1887

Abstract

is a genus of soil bacteria, some isolates of which form an endosymbiotic relationship with diverse legumes of the Loteae tribe. The symbiotic genes of these mesorhizobia are generally carried on integrative and conjugative elements termed symbiosis islands (ICESyms). strains that nodulate spp. have been divided into host-range groupings. Group I (GI) strains nodulate and ecotype Gifu, while group II (GII) strains have a broader host range, which includes . To identify the basis of this extended host range, and better understand and ICESym genomics, the genomes of eight strains were completed using hybrid long- and short-read assembly. Bioinformatic comparison with previously sequenced mesorhizobia genomes indicated host range was not predicted by genospecies but rather by the evolutionary relationship between ICESym symbiotic regions. Three radiating lineages of Loteae ICESyms were identified on this basis, which correlate with spp. host-range grouping and have lineage-specific gene complements. Pangenomic analysis of the completed GI and GII ICESyms identified 155 core genes (on average 30.1 % of a given ICESym). Individual GI or GII ICESyms carried diverse accessory genes with an average of 34.6 % of genes unique to a given ICESym. Identification and comparative analysis of NodD symbiotic regulatory motifs – boxes – identified 21 branches across the NodD regulons. Four of these branches were associated with seven genes unique to the five GII ICESyms. The boxes preceding the host-range gene in GI and GII ICESyms were disparate, suggesting regulation of may differ between GI and GII ICESyms. The broad host-range determinant(s) of GII ICESyms that confer nodulation of are likely present amongst the 53 GII-unique genes identified.

Funding
This study was supported by the:
  • University of Otago School of Biomedical Sciences Dean’s Bequest Fund
    • Principle Award Recipient: Clive W. Ronson
  • University of Otago Research Committee
    • Principle Award Recipient: Clive W. Ronson
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
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2024-10-03
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References

  1. Sullivan JT, Patrick HN, Lowther WL, Scott DB, Ronson CW. Nodulating strains of Rhizobium loti arise through chromosomal symbiotic gene transfer in the environment. Proc Natl Acad Sci U S A 1995; 92:8985–8989 [View Article]
    [Google Scholar]
  2. Sullivan JT, Ronson CW. Evolution of rhizobia by acquisition of a 500-kb symbiosis island that integrates into a phe-tRNA gene. Proc Natl Acad Sci U S A 1998; 95:5145–5149 [View Article][PubMed]
    [Google Scholar]
  3. Sullivan JT, Trzebiatowski JR, Cruickshank RW, Gouzy J, Brown SD et al. Comparative sequence analysis of the symbiosis island of Mesorhizobium loti strain R7A. J Bacteriol 2002; 184:3086–3095 [View Article][PubMed]
    [Google Scholar]
  4. Kasai-Maita H, Hirakawa H, Nakamura Y, Kaneko T, Miki K et al. Commonalities and differences among symbiosis islands of three Mesorhizobium loti strains. Microbes Environ 2013; 28:275–278 [View Article][PubMed]
    [Google Scholar]
  5. Haskett TL, Ramsay JP, Bekuma AA, Sullivan JT, O’Hara GW et al. Evolutionary persistence of tripartite integrative and conjugative elements. Plasmid 2017; 92:30–36
    [Google Scholar]
  6. Nandasena KG, O'Hara GW, Tiwari RP, Sezmiş E, Howieson JG. In situ lateral transfer of symbiosis islands results in rapid evolution of diverse competitive strains of mesorhizobia suboptimal in symbiotic nitrogen fixation on the pasture legume Biserrula pelecinus L. Environ Microbiol 2007; 9:2496–2511 [View Article][PubMed]
