Rhizobium Symbiosis and Regulation Networks: Comparison
View Latest Version
Please note this is a comparison between Version 2 by Jessie Wu and Version 1 by Chang-Fu Tian.

Rhizobia refer to a polyphyletic group of Gram-negative bacteria that induce nodule formation on roots, or occasionally stems, of leguminous plants, where they reduce N2 into ammonia. The rhizobium symbiosis involves biological processes including communication with plant host, migration to the rhizosphere, rhizoplane colonization, induction of nodule and infection thread, intracellular host infection, accommodation in the plant cell, morphological differentiation, lifestyle change and cell function specialization. This represents a typical complicated trait that needs not only key symbiosis genes but also a large number of core and lineage-specific functions. 

  • rhizobia
  • adaptive evolution
  • symbiosis
  • nitrogen fixation
  • nodulation

1. Recruitment of Indigenous Functions to Support Symbiosis

Like any bacteria-plant interactions, the rhizobium–legume symbiosis is a complex and delicate process, which involves the cooperation of multiple cellular functions. Metabolic modeling of S. meliloti suggests that chromid genes are more actively involved in rhizosphere fitness than in bulk soils, while chromosome has a similar contribution to fitness in two niches [116,117][1][2]. A large number of R. leguminosarum genes are differentially expressed in rhizospheres of pea, alfalfa and sugar beet [118][3]. Some host-specific genes are related to C metabolism, and many are located on the non-symbiosis accessory plasmids [118][3]. These findings indicate that non-symbiosis genes are extensively involved in rhizosphere fitness. By using the transposon insertion sequencing method, about 600 genes of R. leguminosarum are identified as fitness genes during lifestyle adaptations from rhizosphere to symbiosis with pea plants [115][4]. Comparative transcriptomics independently demonstrates that hundreds of rhizobial genes are differentially expressed in nodules compared to free-living cells [114,119,120,121,122][5][6][7][8][9]. Metabolic modeling suggests global coordination of carbon and nitrogen allocation in bacteroids [123][10]. The broad-host-range strain S. fredii NGR234 shows considerable differences in transcriptomes of bacteroids in Leucaena leucocephala and Vigna unguiculata [121][8]. Key nitrogen fixation genes on the symbiosis plasmid of S. fredii strains in Glycine nodules are characterized by high connectivity in both intra- and inter-replicon co-expression analyses [114][5], which allow further identification of chromosomal core znu and accessory mdt operons involved in host-specific symbiotic adaptation [114][5]. However, functional characterizations post genome-wide surveys are usually limited [114,115][4][5].
Based on scattered genetic and molecular biological evidence, a general picture of extensive recruitment of core and accessory functions, in addition to key nodulation and nitrogen fixation genes, in optimizing symbiotic efficiency has been proposed earlier [16,17][11][12]. The list of core and accessory functions contributing to rhizobial fitness, from rhizosphere to rhizoplane to nodules, is ever-increasing (above 900 genes) and usually in a strain–host-dependent manner [52][13], e.g., motility and chemotaxis [124][14], surface polysaccharides [125[15][16][17][18][19],126,127,128,129], outer membrane vesicles [130][20], quorum sensing [131,132,133,134[21][22][23][24][25],135], T1SS, T3SS, T4SS and T6SS [136[26][27][28][29][30][31][32],137,138,139,140,141,142], dicarboxylate transport [143][33], poly-3-hydroxybutyrate [144,145[34][35][36],146], transporters of branched amino acids [147[37][38][39],148,149], uptake of ions (phosphorus [150[40][41][42],151,152], potassium [153[43][44],154], molybdenum [155][45], iron [156,157][46][47], sulfur [155][45], zinc [94][48] and manganese [158][49]), nitrate reduction [40][50], NO modulation [159[51][52],160], oxygen limitation responses [40,161,162[50][53][54][55],163], cell cycle [164[56][57][58],165,166], peptide importers [167[59][60][61][62][63],168,169,170,171], regulatory non-coding RNAs (e.g., globally acting trans-small RNA AbcR1/2 and those fragments derived from transfer RNA) [172,173][64][65] and carbon–nitrogen metabolism coordination by nitrogen-related phosphotransferase system [153,174,175][43][66][67]. These efforts indicate that the successful integration of key nodulation and nitrogen fixation circuits in various bacterial recipients involves systematic and dynamic coordination with other functions during the establishment of symbiosis.

2. Integration of Key Symbiosis Circuits with Recipient Regulation Network

Although all key nitrogen-fixing genes are directly activated by NifA in Proteobacteria [11][68], a constitutive expression of nitrogenase should be avoided under fluctuating conditions. The nifA gene can be transcriptionally activated by different upstream regulators, e.g., the FixL-FixJ two-component system in S. meliloti [176][69], the FixL-FixJ-FixK cascade in A. caulinodans [177,178][70][71], the redox responsive regulator RegR and its upstream kinases in B. diazoefficiens [162,179,180][54][72][73]. Nitrogenase is O2 sensitive and microaerobic fitness machineries seem to be relatively conserved in test rhizobia. The fixNOQP operon, encoding the cbb3 terminal oxidase, is transcriptionally activated by the FixL-FixJ-FixK cascade in S. meliloti, A. caulinodans and B. diazoefficiens [176[69][70][74][75][76],177,181,182,183], and the hFixL-FxkR-FixKf-FnrN cascade in R. etli and R. leguminosarum [163,184][55][77]. On the other hand, NifA can activate the transcription of fixABCX, encoding an electron bifurcating complex that provides low-potential reducing equivalents for nitrogenase [185][78], in S. meliloti, R. etli and R. leguminosarum [186,187,188,189][79][80][81][82]. Ferredoxin, likely reduced by FixABCX during nitrogen fixation [185][78], is a reductant of nitrogenase and its gene transcription is also activated by NifA in S. meliloti, B. diazoefficiens and R. etli [190,191][83][84]. Available transcriptomic evidence in B. diazoefficiens, S. meliloti and R. etli indicates that NifA may regulate more functional genes, e.g., molybdenum transporter, cytochrome P450 proteins, GroES, GroEL and uptake hydrogenase in a strain-dependent manner [161,189,190][53][82][83]. Notably, stringent sets of NifA regulon in these three rhizobia (19–67 genes) are on the symbiosis plasmid or symbiosis island with rare exceptions [161,189,190][53][82][83]. These findings imply that the integration of the key nitrogen fixation gene circuit in terms of transcriptional activation is strain-dependent, and the transcriptional regulation network of bacterial recipients seems to be limitedly subject to direct interference by NifA.
An efficient nitrogen fixation process of rhizobia is structurally ensured by nodule organogenesis that is initiated by specific recognition of host symbiotic signals by NodD in most rhizobia. The divergence of NodD and multiple NodD copies facilitate rhizobia efficiently establishing symbiosis under fluctuating conditions and/or exploring more host plants [64,67,68,192,193][85][86][87][88][89]. Available studies support a model where a primary NodD binds DNA in the absence of host symbiotic signals while signal–NodD binding enhances DNA bending that allows transcription [194,195][90][91]. NodD autoregulates its own transcription in R. leguminosarum bv. trifolii and R. leguminosarum bv. viciae [196,197][92][93]. When two or more NodDs are encoded within a genome, these NodDs usually act as a coordination module in a rhizobium- and condition-dependent way. For example, a second NodD copy in some R. leguminosarum bv. trifolii strains enhances nodule colonization competitiveness [198][94]. In S. meliloti, NodD1Sm and NodD2Sm respond to plant signals and the overexpressed NodD3Sm can function without flavonoids [62,199][95][96]. Among five NodD copies of R. tropici CIAT899, nodD2Rt expression is induced by osmotic stress, and the engineered overexpression of NodD2Rt alone is sufficient to replace the other NodD copies [200][97]. Mesorhizobium loti R7A has two NodD1Ml and NodD2Ml, showing a degree of functional redundancy [201][98]. More detailed investigation demonstrates that NodD1Ml mainly function in infection threads while NodD2Ml primarily acts in the rhizosphere and within nodules [202][99]. This observed division of labor is likely due to their divergence at the signal binding cleft [202][99]. Noteworthy, NodD2Ml activity is negatively affected by NodD1Ml at the pre-infection stage [202][99]. Two NodD copies are also found in other rhizobia, e.g., S. fredii and B. diazoefficiens, where NodD2 can negatively regulate the transcription of nodD1 [193,203,204][89][100][101]. The nodD2Sf mutant shows impaired nodulation on soybean but improved compatibility with Lotus species [205][102]. Collectively, these findings suggest a working model where rhizobial NodD and its regulon may be divergently selected in at least two dimensions: 1) from rhizosphere to rhizoplane to infection threads to nodules; 2) different host plants.
