains and motifs of bacterial type III effector proteins and their roles in infection Dean, Paul FEMS Microbiology Reviews, Vol. 35, Issue 6 https://doi.org/10.1111/j.1574-6976.2011.00271.x	journal	November 2011
CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes Parks, Donovan H.; Imelfort, Michael; Skennerton, Connor T. Genome Research, Vol. 25, Issue 7 https://doi.org/10.1101/gr.186072.114	journal	May 2015
The COG database: a tool for genome-scale analysis of protein functions and evolution Tatusov, R. L. Nucleic Acids Research, Vol. 28, Issue 1 https://doi.org/10.1093/nar/28.1.33	journal	January 2000
Fast and sensitive protein alignment using DIAMOND Buchfink, Benjamin; Xie, Chao; Huson, Daniel H. Nature Methods, Vol. 12, Issue 1 https://doi.org/10.1038/nmeth.3176	journal	November 2014
Bacterial pathogenesis of plants: future challenges from a microbial perspective: Challenges in Bacterial Molecular Plant Pathology Pfeilmeier, Sebastian; Caly, Delphine L.; Malone, Jacob G. Molecular Plant Pathology, Vol. 17, Issue 8 https://doi.org/10.1111/mpp.12427	journal	August 2016
Microbiota and Host Nutrition across Plant and Animal Kingdoms Gail, Ackermann,; Antonio, González,; Paul, Schulze-Lefert, The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/jekh-8p11	text	January 2015
Genome-Scale Identification of Legionella pneumophila Effectors Using a Machine Learning Approach Burstein, David; Zusman, Tal; Degtyar, Elena PLoS Pathogens, Vol. 5, Issue 7 https://doi.org/10.1371/journal.ppat.1000508	journal	July 2009
KEGG as a reference resource for gene and protein annotation Kanehisa, Minoru; Sato, Yoko; Kawashima, Masayuki Nucleic Acids Research, Vol. 44, Issue D1 https://doi.org/10.1093/nar/gkv1070	journal	October 2015
Global abundance of microbial rhodopsins Finkel, Omri M.; Béjà, Oded; Belkin, Shimshon The ISME Journal, Vol. 7, Issue 2 https://doi.org/10.1038/ismej.2012.112	journal	October 2012
Defining the core Arabidopsis thaliana root microbiome E., Ley, Ruth; Julien, Tremblay,; L., Dangl, Jeffery The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/w03e-5q36	text	January 2012
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
MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform Katoh, K. Nucleic Acids Research, Vol. 30, Issue 14 https://doi.org/10.1093/nar/gkf436	journal	July 2002
The TIGRFAMs database of protein families Haft, D. H. Nucleic Acids Research, Vol. 31, Issue 1 https://doi.org/10.1093/nar/gkg128	journal	January 2003
The Pfam protein families database: towards a more sustainable future Finn, Robert D.; Coggill, Penelope; Eberhardt, Ruth Y. Nucleic Acids Research, Vol. 44, Issue D1 https://doi.org/10.1093/nar/gkv1344	journal	December 2015
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
Comparative analysis of plant immune receptor architectures uncovers host proteins likely targeted by pathogens Sarris, Panagiotis F.; Cevik, Volkan; Dagdas, Gulay BMC Biology, Vol. 14, Issue 1 https://doi.org/10.1186/s12915-016-0228-7	journal	February 2016
60 Ma of legume nodulation? What's new? What's changing? Sprent, J. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, Vol. 146, Issue 4 https://doi.org/10.1016/j.cbpa.2007.01.468	journal	April 2007
Lipopolysaccharide of the Gram-Negative Cell Wall: Biosynthesis of a complex heteropolysaccharide occurs by successive addition of specific sugar residues Osborn, M. J.; Rosen, S. M.; Rothfield, L. Science, Vol. 145, Issue 3634 https://doi.org/10.1126/science.145.3634.783	journal	August 1964
Niche and host-associated functional signatures of the root surface microbiome Ofek-Lalzar, Maya; Sela, Noa; Goldman-Voronov, Milana Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms5950	journal	September 2014
