{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,5]],"date-time":"2026-10-05T21:20:46Z","timestamp":1791235246448,"version":"4.1.0"},"reference-count":50,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2020,9,11]],"date-time":"2020-09-11T00:00:00Z","timestamp":1599782400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2020,9,11]],"date-time":"2020-09-11T00:00:00Z","timestamp":1599782400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"name":"Edward Via College of Osteopathic Medicine","award":["1-One Health Grant"],"award-info":[{"award-number":["1-One Health Grant"]}]},{"name":"W.W. Smith Charitable Trust","award":["H1804"],"award-info":[{"award-number":["H1804"]}]},{"DOI":"10.13039\/100000057","name":"National Institute of General Medical Sciences","doi-asserted-by":"publisher","award":["1R15GM135933-01"],"award-info":[{"award-number":["1R15GM135933-01"]}],"id":[{"id":"10.13039\/100000057","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>\n                    LysR-type transcriptional regulators (LTTRs) are the most common type of transcriptional regulators in prokaryotes and function by altering gene expression in response to environmental stimuli. In the class\n                    <jats:italic>Alphaproteobacteria<\/jats:italic>\n                    , a conserved LTTR named VtlR is critical to the establishment of host-microbe interactions. In the mammalian pathogen\n                    <jats:italic>Brucella abortus<\/jats:italic>\n                    , VtlR is required for full virulence in a mouse model of infection, and VtlR activates the expression of\n                    <jats:italic>abcR2<\/jats:italic>\n                    , which encodes a small regulatory RNA (sRNA). In the plant symbiont\n                    <jats:italic>Sinorhizobium meliloti<\/jats:italic>\n                    , the ortholog of VtlR, named LsrB, is involved in the symbiosis of the bacterium with alfalfa.\n                    <jats:italic>Agrobacterium tumefaciens<\/jats:italic>\n                    is a close relative of both\n                    <jats:italic>B. abortus<\/jats:italic>\n                    and\n                    <jats:italic>S. meliloti<\/jats:italic>\n                    , and this bacterium is the causative agent of crown gall disease in plants. In the present study, we demonstrate that VtlR is involved in the ability of\n                    <jats:italic>A. tumefaciens<\/jats:italic>\n                    to grow appropriately in artificial medium, and an\n                    <jats:italic>A. tumefaciens vtlR<\/jats:italic>\n                    deletion strain is defective in motility, biofilm formation, and tumorigenesis of potato discs. RNA-sequencing analyses revealed that more than 250 genes are dysregulated in the \u2206\n                    <jats:italic>vtlR<\/jats:italic>\n                    strain, and importantly, VtlR directly controls the expression of three sRNAs in\n                    <jats:italic>A. tumefaciens<\/jats:italic>\n                    . Taken together, these data support a model in which VtlR indirectly regulates hundreds of genes via manipulation of sRNA pathways in\n                    <jats:italic>A. tumefaciens<\/jats:italic>\n                    , and moreover, while the VtlR\/LsrB protein is present and structurally conserved in many members of the\n                    <jats:italic>Alphaproteobacteria<\/jats:italic>\n                    , the VtlR\/LsrB regulatory circuitry has diverged in order to accommodate the unique environmental niche of each organism.