Various variables in these niches may interact with the key symbiotic interaction signaling pathway/network. Indeed, NFs are required for the biofilm establishment [206[103][104],207], which generally enhances bacterial resilience to various stress factors [208][105]. The production of exopolysaccharide (EPS), a common component of biofilm matrix, is negatively regulated by NodD in S. fredii [65,209][106][107] while positively regulated by the NodD3-SyrM-SyrA regulatory module in S. meliloti [210][108]. This is in line with the fact that EPS is an important symbiotic signal for the host infection of S. meliloti but dispensable in S. fredii symbiosis with test legumes [211,212][109][110]. In the presence of symbiotic signal daidzein, S. fredii NGR234 produces the phytohormone indole-3-acetic acid (IAA) in a NodD-dependent manner, and overexpression of NodD2Sf enhances the transcription of IAA synthesis genes and IAA production [213][111]. The positive regulation of IAA production by NodD is also found in R. tropici CIAT 899 [192][88]. There is evidence showing that flavonoids induce an NodD-dependent expression of traI that is responsible for the synthesis of short-chain quorum-sensing 3-oxo-C8-HSL in S. fredii [207][104]. Independent studies also reveal that the transcription of T3SS and effector coding genes depends on the positive regulator TtsI, while the expression of ttsI can be activated by NodD and plant flavonoids [214][112]. In NodD3Sm over-expressing S. meliloti, more than 200 genes are differentially expressed including upregulated EPS biosynthesis, and downregulated motility and chemotaxis functions [215][113]. Among those upregulated genes (above 70 genes), 69% are located on the chromosome and chromid [215][113]. Although a systematic survey of direct targets of NodD is not available yet, these examples suggest that NodDs have been evolving to differentially modulate other non-symbiosis functions to improve fitness from rhizosphere to rhizoplane to infection in a strain–host-dependent manner.
In addition to NodD, lineage-specific parts regulating nod genes have been identified in a few model rhizobia, e.g., the two-component system NodV-NodW, NwsB and NolA in B. diazoefficiens [204][101], SyrM, a NodD homolog, in Sinorhizobium [210,216[108][114][115],217], NolR homologs in Sinorhizobium and Rhizobium [218,219,220,221,222][116][117][118][119][120]. NodV-NodW positively regulates nodulation genes and is essential for symbiosis with mung bean, cowpea and siratro, but only marginally contributes to nodulation on soybean [223][121]. NwsB, a homolog of NodW, is required for both induction and the population density-dependent repression of nodulation genes [224][122]. NolA induces nodD2Bd and consequently represses the transcription of nodulation genes [225][123]. SyrMSm activates nodD3Sm transcription and NodD3Sm induces syrMSm, forming a self-amplifying circuit in S. meliloti [210][108]. NodD1Sf induces the transcription of SyrMSf that in turn induces NodD2Sf that represses nodulation genes in S. fredii [216][114]. Chromosomal NolR directly targets nodD1Sm, nodD2Sm and nodABCSm operons in S. meliloti [220,226,227][118][124][125] and downregulates nodulation and T3SS genes in S. fredii [222][120].
MucR/RosR/Ros/MI (hereafter MucR), a conserved zinc-finger regulator in Alphaproteobacteria, enhances the induction of key nodulation genes by the host signal luteolin in S. meliloti [228][126]. The disruption of mucR leads to delayed nodule development in the S. meliloti-alfalfa pair [228][126], reduced nodulation competitiveness in R. etli (common bean) [229][127], impaired nodulation and nitrogen fixation in R. leguminosarum bv. trifolii (clover) [230][128] and deficient nitrogen fixation in broad-host-range S. fredii strains (e.g., increased nodule number on soybean while decreased nodule number on Lotus burttii) [231,232][129][130]. Available transcriptomic analyses independently show that MucR is a pleiotropic regulator, e.g., in R. leguminosarum bv. trifolii, S. meliloti, S. fredii and other members of Alphaproteobacteria [113,228,231,232,233,234][126][129][130][131][132][133] (Figure 1). MucR autoregulates its transcription and recent ChIP-seq analysis further revealed more than 1350 direct target genes of MucR in the multipartite genome of S. fredii [111][134], among which a considerable number of known circuits were identified, e.g., NodD2Sf [193[89][100],203], TtsI, T3SS and its effector NopP [84][135], SyrB (negative regulator for SyrM in S. meliloti) [235][136], pilus assembly (Cpa), motility (Fla/Fli/Mot/Flg) and chemotaxis (Che/Mcp) [124][14], diguanylate cyclases [236][137], general stress response (RpoE5 and CspA8) [237][138], surface polysaccharides (ExoY and Uxs1) [238[139][140],239], carbon–nitrogen metabolism coordination (PtsN3) [153[43][66],174], nitric oxide reduction (Nor) [40][50], and uptake of potassium (Kdp) [153[43][44],154], iron (RirA) [156][46] and phosphorus (PhoUB) [150][40]. It should be noted that MucR rarely activates its target genes and prefers to bind AT-rich DNA (periodic repeats of “Ts”) that represents a characteristic feature of the symbiosis plasmid, genomic islands and xenogeneic DNA [111][134]. More molecular biology evidence shows that MucR shares convergently evolved features of xenogeneic silencers with H-NS, Lsr2, MvaT and Rok from either Gram-positive or Gram-negative bacteria [112][141], i.e., oligomerization mediated by N-terminal domain and forming DNA-protein-DNA bridging complex. The importance of these convergent functions in integrating symbiosis/pathogenesis functions is demonstrated by the H-NS from E. coli being interchangeable with MucR from S. fredii in the hemolysis activity assay and symbiotic performance [112][141]. Indeed, H-NS and other functional H-NS/MucR or Lsr2/MucR chimeric proteins, show similar ChIP-seq profiles in the multipartite genome of S. fredii and share 286 target genes including those encoding NodD2Sf, TtsI, T3SS, NopP, RirA, ExoY, Uxs1, TraI, TraR and VisN [112][141]. This evidence highlights that the convergent xenogeneic silencer MucR predisposes Alphaproteobacteria to integrate AT-rich symbiosis genes.
Genes 14 00274 g003 550
Figure 1. Working model for transcriptional integration of key symbiosis genes. Red arrow, positive regulation; green line, negative regulation. Solid lines indicate cases with molecular evidence. EPS, exopolysaccharide; APS, arabinose-containing polysaccharide; NO, nitric oxide. Sf, S. fredii; Sm, S. meliloti. For simplicity, functional genes in broad-host-range S. fredii are shown. The negative regulation of syrM by SyrB and positive regulation of nifA by FixJ are demonstrated in S. meliloti.