Phylogeny of the class Actinobacteria revisited in the light of complete genomes. The orders 'Frankiales' and Micrococcales should be split into coherent entities: proposal of Frankiales ord. nov., Geodermatophilales ord. nov., Acidothermales ord. nov. and Nakamurellales ord. nov. Sen, A.; Daubin, V.; Abrouk, D. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 64, Issue Pt 11 https://doi.org/10.1099/ijs.0.063966-0	journal	August 2014
Native root-associated bacteria rescue a plant from a sudden-wilt disease that emerged during continuous cropping Santhanam, Rakesh; Luu, Van Thi; Weinhold, Arne Proceedings of the National Academy of Sciences, Vol. 112, Issue 36 https://doi.org/10.1073/pnas.1505765112	journal	August 2015
A plant flavone, luteolin, induces expression of Rhizobium meliloti nodulation genes Peters, N.; Frost, J.; Long, S. Science, Vol. 233, Issue 4767 https://doi.org/10.1126/science.3738520	journal	August 1986
A Rapid Bootstrap Algorithm for the RAxML Web Servers Stamatakis, Alexandros; Hoover, Paul; Rougemont, Jacques Systematic Biology, Vol. 57, Issue 5 https://doi.org/10.1080/10635150802429642	journal	October 2008
Average genome size: a potential source of bias in comparative metagenomics Beszteri, Bánk; Temperton, Ben; Frickenhaus, Stephan The ISME Journal, Vol. 4, Issue 8 https://doi.org/10.1038/ismej.2010.29	journal	March 2010
HMMER web server: 2015 update Finn, Robert D.; Clements, Jody; Arndt, William Nucleic Acids Research, Vol. 43, Issue W1 https://doi.org/10.1093/nar/gkv397	journal	May 2015
Activation of Ran GTPase by a Legionella Effector Promotes Microtubule Polymerization, Pathogen Vacuole Motility and Infection Rothmeier, Eva; Pfaffinger, Gudrun; Hoffmann, Christine PLoS Pathogens, Vol. 9, Issue 9 https://doi.org/10.1371/journal.ppat.1003598	journal	September 2013
Insights into the phylogeny and coding potential of microbial dark matter Rinke, Christian; Schwientek, Patrick; Sczyrba, Alexander Nature, Vol. 499, Issue 7459 https://doi.org/10.1038/nature12352	journal	July 2013
Plant compartment and biogeography affect microbiome composition in cultivated and native Agave species Coleman-Derr, Devin; Desgarennes, Damaris; Fonseca-Garcia, Citlali New Phytologist, Vol. 209, Issue 2 https://doi.org/10.1111/nph.13697	journal	October 2015
A Complete Set of Flagellar Genes Acquired by Horizontal Transfer Coexists with the Endogenous Flagellar System in Rhodobacter sphaeroides Poggio, S.; Abreu-Goodger, C.; Fabela, S. Journal of Bacteriology, Vol. 189, Issue 8 https://doi.org/10.1128/JB.01681-06	journal	February 2007
Structure and Functions of the Bacterial Microbiota of Plants Bulgarelli, Davide; Schlaeppi, Klaus; Spaepen, Stijn Annual Review of Plant Biology, Vol. 64, Issue 1 https://doi.org/10.1146/annurev-arplant-050312-120106	journal	April 2013
Flagella of a plant-growth-stimulating Pseudomonas fluorescens strain are required for colonization of potato roots. De Weger, L. A.; van der Vlugt, C. I.; Wijfjes, A. H. Journal of Bacteriology, Vol. 169, Issue 6 https://doi.org/10.1128/jb.169.6.2769-2773.1987	journal	June 1987
Independently Evolved Virulence Effectors Converge onto Hubs in a Plant Immune System Network Mukhtar, M. S.; Carvunis, A. -R.; Dreze, M. Science, Vol. 333, Issue 6042 https://doi.org/10.1126/science.1203659	journal	July 2011
Distinct Microbial Communities within the Endosphere and Rhizosphere of Populus deltoides Roots across Contrasting Soil Types Gottel, Neil R.; Castro, Hector F.; Kerley, Marilyn Applied and Environmental Microbiology, Vol. 77, Issue 17 https://doi.org/10.1128/AEM.05255-11	journal	July 2011
Polinton-like viruses are abundant in aquatic ecosystems Bellas, Christopher M.; Sommaruga, Ruben Microbiome, Vol. 9, Issue 1 https://doi.org/10.1186/s40168-020-00956-0	journal	January 2021