\n                  <\/jats:p>","DOI":"10.1038\/s41598-020-72117-0","type":"journal-article","created":{"date-parts":[[2020,9,11]],"date-time":"2020-09-11T06:09:21Z","timestamp":1599804561000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":17,"title":["A central role for the transcriptional regulator VtlR in small RNA-mediated gene regulation in\u00a0Agrobacterium tumefaciens"],"prefix":"10.1038","volume":"10","author":[{"given":"James A.","family":"Budnick","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lauren M.","family":"Sheehan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Miranda. J.","family":"Ginder","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kevin C.","family":"Failor","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Julia. M.","family":"Perkowski","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"John. F.","family":"Pinto","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kirsten A.","family":"Kohl","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lin","family":"Kang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pawel","family":"Michalak","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Li","family":"Luo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jason E.","family":"Heindl","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Clayton C.","family":"Caswell","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2020,9,11]]},"reference":[{"key":"72117_CR1","doi-asserted-by":"publisher","first-page":"3609","DOI":"10.1099\/mic.0.2008\/022772-0","volume":"154","author":"SE Maddocks","year":"2008","unstructured":"Maddocks, S. E. & Oyston, P. C. Structure and function of the LysR-type transcriptional regulator (LTTR) family proteins. Microbiology 154, 3609\u20133623. https:\/\/doi.org\/10.1099\/mic.0.2008\/022772-0 (2008).","journal-title":"Microbiology"},{"key":"72117_CR2","doi-asserted-by":"publisher","first-page":"6602","DOI":"10.1073\/pnas.85.18.6602","volume":"85","author":"S Henikoff","year":"1988","unstructured":"Henikoff, S., Haughn, G. W., Calvo, J. M. & Wallace, J. C. A large family of bacterial activator proteins. Proc. Natl. Acad. Sci. USA 85, 6602\u20136606 (1988).","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"72117_CR3","doi-asserted-by":"publisher","first-page":"4181","DOI":"10.1128\/JB.00193-10","volume":"192","author":"G Kovacikova","year":"2010","unstructured":"Kovacikova, G., Lin, W. & Skorupski, K. The LysR-type virulence activator AphB regulates the expression of genes in Vibrio cholerae in response to low pH and anaerobiosis. J. Bacteriol. 192, 4181\u20134191. https:\/\/doi.org\/10.1128\/JB.00193-10 (2010).","journal-title":"J. Bacteriol."},{"key":"72117_CR4","doi-asserted-by":"publisher","first-page":"810","DOI":"10.1073\/pnas.1014640108","volume":"108","author":"Z Liu","year":"2011","unstructured":"Liu, Z. et al. Vibrio cholerae anaerobic induction of virulence gene expression is controlled by thiol-based switches of virulence regulator AphB. Proc. Natl. Acad. Sci. USA 108, 810\u2013815. https:\/\/doi.org\/10.1073\/pnas.1014640108 (2011).","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"72117_CR5","doi-asserted-by":"publisher","first-page":"347","DOI":"10.1016\/j.celrep.2015.12.038","volume":"14","author":"Z Liu","year":"2016","unstructured":"Liu, Z. et al. Differential thiol-based switches jump-start Vibrio cholerae pathogenesis. Cell Rep 14, 347\u2013354. https:\/\/doi.org\/10.1016\/j.celrep.2015.12.038 (2016).","journal-title":"Cell Rep"},{"key":"72117_CR6","doi-asserted-by":"publisher","first-page":"3840","DOI":"10.1021\/acs.biochem.7b00337","volume":"56","author":"BR Privett","year":"2017","unstructured":"Privett, B. R. et al. Identification of a small molecule activator for AphB, a LysR-type virulence transcriptional regulator in Vibrio cholerae. Biochemistry 56, 3840\u20133849. https:\/\/doi.org\/10.1021\/acs.biochem.7b00337 (2017).","journal-title":"Biochemistry"},{"key":"72117_CR7","doi-asserted-by":"publisher","first-page":"457","DOI":"10.1111\/j.1365-2958.2011.07919.x","volume":"83","author":"JL Taylor","year":"2012","unstructured":"Taylor, J. L. et al. The crystal structure of AphB, a virulence gene activator from Vibrio cholerae, reveals residues that influence its response to oxygen and pH. Mol. Microbiol. 