References

  1. DiCenzo, G.C.; Checcucci, A.; Bazzicalupo, M.; Mengoni, A.; Viti, C.; Dziewit, L.; Finan, T.M.; Galardini, M.; Fondi, M. Metabolic Modelling Reveals the Specialization of Secondary Replicons for Niche Adaptation in Sinorhizobium meliloti. Nat. Commun. 2016, 7, 12219.
  2. Galardini, M.; Pini, F.; Bazzicalupo, M.; Biondi, E.G.; Mengoni, A. Replicon-Dependent Bacterial Genome Evolution: The Case of Sinorhizobium meliloti. Genome Biol. Evol. 2013, 5, 542–558.
  3. Ramachandran, V.K.; East, A.K.; Karunakaran, R.; Downie, J.A.; Poole, P.S. Adaptation of Rhizobium leguminosarum to Pea, Alfalfa and Sugar Beet Rhizospheres Investigated by Comparative Transcriptomics. Genome Biol. 2011, 12, R106.
  4. Wheatley, R.M.; Ford, B.L.; Li, L.; Aroney, S.T.N.; Knights, H.E.; Ledermann, R.; East, A.K.; Ramachandran, V.K.; Poole, P.S. Lifestyle Adaptations of Rhizobium from Rhizosphere to Symbiosis. Proc. Natl. Acad. Sci. USA 2020, 117, 23823–23834.
  5. Jiao, J.; Ni, M.; Zhang, B.; Zhang, Z.; Young, J.P.W.; Chan, T.-F.; Chen, W.X.; Lam, H.-M.; Tian, C.F. Coordinated Regulation of Core and Accessory Genes in the Multipartite Genome of Sinorhizobium fredii. PLoS Genet. 2018, 14, e1007428.
  6. Vercruysse, M.; Fauvart, M.; Beullens, S.; Braeken, K.; Cloots, L.; Engelen, K.; Marchal, K.; Michiels, J. A Comparative Transcriptome Analysis of Rhizobium etli Bacteroids: Specific Gene Expression During Symbiotic Nongrowth. Mol. Plant Microbe Interact. 2011, 24, 1553–1561.
  7. Capela, D.; Filipe, C.; Bobilk, C.; Batut, J.; Bruand, C.; Bobik, C.; Plantes-microorganismes, L.I.; Inra-cnrs, U.M.R. Sinorhizobium meliloti Differentiation during Symbiosis with Alfalfa: A Transcriptomic Dissection. Mol. Plant Microbe Interact. 2006, 19, 363–372.
  8. Li, Y.; Tian, C.F.; Chen, W.F.; Wang, L.; Sui, X.H.; Chen, W.X. High-Resolution Transcriptomic Analyses of Sinorhizobium sp. NGR234 Bacteroids in Determinate Nodules of Vigna unguiculata and Indeterminate Nodules of Leucaena leucocephala. PLoS ONE 2013, 8, e70531.
  9. Green, R.T.; East, A.K.; Karunakaran, R.; Downie, J.A.; Poole, P.S. Transcriptomic Analysis of Rhizobium leguminosarum Bacteroids in Determinate and Indeterminate Nodules. Microb. Genom. 2019, 5, e000254.
  10. Schulte, C.C.M.; Borah, K.; Wheatley, R.M.; Terpolilli, J.J.; Saalbach, G.; Crang, N.; de Groot, D.H.; Ratcliffe, R.G.; Kruger, N.J.; Papachristodoulou, A.; et al. Metabolic Control of Nitrogen Fixation in Rhizobium-Legume Symbioses. Sci. Adv. 2021, 7, eabh2433.
  11. Masson-Boivin, C.; Giraud, E.; Perret, X.; Batut, J. Establishing Nitrogen-Fixing Symbiosis with Legumes: How Many Rhizobium Recipes? Trends Microbiol. 2009, 17, 458–466.
  12. Remigi, P.; Zhu, J.; Young, J.P.W.; Masson-Boivin, C. Symbiosis within Symbiosis: Evolving Nitrogen-Fixing Legume Symbionts. Trends Microbiol. 2016, 24, 63–75.
  13. Tian, C.F.; Zhou, Y.J.; Zhang, Y.M.; Li, Q.Q.; Zhang, Y.Z.; Li, D.F.; Wang, S.; Wang, J.; Gilbert, L.B.; Li, Y.R.; et al. Comparative Genomics of Rhizobia Nodulating Soybean Suggests Extensive Recruitment of Lineage-Specific Genes in Adaptations. Proc. Natl. Acad. Sci. USA 2012, 109, 8629–8634.
  14. Aroney, S.T.N.; Poole, P.S.; Sánchez-Cañizares, C. Rhizobial Chemotaxis and Motility Systems at Work in the Soil. Front. Plant Sci. 2021, 12, 1856.
  15. Acosta-jurado, S.; Fuentes-romero, F.; Ruiz-sainz, J.E.; Janczarek, M.; Vinardell, J.M. Rhizobial Exopolysaccharides: Genetic Regulation of Their Synthesis and Relevance in Symbiosis with Legumes. Int. J. Mol. Sci. 2021, 22, 6233.
  16. Janczarek, M.; Rachwał, K.; Marzec, A.; Grzadziel, J.; Palusińska-Szysz, M. Signal Molecules and Cell-Surface Components Involved in Early Stages of the Legume-Rhizobium Interactions. Appl. Soil Ecol. 2015, 85, 94–113.
  17. Kawaharada, Y.; Kelly, S.; Nielsen, M.W.; Hjuler, C.T.; Gysel, K.; Muszyński, A.; Carlson, R.W.; Thygesen, M.B.; Sandal, N.; Asmussen, M.H.; et al. Receptor-Mediated Exopolysaccharide Perception Controls Bacterial Infection. Nature 2015, 523, 308–312.
  18. Kawaharada, Y.; Nielsen, M.W.; Kelly, S.; James, E.K.; Andersen, K.R.; Madsen, L.H.; Heckmann, A.B.; Radutoiu, S.; Rasmussen, S.R.; Fu, W.; et al. Differential Regulation of the Epr3 Receptor Coordinates Membrane-Restricted Rhizobial Colonization of Root Nodule Primordia. Nat. Commun. 2017, 8, 14534.
  19. Arnold, M.F.F.; Penterman, J.; Shabab, M.; Chen, E.J.; Walker, C. Important Late-Stage Symbiotic Role of the Sinorhizobium meliloti Exopolysaccharide Succinoglycan. J. Bacteriol. 2018, 200, e00665-17.
  20. Li, D.; Li, Z.; Wu, J.; Tang, Z.; Xie, F.; Chen, D.; Lin, H.; Li, Y. Analysis of Outer Membrane Vesicles Indicates That Glycerophospholipid Metabolism Contributes to Early Symbiosis Between Sinorhizobium fredii HH103 and Soybean. Mol. Plant-Microbe Interact. 2022, 35, 311–322.
  21. Yang, M.H.; Sun, K.J.; Zhou, L.; Yang, R.F.; Zhong, Z.T.; Zhu, J. Functional Analysis of Three AHL Autoinducer Synthase Genes in Mesorhizobium loti Reveals the Important Role of Quorum Sensing in Symbiotic Nodulation. Can. J. Microbiol. 2009, 55, 210–214.
  22. Marketon, M.M.; Gronquist, M.R.; Eberhard, A.; Gonza, J.E. Characterization of the Sinorhizobium meliloti sinR/sinI Locus and the Production of Novel N-Acyl Homoserine Lactones. J. Bacteriol. 2002, 184, 5686–5695.
  23. Gurich, N.; Gonzalez, J.E. Role of Quorum Sensing in Sinorhizobium meliloti-Alfalfa Symbiosis. J. Bacteriol. 2009, 191, 4372–4382.
  24. Acosta-Jurado, S.; Alías-Villegas, C.; Almozara, A.; Espuny, M.R.; Vinardell, J.M.; Pérez-Montaño, F. Deciphering the Symbiotic Significance of Quorum Sensing Systems of Sinorhizobium fredii HH103. Microorganisms 2020, 8, 68.