Integrating biogeochemistry with multiomic sequence information in a model oxygen minimum zone Louca, Stilianos; Hawley, Alyse K.; Katsev, Sergei Proceedings of the National Academy of Sciences, Vol. 113, Issue 40 https://doi.org/10.1073/pnas.1602897113	journal	September 2016
The Hidden World within Plants: Ecological and Evolutionary Considerations for Defining Functioning of Microbial Endophytes Hardoim, Pablo R.; van Overbeek, Leonard S.; Berg, Gabriele Microbiology and Molecular Biology Reviews, Vol. 79, Issue 3 https://doi.org/10.1128/MMBR.00050-14	journal	July 2015
Directed transposon Tn5 mutagenesis and complementation analysis of rhizobium meliloti symbiotic nitrogen fixation genes Ruvkun, Gary B.; Sundaresan, Venkatesan; Ausubel, Frederick M. Cell, Vol. 29, Issue 2 https://doi.org/10.1016/0092-8674(82)90171-4	journal	June 1982
PNAS Plus: From the Cover: Microbial biogeography of wine grapes is conditioned by cultivar, vintage, and climate Bokulich, N. A.; Thorngate, J. H.; Richardson, P. M. Proceedings of the National Academy of Sciences, Vol. 111, Issue 1 https://doi.org/10.1073/pnas.1317377110	journal	November 2013
To sialylate, or not to sialylate: that is the question Vimr, Eric; Lichtensteiger, Carol Trends in Microbiology, Vol. 10, Issue 6 https://doi.org/10.1016/S0966-842X(02)02361-2	journal	June 2002
Molecular Mimicry by an F-Box Effector of Legionella pneumophila Hijacks a Conserved Polyubiquitination Machinery within Macrophages and Protozoa Price, Christopher T.; Al-Khodor, Souhaila; Al-Quadan, Tasneem PLoS Pathogens, Vol. 5, Issue 12 https://doi.org/10.1371/journal.ppat.1000704	journal	December 2009
Ralstonia solanacearum Needs Motility for Invasive Virulence on Tomato Tans-Kersten, J.; Huang, H.; Allen, C. Journal of Bacteriology, Vol. 183, Issue 12 https://doi.org/10.1128/JB.183.12.3597-3605.2001	journal	June 2001
Microbiota and Host Nutrition across Plant and Animal Kingdoms Hacquard, Stéphane; Garrido-Oter, Ruben; González, Antonio Cell Host & Microbe, Vol. 17, Issue 5 https://doi.org/10.1016/j.chom.2015.04.009	journal	May 2015
Unexpected Diversity during Community Succession in the Apple Flower Microbiome Shade, Ashley; McManus, Patricia S.; Handelsman, Jo mBio, Vol. 4, Issue 2 https://doi.org/10.1128/mBio.00602-12	journal	February 2013
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
Overexpression of a wheat jasmonate-regulated lectin increases pathogen resistance Ma, Qing-Hu; Tian, Bing; Li, Yun-Liang Biochimie, Vol. 92, Issue 2 https://doi.org/10.1016/j.biochi.2009.11.008	journal	February 2010
A Phylum-Level Bacterial Phylogenetic Marker Database Wang, Zhang; Wu, Martin Molecular Biology and Evolution, Vol. 30, Issue 6 https://doi.org/10.1093/molbev/mst059	journal	March 2013
Search and clustering orders of magnitude faster than BLAST Edgar, Robert C. Bioinformatics, Vol. 26, Issue 19, p. 2460-2461 https://doi.org/10.1093/bioinformatics/btq461	journal	August 2010
Chemotaxis signaling systems in model beneficial plant–bacteria associations Scharf, Birgit E.; Hynes, Michael F.; Alexandre, Gladys M. Plant Molecular Biology, Vol. 90, Issue 6 https://doi.org/10.1007/s11103-016-0432-4	journal	January 2016
Independently Evolved Virulence Effectors Converge onto Hubs in a Plant Immune System Network P., Roth, F.; J., Harbort, C.; M., Vidal, The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/yzgx-2t78	text	January 2011
A novel conserved mechanism for plant NLR protein pairs: the â€œintegrated decoyâ€ hypothesis Cesari, Stella; Bernoux, Maud; Moncuquet, Philippe Frontiers in Plant Science, Vol. 5 https://doi.org/10.3389/fpls.2014.00606	journal	November 2014