83, 457\u2013470. https:\/\/doi.org\/10.1111\/j.1365-2958.2011.07919.x (2012).","journal-title":"Mol. Microbiol."},{"key":"72117_CR8","doi-asserted-by":"publisher","first-page":"881","DOI":"10.1111\/j.1365-2958.2009.06686.x","volume":"72","author":"SH Craven","year":"2009","unstructured":"Craven, S. H. et al. Inducer responses of BenM, a LysR-type transcriptional regulator from Acinetobacter baylyi ADP1. Mol. Microbiol. 72, 881\u2013894. https:\/\/doi.org\/10.1111\/j.1365-2958.2009.06686.x (2009).","journal-title":"Mol. Microbiol."},{"key":"72117_CR9","doi-asserted-by":"publisher","first-page":"1749","DOI":"10.1128\/AEM.72.3.1749-1758.2006","volume":"72","author":"OC Ezezika","year":"2006","unstructured":"Ezezika, O. C., Collier-Hyams, L. S., Dale, H. A., Burk, A. C. & Neidle, E. L. CatM regulation of the benABCDE operon: Functional divergence of two LysR-type paralogs in Acinetobacter baylyi ADP1. Appl. Environ. Microbiol. 72, 1749\u20131758. https:\/\/doi.org\/10.1128\/AEM.72.3.1749-1758.2006 (2006).","journal-title":"Appl. Environ. Microbiol."},{"key":"72117_CR10","doi-asserted-by":"publisher","first-page":"568","DOI":"10.1016\/j.jmb.2010.09.053","volume":"404","author":"A Ruangprasert","year":"2010","unstructured":"Ruangprasert, A., Craven, S. H., Neidle, E. L. & Momany, C. Full-length structures of BenM and two variants reveal different oligomerization schemes for LysR-type transcriptional regulators. J. Mol. Biol. 404, 568\u2013586. https:\/\/doi.org\/10.1016\/j.jmb.2010.09.053 (2010).","journal-title":"J. Mol. Biol."},{"key":"72117_CR11","doi-asserted-by":"publisher","first-page":"1397","DOI":"10.1111\/j.1365-2958.2005.04783.x","volume":"57","author":"AW Dangel","year":"2005","unstructured":"Dangel, A. W., Gibson, J. L., Janssen, A. P. & Tabita, F. R. Residues that influence in vivo and in vitro CbbR function in Rhodobacter sphaeroides and identification of a specific region critical for co-inducer recognition. Mol. Microbiol. 57, 1397\u20131414. https:\/\/doi.org\/10.1111\/j.1365-2958.2005.04783.x (2005).","journal-title":"Mol. Microbiol."},{"key":"72117_CR12","doi-asserted-by":"publisher","first-page":"6721","DOI":"10.1128\/JB.184.23.6721-6724.2002","volume":"184","author":"SA Smith","year":"2002","unstructured":"Smith, S. A. & Tabita, F. R. Up-regulated expression of the cbb(I) and cbb(II) operons during photoheterotrophic growth of a ribulose 1,5-bisphosphate carboxylase-oxygenase deletion mutant of Rhodobacter sphaeroides. J. Bacteriol. 184, 6721\u20136724 (2002).","journal-title":"J. Bacteriol."},{"key":"72117_CR13","doi-asserted-by":"publisher","first-page":"1905","DOI":"10.1128\/JB.184.7.1905-1915.2002","volume":"184","author":"MA Tichi","year":"2002","unstructured":"Tichi, M. A. & Tabita, F. R. Metabolic signals that lead to control of CBB gene expression in Rhodobacter capsulatus. J. Bacteriol. 184, 1905\u20131915 (2002).","journal-title":"J. Bacteriol."},{"key":"72117_CR14","doi-asserted-by":"publisher","first-page":"5866","DOI":"10.1074\/jbc.M110555200","volume":"277","author":"R Akakura","year":"2002","unstructured":"Akakura, R. & Winans, S. C. Constitutive mutations of the OccR regulatory protein affect DNA bending in response to metabolites released from plant tumors. J. Biol. Chem. 277, 5866\u20135874. https:\/\/doi.org\/10.1074\/jbc.M110555200 (2002).","journal-title":"J. Biol. Chem."