  25. Calatrava-Morales, N.; McIntosh, M.; Soto, M.J. Regulation Mediated by N-Acyl Homoserine Lactone Quorum Sensing Signals in the Rhizobium-Legume Symbiosis. Genes 2018, 9, 263.
  26. Jiménez-Guerrero, I.; Medina, C.; Vinardell, J.M.; Ollero, F.J.; López-Baena, F.J. The Rhizobial Type 3 Secretion System: The Dr. Jekyll and Mr. Hyde in the Rhizobium–Legume Symbiosis. Int. J. Mol. Sci. 2022, 23, 11089.
  27. Ratu, S.T.N.; Amelia, L.; Okazaki, S. Type III Effector Provides a Novel Symbiotic Pathway in Legume-Rhizobia Symbiosis. Biosci. Biotechnol. Biochem. 2023, 87, 28–37.
  28. De Sousa, B.F.S.; Castellane, T.C.L.; Tighilt, L.; Lemos, E.G. de M.; Rey, L. Rhizobial Exopolysaccharides and Type VI Secretion Systems: A Promising Way to Improve Nitrogen Acquisition by Legumes. Front. Agron. 2021, 3, e661468.
  29. Salinero-Lanzarote, A.; Pacheco-Moreno, A.; Domingo-Serrano, L.; Durán, D.; Ormeño-Orrillo, E.; Martínez-Romero, E.; Albareda, M.; Palacios, J.M.; Rey, L. The Type VI Secretion System of Rhizobium etli Mim1 Has a Positive Effect in Symbiosis. FEMS Microbiol. Ecol. 2019, 95, efiz054.
  30. Fauvart, M.; Michiels, J. Rhizobial Secreted Proteins as Determinants of Host Specificity in the Rhizobium-Legume Symbiosis. FEMS Microbiol. Lett. 2008, 285, 1–9.
  31. Finnie, C.; Hartley, N.M.; Findlay, K.C.; Downie, J.A. The Rhizobium leguminosarum prsDE Genes Are Required for Secretion of Several Proteins, Some of Which Influence Nodulation, Symbiotic Nitrogen Fixation and Exopolysaccharide Modification. Mol. Microbiol. 1997, 25, 135–146.
  32. Liu, J.; Wang, T.; Qin, Q.; Yu, X.; Yang, S.; Dinkins, R.D.; Kuczmog, A.; Putnoky, P.; Muszyński, A.; Griffitts, J.S.; et al. Paired Medicago Receptors Mediate Broad-Spectrum Resistance to Nodulation by Sinorhizobium meliloti Carrying a Species-Specific Gene. Proc. Natl. Acad. Sci. USA 2022, 119, e2214703119.
  33. Yurgel, S.N.; Kahn, M.L. Dicarboxylate Transport by Rhizobia. FEMS Microbiol. Rev. 2004, 28, 489–501.
  34. Wang, C.; Saldanha, M.; Sheng, X.; Shelswell, K.J.; Walsh, K.T.; Sobral, B.W.S.; Charles, T.C. Roles of Poly-3-Hydroxybutyrate (PHB) and Glycogen in Symbiosis of Sinorhizobium meliloti with Medicago sp. Microbiology 2007, 153, 388–398.
  35. Mandon, K.; Michel-reydellet, N.; Encarnacio, S.; Kaminski, P.A.; Leija, A.; Cevallos, M.A.; Elmerich, C.; Mora, J. Poly-β-Hydroxybutyrate Turnover in Azorhizobium caulinodans Is Required for Growth and Affects nifA Expression. J. Bacteriol. 1998, 180, 5070–5076.
  36. Sun, Y.-W.; Li, Y.; Hu, Y.; Chen, W.-X.; Tian, C.-F. Coordinated Regulation of the Size and Number of Polyhydroxybutyrate Granules by Core and Accessory Phasins in the Facultative Microsymbiont Sinorhizobium fredii NGR234. Appl. Environ. Microbiol. 2019, 85, e00717-19.
  37. Lodwig, E.M.; Hosie, A.H.; Bourdes, A.; Findlay, K.; Allaway, D.; Karunakaran, R.; Downie, J.A.; Poole, P.S. Amino-Acid Cycling Drives Nitrogen Fixation in the Legume-Rhizobium Symbiosis. Nature 2003, 422, 722–726.
  38. Prell, J.; White, J.P.; Bourdes, A.; Bunnewell, S.; Bongaerts, R.J.; Poole, P.S. Legumes Regulate Rhizobium Bacteroid Development and Persistence by the Supply of Branched-Chain Amino Acids. Proc. Natl. Acad. Sci. USA 2009, 106, 12477–12482.
  39. Prell, J.; Bourdes, A.; Kumar, S.; Lodwig, E.; Hosie, A.; Kinghorn, S.; White, J.; Poole, P. Role of Symbiotic Auxotrophy in the Rhizobium-Legume Symbioses. PLoS ONE 2010, 5, e13933.
  40. Hu, Y.; Jiao, J.; Liu, L.X.; Sun, Y.W.; Chen, W.; Sui, X.; Chen, W.; Tian, C.F. Evidence for Phosphate Starvation of Rhizobia without Terminal Differentiation in Legume Nodules. Mol. Plant-Microbe Interact. 2018, 31, 1060–1068.
  41. Bardin, S.D.; Finan, T.M. Regulation of Phosphate Assimilation in Rhizobium (Sinorhizobium) meliloti. Genetics 1998, 148, 1689–1700.
  42. Yuan, Z.C.; Zaheer, R.; Finan, T.M. Regulation and Properties of PstSCAB, a High-Affinity, High-Velocity Phosphate Transport System of Sinorhizobium meliloti. J. Bacteriol. 2006, 188, 1089–1102.
  43. Feng, X.-Y.; Tian, Y.; Cui, W.-J.; Li, Y.-Z.; Wang, D.; Liu, Y.; Jiao, J.; Chen, W.-X.; Tian, C.-F. The PTSNtr-KdpDE-KdpFABC Pathway Contributes to Low Potassium Stress Adaptation and Competitive Nodulation of Sinorhizobium fredii. mBio 2022, 13, e03721-21.
  44. Dominguez-Ferreras, A.; Munoz, S.; Olivares, J.; Soto, M.J.; Sanjuan, J.; Domínguez-ferreras, A.; Mun, S.; Sanjua, J. Role of Potassium Uptake Systems in Sinorhizobium meliloti Osmoadaptation and Symbiotic Performance. J. Bacteriol. 2009, 191, 2133–2143.
  45. Cheng, G.; Karunakaran, R.; East, A.K.; Poole, P.S. Multiplicity of Sulfate and Molybdate Transporters and Their Role in Nitrogen Fixation in Rhizobium leguminosarum bv. viciae Rlv3841. Mol. Plant-Microbe Interact. 2016, 29, 143–152.
  46. Liu, K.-H.; Zhang, B.; Yang, B.-S.; Shi, W.-T.; Li, Y.-F.; Wang, Y.; Zhang, P.; Jiao, J.; Tian, C.-F. Rhizobiales-Specific RirA Represses a Naturally “Synthetic” Foreign Siderophore Gene Cluster to Maintain Sinorhizobium-Legume Mutualism. mBio 2022, 13, e02900-21.
  47. Sankari, S.; Babu, V.M.P.; Bian, K.; Alhhazmi, A.; Andorfer, M.C.; Avalos, D.M.; Smith, T.A.; Yoon, K.; Drennan, C.L.; Yaffe, M.B.; et al. A Haem-Sequestering Plant Peptide Promotes Iron Uptake in Symbiotic Bacteria. Nat. Microbiol. 2022, 7, 1453–1465.