    [Google Scholar]
  7. Poole P, Ramachandran V, Terpolilli J. Rhizobia: from saprophytes to endosymbionts. Nat Rev Microbiol 2018; 16:291–303 [View Article][PubMed]
    [Google Scholar]
  8. Rodpothong P, Sullivan JT, Songsrirote K, Sumpton D, Cheung KWJ-T et al. Nodulation gene mutants of Mesorhizobium loti R7A-nodZ and nolL mutants have host-specific phenotypes on Lotus spp. Mol Plant Microbe Interact 2009; 22:1546–1554 [View Article][PubMed]
    [Google Scholar]
  9. Madsen LH, Tirichine L, Jurkiewicz A, Sullivan JT, Heckmann AB et al. The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus . Nat Commun 2010; 1:ncomms1009 [View Article][PubMed]
    [Google Scholar]
  10. Mulligan JT, Long SR. Induction of Rhizobium meliloti nodC expression by plant exudate requires nodD . Proc Natl Acad Sci U S A 1985; 82:6609–6613 [View Article][PubMed]
    [Google Scholar]
  11. Rostas K, Kondorosi E, Horvath B, Simoncsits A, Kondorosi A. Conservation of extended promoter regions of nodulation genes in Rhizobium . Proc Natl Acad Sci U S A 1986; 83:1757–1761 [View Article][PubMed]
    [Google Scholar]
  12. Hong GF, Burn JE, Johnston AW. Evidence that DNA involved in the expression of nodulation (nod) genes in Rhizobium binds to the product of the regulatory gene nodD . Nucleic Acids Res 1987; 15:9677–9690 [View Article][PubMed]
    [Google Scholar]
  13. Fisher RF, Egelhoff TT, Mulligan JT, Long SR. Specific binding of proteins from Rhizobium meliloti cell-free extracts containing NodD to DNA sequences upstream of inducible nodulation genes. Genes Dev 1988; 2:282–293 [View Article][PubMed]
    [Google Scholar]
  14. Hu H, Liu S, Yang Y, Chang W, Hong G. In Rhizobium leguminosarum, NodD represses its own transcription by competing with RNA polymerase for binding sites. Nucleic Acids Res 2000; 28:2784–2793 [View Article][PubMed]
    [Google Scholar]
  15. Chen X-C, Feng J, Hou B-H, Li F-Q, Li Q et al. Modulating DNA bending affects NodD-mediated transcriptional control in Rhizobium leguminosarum . Nucleic Acids Res 2005; 33:2540–2548 [View Article][PubMed]
    [Google Scholar]
  16. Peck MC, Fisher RF, Long SR. Diverse flavonoids stimulate NodD1 binding to nod gene promoters in Sinorhizobium meliloti . J Bacteriol 2006; 188:5417–5427 [View Article][PubMed]
    [Google Scholar]
  17. Dénarié J, Debellé F, Promé JC. Rhizobium lipo-chitooligosaccharide nodulation factors: signaling molecules mediating recognition and morphogenesis. Annu Rev Biochem 1996; 65:503–535 [View Article][PubMed]
    [Google Scholar]
  18. Poinsot V, Couderc F. Formation of lipochitin oligosaccharide signaling molecules. In Geiger O. editor Biogenesis of Fatty Acids, Lipids and Membranes Cham: Springer International Publishing; 2017 pp 1–23
    [Google Scholar]
  19. Economou A, Davies AE, Johnston AWB, Downie JA. The Rhizobium leguminosarum biovar viciae nodO gene can enable a nodE mutant of Rhizobium leguminosarum biovar trifolii to nodulate vetch. Microbiology 1994; 140:2341–2347 [View Article]
    [Google Scholar]
  20. Viprey V, Del Greco A, Golinowski W, Broughton WJ, Perret X. Symbiotic implications of Type III protein secretion machinery in Rhizobium . Mol Microbiol 1998; 28:1381–1389 [View Article][PubMed]
    [Google Scholar]
  21. Krause A, Doerfel A, Göttfert M. Mutational and transcriptional analysis of the Type III secretion system of Bradyrhizobium japonicum . Mol Plant-Microbe Interact 2002; 15:1228–1235
    [Google Scholar]
  22. Hubber AM, Sullivan JT, Ronson CW. Symbiosis-induced cascade regulation of the Mesorhizobium loti R7A VirB/D4 Type IV secretion system. Mol Plant Microbe Interact 2007; 20:255–261
