DNA Methylation in Ensifer Species during Free-Living Growth and during Nitrogen-Fixing Symbiosis with Medicago spp.

diCenzo, George C.; Cangioli, Lisa; Nicoud, Quentin; Cheng, Janis H. T.; Blow, Matthew J.; Shapiro, Nicole; Woyke, Tanja; Biondi, Emanuele G.; Alunni, Benoît; Mengoni, Alessio; Mergaert, Peter; Bulgarelli, ed., Davide

doi:10.1128/mSystems.01092-21

Title: DNA Methylation in Ensifer Species during Free-Living Growth and during Nitrogen-Fixing Symbiosis with Medicago spp.

Journal Article · 21 February 2022 · mSystems

DOI: https://doi.org/10.1128/mSystems.01092-21 · OSTI ID:1838230

^[1];

^[2]; Nicoud, Quentin ^[3];

^[4];

^[5]; Shapiro, Nicole ^[5];

^[5];

^[3];

^[2];

^[3]; Bulgarelli, ed., Davide

Department of Biology, Queen’s University, Kingston, Ontario, Canada, Department of Biology, University of Florence, Florence, Italy
Department of Biology, University of Florence, Florence, Italy
Université Paris-Saclay, CEA, CNRS, Institute for Integrative Biology of the Cell, Gif-sur-Yvette, France
Department of Biology, Queen’s University, Kingston, Ontario, Canada
U.S. Department of Energy Joint Genome Institute, Berkeley, California, USA

Nitrogen fixation by rhizobia in symbiosis with legumes is economically and ecologically important. The symbiosis can involve a complex bacterial transformation—terminal differentiation—that includes major shifts in the transcriptome and cell cycle.

View Journal Article

Cite

Export

Save

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1838230

Journal Information:: mSystems, Journal Name: mSystems Journal Issue: 1 Vol. 7; ISSN 2379-5077

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

References (79)