  48. Zhang, P.; Zhang, B.; Jiao, J.; Dai, S.-Q.; Chen, W.-X.; Tian, C.-F. Modulation of Symbiotic Compatibility by Rhizobial Zinc Starvation Machinery. mBio 2020, 11, e03193-19.
  49. Hood, G.; Ramachandran, V.K.; East, A.; Downie, J.A.; Poole, P.S. Manganese Transport Is Essential for N2-Fixation by Rhizobium leguminosarum in Bacteroids from Galegoid but Not Phaseoloid Nodules. Environ. Microbiol. 2017, 19, 2715–2726.
  50. Liu, L.X.; Li, Q.Q.; Zhang, Y.Z.; Hu, Y.; Jiao, J.; Guo, H.J.; Zhang, X.X.; Zhang, B.; Chen, W.X.; Tian, C.F. The Nitrate-Reduction Gene Cluster Components Exert Lineage-Dependent Contributions to Optimization of Sinorhizobium Symbiosis with Soybeans. Environ. Microbiol. 2017, 19, 4926–4938.
  51. Ruiz, B.; Le Scornet, A.; Sauviac, L.; Rémy, A.; Bruand, C.; Meilhoc, E. The Nitrate Assimilatory Pathway in Sinorhizobium meliloti: Contribution to NO Production. Front. Microbiol. 2019, 10, 1526.
  52. Cam, Y.; Pierre, O.; Boncompagni, E.; Herouart, D.; Meilhoc, E.; Bruand, C. Nitric Oxide (NO) a Key Player in the Senescence of Medicago truncatula Root Nodules. New Phytol. 2012, 196, 548–560.
  53. Bobik, C.; Meilhoc, E.; Batut, J. FixJ: A Major Regulator of the Oxygen Limitation Response and Late Symbiotic Functions of Sinorhizobium meliloti. J. Bacteriol. 2006, 188, 4890–4902.
  54. Bauer, E.; Kaspar, T.; Fischer, H.M.; Hennecke, H. Expression of the fixR-nifA Operon in Bradyrhizobium japonicum Depends on a New Response Regulator, RegR. J. Bacteriol. 1998, 180, 3853–3863.
  55. Rutten, P.J.; Steel, H.; Hood, G.A.; Ramachandran, V.K.; McMurtry, L.; Geddes, B.; Papachristodoulou, A.; Poole, P.S. Multiple Sensors Provide Spatiotemporal Oxygen Regulation of Gene Expression in a Rhizobium-Legume Symbiosis. PLoS Genet. 2021, 17, e1009099.
  56. De Nisco, N.J.; Abo, R.P.; Wu, C.M.; Penterman, J.; Walker, G.C. Global Analysis of Cell Cycle Gene Expression of the Legume Symbiont Sinorhizobium meliloti. Proc. Natl. Acad. Sci. USA 2014, 111, 3217–3224.
  57. Gibson, K.E.; Campbell, G.R.; Lloret, J.; Walker, G.C. CbrA Is a Stationary-Phase Regulator of Cell Surface Physiology and Legume Symbiosis in Sinorhizobium meliloti. J. Bacteriol. 2006, 188, 4508–4521.
  58. Kobayashi, H.; De Nisco, N.J.; Chien, P.; Simmons, L.A.; Walker, G.C. Sinorhizobium meliloti CpdR1 Is Critical for Co-Ordinating Cell Cycle Progression and the Symbiotic Chronic Infection. Mol. Microbiol. 2009, 73, 586–600.
  59. diCenzo, G.C.; Zamani, M.; Ludwig, H.N.; Finan, T.M. Heterologous Complementation Reveals a Specialized Activity for BacA in the Medicago-Sinorhizobium meliloti Symbiosis. Mol. Plant-Microbe Interact. 2017, 30, 312–324.
  60. Marlow, V.L.; Haag, A.F.; Kobayashi, H.; Fletcher, V.; Scocchi, M.; Walker, G.C.; Ferguson, G.P. Essential Role for the BacA Protein in the Uptake of a Truncated Eukaryotic Peptide in Sinorhizobium meliloti. J. Bacteriol. 2009, 191, 1519–1527.
  61. Karunakaran, R.; Haag, A.F.; East, A.K.; Ramachandran, V.K.; Prell, J.; James, E.K.; Scocchi, M.; Ferguson, G.P.; Poole, P.S. BacA Is Essential for Bacteroid Development in Nodules of Galegoid, but Not Phaseoloid, Legumes. J. Bacteriol. 2010, 192, 2920–2928.
  62. Haag, A.F.; Baloban, M.; Sani, M.; Kerscher, B.; Pierre, O.; Farkas, A.; Longhi, R.; Boncompagni, E.; Hérouart, D.; Dall’Angelo, S.; et al. Protection of Sinorhizobium against Host Cysteine-Rich Antimicrobial Peptides Is Critical for Symbiosis. PLoS Biol. 2011, 9, e1001169.
  63. Nicoud, Q.; Barrière, Q.; Busset, N.; Dendene, S.; Travin, D.; Bourge, M.; Le Bars, R.; Boulogne, C.; Lecroël, M.; Jenei, S.; et al. Sinorhizobium meliloti Functions Required for Resistance to Antimicrobial NCR Peptides and Bacteroid Differentiation. mBio 2021, 12, e00895-21.
  64. Ren, B.; Wang, X.; Duan, J.; Ma, J. Rhizobial tRNA-Derived Small RNAs Are Signal Molecules Regulating Plant Nodulation. Science 2019, 365, 919–922.
  65. García-Tomsig, N.I.; Robledo, M.; diCenzo, G.C.; Mengoni, A.; Millán, V.; Peregrina, A.; Uceta, A.; Jiménez-Zurdo, J.I. Pervasive RNA Regulation of Metabolism Enhances the Root Colonization Ability of Nitrogen-Fixing Symbiotic α-Rhizobia. mBio 2022, 13, e03576-21.
  66. Sánchez-Cañizares, C.; Prell, J.; Pini, F.; Rutten, P.; Kraxner, K.; Wynands, B.; Karunakaran, R.; Poole, P.S. Global Control of Bacterial Nitrogen and Carbon Metabolism by a PTSNtr-Regulated Switch. Proc. Natl. Acad. Sci. USA 2020, 117, 10234–10245.
  67. Li, Y.Z.; Wang, D.; Feng, X.Y.; Jiao, J.; Chen, W.X.; Tian, C.F. Genetic Analysis Reveals the Essential Role of Nitrogen Phosphotransferase System Components in Sinorhizobium fredii CCBAU 45436 Symbioses with Soybean and Pigeonpea Plants. Appl. Environ. Microbiol. 2016, 82, 1305–1315.
  68. Dixon, R.; Kahn, D. Genetic Regulation of Biological Nitrogen Fixation. Nat. Rev. Microbiol. 2004, 2, 621–631.
  69. David, M.; Daveran, M.L.; Batut, J.; Dedieu, A.; Domergue, O.; Ghai, J.; Hertig, C.; Boistard, P.; Kahn, D. Cascade Regulation of nif Gene Expression in Rhizobium meliloti. Cell 1988, 54, 671–683.
  70. Kaminski, P.A.; Elmerich, C. Involvement of fixLJ in the Regulation of Nitrogen Fixation in Azorhizobium caulinodans. Mol. Microbiol. 1991, 5, 665–673.
  71. Kaminski, P.A.; Mandon, K.; Arigoni, F.; Desnoues, N.; Elmerich, C. Regulation of Nitrogen Fixation in Azorhizobium caulinodans: Identification of a fixK-like Gene, a Positive Regulator of nifA. Mol. Microbiol. 1991, 5, 1983–1991.