Plant-Influenced Gene Expression in the Rice Endophyte Burkholderia kururiensis M130 Coutinho, Bruna G.; Licastro, Danilo; Mendonça-Previato, Lucia Molecular Plant-Microbe Interactions, Vol. 28, Issue 1 https://doi.org/10.1094/MPMI-07-14-0225-R	journal	January 2015
Flagella-Driven Chemotaxis Towards Exudate Components Is an Important Trait for Tomato Root Colonization by Pseudomonas fluorescens de Weert, Sandra; Vermeiren, Hans; Mulders, Ine H. M. Molecular Plant-Microbe Interactions, Vol. 15, Issue 11 https://doi.org/10.1094/MPMI.2002.15.11.1173	journal	November 2002
Type III Protein Secretion in Plant Pathogenic Bacteria Büttner, Daniela; He, Sheng Yang Plant Physiology, Vol. 150, Issue 4 https://doi.org/10.1104/pp.109.139089	journal	May 2009
Biology of Bacteriocyte-Associated Endosymbionts of Plant Sap-Sucking Insects Baumann, Paul Annual Review of Microbiology, Vol. 59, Issue 1 https://doi.org/10.1146/annurev.micro.59.030804.121041	journal	October 2005
IMG-ABC: A Knowledge Base To Fuel Discovery of Biosynthetic Gene Clusters and Novel Secondary Metabolites Hadjithomas, Michalis; Chen, I-Min Amy; Chu, Ken mBio, Vol. 6, Issue 4 https://doi.org/10.1128/mBio.00932-15	journal	July 2015
A View to a Kill: The Bacterial Type VI Secretion System Ho, Brian T.; Dong, Tao G.; Mekalanos, John J. Cell Host & Microbe, Vol. 15, Issue 1 https://doi.org/10.1016/j.chom.2013.11.008	journal	January 2014
Biocontrol mechanism by root-associated Bacillus amyloliquefaciens FZB42 – a review Chowdhury, Soumitra Paul; Hartmann, Anton; Gao, XueWen Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00780	journal	July 2015
Structure and Function of the Bacterial Root Microbiota in Wild and Domesticated Barley Bulgarelli, Davide; Garrido-Oter, Ruben; Münch, Philipp C. Cell Host & Microbe, Vol. 17, Issue 3 https://doi.org/10.1016/j.chom.2015.01.011	journal	March 2015
Swimming and twitching motility are essential for attachment and virulence of Pantoea ananatis in onion seedlings : Motility affects pathogenicity of Weller-Stuart, Tania; Toth, Ian; De Maayer, Pieter Molecular Plant Pathology, Vol. 18, Issue 5 https://doi.org/10.1111/mpp.12432	journal	July 2016
Tit-for-Tat: Type VI Secretion System Counterattack during Bacterial Cell-Cell Interactions Basler, Marek; Ho, Brian T.; Mekalanos, John J. Cell, Vol. 152, Issue 4 https://doi.org/10.1016/j.cell.2013.01.042	journal	February 2013
The type VI protein secretion system contributes to biofilm formation and seed-to-seedling transmission of Acidovorax citrulli on melon : T6SS contributes to biofilm formation and seed-to-seedling transmission of Tian, Yanli; Zhao, Yuqiang; Wu, Xinrong Molecular Plant Pathology, Vol. 16, Issue 1 https://doi.org/10.1111/mpp.12159	journal	July 2014
Pectate lyase PelI of Erwinia chrysanthemi 3937 belongs to a new family. Shevchik, V. E.; Robert-Baudouy, J.; Hugouvieux-Cotte-Pattat, N. Journal of Bacteriology, Vol. 179, Issue 23 https://doi.org/10.1128/jb.179.23.7321-7330.1997	journal	December 1997
Functional Conservation of the Capacity for ent-Kaurene Biosynthesis and an Associated Operon in Certain Rhizobia Hershey, D. M.; Lu, X.; Zi, J. Journal of Bacteriology, Vol. 196, Issue 1 https://doi.org/10.1128/JB.01031-13	journal	October 2013
A Receptor Pair with an Integrated Decoy Converts Pathogen Disabling of Transcription Factors to Immunity Le Roux, Clémentine; Huet, Gaëlle; Jauneau, Alain Cell, Vol. 161, Issue 5 https://doi.org/10.1016/j.cell.2015.04.025	journal	May 2015
Functional overlap of the Arabidopsis leaf and root microbiota Bai, Yang; Müller, Daniel B.; Srinivas, Girish Nature, Vol. 528, Issue 7582 https://doi.org/10.1038/nature16192	journal	December 2015