A Caulobacter DNA Methyltransferase that Functions only in the Predivisional Cell Zweiger, Gary; Marczynski, Gregory; Shapiro, Lucille Journal of Molecular Biology, Vol. 235, Issue 2 https://doi.org/10.1006/jmbi.1994.1007	journal	January 1994
E. coli oriC and the dnaA gene promoter are sequestered from dam methyltransferase following the passage of the chromosomal replication fork Campbell, Joseph L.; Kleckner, Nancy Cell, Vol. 62, Issue 5 https://doi.org/10.1016/0092-8674(90)90271-f	journal	September 1990
DNA methylation in bacteria: from the methyl group to the methylome Sánchez-Romero, María A.; Cota, Ignacio; Casadesús, Josep Current Opinion in Microbiology, Vol. 25 https://doi.org/10.1016/j.mib.2015.03.004	journal	June 2015
DNA methylation in development and human disease Gopalakrishnan, Suhasni; Van Emburgh, Beth O.; Robertson, Keith D. Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis, Vol. 647, Issue 1-2 https://doi.org/10.1016/j.mrfmmm.2008.08.006	journal	December 2008
The repABC plasmid family Cevallos, Miguel A.; Cervantes-Rivera, Ramón; Gutiérrez-Ríos, Rosa María Plasmid, Vol. 60, Issue 1 https://doi.org/10.1016/j.plasmid.2008.03.001	journal	July 2008
Plasmid electroporation of Sinorhizobium strains: The role of the restriction gene hsdR in type strain Rm1021 Ferri, Lorenzo; Gori, Alessandro; Biondi, Emanuele G. Plasmid, Vol. 63, Issue 3 https://doi.org/10.1016/j.plasmid.2010.01.001	journal	May 2010
DNA methylation in Caulobacter and other Alphaproteobacteria during cell cycle progression Mohapatra, Saswat S.; Fioravanti, Antonella; Biondi, Emanuele G. Trends in Microbiology, Vol. 22, Issue 9 https://doi.org/10.1016/j.tim.2014.05.003	journal	September 2014
Phasevarions of Bacterial Pathogens: Methylomics Sheds New Light on Old Enemies Atack, John M.; Tan, Aimee; Bakaletz, Lauren O. Trends in Microbiology, Vol. 26, Issue 8 https://doi.org/10.1016/j.tim.2018.01.008	journal	August 2018
Widespread Existence of Cytosine Methylation in Yeast DNA Measured by Gas Chromatography/Mass Spectrometry Tang, Yang; Gao, Xiang-Dong; Wang, Yinsheng Analytical Chemistry, Vol. 84, Issue 16 https://doi.org/10.1021/ac301727c	journal	August 2012
Direct detection of DNA methylation during single-molecule, real-time sequencing Flusberg, Benjamin A.; Webster, Dale R.; Lee, Jessica H. Nature Methods, Vol. 7, Issue 6 https://doi.org/10.1038/nmeth.1459	journal	May 2010
Reprogramming of DNA methylation is critical for nodule development in Medicago truncatula Satgé, Carine; Moreau, Sandra; Sallet, Erika Nature Plants, Vol. 2, Issue 11 https://doi.org/10.1038/nplants.2016.166	journal	October 2016
Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants Oldroyd, Giles E. D. Nature Reviews Microbiology, Vol. 11, Issue 4 https://doi.org/10.1038/nrmicro2990	journal	March 2013
Genome-scale metabolic reconstruction of the symbiosis between a leguminous plant and a nitrogen-fixing bacterium diCenzo, George C.; Tesi, Michelangelo; Pfau, Thomas Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-16484-2	journal	May 2020
Whole-genome landscape of Medicago truncatula symbiotic genes Pecrix, Yann; Staton, S. Evan; Sallet, Erika Nature Plants, Vol. 4, Issue 12 https://doi.org/10.1038/s41477-018-0286-7	journal	November 2018
Dynamics and function of DNA methylation in plants Zhang, Huiming; Lang, Zhaobo; Zhu, Jian-Kang Nature Reviews Molecular Cell Biology, Vol. 19, Issue 8 https://doi.org/10.1038/s41580-018-0016-z	journal	May 2018
The diverse roles of DNA methylation in mammalian development and disease Greenberg, Maxim V. C.; Bourc’his, Deborah Nature Reviews Molecular Cell Biology, Vol. 20, Issue 10 https://doi.org/10.1038/s41580-019-0159-6	journal	August 2019
Integrated roles of BclA and DD-carboxypeptidase 1 in Bradyrhizobium differentiation within NCR-producing and NCR-lacking root nodules Barrière, Quentin; Guefrachi, Ibtissem; Gully, Djamel Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-08830-0	journal	August 2017
The two chromosomes of Vibrio cholerae are initiated at different time points in the cell cycle Rasmussen, Tue; Jensen, Rasmus Bugge; Skovgaard, Ole The EMBO Journal, Vol. 26, Issue 13 https://doi.org/10.1038/sj.emboj.7601747	journal	June 2007
Cooperation and competition in mismatch repair: very short-patch repair and methyl-directed mismatch repair in Escherichia coli: VSP repair and MMR Bhagwat, Ashok S.; Lieb, Margaret Molecular Microbiology, Vol. 44, Issue 6 https://doi.org/10.1046/j.1365-2958.2002.02989.x	journal	June 2002
A dual-genome Symbiosis Chip for coordinate study of signal exchange and development in a prokaryote-host interaction Barnett, M. J.; Toman, C. J.; Fisher, R. F. Proceedings of the National Academy of Sciences, Vol. 101, Issue 47 https://doi.org/10.1073/pnas.0407269101	journal	November 2004