  72. Emmerich, R.; Hennecke, H.; Fischer, H.M. Evidence for a Functional Similarity between the Two-Component Regulatory Systems RegSR, ActSR, and RegBA (PrrBA) in α-Proteobacteria. Arch. Microbiol. 2000, 174, 307–313.
  73. Lindemann, A.; Moser, A.; Pessi, G.; Hauser, F.; Friberg, M.; Hennecke, H.; Fischer, H.M. New Target Genes Controlled by the Bradyrhizobium japonicum Two-Component Regulatory System RegSR. J. Bacteriol. 2007, 189, 8928–8943.
  74. Anthamatten, D.; Scherb, B.; Hennecke, H. Characterization of a fixLJ-Regulated Bradyrhizobium japonicum Gene Sharing Similarity with the Escherichia coli fnr and Rhizobium meliloti fixK Genes. J. Bacteriol. 1992, 174, 2111–2120.
  75. Cabrera, J.J.; Jiménez-Leiva, A.; Tomás-Gallardo, L.; Parejo, S.; Casado, S.; Torres, M.J.; Bedmar, E.J.; Delgado, M.J.; Mesa, S. Dissection of FixK2 Protein–DNA Interaction Unveils New Insights into Bradyrhizobium diazoefficiens Lifestyles Control. Environ. Microbiol. 2021, 23, 6194–6209.
  76. Galinier, A.; Garnerone, A.M.; Reyrat, J.M.; Kahn, D.; Batut, J.; Boistard, P. Phosphorylation of the Rhizobium meliloti FixJ Protein Induces Its Binding to a Compound Regulatory Region at the fixK Promoter. J. Biol. Chem. 1994, 269, 23784–23789.
  77. Lopez, O.; Morera, C.; Miranda-Rios, J.; Girard, L.; Romero, D.; Soberon, M. Regulation of Gene Expression in Response to Oxygen in Rhizobium etli: Role of FnrN in fixNOQP Expression and in Symbiotic Nitrogen Fixation. J. Bacteriol. 2001, 183, 6999–7006.
  78. Ledbetter, R.N.; Garcia Costas, A.M.; Lubner, C.E.; Mulder, D.W.; Tokmina-Lukaszewska, M.; Artz, J.H.; Patterson, A.; Magnuson, T.S.; Jay, Z.J.; Duan, H.D.; et al. The Electron Bifurcating FixABCX Protein Complex from Azotobacter vinelandii: Generation of Low-Potential Reducing Equivalents for Nitrogenase Catalysis. Biochemistry 2017, 56, 4177–4190.
  79. Kim, C.H.; Helinski, D.R.; Ditta, G. Overlapping Transcription of the nifA Regulatory Gene in Rhizobium meliloti. Gene 1986, 50, 141–148.
  80. Martínez, M.; Palacios, J.M.; Imperial, J.; Ruiz-Argüeso, T. Symbiotic Autoregulation of nifA Expression in Rhizobium leguminosarum bv. viciae. J. Bacteriol. 2004, 186, 6586–6594.
  81. Webb, I.U.C.; Xu, J.; Sanchez-Cañizares, C.; Karunakaran, R.; Ramachandran, V.K.; Rutten, P.J.; East, A.K.; Huang, W.E.; Watmough, N.J.; Poole, P.S. Regulation and Characterization of Mutants of fixABCX in Rhizobium leguminosarum. Mol. Plant-Microbe Interact. 2021, 34, 1167–1180.
  82. Salazar, E.; Javier Díaz-Mejía, J.; Moreno-Hagelsieb, G.; Martínez-Batallar, G.; Mora, Y.; Mora, J.; Encarnación, S. Characterization of the NifA-RpoN Regulon in Rhizobium etli in Free Life and in Symbiosis with Phaseolus vulgaris. Appl. Environ. Microbiol. 2010, 76, 4510–4520.
  83. Hauser, F.; Pessi, G.; Friberg, M.; Weber, C.; Rusca, N.; Lindemann, A.; Fischer, H.M.; Hennecke, H. Dissection of the Bradyrhizobium japonicum NifA+σ54 Regulon, and Identification of a Ferredoxin Gene (fdxN) for Symbiotic Nitrogen Fixation. Mol. Genet. Genomics 2007, 278, 255–271.
  84. Klipp, W.; Reiländer, H.; Schlüter, A.; Krey, R.; Pühler, A. The Rhizobium meliloti fdxN Gene Encoding a Ferredoxin-like Protein Is Necessary for Nitrogen Fixation and Is Cotranscribed with nifA and nifB. Mol. Gen. Genet. 1989, 216, 293–302.
  85. Györgypal, Z.; Kondorosi, É.; Kondorosi, A. Diverse Signal Sensitivity of NodD Protein Homologs from Narrow and Broad Host Range Rhizobia. Mol. Plant Microbe Interact. 1991, 4, 356–364.
  86. del Cerro, P.; Rolla-Santos, A.A.P.; Gomes, D.F.; Marks, B.B.; Espuny, M.d.R.; Rodríguez-Carvajal, M.Á.; Soria-Díaz, M.E.; Nakatani, A.S.; Hungria, M.; Ollero, F.J.; et al. Opening the “black Box” of nodD3, nodD4 and nodD5 Genes of Rhizobium tropici Strain CIAT 899. BMC Genom. 2015, 16, 864.
  87. Lestrange, K.K.; Bender, G.L.; Djordjevic, M.A.; Rolfe, B.G.; Redmond, J.W. The Rhizobium Strain NGR234 nodD1 Gene-Product Responds to Activation by the Simple Phenolic-Compounds Vanillin and Isovanillin Present in Wheat Seedling Extracts. Mol. Plant Microbe Interact. 1990, 3, 214–220.
  88. del Cerro, P.; Rolla-Santos, A.A.P.; Gomes, D.F.; Marks, B.B.; Pérez-Montaño, F.; Rodríguez-Carvajal, M.Á.; Nakatani, A.S.; Gil-Serrano, A.; Megías, M.; Ollero, F.J.; et al. Regulatory nodD1 and nodD2 Genes of Rhizobium tropici Strain CIAT 899 and Their Roles in the Early Stages of Molecular Signaling and Host-Legume Nodulation. BMC Genom. 2015, 16, 251.
  89. Machado, D.; Pueppke, S.G.; Vinardel, J.M.; Ruiz-Sainz, J.E.; Krishnan, H.B. Expression of nodD1 and nodD2 in Sinorhizobium fredii, a Nitrogen-Fixing Symbiont of Soybean and Other Legumes. Mol. Plant-Microbe Interact. 1998, 11, 375–382.
  90. Chen, X.C.; Feng, J.; Hou, B.H.; Li, F.Q.; Li, Q.; Hong, G.F. Modulating DNA Bending Affects NodD-Mediated Transcriptional Control in Rhizobium leguminosarum. Nucleic Acids Res. 2005, 33, 2540–2548.
  91. Peck, M.C.; Fisher, R.F.; Long, S.R. Diverse Flavonoids Stimulate NodD1 Binding to nod Gene Promoters in Sinorhizobium meliloti. J. Bacteriol. 2006, 188, 5417–5427.
  92. Rossen, L.; Shearman, C.A.; Johnston, A.W.B.; Downie, J.A. The nodD Gene of Rhizobium leguminosarum Is Autoregulatory and in the Presence of Plant Exudate Induces the nodA,B,C Genes. EMBO J. 1985, 4, 3369–3373.
  93. McIver, J.; Djordjevic, M.A.; Weinman, J.J.; Bender, G.L.; Rolfe, B.G. Extension of Host Range of Rhizobium leguminosarum bv. trifolii Caused by Point Mutations in nodD That Result in Alterations in Regulatory Function and Recognition of Inducer Molecules. Mol. Plant. Microbe. Interact. 1989, 2, 97–106.