Microbial Hub Taxa Link Host and Abiotic Factors to Plant Microbiome Variation Agler, Matthew T.; Ruhe, Jonas; Kroll, Samuel PLOS Biology, Vol. 14, Issue 1 https://doi.org/10.1371/journal.pbio.1002352	journal	January 2016
A Plant Immune Receptor Detects Pathogen Effectors that Target WRKY Transcription Factors Sarris, Panagiotis F.; Duxbury, Zane; Huh, Sung Un Cell, Vol. 161, Issue 5 https://doi.org/10.1016/j.cell.2015.04.024	journal	May 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
Phylogenetic Logistic Regression for Binary Dependent Variables Ives, Anthony R.; Garland, Theodore Systematic Biology, Vol. 59, Issue 1 https://doi.org/10.1093/sysbio/syp074	journal	November 2009
The Vibrio cholerae type VI secretion system displays antimicrobial properties MacIntyre, D. L.; Miyata, S. T.; Kitaoka, M. Proceedings of the National Academy of Sciences, Vol. 107, Issue 45 https://doi.org/10.1073/pnas.1012931107	journal	October 2010
Diversity and heritability of the maize rhizosphere microbiome under field conditions Z., Jin,; S., Buckler, E.; O., Koren, The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/rzga-0c56	text	January 2013
Diversity and heritability of the maize rhizosphere microbiome under field conditions Peiffer, J. A.; Spor, A.; Koren, O. Proceedings of the National Academy of Sciences, Vol. 110, Issue 16 https://doi.org/10.1073/pnas.1302837110	journal	April 2013
Diazotrophic endophytes of native black cottonwood and willow Doty, Sharon L.; Oakley, Brian; Xin, Gang Symbiosis, Vol. 47, Issue 1 https://doi.org/10.1007/BF03179967	journal	February 2009
The pKNOCK Series of Broad-Host-Range Mobilizable Suicide Vectors for Gene Knockout and Targeted DNA Insertion into the Chromosome of Gram-Negative Bacteria Alexeyev, Mikhail F. BioTechniques, Vol. 26, Issue 5 https://doi.org/10.2144/99265bm05	journal	May 1999
OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy Emms, David M.; Kelly, Steven Genome Biology, Vol. 16, Issue 1 https://doi.org/10.1186/s13059-015-0721-2	journal	August 2015
Rapid scoring of genes in microbial pan-genome-wide association studies with Scoary Brynildsrud, Ola; Bohlin, Jon; Scheffer, Lonneke Genome Biology, Vol. 17, Issue 1 https://doi.org/10.1186/s13059-016-1108-8	journal	November 2016
Genome-wide identification of bacterial plant colonization genes Cole, Benjamin J.; Feltcher, Meghan E.; Waters, Robert J. PLOS Biology, Vol. 15, Issue 9 https://doi.org/10.1371/journal.pbio.2002860	journal	September 2017
DOMAINS REARRANGED METHYLTRANSFERASE3 controls DNA methylation and regulates RNA polymerase V transcript abundance in Arabidopsis Zhong, Xuehua; Hale, Christopher J.; Nguyen, Minh Proceedings of the National Academy of Sciences, Vol. 112, Issue 3 https://doi.org/10.1073/pnas.1423603112	journal	January 2015
Accounting For Alignment Uncertainty in Phylogenomics Wu, Martin; Chatterji, Sourav; Eisen, Jonathan A. PLoS ONE, Vol. 7, Issue 1 https://doi.org/10.1371/journal.pone.0030288	journal	January 2012
FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments Price, Morgan N.; Dehal, Paramvir S.; Arkin, Adam P. PLoS ONE, Vol. 5, Issue 3 https://doi.org/10.1371/journal.pone.0009490	journal	March 2010

Cited By (46)

Genetic and molecular characterization of multicomponent resistance of Pseudomonas against allicin Borlinghaus, Jan; Bolger, Anthony M.; Schier, Christina RWTH Aachen University https://doi.org/10.18154/rwth-2020-04408	text	January 2020
Impact of intercropping on the coupling between soil microbial community structure, activity, and nutrient-use efficiencies Lian, Tengxiang; Mu, Yinghui; Jin, Jian PeerJ, Vol. 7 https://doi.org/10.7717/peerj.6412	journal	January 2019