Eukaryotic control on bacterial cell cycle and differentiation in the Rhizobium-legume symbiosis Mergaert, P.; Uchiumi, T.; Alunni, B. Proceedings of the National Academy of Sciences, Vol. 103, Issue 13 https://doi.org/10.1073/pnas.0600912103	journal	March 2006
Global methylation state at base-pair resolution of the Caulobacter genome throughout the cell cycle Kozdon, J. B.; Melfi, M. D.; Luong, K. Proceedings of the National Academy of Sciences, Vol. 110, Issue 48 https://doi.org/10.1073/pnas.1319315110	journal	November 2013
Global analysis of cell cycle gene expression of the legume symbiont Sinorhizobium meliloti De Nisco, Nicole J.; Abo, Ryan P.; Wu, C. Max Proceedings of the National Academy of Sciences, Vol. 111, Issue 9 https://doi.org/10.1073/pnas.1400421111	journal	February 2014
Host plant peptides elicit a transcriptional response to control the Sinorhizobium meliloti cell cycle during symbiosis Penterman, Jon; Abo, Ryan P.; De Nisco, Nicole J. Proceedings of the National Academy of Sciences, Vol. 111, Issue 9 https://doi.org/10.1073/pnas.1400450111	journal	February 2014
Medicago truncatula symbiotic peptide NCR247 contributes to bacteroid differentiation through multiple mechanisms Farkas, A.; Maroti, G.; Durg , H. Proceedings of the National Academy of Sciences, Vol. 111, Issue 14 https://doi.org/10.1073/pnas.1404169111	journal	March 2014
An antimicrobial peptide essential for bacterial survival in the nitrogen-fixing symbiosis Kim, Minsoo; Chen, Yuhui; Xi, Jiejun Proceedings of the National Academy of Sciences, Vol. 112, Issue 49 https://doi.org/10.1073/pnas.1500123112	journal	November 2015
Loss of the nodule-specific cysteine rich peptide, NCR169, abolishes symbiotic nitrogen fixation in the Medicago truncatula dnf7 mutant Horváth, Beatrix; Domonkos, Ágota; Kereszt, Attila Proceedings of the National Academy of Sciences, Vol. 112, Issue 49 https://doi.org/10.1073/pnas.1500777112	journal	September 2015
Ploidy-dependent changes in the epigenome of symbiotic cells correlate with specific patterns of gene expression Nagymihály, Marianna; Veluchamy, Alaguraj; Györgypál, Zoltán Proceedings of the National Academy of Sciences, Vol. 114, Issue 17 https://doi.org/10.1073/pnas.1704211114	journal	April 2017
Detergent extraction identifies different VirB protein subassemblies of the type IV secretion machinery in the membranes of Agrobacterium tumefaciens Krall, L.; Wiedemann, U.; Unsin, G. Proceedings of the National Academy of Sciences, Vol. 99, Issue 17 https://doi.org/10.1073/pnas.172390699	journal	August 2002
Interaction of SeqA and Dam Methylase on the Hemimethylated Origin of Escherichia coli Chromosomal DNA Replication Kang, Sukhyun; Lee, Ho; Han, Joo Seok Journal of Biological Chemistry, Vol. 274, Issue 17 https://doi.org/10.1074/jbc.274.17.11463	journal	April 1999
trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses Capella-Gutierrez, S.; Silla-Martinez, J. M.; Gabaldon, T. Bioinformatics, Vol. 25, Issue 15 https://doi.org/10.1093/bioinformatics/btp348	journal	June 2009
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies Stamatakis, Alexandros Bioinformatics, Vol. 30, Issue 9 https://doi.org/10.1093/bioinformatics/btu033	journal	January 2014
Prokka: rapid prokaryotic genome annotation Seemann, T. Bioinformatics, Vol. 30, Issue 14 https://doi.org/10.1093/bioinformatics/btu153	journal	March 2014
Roary: rapid large-scale prokaryote pan genome analysis Page, Andrew J.; Cummins, Carla A.; Hunt, Martin Bioinformatics, Vol. 31, Issue 22 https://doi.org/10.1093/bioinformatics/btv421	journal	July 2015
Multiple links connect central carbon metabolism to DNA replication initiation and elongation in Bacillus subtilis Nouri, Hamid; Monnier, Anne-Françoise; Fossum-Raunehaug, Solveig DNA Research, Vol. 25, Issue 6 https://doi.org/10.1093/dnares/dsy031	journal	September 2018
DNA methyltransferases and epigenetic regulation in bacteria Adhikari, Satish; Curtis, Patrick D. FEMS Microbiology Reviews, Vol. 40, Issue 5 https://doi.org/10.1093/femsre/fuw023	journal	July 2016
Symbiotic and Nonsymbiotic Members of the Genus Ensifer (syn. Sinorhizobium ) Are Separated into Two Clades Based on Comparative Genomics and High-Throughput Phenotyping Fagorzi, Camilla; Ilie, Alexandru; Decorosi, Francesca Genome Biology and Evolution, Vol. 12, Issue 12 https://doi.org/10.1093/gbe/evaa221	journal	October 2020
The model symbiotic association between Medicago truncatula cv. Jemalong and Rhizobium meliloti strain 2011 leads to N-stressed plants when symbiotic N2 fixation is the main N source for plant growth Moreau, Delphine; Voisin, Anne-Sophie; Salon, Christophe Journal of Experimental Botany, Vol. 59, Issue 13 https://doi.org/10.1093/jxb/ern203	journal	August 2008
Characterization of DNA methyltransferase specificities using single-molecule, real-time DNA sequencing Clark, Tyson A.; Murray, Iain A.; Morgan, Richard D. Nucleic Acids Research, Vol. 40, Issue 4 https://doi.org/10.1093/nar/gkr1146	journal	December 2011