  94. Ferguson, S.; Major, A.S.; Sullivan, J.T.; Bourke, S.D.; Kelly, S.J.; Perry, B.J.; Ronson, C.W. Rhizobium leguminosarum bv. trifolii NodD2 Enhances Competitive Nodule Colonization in the Clover-Rhizobium Symbiosis. Appl. Environ. Microbiol. 2020, 86, e01268-20.
  95. Mulligan, J.T.; Long, S.R. Induction of Rhizobium meliloti nodC Expression by Plant Exudate Requires nodD. Proc. Natl. Acad. Sci. USA 1985, 82, 6609–6613.
  96. Honma, M.A.; Asomaning, M.; Ausubel, F.M. Rhizobium meliloti nodD Genes Mediate Host-Specific Activation of nodABC. J. Bacteriol. 1990, 172, 901–911.
  97. Ayala-García, P.; Jiménez-Guerrero, I.; Jacott, C.N.; López-Baena, F.J.; Ollero, F.J.; del Cerro, P.; Pérez-Montaño, F. The Rhizobium tropici CIAT 899 NodD2 Protein Promotes Symbiosis and Extends Rhizobial Nodulation Range by Constitutive Nodulation Factor Synthesis. J. Exp. Bot. 2022, 73, 6931–6941.
  98. Rodpothong, P.; Sullivan, J.T.; Songsrirote, K.; Sumpton, D.; Cheung, K.W.J.T.; Thomas-Oates, J.; Radutoiu, S.; Stougaard, J.; Ronson, C.W. 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.
  99. Kelly, S.; Sullivan, J.T.; Kawaharada, Y.; Radutoiu, S.; Ronson, C.W.; Stougaard, J. Regulation of Nod Factor Biosynthesis by Alternative NodD Proteins at Distinct Stages of Symbiosis Provides Additional Compatibility Scrutiny. Environ. Microbiol. 2018, 20, 97–110.
  100. Fellay, R.; Hanin, M.; Montorzi, G.; Frey, J.; Freiberg, C.; Golinowski, W.; Staehelin, C.; Broughton, W.J.; Jabbouri, S. nodD2 of Rhizobium sp. NGR234 Is Involved in the Repression of the nodABC Operon. Mol. Microbiol. 1998, 27, 1039–1050.
  101. Loh, J.; Stacey, G. Nodulation Gene Regulation in Bradyrhizobium japonicum: A Unique Integration of Global Regulatory Circuits. Appl. Environ. Microbiol. 2003, 69, 10–17.
  102. Acosta-Jurado, S.; Rodríguez-Navarro, D.-N.; Kawaharada, Y.; Rodríguez-Carvajal, M.A.; Gil-Serrano, A.; Soria-Díaz, M.E.; Pérez-Montaño, F.; Fernández-Perea, J.; Yanbo, N.; Alias-Villegas, C.; et al. Sinorhizobium fredii HH103 nolR and nodD2 Mutants Gain Capacity for Infection Thread Invasion of Lotus japonicus Gifu and Lotus Burttii. Environ. Microbiol. 2019, 21, 1718–1739.
  103. Fujishige, N.A.; Lum, M.R.; De Hoff, P.L.; Whitelegge, J.P.; Faull, K.F.; Hirsch, A.M. Rhizobium Common nod Genes Are Required for Biofilm Formation. Mol. Microbiol. 2008, 67, 504–515.
  104. Pérez-Montaño, F.; Jiménez-Guerrero, I.; Del Cerro, P.; Baena-Ropero, I.; López-Baena, F.J.; Ollero, F.J.; Bellogín, R.; Lloret, J.; Espuny, R. The Symbiotic Biofilm of Sinorhizobium fredii SMH12, Necessary for Successful Colonization and Symbiosis of Glycine max cv Osumi, Is Regulated by Quorum Sensing Systems and Inducing Flavonoids via NodD1. PLoS ONE 2014, 9, e0105901.
  105. Rumbaugh, K.P.; Sauer, K. Biofilm Dispersion. Nat. Rev. Microbiol. 2020, 18, 571–586.
  106. Machado, D.; Krishnan, H.B. nodD Alleles of Sinorhizobium fredii USDA191 Differentially Influence Soybean Nodulation, nodC Expression, and Production of Exopolysaccharides. Curr. Microbiol. 2003, 47, 134–137.
  107. Crespo-rivas, J.C.; Cuesta-berrio, L.; Ruiz-sainz, J.E. Exopolysaccharide Production by Sinorhizobium fredii HH103 Is Repressed by Genistein in a NodD1-Dependent Manner. PLoS ONE 2016, 11, e0160499.
  108. Barnett, M.J.; Long, S.R. The Sinorhizobium meliloti SyrM Regulon: Effects on Global Gene Expression Are Mediated by syrA and nodD3. J. Bacteriol. 2015, 197, 1792–1806.
  109. Cheng, H.P.; Walker, G.C. Succinoglycan Is Required for Initiation and Elongation of Infection Threads during Nodulation of Alfalfa by Rhizobium meliloti. J. Bacteriol. 1998, 180, 5183–5191.
  110. Rodríguez-Navarro, D.N.; Rodríguez-Carvajal, M.A.; Acosta-Jurado, S.; Soto, M.J.; Margaret, I.; Crespo-Rivas, J.C.; Sanjuan, J.; Temprano, F.; Gil-Serrano, A.; Ruiz-Sainz, J.E.; et al. Structure and Biological Roles of Sinorhizobium fredii HH103 Exopolysaccharide. PLoS ONE 2014, 9, e115391.
  111. Theunis, M.; Kobayashi, H.; Broughton, W.J.; Prinsen, E. Flavonoids, NodD1, NodD2, and Nod-Box NB15 Modulate Expression of the Y4wEFG Locus That Is Required for Indole-3-Acetic Acid Synthesis in Rhizobium sp. Strain NGR234. Mol. Plant-Microbe Interact. 2004, 17, 1153–1161.
  112. Deakin, W.J.; Broughton, W.J. Symbiotic Use of Pathogenic Strategies: Rhizobial Protein Secretion Systems. Nat. Rev. Microbiol. 2009, 7, 312–320.
  113. Barnett, M.J.; Toman, C.J.; Fisher, R.F.; Long, S.R. A Dual-Genome Symbiosis Chip for Coordinate Study of Signal Exchange and Development in a Prokaryote-Host Interaction. Proc. Natl. Acad. Sci. USA 2004, 101, 16636–16641.
  114. Acosta-Jurado, S.; Alias-Villegas, C.; Navarro-Gómez, P.; Almozara, A.; Rodríguez-Carvajal, M.A.; Medina, C.; Vinardell, J.M. Sinorhizobium fredii HH103 syrM Inactivation Affects the Expression of a Large Number of Genes, Impairs Nodulation with Soybean and Extends the Host-Range to Lotus japonicus. Environ. Microbiol. 2020, 22, 1104–1124.
  115. Mulligan, J.T.; Long, S.R. A Family of Activator Genes Regulates Expression of Rhizobium meliloti Nodulation Genes. Genetics 1989, 122, 7–18.
  116. Kiss, E.; Mergaert, P.; Olah, B.; Kereszt, A.; Staehelin, C.; Davies, A.E.; Downie, J.A.; Kondorosi, A.; Kondorosi, E. Conservation of nolR in the Sinorhizobium and Rhizobium Genera of the Rhizobiaceae Family. Mol. Plant-Microbe Interact. 1998, 11, 1186–1195.
  117. Lee, S.G.; Krishnan, H.B.; Jez, J.M. Structural Basis for Regulation of Rhizobial Nodulation and Symbiosis Gene Expression by the Regulatory Protein NolR. Proc. Natl. Acad. Sci. USA 2014, 111, 6509–6514.