    [Google Scholar]
  23. Sugawara M, Takahashi S, Umehara Y, Iwano H, Tsurumaru H et al. Variation in bradyrhizobial NopP effector determines symbiotic incompatibility with Rj2-soybeans via effector-triggered immunity. Nat Commun 2018; 9:6–10 [View Article]
    [Google Scholar]
  24. Teulet A, Busset N, Fardoux J, Gully D, Chaintreuil C et al. The rhizobial Type III effector ErnA confers the ability to form nodules in legumes. Proc Natl Acad Sci U S A 2019; 116:21758–21768
    [Google Scholar]
  25. Kusakabe S, Higasitani N, Kaneko T, Yasuda M, Miwa H et al. Lotus accessions possess multiple checkpoints triggered by different Type III secretion system effectors of the wide-host-range symbiont Bradyrhizobium elkanii USDA61. Microbes Environ 2020; 35:1–16 [View Article]
    [Google Scholar]
  26. Salinero-Lanzarote A, Pacheco-Moreno A, Domingo-Serrano L, Durán D, Ormeño-Orrillo E et al. The Type VI secretion system of Rhizobium etli Mim1 has a positive effect in symbiosis. FEMS Microbiol Ecol 2019; 95:fiz054 [View Article][PubMed]
    [Google Scholar]
  27. Finan TM, Hirsch AM, Leigh JA, Johansen E, Kuldau GA et al. Symbiotic mutants of Rhizobium meliloti that uncouple plant from bacterial differentiation. Cell 1985; 40:869–877 [View Article][PubMed]
    [Google Scholar]
  28. Hotter GS, Scott DB. Exopolysaccharide mutants of Rhizobium loti are fully effective on a determinate nodulating host but are ineffective on an indeterminate nodulating host. J Bacteriol 1991; 173:851–859 [View Article][PubMed]
    [Google Scholar]
  29. Leigh JA, Signer ER, Walker GC. Exopolysaccharide-deficient mutants of Rhizobium meliloti that form ineffective nodules. Proc Natl Acad Sci U S A 1985; 82:6231–6235 [View Article][PubMed]
    [Google Scholar]
  30. Borthakur D, Barber CE, Lamb JW, Daniels MJ, Downie JA et al. A mutation that blocks exopolysaccharide synthesis prevents nodulation of peas by Rhizobium leguminosarum but not of beans by R. phaseoli and is corrected by cloned DNA from Rhizobium or the phytopathogen Xanthomonas . Mol Gen Genet 1986; 203:320–323 [View Article]
    [Google Scholar]
  31. Glazebrook J, Walker GC. A novel exopolysaccharide can function in place of the Calcofluor-binding exopolysaccharide in nodulation of alfalfa by Rhizobium meliloti . Cell 1989; 56:661–672 [View Article]
    [Google Scholar]
  32. Parniske M. ExoB mutants of Bradyrhizobium japonicum with reduced competitiveness for nodulation of Glycine max . Mol Plant-Microbe Interact 1993; 6:99
    [Google Scholar]
  33. Kelly SJ, Muszyński A, Kawaharada Y, Hubber AM, Sullivan JT et al. Conditional requirement for exopolysaccharide in the Mesorhizobium-Lotus symbiosis. Mol Plant-Microbe Interact 2013; 26:319–329 [View Article][PubMed]
    [Google Scholar]
  34. Allan GJ, Zimmer EA, Wagner WL, Sokoloff DD. Molecular phylogenetic analyses of tribe Loteae (Leguminosae): implications for classification and biogeography. Adv Legum Syst 2003371–393
    [Google Scholar]
  35. Degtjareva GV, Kramina TE, Sokoloff DD, Samigullin TH, Valiejo-Roman CM et al. Phylogeny of the genus Lotus (Leguminosae, Loteae): evidence from nrITS sequences and morphology. Can J Bot 2006; 84:813–830 [View Article]
    [Google Scholar]
  36. Degtjareva G V, Kramina TE, Sokoloff DD, Samigullin TH, Sandral GA et al. New data on nrITS phylogeny of Lotus (Leguminosae, Loteae). Wulfenia 2008; 15:35–49
    [Google Scholar]
  37. Charlton JFL, Wilson ERL, Ross MD. Plant introduction trials. New Zealand Journal of Experimental Agriculture 1978; 6:201–206 [View Article]
    [Google Scholar]