TIGRFAMs and Genome Properties in 2013 Haft, Daniel H.; Selengut, Jeremy D.; Richter, Roland A. Nucleic Acids Research, Vol. 41, Issue D1 https://doi.org/10.1093/nar/gks1234	journal	November 2012
The functions of DNA methylation by CcrM in Caulobacter crescentus: a global approach Gonzalez, Diego; Kozdon, Jennifer B.; McAdams, Harley H. Nucleic Acids Research, Vol. 42, Issue 6 https://doi.org/10.1093/nar/gkt1352	journal	January 2014
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
Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees Letunic, Ivica; Bork, Peer Nucleic Acids Research, Vol. 44, Issue W1 https://doi.org/10.1093/nar/gkw290	journal	April 2016
Specific Host-Responsive Associations Between Medicago truncatula Accessions and Sinorhizobium Strains Kazmierczak, Théophile; Nagymihály, Marianna; Lamouche, Florian Molecular Plant-Microbe Interactions®, Vol. 30, Issue 5 https://doi.org/10.1094/MPMI-01-17-0009-R	journal	May 2017
Transcriptomic Analysis of Sinorhizobium meliloti and Medicago truncatula Symbiosis Using Nitrogen Fixation–Deficient Nodules Lang, Claus; Long, Sharon R. Molecular Plant-Microbe Interactions®, Vol. 28, Issue 8 https://doi.org/10.1094/MPMI-12-14-0407-R	journal	August 2015
Caulobacter Lon protease has a critical role in cell-cycle control of DNA methylation. Wright, R.; Stephens, C.; Zweiger, G. Genes & Development, Vol. 10, Issue 12 https://doi.org/10.1101/gad.10.12.1532	journal	June 1996
The bacterial cell cycle regulator GcrA is a σ ⁷⁰ cofactor that drives gene expression from a subset of methylated promoters Haakonsen, Diane L.; Yuan, Andy H.; Laub, Michael T. Genes & Development, Vol. 29, Issue 21 https://doi.org/10.1101/gad.270660.115	journal	November 2015
Nitrogen Fixation Mutants of Medicago truncatula Fail to Support Plant and Bacterial Symbiotic Gene Expression Starker, Colby G.; Parra-Colmenares, Adriana L.; Smith, Lucinda Plant Physiology, Vol. 140, Issue 2 https://doi.org/10.1104/pp.105.072132	journal	January 2006
Convergent Evolution of Endosymbiont Differentiation in Dalbergioid and Inverted Repeat-Lacking Clade Legumes Mediated by Nodule-Specific Cysteine-Rich Peptides Czernic, Pierre; Gully, Djamel; Cartieaux, Fabienne Plant Physiology, Vol. 169, Issue 2 https://doi.org/10.1104/pp.15.00584	journal	August 2015
Sinorhizobium meliloti CpdR1 is critical for co-ordinating cell cycle progression and the symbiotic chronic infection Kobayashi, Hajime; De Nisco, Nicole J.; Chien, Peter Molecular Microbiology, Vol. 73, Issue 4 https://doi.org/10.1111/j.1365-2958.2009.06794.x	journal	August 2009
DNA methylation by CcrM activates the transcription of two genes required for the division of C aulobacter crescentus Gonzalez, Diego; Collier, Justine Molecular Microbiology, Vol. 88, Issue 1 https://doi.org/10.1111/mmi.12180	journal	March 2013
The DivJ, CbrA and PleC system controls DivK phosphorylation and symbiosis in Sinorhizobium meliloti: The cell cycle kinase DivJ in Sinorhizobium meliloti Pini, Francesco; Frage, Benjamin; Ferri, Lorenzo Molecular Microbiology https://doi.org/10.1111/mmi.12347	journal	August 2013
Spatiotemporal choreography of chromosome and megaplasmids in the Sinorhizobium meliloti cell cycle: Spatiotemporal dynamics of rhizobial megaplasmids Frage, Benjamin; Döhlemann, Johannes; Robledo, Marta Molecular Microbiology, Vol. 100, Issue 5 https://doi.org/10.1111/mmi.13351	journal	April 2016
Medicago truncatula DNF 2 is a PI ‐ PLC ‐ XD ‐containing protein required for bacteroid persistence and prevention of nodule early senescence and defense‐like reactions Bourcy, Marie; Brocard, Lysiane; Pislariu, Catalina I. New Phytologist, Vol. 197, Issue 4 https://doi.org/10.1111/nph.12091	journal	December 2012
An integrated analysis of plant and bacterial gene expression in symbiotic root nodules using laser-capture microdissection coupled to RNA sequencing Roux, Brice; Rodde, Nathalie; Jardinaud, Marie-Françoise The Plant Journal, Vol. 77, Issue 6 https://doi.org/10.1111/tpj.12442	journal	February 2014
Real-Time DNA Sequencing from Single Polymerase Molecules Eid, John; Fehr, Adrian; Gray, Jeremy Science, Vol. 323, Issue 5910, p. 133-138 https://doi.org/10.1126/science.1162986	journal	January 2009
Plant Peptides Govern Terminal Differentiation of Bacteria in Symbiosis Van de Velde, W.; Zehirov, G.; Szatmari, A. Science, Vol. 327, Issue 5969 https://doi.org/10.1126/science.1184057	journal	February 2010
A Nodule-Specific Protein Secretory Pathway Required for Nitrogen-Fixing Symbiosis Wang, D.; Griffitts, J.; Starker, C. Science, Vol. 327, Issue 5969 https://doi.org/10.1126/science.1184096	journal	February 2010
DNA Mismatch Correction in a Defined System Lahue, R. S.; Au, K. G.; Modrich, P. Science, Vol. 245, Issue 4914 https://doi.org/10.1126/science.2665076	journal	July 1989
An Integrated Approach to Functional Genomics: Construction of a Novel Reporter Gene Fusion Library for Sinorhizobium meliloti Cowie, Alison; Cheng, Jiujun; Sibley, Christopher D. Applied and Environmental Microbiology, Vol. 72, Issue 11 https://doi.org/10.1128/AEM.01397-06	journal	November 2006