},{"key":"72117_CR15","doi-asserted-by":"publisher","first-page":"659","DOI":"10.1016\/0092-8674(92)90229-6","volume":"69","author":"L Wang","year":"1992","unstructured":"Wang, L., Helmann, J. D., Winans, S. C. & The, A. tumefaciens transcriptional activator OccR causes a bend at a target promoter, which is partially relaxed by a plant tumor metabolite. Cell 69, 659\u2013667 (1992).","journal-title":"Cell"},{"key":"72117_CR16","doi-asserted-by":"publisher","first-page":"1275","DOI":"10.1128\/JB.177.5.1275-1284.1995","volume":"177","author":"I Kullik","year":"1995","unstructured":"Kullik, I., Toledano, M. B., Tartaglia, L. A. & Storz, G. Mutational analysis of the redox-sensitive transcriptional regulator OxyR: Regions important for oxidation and transcriptional activation. J. Bacteriol. 177, 1275\u20131284 (1995).","journal-title":"J. Bacteriol."},{"key":"72117_CR17","doi-asserted-by":"publisher","first-page":"1718","DOI":"10.1126\/science.279.5357.1718","volume":"279","author":"M Zheng","year":"1998","unstructured":"Zheng, M., Aslund, F. & Storz, G. Activation of the OxyR transcription factor by reversible disulfide bond formation. Science 279, 1718\u20131721 (1998).","journal-title":"Science"},{"key":"72117_CR18","doi-asserted-by":"publisher","first-page":"4562","DOI":"10.1128\/JB.187.13.4562-4572.2005","volume":"187","author":"L Luo","year":"2005","unstructured":"Luo, L. et al. Two new Sinorhizobium meliloti LysR-type transcriptional regulators required for nodulation. J. Bacteriol. 187, 4562\u20134572. https:\/\/doi.org\/10.1128\/JB.187.13.4562-4572.2005 (2005).","journal-title":"J. Bacteriol."},{"key":"72117_CR19","doi-asserted-by":"publisher","first-page":"882","DOI":"10.1093\/abbs\/gmt083","volume":"45","author":"D Lu","year":"2013","unstructured":"Lu, D., Tang, G., Wang, D. & Luo, L. The Sinorhizobium meliloti LysR family transcriptional factor LsrB is involved in regulation of glutathione biosynthesis. Acta Biochim. Biophys. Sin. (Shanghai) 45, 882\u2013888. https:\/\/doi.org\/10.1093\/abbs\/gmt083 (2013).","journal-title":"Acta Biochim. Biophys. Sin. (Shanghai)"},{"key":"72117_CR20","doi-asserted-by":"publisher","first-page":"5265","DOI":"10.1128\/AEM.01393-14","volume":"80","author":"G Tang","year":"2014","unstructured":"Tang, G., Wang, Y. & Luo, L. Transcriptional regulator LsrB of Sinorhizobium meliloti positively regulates the expression of genes involved in lipopolysaccharide biosynthesis. Appl. Environ. Microbiol. 80, 5265\u20135273. https:\/\/doi.org\/10.1128\/AEM.01393-14 (2014).","journal-title":"Appl. Environ. Microbiol."},{"key":"72117_CR21","doi-asserted-by":"publisher","first-page":"5130","DOI":"10.1111\/1462-2920.13992","volume":"19","author":"G Tang","year":"2017","unstructured":"Tang, G. et al. Regulation of cysteine residues in LsrB proteins from Sinorhizobium meliloti under free-living and symbiotic oxidative stress. Environ. Microbiol. 19, 5130\u20135145. https:\/\/doi.org\/10.1111\/1462-2920.13992 (2017).","journal-title":"Environ. Microbiol."},{"key":"72117_CR22","doi-asserted-by":"publisher","DOI":"10.1111\/mmi.13123","author":"LM Sheehan","year":"2015","unstructured":"Sheehan, L. M., Budnick, J. A., Blanchard, C., Dunman, P. M. & Caswell, C. C. A LysR-family transcriptional regulator required for virulence in Brucella abortus is highly conserved among the alpha-proteobacteria. Mol. Microbiol. https:\/\/doi.org\/10.1111\/mmi.13123 (2015).","journal-title":"Mol. Microbiol."},{"key":"72117_CR23","doi-asserted-by":"publisher","first-page":"550","DOI":"10.4161\/rna.29625","volume":"11","author":"A Becker","year":"2014","unstructured":"Becker, A., Overl\u00f6per, A., Schl\u00fcter, J.-P. & Reinkensmeier, J. Riboregulation in plant-associated \u03b1-proteobacteria. RNA Biol. 11, 550\u2013562. https:\/\/doi.org\/10.4161\/rna.29625 (2014).","journal-title":"RNA Biol."},{"key":"72117_CR24","doi-asserted-by":"publisher","first-page":"345","DOI":"10.1111\/j.1365-2958.2012.08117.x","volume":"85","author":"CC Caswell","year":"2012","unstructured":"Caswell, C. C. et al. Identification of two small regulatory RNAs linked to virulence in Brucella abortus 2308. Mol. Microbiol. 85, 345\u2013360. https:\/\/doi.org\/10.1111\/j.1365-2958.2012.08117.x (2012).","journal-title":"Mol. Microbiol."