Exploring the Evolution of Virulence Factors through Bioinformatic Data Mining Doxey, Andrew C.; Mansfield, Michael J.; Lobb, Briallen mSystems, Vol. 4, Issue 3 https://doi.org/10.1128/msystems.00162-19	journal	May 2019
Engineering root microbiomes for healthier crops and soils using beneficial, environmentally safe bacteria Martínez-Hidalgo, Pilar; Maymon, Maskit; Pule-Meulenberg, Flora Canadian Journal of Microbiology, Vol. 65, Issue 2 https://doi.org/10.1139/cjm-2018-0315	journal	February 2019
Evolving together, evolving apart: measuring the fitness of rhizobial bacteria in and out of symbiosis with leguminous plants Burghardt, Liana T. New Phytologist, Vol. 228, Issue 1 https://doi.org/10.1111/nph.16045	journal	August 2019
Defining the Genetic Basis of Plant–Endophytic Bacteria Interactions Pinski, Artur; Betekhtin, Alexander; Hupert-Kocurek, Katarzyna International Journal of Molecular Sciences, Vol. 20, Issue 8 https://doi.org/10.3390/ijms20081947	journal	April 2019
The Parauncinula polyspora Draft Genome Provides Insights into Patterns of Gene Erosion and Genome Expansion in Powdery Mildew Fungi Frantzeskakis, Lamprinos; Németh, Márk Z.; Barsoum, Mirna RWTH Aachen University https://doi.org/10.18154/rwth-2019-08846	text	January 2019
Niche differentiation is spatially and temporally regulated in the rhizosphere Nuccio, Erin E.; Starr, Evan; Karaoz, Ulas The ISME Journal, Vol. 14, Issue 4 https://doi.org/10.1038/s41396-019-0582-x	journal	January 2020
Interdomain ecological networks between plants and microbes Feng, Kai; Zhang, Yuguang; He, Zhili Molecular Ecology Resources, Vol. 19, Issue 6 https://doi.org/10.1111/1755-0998.13081	journal	September 2019
Protective microbiomes can limit the evolution of host pathogen defense Metcalf, C. Jessica E.; Koskella, Britt Evolution Letters, Vol. 3, Issue 5 https://doi.org/10.1002/evl3.140	journal	September 2019
Modeling population heterogeneity from microbial communities to immune response in cells Pecht, Tal; Aschenbrenner, Anna C.; Ulas, Thomas Cellular and Molecular Life Sciences, Vol. 77, Issue 3 https://doi.org/10.1007/s00018-019-03378-w	journal	November 2019
Genomic analyses of Burkholderia cenocepacia reveal multiple species with differential host-adaptation to plants and humans Wallner, Adrian; King, Eoghan; Ngonkeu, Eddy L. M. BMC Genomics, Vol. 20, Issue 1 https://doi.org/10.1186/s12864-019-6186-z	journal	November 2019
Plantibacter flavus , Curtobacterium herbarum , Paenibacillus taichungensis , and Rhizobium selenitireducens Endophytes Provide Host-Specific Growth Promotion of Arabidopsis thaliana , Basil, Lettuce, and Bok Choy Plants Mayer, Evan; Dörr de Quadros, Patricia; Fulthorpe, Roberta Applied and Environmental Microbiology, Vol. 85, Issue 19 https://doi.org/10.1128/aem.00383-19	journal	July 2019
Identification of a novel anthocyanin synthesis pathway in the fungus Aspergillus sydowii H-1 Bu, Congfan; Zhang, Qian; Zeng, Jie BMC Genomics, Vol. 21, Issue 1 https://doi.org/10.1186/s12864-019-6442-2	journal	January 2020
A Third Class: Functional Gibberellin Biosynthetic Operon in Beta-Proteobacteria Nagel, Raimund; Bieber, John E.; Schmidt-Dannert, Mark G. Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.02916	journal	November 2018
Genetic and molecular characterization of multicomponent resistance of Pseudomonas against allicin Borlinghaus, Jan; Bolger, Anthony; Schier, Christina Life Science Alliance, Vol. 3, Issue 5 https://doi.org/10.26508/lsa.202000670	journal	March 2020
Soil microbiomes with distinct assemblies through vertical soil profiles drive the cycling of multiple nutrients in reforested ecosystems Jiao, Shuo; Chen, Weimin; Wang, Jieli Microbiome, Vol. 6, Issue 1 https://doi.org/10.1186/s40168-018-0526-0	journal	August 2018