  38. Bailey RW, Greenwood RM, Craig A. Extracellular polysaccharides of Rhizobium strains associated with Lotus species. J Gen Microbiol 1971; 65:315–324 [View Article]
    [Google Scholar]
  39. Charlton JFL, Greenwood RM, Clark KW. Comparison of the effectiveness of Rhizobium strains during establishment of Lotus corniculatus in hill country. New Zealand Journal of Experimental Agriculture 1981; 9:173–177 [View Article]
    [Google Scholar]
  40. Crow VL, Jarvis BDW, Greenwood RM. Deoxyribonucleic acid homologies among acid-producing strains of Rhizobium . Int J Syst Bacteriol 1981; 31:152–172 [View Article]
    [Google Scholar]
  41. Jarvis BDW, Pankhurst CE, Patel JJ. Rhizobium loti, a new species of legume root nodule bacteria. Int J Syst Bacteriol 1982; 32:378–380 [View Article]
    [Google Scholar]
  42. Handberg K, Stougaard J. Lotus japonicus, an autogamous, diploid legume species for classical and molecular genetics. Plant J 1992; 2:487–496 [View Article]
    [Google Scholar]
  43. Pankhurst CE, Hopcroft DH, Jones WT. Comparative morphology and flavolan content of Rhizobium loti induced effective and ineffective root nodules on Lotus species, Leuceana leucocephala, Carmichaelia flagelliformis, Ornithopus sativus, and Clianthus puniceus . Can J Bot 1987; 65:2676–2685 [View Article]
    [Google Scholar]
  44. Lorite MJ, Estrella MJ, Escaray FJ, Sannazzaro A, Videira e Castro IM et al. The rhizobia-Lotus symbioses: deeply specific and widely diverse. Front Microbiol 2018; 9:1–17 [View Article]
    [Google Scholar]
  45. Ronson CW, Astwood PM, Nixon BT, Ausubel FM. Deduced products of C4-dicarboxylate transport regulatory genes of Rhizobium leguminosarum are homologous to nitrogen regulatory gene products. Nucleic Acids Res 1987; 15:7921–7934 [View Article][PubMed]
    [Google Scholar]
  46. Meade HM, Long SR, Ruvkun GB, Brown SE, Ausubel FM. Physical and genetic characterization of symbiotic and auxotrophic mutants of Rhizobium meliloti induced by transposon Tn5 mutagenesis. J Bacteriol 1982; 149:114–122 [View Article][PubMed]
    [Google Scholar]
  47. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article][PubMed]
    [Google Scholar]
  48. Nikolenko SI, Korobeynikov AI, Alekseyev MA. BayesHammer: Bayesian clustering for error correction in single-cell sequencing. BMC Genomics 2013; 14 Suppl 1:S7 [View Article][PubMed]
    [Google Scholar]
  49. Salmela L, Rivals E. LoRDEC: accurate and efficient long read error correction. Bioinformatics 2014; 30:3506–3514 [View Article][PubMed]
    [Google Scholar]
  50. Lin Y, Yuan J, Kolmogorov M, Shen MW, Chaisson M et al. Assembly of long error-prone reads using de Bruijn graphs. Proc Natl Acad Sci U S A 2016; 113:E8396–E8405 [View Article][PubMed]
    [Google Scholar]
  51. Wick RR, Judd LM, Gorrie CL, Holt KE. Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol 2017; 13:e1005595–22 [View Article]
    [Google Scholar]
  52. Hunt M, Silva ND, Otto TD, Parkhill J, Keane JA et al. Circlator: automated circularization of genome assemblies using long sequencing reads. Genome Biol 2015; 16:1–10 [View Article]
    [Google Scholar]
  53. Tatusova T, DiCuccio M, Badretdin A, Chetvernin V, Nawrocki EP et al. NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res 2016; 44:6614–6624 [View Article][PubMed]
    [Google Scholar]
  54. Haskett TL, Terpolilli JJ, Bekuma A, O'Hara GW, Sullivan JT et al. Assembly and transfer of tripartite integrative and conjugative genetic elements. Proc Natl Acad Sci U S A 2016; 113:12268–12273 [View Article][PubMed]
    [Google Scholar]
  55. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article][PubMed]