},{"key":"72117_CR25","doi-asserted-by":"publisher","first-page":"624","DOI":"10.4161\/rna.29145","volume":"11","author":"A Overloper","year":"2014","unstructured":"Overloper, A. et al. Two separate modules of the conserved regulatory RNA AbcR1 address multiple target mRNAs in and outside of the translation initiation region. RNA Biol. 11, 624\u2013640 (2014).","journal-title":"RNA Biol."},{"key":"72117_CR26","doi-asserted-by":"publisher","DOI":"10.1128\/mBio.00473-17","author":"LM Sheehan","year":"2017","unstructured":"Sheehan, L. M. & Caswell, C. C. A 6-nucleotide regulatory motif within the AbcR small RNAs of Brucella abortus mediates host\u2013pathogen interactions. MBio https:\/\/doi.org\/10.1128\/mBio.00473-17 (2017).","journal-title":"MBio"},{"key":"72117_CR27","doi-asserted-by":"publisher","first-page":"e68147","DOI":"10.1371\/journal.pone.0068147","volume":"8","author":"O Torres-Quesada","year":"2013","unstructured":"Torres-Quesada, O. et al. Independent activity of the homologous small regulatory RNAs AbcR1 and AbcR2 in the legume symbiont Sinorhizobium meliloti. PLoS\u00a0One 8, e68147. https:\/\/doi.org\/10.1371\/journal.pone.0068147 (2013).","journal-title":"PLoS\u00a0One"},{"key":"72117_CR28","doi-asserted-by":"publisher","first-page":"563","DOI":"10.4161\/rna.28239","volume":"11","author":"O Torres-Quesada","year":"2014","unstructured":"Torres-Quesada, O. et al. Genome-wide profiling of Hfq-binding RNAs uncovers extensive post-transcriptional rewiring of major stress response and symbiotic regulons in Sinorhizobium meliloti. RNA Biol. 11, 563\u2013579 (2014).","journal-title":"RNA Biol."},{"key":"72117_CR29","doi-asserted-by":"publisher","first-page":"492","DOI":"10.1111\/j.1365-2958.2011.07589.x","volume":"80","author":"I Wilms","year":"2011","unstructured":"Wilms, I., Voss, B., Hess, W. R., Leichert, L. I. & Narberhaus, F. Small RNA-mediated control of the Agrobacterium tumefaciens GABA binding protein. Mol. Microbiol. 80, 492\u2013506. https:\/\/doi.org\/10.1111\/j.1365-2958.2011.07589.x (2011).","journal-title":"Mol. Microbiol."},{"key":"72117_CR30","doi-asserted-by":"publisher","first-page":"880","DOI":"10.1016\/j.molcel.2011.08.022","volume":"43","author":"G Storz","year":"2011","unstructured":"Storz, G., Vogel, J. & Wassarman, K. M. Regulation by small RNAs in bacteria: Expanding frontiers. Mol. Cell 43, 880\u2013891. https:\/\/doi.org\/10.1016\/j.molcel.2011.08.022 (2011).","journal-title":"Mol. Cell"},{"key":"72117_CR31","doi-asserted-by":"publisher","first-page":"24","DOI":"10.1111\/mmi.13869","volume":"107","author":"LM Sheehan","year":"2018","unstructured":"Sheehan, L. M. & Caswell, C. C. An account of evolutionary specialization: The AbcR small RNAs in the Rhizobiales. Mol. Microbiol. 107, 24\u201333. https:\/\/doi.org\/10.1111\/mmi.13869 (2018).","journal-title":"Mol. Microbiol."},{"key":"72117_CR32","doi-asserted-by":"publisher","DOI":"10.1094\/MPMI-02-18-0041-R","author":"G Tang","year":"2018","unstructured":"Tang, G. et al. The LsrB protein is required for Agrobacterium tumefaciens interaction with host plants. Mol. Plant Microbe Interact. https:\/\/doi.org\/10.1094\/MPMI-02-18-0041-R (2018).","journal-title":"Mol. Plant Microbe Interact."},{"key":"72117_CR33","doi-asserted-by":"publisher","first-page":"5053","DOI":"10.1128\/AEM.01098-08","volume":"74","author":"SR Khan","year":"2008","unstructured":"Khan, S. R., Gaines, J., Roop, R. M. 2nd. & Farrand, S. K. Broad-host-range expression vectors with tightly regulated promoters and their use to examine the influence of TraR and TraM expression on Ti plasmid quorum sensing. Appl. Environ. Microbiol. 74, 5053\u20135062. https:\/\/doi.org\/10.1128\/AEM.01098-08 (2008).","journal-title":"Appl. Environ. Microbiol."