  118. Cren, M.; Kondorosi, A.; Kondorosi, E. NolR Controls Expression of the Rhizobium meliloti Nodulation Genes Involved in the Core Nod Factor Synthesis. Mol. Microbiol. 1995, 15, 733–747.
  119. del Cerro, P.; Rolla-Santos, A.A.P.; Valderrama-Fernández, R.; Gil-Serrano, A.; Bellogín, R.A.; Gomes, D.F.; Pérez-Montaño, F.; Megías, M.; Hungría, M.; Ollero, F.J. NrcR, a New Transcriptional Regulator of Rhizobium tropici CIAT 899 Involved in the Legume Root-Nodule Symbiosis. PLoS ONE 2016, 11, e0154029.
  120. Vinardell, J.M.; Ollero, F.J.; Hidalgo, A.; Lopez-Baena, F.J.; Medina, C.; Ivanov-Vangelov, K.; Parada, M.; Madinabeitia, N.; Espuny Mdel, R.; Bellogin, R.A.; et al. NoIR Regulates Diverse Symbiotic Signals of Sinorhizobium fredii HH103. Mol. Plant-Microbe Interact. 2004, 17, 676–685.
  121. Göttfert, M.; Grob, P.; Hennecke, H. Proposed Regulatory Pathway Encoded by the nodV and nodW Genes, Determinants of Host Specificity in Bradyrhizobium japonicum. Proc. Natl. Acad. Sci. USA 1990, 87, 2680–2684.
  122. Loh, J.; Lohar, D.P.; Andersen, B.; Stacey, G. A Two-Component Regulator Mediates Population-Density-Dependent Expression of the Bradyrhizobium japonicum Nodulation Genes. J. Bacteriol. 2002, 184, 1759–1766.
  123. Garcia, M.; Dunlap, J.; Loh, J.; Stacey, G. Phenotypic Characterization and Regulation of the nolA Gene of Bradyrhizobium japonicum. Mol. Plant-Microbe Interact. 1996, 9, 625–635.
  124. Kondorosi, E.; Pierre, M.; Cren, M.; Haumann, U.; Buiré, M.; Hoffmann, B.; Schell, J.; Kondorosi, A. Identification of NoIR, a Negative Transacting Factor Controlling the nod Regulon in Rhizobium meliloti. J. Mol. Biol. 1991, 222, 885–896.
  125. Kondorosi, E.; Gyuris, J.; Schmidt, J.; John, M.; Duda, E.; Hoffmann, B.; Schell, J.; Kondorosi, A. Positive and Negative Control of nod Gene Expression in Rhizobium meliloti Is Required for Optimal Nodulation. EMBO J. 1989, 8, 1331–1340.
  126. Mueller, K.; Gonzalez, J.E. Complex Regulation of Symbiotic Functions Is Coordinated by MucR and Quorum Sensing in Sinorhizobium meliloti. J. Bacteriol. 2011, 193, 485–496.
  127. Bittinger, M.A.; Milner, J.L.; Saville, B.J.; Handelsman, J. rosR, a Determinant of Nodulation Competitiveness in Rhizobium etli. Mol. Plant-Microbe Interact. 1997, 10, 180–186.
  128. Janczarek, M.; Kutkowska, J.; Piersiak, T.; Skorupska, A. Rhizobium leguminosarum bv. trifolii RosR Is Required for Interaction with Clover, Biofilm Formation and Adaptation to the Environment. BMC Microbiol. 2010, 10, 284.
  129. Jiao, J.; Wu, L.J.; Zhang, B.; Hu, Y.; Li, Y.; Zhang, X.X.; Guo, H.J.; Liu, L.X.; Chen, W.X.; Zhang, Z.; et al. MucR Is Required for Transcriptional Activation of Conserved Ion Transporters to Support Nitrogen Fixation of Sinorhizobium fredii in Soybean Nodules. Mol. Plant-Microbe Interact. 2016, 29, 352–361.
  130. Acosta-Jurado, S.; Alias-Villegas, C.; Navarro-Gomez, P.; Zehner, S.; Del Socorro Murdoch, P.; Rodríguez-Carvajal, M.A.; Soto, M.J.; Ollero, F.J.; Ruiz-Sainz, J.E.; Göttfert, M.; et al. The Sinorhizobium fredii HH103 MucR1 Global Regulator Is Connected with the nod Regulon and Is Required for Efficient Symbiosis with Lotus burttii and Glycine max cv. Williams. Mol. Plant-Microbe Interact. 2016, 29, 700–712.
  131. Jiao, J.; Tian, C.-F. Ancestral Zinc-Finger Bearing Protein MucR in Alpha-Proteobacteria: A Novel Xenogeneic Silencer? Comput. Struct. Biotechnol. J. 2020, 18, 3623–3631.
  132. Janczarek, M. The Ros/MucR Zinc-Finger Protein Family in Bacteria: Structure and Functions. Int. J. Mol. Sci. 2022, 23, 15536.
  133. Rachwał, K.; Matczyńska, E.; Janczarek, M. Transcriptome Profiling of a Rhizobium leguminosarum bv. trifolii rosR Mutant Reveals the Role of the Transcriptional Regulator RosR in Motility, Synthesis of Cell-Surface Components, and Other Cellular Processes. BMC Genom. 2015, 16, 1111.
  134. Jiao, J.; Zhang, B.; Li, M.-L.; Zhang, Z.; Tian, C.-F. The Zinc-Finger Bearing Xenogeneic Silencer MucR in α-Proteobacteria Balances Adaptation and Regulatory Integrity. ISME J. 2022, 16, 738–749.
  135. Zhao, R.; Liu, L.X.; Zhang, Y.Z.; Jiao, J.; Cui, W.J.; Zhang, B.; Wang, X.L.; Li, M.L.; Chen, Y.; Xiong, Z.Q.; et al. Adaptive Evolution of Rhizobial Symbiotic Compatibility Mediated by Co-Evolved Insertion Sequences. ISME J. 2018, 12, 101–111.
  136. Barnett, M.J.; Long, S.R. Identification and Characterization of a Gene on Rhizobium meliloti pSymA, syrB, That Negatively Affects syrM Expression. Mol. Plant Microbe Interact. 1997, 10, 550–559.
  137. Li, M.-L.; Jiao, J.; Zhang, B.; Shi, W.-T.; Yu, W.-H.; Tian, C.-F. Global Transcriptional Repression of Diguanylate Cyclases by MucR1 Is Essential for Sinorhizobium-Soybean Symbiosis. mBio 2021, 12, e01192-21.
  138. Sauviac, L.; Philippe, H.; Phok, K.; Bruand, C. An Extracytoplasmic Function Sigma Factor Acts as a General Stress Response Regulator in Sinorhizobium meliloti. J. Bacteriol. 2007, 189, 4204–4216.
  139. Bertram-Drogatz, P.A.; Quester, I.; Becker, A.; Puhler, A. The Sinorhizobium meliloti MucR Protein, Which Is Essential for the Production of High-Molecular-Weight Succinoglycan Exopolysaccharide, Binds to Short DNA Regions Upstream of exoH and exoY. Mol. Gen. Genet. 1998, 257, 433–441.
  140. Schäper, S.; Wendt, H.; Bamberger, J.; Sieber, V.; Schmid, J.; Becker, A. A Bifunctional UDP-Sugar 4-Epimerase Supports Biosynthesis of Multiple Cell Surface Polysaccharides in Sinorhizobium meliloti. J. Bacteriol. 2019, 201, e00801-18.
  141. Shi, W.-T.; Zhang, B.; Li, M.-L.; Liu, K.-H.; Jiao, J.; Tian, C.-F. The Convergent Xenogeneic Silencer MucR Predisposes α-Proteobacteria to Integrate AT-Rich Symbiosis Genes. Nucleic Acids Res. 2022, 50, 8580–8598.
More
© Text is available under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/)
ScholarVision Creations
Feedback