    [Google Scholar]
  56. Darling ACE, Mau B, Blattner FR, Perna NT. Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 2004; 14:1394–1403 [View Article][PubMed]
    [Google Scholar]
  57. Eddy SR. Accelerated profile HMM searches. PLoS Comput Biol 2011; 7:e1002195 [View Article][PubMed]
    [Google Scholar]
  58. Wheeler TJ, Eddy SR. nhmmer: DNA homology search with profile HMMs. Bioinformatics 2013; 29:2487–2489 [View Article][PubMed]
    [Google Scholar]
  59. Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 2016; 33:1870–1874 [View Article][PubMed]
    [Google Scholar]
  60. Page AJ, Cummins CA, Hunt M, Wong VK, Reuter S et al. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics 2015; 31:3691–3693 [View Article][PubMed]
    [Google Scholar]
  61. Brynildsrud O, Bohlin J, Scheffer L, Eldholm V. Rapid scoring of genes in microbial pan-genome-wide association studies with Scoary. Genome Biol 2016; 17:1–9 [View Article]
    [Google Scholar]
  62. Huerta-Cepas J, Forslund K, Coelho LP, Szklarczyk D, Jensen LJ et al. Fast genome-wide functional annotation through orthology assignment by eggNOG-mapper. Mol Biol Evol 2017; 34:2115–2122 [View Article][PubMed]
    [Google Scholar]
  63. Huerta-Cepas J, Szklarczyk D, Heller D, Hernández-Plaza A, Forslund SK et al. eggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses. Nucleic Acids Res 2019; 47:D309–D314 [View Article][PubMed]
    [Google Scholar]
  64. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J et al. BLAST+: architecture and applications. BMC Bioinformatics 2009; 10:421–429 [View Article]
    [Google Scholar]
  65. Jain C, Rodriguez-R LM, Phillippy AM, Konstantinidis KT, Aluru S. High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries. Nat Commun 2018; 9:1–8 [View Article]
    [Google Scholar]
  66. R Core Team 2020; R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
  67. Galili T, O'Callaghan A, Sidi J, Sievert C. heatmaply: an R package for creating interactive cluster heatmaps for online publishing. Bioinformatics 2018; 34:1600–1602 [View Article][PubMed]
    [Google Scholar]
  68. Kaneko T, Nakamura Y, Sato S, Asamizu E, Kato T et al. Complete genome structure of the nitrogen-fixing symbiotic bacterium Mesorhizobium loti . DNA Res 2000; 7:331–338 [View Article][PubMed]
    [Google Scholar]
  69. Kelly S, Sullivan J, Ronson C, Tian R, Bräu L et al. Genome sequence of the Lotus spp. microsymbiont Mesorhizobium loti strain R7A. Stand Genomic Sci 2014; 9:6 [View Article][PubMed]
    [Google Scholar]
  70. Reeve W, Sullivan J, Ronson C, Tian R, Bräu L et al. Genome sequence of the Lotus corniculatus microsymbiont Mesorhizobium loti strain R88B. Stand Genomic Sci 2014; 9:3 [View Article][PubMed]
    [Google Scholar]
  71. Martínez-Hidalgo P, Ramírez-Bahena MH, Flores-Félix JD, Rivas R, Igual JM, Martínez-Molina E, Mateos PF, Velázquez E, Á P et al. Revision of the taxonomic status of type strains of Mesorhizobium loti and reclassification of strain USDA 3471T as the type strain of Mesorhizobium erdmanii sp. nov. and ATCC 33669T as the type strain of Mesorhizobium jarvisii sp. nov. Int J Syst Evol Microbiol 2015; 65:1703–1708 [View Article][PubMed]
    [Google Scholar]
  72. Stepkowski T, Rudzinska A, Biesiadka J, Legocki AB. Characterization of the nodulation functions in Bradyrhizobium sp. WM9 (Lupinus). In Elmerich C, Kondorosi A, Newton WE. (editors) Biological Nitrogen Fixation for the 21st Century Dordrecht: Springer Netherlands; 1998 p 242
    [Google Scholar]