},{"key":"72117_CR34","doi-asserted-by":"publisher","first-page":"4187","DOI":"10.1093\/bioinformatics\/bti635","volume":"21","author":"R Munch","year":"2005","unstructured":"Munch, R. et al. Virtual Footprint and PRODORIC: An integrative framework for regulon prediction in prokaryotes. Bioinformatics 21, 4187\u20134189. https:\/\/doi.org\/10.1093\/bioinformatics\/bti635 (2005).","journal-title":"Bioinformatics"},{"key":"72117_CR35","doi-asserted-by":"publisher","first-page":"446","DOI":"10.4161\/rna.17212","volume":"9","author":"I Wilms","year":"2012","unstructured":"Wilms, I., Overloper, A., Nowrousian, M., Sharma, C. M. & Narberhaus, F. Deep sequencing uncovers numerous small RNAs on all four replicons of the plant pathogen Agrobacterium tumefaciens. RNA Biol. 9, 446\u2013457. https:\/\/doi.org\/10.4161\/rna.17212 (2012).","journal-title":"RNA Biol."},{"key":"72117_CR36","doi-asserted-by":"publisher","first-page":"2452","DOI":"10.1128\/JB.179.7.2452-2458.1997","volume":"179","author":"JM Kemner","year":"1997","unstructured":"Kemner, J. M., Liang, X. & Nester, E. W. The Agrobacterium tumefaciens virulence gene chvE is part of a putative ABC-type sugar transport operon. J. Bacteriol. 179, 2452\u20132458 (1997).","journal-title":"J. Bacteriol."},{"key":"72117_CR37","doi-asserted-by":"publisher","first-page":"241","DOI":"10.1139\/w08-005","volume":"54","author":"AG Matthysse","year":"2008","unstructured":"Matthysse, A. G., Jaeckel, P. & Jeter, C. attG and attC mutations of Agrobacterium tumefaciens are dominant negative mutations that block attachment and virulence. Can J Microbiol 54, 241\u2013247. https:\/\/doi.org\/10.1139\/w08-005 (2008).","journal-title":"Can J Microbiol"},{"key":"72117_CR38","doi-asserted-by":"publisher","first-page":"4838","DOI":"10.1128\/JB.184.17.4838-4845.2002","volume":"184","author":"L Chen","year":"2002","unstructured":"Chen, L., Chen, Y., Wood, D. W. & Nester, E. W. A new type IV secretion system promotes conjugal transfer in Agrobacterium tumefaciens. J. Bacteriol. 184, 4838\u20134845 (2002).","journal-title":"J. Bacteriol."},{"key":"72117_CR39","doi-asserted-by":"publisher","first-page":"e56682","DOI":"10.1371\/journal.pone.0056682","volume":"8","author":"J Kim","year":"2013","unstructured":"Kim, J., Heindl, J. E. & Fuqua, C. Coordination of division and development influences complex multicellular behavior in Agrobacterium tumefaciens. PLoS\u00a0One 8, e56682. https:\/\/doi.org\/10.1371\/journal.pone.0056682 (2013).","journal-title":"PLoS\u00a0One"},{"key":"72117_CR40","doi-asserted-by":"publisher","first-page":"816","DOI":"10.1128\/JB.00668-15","volume":"198","author":"JE Heindl","year":"2015","unstructured":"Heindl, J. E. et al. Discrete responses to limitation for iron and manganese in Agrobacterium tumefaciens: Influence on attachment and biofilm formation. J. Bacteriol. 198, 816\u2013829. https:\/\/doi.org\/10.1128\/JB.00668-15 (2015).","journal-title":"J. Bacteriol."},{"key":"72117_CR41","doi-asserted-by":"publisher","first-page":"167","DOI":"10.1016\/S0378-1097(03)00511-1","volume":"225","author":"W Eiamphungporn","year":"2003","unstructured":"Eiamphungporn, W., Nakjarung, K., Prapagdee, B., Vattanaviboon, P. & Mongkolsuk, S. Oxidant-inducible resistance to hydrogen peroxide killing in Agrobacterium tumefaciens requires the global peroxide sensor-regulator OxyR and KatA. FEMS Microbiol. Lett. 225, 167\u2013172 (2003).","journal-title":"FEMS Microbiol. Lett."},{"key":"72117_CR42","doi-asserted-by":"publisher","first-page":"41","DOI":"10.1016\/S0006-291X(03)00535-7","volume":"304","author":"K Nakjarung","year":"2003","unstructured":"Nakjarung, K., Mongkolsuk, S. & Vattanaviboon, P. The oxyR from Agrobacterium tumefaciens: Evaluation of its role in the regulation of catalase and peroxide responses. Biochem. Biophys. Res. Commun. 