The effects of soil phosphorus content on plant microbiota are driven by the plant phosphate starvation response Finkel, Omri M.; Salas-González, Isai; Castrillo, Gabriel PLOS Biology, Vol. 17, Issue 11 https://doi.org/10.1371/journal.pbio.3000534	journal	November 2019
Phylogeny-corrected identification of microbial gene families relevant to human gut colonization Bradley, Patrick H.; Nayfach, Stephen; Pollard, Katherine S. PLOS Computational Biology, Vol. 14, Issue 8 https://doi.org/10.1371/journal.pcbi.1006242	journal	August 2018
Antimicrobial peptide expression in a wild tobacco plant reveals the limits of host-microbe-manipulations in the field Weinhold, Arne; Karimi Dorcheh, Elham; Li, Ran eLife, Vol. 7 https://doi.org/10.7554/elife.28715	journal	April 2018
The structure and function of the global citrus rhizosphere microbiome Xu, Jin; Zhang, Yunzeng; Zhang, Pengfan Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-07343-2	journal	November 2018
Challenges and Approaches in Microbiome Research: From Fundamental to Applied Sergaki, Chrysi; Lagunas, Beatriz; Lidbury, Ian Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.01205	journal	August 2018
Are we there yet? The long walk towards the development of efficient symbiotic associations between nitrogen-fixing bacteria and non-leguminous crops Pankievicz, Vânia C. S.; Irving, Thomas B.; Maia, Lucas G. S. BMC Biology, Vol. 17, Issue 1 https://doi.org/10.1186/s12915-019-0710-0	journal	December 2019
Unraveling a Tangled Skein: Evolutionary Analysis of the Bacterial Gibberellin Biosynthetic Operon Nett, Ryan S.; Nguyen, Huy; Nagel, Raimund mSphere, Vol. 5, Issue 3 https://doi.org/10.1128/mSphere.00292-20	journal	June 2020
Host species identity in annual Brassicaceae has a limited effect on the assembly of root-endophytic fungal communities Glynou, Kyriaki; Thines, Marco; Maciá-Vicente, Jose G. Plant Ecology & Diversity, Vol. 11, Issue 5-6 https://doi.org/10.1080/17550874.2018.1504332	journal	September 2018
Abundance, diversity and plant‐specific adaptations of plant‐associated lactic acid bacteria Yu, Annabelle O.; Leveau, Johan H. J.; Marco, Maria L. Environmental Microbiology Reports, Vol. 12, Issue 1 https://doi.org/10.1111/1758-2229.12794	journal	October 2019
Select and resequence reveals relative fitness of bacteria in symbiotic and free-living environments Burghardt, Liana T.; Epstein, Brendan; Guhlin, Joseph Proceedings of the National Academy of Sciences, Vol. 115, Issue 10 https://doi.org/10.1073/pnas.1714246115	journal	February 2018
Nitrogen Fertilizers Shape the Composition and Predicted Functions of the Microbiota of Field-Grown Tomato Plants Caradonia, Federica; Ronga, Domenico; Catellani, Marcello Phytobiomes Journal, Vol. 3, Issue 4 https://doi.org/10.1094/pbiomes-06-19-0028-r	journal	January 2019
Root microbiota assembly and adaptive differentiation among European Arabidopsis populations Thiergart, Thorsten; Durán, Paloma; Ellis, Thomas Nature Ecology & Evolution, Vol. 4, Issue 1 https://doi.org/10.1038/s41559-019-1063-3	journal	December 2019
Genomic, metabolic and phenotypic variability shapes ecological differentiation and intraspecies interactions of Alteromonas macleodii Koch, Hanna; Germscheid, Nora; Freese, Heike M. Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-57526-5	journal	January 2020
Duckweed hosts a taxonomically similar bacterial assemblage as the terrestrial leaf microbiome Acosta, Kenneth; Xu, Jenny; Gilbert, Sarah PLOS ONE, Vol. 15, Issue 2 https://doi.org/10.1371/journal.pone.0228560	journal	February 2020
Genome-wide identification of Pseudomonas syringae genes required for fitness during colonization of the leaf surface and apoplast Helmann, Tyler C.; Deutschbauer, Adam M.; Lindow, Steven E. Proceedings of the National Academy of Sciences, Vol. 116, Issue 38 https://doi.org/10.1073/pnas.1908858116	journal	September 2019