CbrA Is a Stationary-Phase Regulator of Cell Surface Physiology and Legume Symbiosis in Sinorhizobium meliloti Gibson, Katherine E.; Campbell, Gordon R.; Lloret, Javier Journal of Bacteriology, Vol. 188, Issue 12 https://doi.org/10.1128/JB.01923-05	journal	June 2006
The CcrM DNA Methyltransferase of Agrobacterium tumefaciens Is Essential, and Its Activity Is Cell Cycle Regulated Kahng, Lyn Sue; Shapiro, Lucy Journal of Bacteriology, Vol. 183, Issue 10 https://doi.org/10.1128/JB.183.10.3065-3075.2001	journal	May 2001
Diverse Functions of Restriction-Modification Systems in Addition to Cellular Defense Vasu, K.; Nagaraja, V. Microbiology and Molecular Biology Reviews, Vol. 77, Issue 1 https://doi.org/10.1128/MMBR.00044-12	journal	March 2013
Correlation between ultrastructural differentiation of bacteroids and nitrogen fixation in alfalfa nodules. Vasse, J.; de Billy, F.; Camut, S. Journal of Bacteriology, Vol. 172, Issue 8 https://doi.org/10.1128/jb.172.8.4295-4306.1990	journal	August 1990
The CcrM DNA methyltransferase is widespread in the alpha subdivision of proteobacteria, and its essential functions are conserved in Rhizobium meliloti and Caulobacter crescentus Wright, R.; Stephens, C.; Shapiro, L. Journal of Bacteriology, Vol. 179, Issue 18 https://doi.org/10.1128/jb.179.18.5869-5877.1997	journal	September 1997
Multidisciplinary approaches for studying rhizobium–legume symbioses diCenzo, George C.; Zamani, Maryam; Checcucci, Alice Canadian Journal of Microbiology, Vol. 65, Issue 1 https://doi.org/10.1139/cjm-2018-0377	journal	January 2019
Mapping single molecule sequencing reads using basic local alignment with successive refinement (BLASR): application and theory Chaisson, Mark J.; Tesler, Glenn BMC Bioinformatics, Vol. 13, Issue 1 https://doi.org/10.1186/1471-2105-13-238	journal	September 2012
The identification of novel loci required for appropriate nodule development in Medicago truncatula Domonkos, Agota; Horvath, Beatrix; Marsh, John F. BMC Plant Biology, Vol. 13, Issue 1 https://doi.org/10.1186/1471-2229-13-157	journal	October 2013
The diversity and evolution of cell cycle regulation in alpha-proteobacteria: a comparative genomic analysis Brilli, Matteo; Fondi, Marco; Fani, Renato BMC Systems Biology, Vol. 4, Issue 1 https://doi.org/10.1186/1752-0509-4-52	journal	January 2010
DNA Binding of the Cell Cycle Transcriptional Regulator GcrA Depends on N6-Adenosine Methylation in Caulobacter crescentus and Other Alphaproteobacteria Fioravanti, Antonella; Fumeaux, Coralie; Mohapatra, Saswat S. PLoS Genetics, Vol. 9, Issue 5 https://doi.org/10.1371/journal.pgen.1003541	journal	May 2013
Examination of Prokaryotic Multipartite Genome Evolution through Experimental Genome Reduction diCenzo, George C.; MacLean, Allyson M.; Milunovic, Branislava PLoS Genetics, Vol. 10, Issue 10 https://doi.org/10.1371/journal.pgen.1004742	journal	October 2014
Cell Cycle Control by the Master Regulator CtrA in Sinorhizobium meliloti Pini, Francesco; De Nisco, Nicole J.; Ferri, Lorenzo PLOS Genetics, Vol. 11, Issue 5 https://doi.org/10.1371/journal.pgen.1005232	journal	May 2015
The Epigenomic Landscape of Prokaryotes Blow, Matthew J.; Clark, Tyson A.; Daum, Chris G. PLOS Genetics, Vol. 12, Issue 2 https://doi.org/10.1371/journal.pgen.1005854	journal	February 2016
Transcriptional rewiring of the GcrA/CcrM bacterial epigenetic regulatory system in closely related bacteria Adhikari, Satish; Erill, Ivan; Curtis, Patrick D. PLOS Genetics, Vol. 17, Issue 3 https://doi.org/10.1371/journal.pgen.1009433	journal	March 2021
Designer Sinorhizobium meliloti strains and multi-functional vectors enable direct inter-kingdom DNA transfer Brumwell, Stephanie L.; MacLeod, Michael R.; Huang, Tony PLOS ONE, Vol. 14, Issue 6 https://doi.org/10.1371/journal.pone.0206781	journal	June 2019
A Key Regulator of the Glycolytic and Gluconeogenic Central Metabolic Pathways in Sinorhizobium meliloti diCenzo, George C.; Muhammed, Zahed; Østerås, Magne Genetics, Vol. 207, Issue 3 https://doi.org/10.1534/genetics.117.300212	journal	August 2017
Integrating DNA Methylation and Gene Expression Data in the Development of the Soybean-Bradyrhizobium N2-Fixing Symbiosis Davis-Richardson, Austin G.; Russell, Jordan T.; Dias, Raquel Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00518	journal	April 2016
Replicate Once Per Cell Cycle: Replication Control of Secondary Chromosomes Fournes, Florian; Val, Marie-Eve; Skovgaard, Ole Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.01833	journal	August 2018
Genomic and Biotechnological Characterization of the Heavy-Metal Resistant, Arsenic-Oxidizing Bacterium Ensifer sp. M14 diCenzo, George C.; Debiec, Klaudia; Krzysztoforski, Jan Genes, Vol. 9, Issue 8 https://doi.org/10.3390/genes9080379	journal	July 2018