  73. Stepkowski T, Świderska A, Miedzinska K, Czaplińska M, Świderski M et al. Low sequence similarity and gene content of symbiotic clusters of Bradyrhizobium sp. WM9 (Lupinus) indicate early divergence of "lupin" lineage in the genus Bradyrhizobium . Antonie Van Leeuwenhoek 2003; 84:115–124 [View Article][PubMed]
    [Google Scholar]
  74. Bras CP, Jordá MA, Wijfjes AHM, Harteveld M, Stuurman N et al. A Lotus japonicus nodulation system based on heterologous expression of the fucosyl transferase NodZ and the acetyl transferase NoIL in Rhizobium leguminosarum . Mol Plant Microbe Interact 2000; 13:475–479
    [Google Scholar]
  75. de Lajudie PM, Andrews M, Ardley J, Eardly B, Jumas-Bilak E et al. Minimal standards for the description of new genera and species of rhizobia and agrobacteria. Int J Syst Evol Microbiol 2019; 69:1852–1863 [View Article][PubMed]
    [Google Scholar]
  76. Howieson JG, Ballard RA, Yates RJ, Charman N. Selecting improved Lotus nodulating rhizobia to expedite the development of new forage species. Plant Soil 2011; 348:231–243 [View Article]
    [Google Scholar]
  77. Sannazzaro AI, Torres Tejerizo G, Fontana MF, Cumpa Velásquez LM, Hansen LH et al. Mesorhizobium sanjuanii sp. nov., isolated from nodules of Lotus tenuis in the saline-alkaline lowlands of flooding Pampa, Argentina. Int J Syst Evol Microbiol 2018; 68:2936–2942 [View Article][PubMed]
    [Google Scholar]
  78. Greenlon A, Chang PL, Damtew ZM, Muleta A, Carrasquilla-Garcia N et al. Global-level population genomics reveals differential effects of geography and phylogeny on horizontal gene transfer in soil bacteria. Proc Natl Acad Sci U S A 2019; 116:15200–15209 [View Article][PubMed]
    [Google Scholar]
  79. Estrella MJ, Fontana MF, Cumpa Velásquez LM, Torres Tejerizo GA, Diambra L et al. Mesorhizobium intechi sp. nov. isolated from nodules of Lotus tenuis in soils of the Flooding Pampa, Argentina. Syst Appl Microbiol 2020; 43:126044 [View Article][PubMed]
    [Google Scholar]
  80. Armas-Capote N, Pérez-Yépez J, Martínez-Hidalgo P, Garzón-Machado V, Del Arco-Aguilar M et al. Core and symbiotic genes reveal nine Mesorhizobium genospecies and three symbiotic lineages among the rhizobia nodulating Cicer canariense in its natural habitat (La Palma, Canary Islands). Syst Appl Microbiol 2014; 37:140–148 [View Article][PubMed]
    [Google Scholar]
  81. Ramsay JP, Sullivan JT, Stuart GS, Lamont IL, Ronson CW. Excision and transfer of the Mesorhizobium loti R7A symbiosis island requires an integrase IntS, a novel recombination directionality factor RdfS, and a putative relaxase RlxS. Mol Microbiol 2006; 62:723–734 [View Article][PubMed]
    [Google Scholar]
  82. Linhartová I, Bumba L, Mašín J, Basler M, Osička R et al. RTX proteins: a highly diverse family secreted by a common mechanism. FEMS Microbiol Rev 2010; 34:1076–1112 [View Article][PubMed]
    [Google Scholar]
  83. Sutton JM, Lea EJ, Downie JA. The nodulation-signaling protein NodO from Rhizobium leguminosarum biovar viciae forms ion channels in membranes. Proc Natl Acad Sci U S A 1994; 91:9990–9994 [View Article][PubMed]
    [Google Scholar]
  84. Sullivan JT, Brown SD, Ronson CW. The NifA-RpoN regulon of Mesorhizobium loti strain R7A and its symbiotic activation by a novel LacI/GalR-family regulator. PLoS One 2013; 8:e53762 [View Article][PubMed]
    [Google Scholar]
  85. Barnett MJ, Swanson JA, Long SR. Multiple genetic controls on Rhizobium meliloti syrA, a regulator of exopolysaccharide abundance. Genetics 1998; 148:19–32[PubMed]
    [Google Scholar]
  86. Kawaharada Y, Kelly S, Nielsen MW, Hjuler CT, Gysel K et al. Receptor-mediated exopolysaccharide perception controls bacterial infection. Nature 2015; 523:308–312 [View Article][PubMed]