304, 41\u201347 (2003).","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"72117_CR43","doi-asserted-by":"publisher","DOI":"10.1128\/JB.00127-18","author":"JA Budnick","year":"2018","unstructured":"Budnick, J. A., Sheehan, L. M., Kang, L., Michalak, P. & Caswell, C. C. Characterization of three small proteins in Brucella abortus linked to fucose utilization. J. Bacteriol. https:\/\/doi.org\/10.1128\/JB.00127-18 (2018).","journal-title":"J. Bacteriol."},{"key":"72117_CR44","doi-asserted-by":"publisher","first-page":"87","DOI":"10.1093\/dnares\/5.2.87","volume":"5","author":"Y Liang","year":"1998","unstructured":"Liang, Y., Aoyama, T. & Oka, A. Structural characterization of the virB operon on the hairy-root-inducing plasmid A4. DNA Res. 5, 87\u201393 (1998).","journal-title":"DNA Res."},{"key":"72117_CR45","doi-asserted-by":"publisher","first-page":"337","DOI":"10.1016\/0378-1119(86)90117-4","volume":"41","author":"BG Spratt","year":"1986","unstructured":"Spratt, B. G., Hedge, P. J., te Heesen, S., Edelman, A. & Broome-Smith, J. K. Kanamycin-resistant vectors that are analogues of plasmids pUC8, pUC9, pEMBL8 and pEMBL9. Gene 41, 337\u2013342 (1986).","journal-title":"Gene"},{"key":"72117_CR46","doi-asserted-by":"publisher","first-page":"1","DOI":"10.2174\/1875036201307010001","volume":"7","author":"E Aronesty","year":"2013","unstructured":"Aronesty, E. Comparison of sequencing utility programs. Open Bioinform. J. 7, 1\u20138. https:\/\/doi.org\/10.2174\/1875036201307010001 (2013).","journal-title":"Open Bioinform. J."},{"key":"72117_CR47","doi-asserted-by":"publisher","first-page":"1754","DOI":"10.1093\/bioinformatics\/btp324","volume":"25","author":"H Li","year":"2009","unstructured":"Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows\u2013Wheeler transform. Bioinformatics 25, 1754\u20131760. https:\/\/doi.org\/10.1093\/bioinformatics\/btp324 (2009).","journal-title":"Bioinformatics"},{"key":"72117_CR48","doi-asserted-by":"publisher","first-page":"139","DOI":"10.1093\/bioinformatics\/btp616","volume":"26","author":"MD Robinson","year":"2010","unstructured":"Robinson, M. D., McCarthy, D. J. & Smyth, G. K. edgeR: A Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139\u2013140. https:\/\/doi.org\/10.1093\/bioinformatics\/btp616 (2010).","journal-title":"Bioinformatics"},{"key":"72117_CR49","doi-asserted-by":"publisher","first-page":"1582","DOI":"10.1128\/JB.02543-14","volume":"197","author":"LM Sheehan","year":"2015","unstructured":"Sheehan, L. M., Budnick, J. A., Roop, R. M. 2nd. & Caswell, C. C. Coordinated zinc homeostasis is essential for the wild-type virulence of Brucella abortus. J. Bacteriol. 197, 1582\u20131591. https:\/\/doi.org\/10.1128\/JB.02543-14 (2015).","journal-title":"J. Bacteriol."},{"key":"72117_CR50","doi-asserted-by":"publisher","first-page":"e45","DOI":"10.1093\/nar\/29.9.e45","volume":"29","author":"MW Pfaffl","year":"2001","unstructured":"Pfaffl, M. W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45 (2001).","journal-title":"Nucleic Acids Res."}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41598-020-72117-0.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-020-72117-0","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-020-72117-0.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,12,6]],"date-time":"2022-12-06T13:53:09Z","timestamp":1670334789000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41598-020-72117-0"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,9,11]]},"references-count":50,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2020,12]]}},"alternative-id":["72117"],"URL":"https:\/\/doi.org\/10.1038\/s41598-020-72117-0","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,9,11]]},"assertion":[{"value":"12 March 2020","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"17 July 2020","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"11 September 2020","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"14968"}}