Similar Records

Sinorhizobium medicae WSM419 Genes That Improve Symbiosis between Sinorhizobium meliloti Rm1021 and Medicago truncatula Jemalong A17 and in Other Symbiosis Systems

Journal Article · 2021 · Applied and Environmental Microbiology · OSTI ID:1850233

Ghosh, Prithwi; Adolphsen, Katie N.; Yurgel, Svetlana N.; +2 more

Transcription Factors Controlling the Rhizobium–Legume Symbiosis: Integrating Infection, Organogenesis and the Abiotic Environment

Journal Article · 2022 · Plant and Cell Physiology · OSTI ID:2422460

Chakraborty, Sanhita; Valdés-López, Oswaldo; Stonoha-Arther, Christina; +1 more

Transcription Factors Controlling the Rhizobium–Legume Symbiosis: Integrating Infection, Organogenesis and the Abiotic Environment

Journal Article · 2022 · Plant and Cell Physiology · OSTI ID:1895497

Chakraborty, Sanhita; Valdés-López, Oswaldo; Stonoha-Arther, Christina; +1 more

Title: DNA Methylation in Ensifer Species during Free-Living Growth and during Nitrogen-Fixing Symbiosis with Medicago spp.

Citation Formats

References (79)

Similar Records

Related Subjects