The effects of soil phosphorus content on plant microbiota are driven by the plant phosphate starvation response G., Castrillo,; P. J. P. L., Teixeira,; S., Spaepen, Public Library of Science https://doi.org/10.17615/khqf-c670	text	January 2019
Genome-Resolved Proteomic Stable Isotope Probing of Soil Microbial Communities Using 13CO2 and 13C-Methanol Li, Zhou; Yao, Qiuming; Guo, Xuan Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.02706	journal	December 2019
Temporal dynamics of soil bacterial communities and multifunctionality are more sensitive to introduced plants than to microbial additions in a multicontaminated soil Jiao, Shuo; Du, Nini; Zai, Xiaoyu Land Degradation & Development, Vol. 30, Issue 7 https://doi.org/10.1002/ldr.3272	journal	February 2019
Genotype and rhizobium inoculation modulate the assembly of soybean rhizobacterial communities Zhong, Yongjia; Yang, Yongqing; Liu, Peng Plant, Cell & Environment, Vol. 42, Issue 6 https://doi.org/10.1111/pce.13519	journal	February 2019
Soil indigenous microbiome and plant genotypes cooperatively modify soybean rhizosphere microbiome assembly Liu, Fang; Hewezi, Tarek; Lebeis, Sarah L. BMC Microbiology, Vol. 19, Issue 1 https://doi.org/10.1186/s12866-019-1572-x	journal	September 2019
Nonadditive Transcriptomic Signatures of Genotype-by-Genotype Interactions during the Initiation of Plant-Rhizobium Symbiosis Fagorzi, Camilla; Bacci, Giovanni; Huang, Rui mSystems, Vol. 6, Issue 1 https://doi.org/10.1128/msystems.00974-20	journal	February 2021
Characterization of novel glycosyl hydrolases discovered by cell wall glycan directed monoclonal antibody screening and metagenome analysis of maize aerial root mucilage Pozzo, Tania; Higdon, Shawn M.; Pattathil, Sivakumar PLOS ONE, Vol. 13, Issue 9 https://doi.org/10.1371/journal.pone.0204525	journal	September 2018
Phenotypic diversity of Methylobacterium associated with rice landraces in North-East India Sanjenbam, Pratibha; Buddidathi, Radhika; Venkatesan, Radhika PLOS ONE, Vol. 15, Issue 2 https://doi.org/10.1371/journal.pone.0228550	journal	February 2020
Comparative Genomics Reveal a Flagellar System, a Type VI Secretion System and Plant Growth-Promoting Gene Clusters Unique to the Endophytic Bacterium Kosakonia radicincitans Becker, Matthias; Patz, Sascha; Becker, Yvonne Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.01997	journal	August 2018
A PilZ-Containing Chemotaxis Receptor Mediates Oxygen and Wheat Root Sensing in Azospirillum brasilense O’Neal, Lindsey; Akhter, Shehroze; Alexandre, Gladys Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.00312	journal	March 2019
Distinct Successions of Common and Rare Bacteria in Soil Under Humic Acid Amendment – A Microcosm Study Li, Pengfa; Liu, Jia; Jiang, Chunyu Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.02271	journal	October 2019
Isolation, Characterization, and Complete Genome Sequence of a Bradyrhizobium Strain Lb8 From Nodules of Peanut Utilizing Crack Entry Infection Paudel, Dev; Liu, Fengxia; Wang, Liping Frontiers in Microbiology, Vol. 11 https://doi.org/10.3389/fmicb.2020.00093	journal	February 2020
Inoculation With the Plant-Growth-Promoting Rhizobacterium Pseudomonas fluorescens LBUM677 Impacts the Rhizosphere Microbiome of Three Oilseed Crops Jiménez, Jesús A.; Novinscak, Amy; Filion, Martin Frontiers in Microbiology, Vol. 11 https://doi.org/10.3389/fmicb.2020.569366	journal	October 2020
Molecular Analyses of the Distribution and Function of Diazotrophic Rhizobia and Methanotrophs in the Tissues and Rhizosphere of Non-Leguminous Plants Plants, Vol. 8, Issue 10 https://doi.org/10.3390/plants8100408	journal	October 2019