    [Google Scholar]
  87. Kawaharada Y, Nielsen MW, Kelly S, James EK, Andersen KR et al. Differential regulation of the Epr3 receptor coordinates membrane-restricted rhizobial colonization of root nodule primordia. Nat Commun 2017; 8:14534 [View Article][PubMed]
    [Google Scholar]
  88. Hritonenko V, Stathopoulos C. Omptin proteins: an expanding family of outer membrane proteases in Gram-negative Enterobacteriaceae. Mol Membr Biol 2007; 24:395–406 [View Article][PubMed]
    [Google Scholar]
  89. Brennan RG. DNA recognition by the helix-turn-helix motif. Curr Opin Struct Biol 1992; 2:100–108 [View Article]
    [Google Scholar]
  90. Kostiuk N V, Belyakova MB, Leshchenko D V, Miniaev M V, Petrova MB et al. Structural characterization of the NodD transcription factor. Am J Bioinforma Res 2013; 3:35–41
    [Google Scholar]
  91. Peck MC, Fisher RF, Bliss R, Long SR. Isolation and characterization of mutant Sinorhizobium meliloti NodD1 proteins with altered responses to luteolin. J Bacteriol 2013; 195:3714–3723 [View Article][PubMed]
    [Google Scholar]
  92. Kelly S, Sullivan JT, Kawaharada Y, Radutoiu S, Ronson CW et al. Regulation of Nod factor biosynthesis by alternative NodD proteins at distinct stages of symbiosis provides additional compatibility scrutiny. Environ Microbiol 2018; 20:97–110 [View Article]
    [Google Scholar]
  93. Kobayashi H, Naciri-Graven Y, Broughton WJ, Perret X. Flavonoids induce temporal shifts in gene-expression of nod-box controlled loci in Rhizobium sp. NGR234. Mol Microbiol 2004; 51:335–347 [View Article][PubMed]
    [Google Scholar]
  94. Ramsay JP, Tester LGL, Major AS, Sullivan JT, Edgar CD et al. Ribosomal frameshifting and dual-target antiactivation restrict quorum-sensing-activated transfer of a mobile genetic element. Proc Natl Acad Sci U S A 2015; 112:4104–4109 [View Article][PubMed]
    [Google Scholar]
  95. Sullivan JT, Brown SD, Yocum RR, Ronson CW. The bio operon on the acquired symbiosis island of Mesorhizobium sp. strain R7A includes a novel gene involved in pimeloyl-CoA synthesis. Microbiology 2001; 147:1315–1322 [View Article][PubMed]
    [Google Scholar]
  96. Tatsukami Y, Ueda M, Ueda M. Rhizobial gibberellin negatively regulates host nodule number. Sci Rep 2016; 6:1–11 [View Article]
    [Google Scholar]
  97. Nukui N, Minamisawa K, Ayabe S-I, Aoki T. Expression of the 1-aminocyclopropane-1-carboxylic acid deaminase gene requires symbiotic nitrogen-fixing regulator gene nifA2 in Mesorhizobium loti MAFF303099. Appl Environ Microbiol 2006; 72:4964–4969 [View Article][PubMed]
    [Google Scholar]
  98. Robledo M, Peregrina A, Millán V, García-Tomsig NI, Torres-Quesada O et al. A conserved α-proteobacterial small RNA contributes to osmoadaptation and symbiotic efficiency of rhizobia on legume roots. Environ Microbiol 2017; 19:2661–2680 [View Article][PubMed]
    [Google Scholar]
  99. Maynaud G, Brunel B, Mornico D, Durot M, Severac D et al. Genome-wide transcriptional responses of two metal-tolerant symbiotic Mesorhizobium isolates to Zinc and Cadmium exposure. BMC Genomics 2013; 14:292 [View Article]
    [Google Scholar]
  100. Porter SS, Chang PL, Conow CA, Dunham JP, Friesen ML. Association mapping reveals novel serpentine adaptation gene clusters in a population of symbiotic Mesorhizobium . ISME J 2017; 11:248–262 [View Article][PubMed]
    [Google Scholar]
  101. Ampomah OY, Huss-Danell K. Genetic diversity of root nodule bacteria nodulating Lotus corniculatus and Anthyllis vulneraria in Sweden. Syst Appl Microbiol 2011; 34:267–275 [View Article][PubMed]
    [Google Scholar]
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