Rhizobial Symbiotic Gene Compendium

Genome Sequences — Bradyrhizobium

R1 Kaneko T, Nakamura Y, Sato S, Minamisawa K, Uchiumi T, et al. (2002). Complete genomic sequence of nitrogen-fixing symbiotic bacterium Bradyrhizobium japonicum USDA110. DNA Research 9(6):189–197. [DOI] [PubMed] [Full Text] Primary USDA110 genome reference; identifies the 681-kb symbiosis island and all nod/nif/fix gene loci.
R2 Kaneko T, Nakamura Y, Sato S, Minamisawa K, Uchiumi T, et al. (2002). Complete genomic sequence of nitrogen-fixing symbiotic bacterium Bradyrhizobium japonicum USDA110 (Supplement). DNA Research 9(6):225–256. [DOI] [PubMed] [Full Text] Supplementary gene tables and annotation for all symbiotic regions of USDA110.
R3 Kaneko T, Maita H, Hirakawa H, Uchiike N, Minamisawa K, et al. (2011). Complete genome sequence of the soybean symbiont Bradyrhizobium japonicum strain USDA6^T. Genes (Basel) 2:763–787. [DOI] [PubMed]
R4 Giraud E, Moulin L, Vallenet D, Barbe V, Cytryn E, et al. (2007). Legumes symbioses: absence of Nod genes in photosynthetic bradyrhizobia. Science 316(5829):1307–1312. [DOI] [PubMed] Photosynthetic BTAi1 and ORS278 genomes; nod-independent symbiosis; nifV requirement for Aeschynomene strains.
R5 Okubo T, Fukushima S, Itakura M, Oshima K, et al. (2013). Genome analysis of Bradyrhizobium oligotrophicum S58. Applied and Environmental Microbiology 79(8):2542–2551. [DOI] [PubMed]
R6 Göttfert M, Röthlisberger S, Kündig C, Beck C, Marty R, Hennecke H. (2001). Potential symbiosis-specific genes uncovered by sequencing a 410-kilobase DNA region of the Bradyrhizobium japonicum chromosome. Journal of Bacteriology 183(4):1405–1412. [DOI] [PubMed] [PMC] Systematic identification of nod/nol/noe genes in the B. japonicum symbiosis island.

nod / nol / noe Genes — Nodulation and Nod Factor Biosynthesis

R7 Dénarié J, Debellé F, Promé J-C. (1996). Rhizobium lipo-chitooligosaccharide nodulation factors: signaling molecules mediating recognition and morphogenesis. Annual Review of Biochemistry 65:503–535. [DOI] [PubMed] Landmark review — covers all nodABC core functions, nol and noe gene roles, host specificity, Nod factor structure.
R8 Spaink HP, Wijfjes AHM, Lugtenberg BJJ. (1995). Rhizobium NodI and NodJ proteins play a role in the efficiency of secretion of lipochitin oligosaccharides. Journal of Bacteriology 177(21):6276–6281. [DOI] [PubMed] [PMC] Defines NodI/NodJ ABC transporter role in LCO export across the inner membrane.
R9 John M, Röhrig H, Schmidt J, Wieneke U, Schell J. (1993). Rhizobium NodB protein involved in nodulation signal synthesis is a chitooligosaccharide deacetylase. PNAS 90(2):625–629. [DOI] [PubMed] [PMC] Defines NodB enzymatic function as chitooligosaccharide deacetylase.
R10 Kamst E, Pilling J, Raamsdonk LM, Lugtenberg BJJ, Spaink HP. (1997). Rhizobium nodulation protein NodC is an important determinant of chitin oligosaccharide chain length in Nod factor biosynthesis. Journal of Bacteriology 179(7):2103–2108. [DOI] [PubMed] [PMC] NodC as N-acetylglucosaminyltransferase; determines chitin chain length.
R11 Stacey G, Luka S, Sanjuan J, Banfalvi Z, Nieuwkoop AJ, et al. (1994). nodZ, a unique host-specific nodulation gene, is involved in the fucosylation of the lipooligosaccharide nodulation signal of Bradyrhizobium japonicum. Journal of Bacteriology 176(3):620–633. [DOI] [PubMed] [PMC] Defines nodZ fucosyltransferase in B. japonicum; key host-range determinant.
R12 Sadowsky MJ, Cregan PB, Göttfert M, Sharma A, Gerhold D, et al. (1991). The Bradyrhizobium japonicum nolA gene and its involvement in the genotype-specific nodulation of soybeans. PNAS 88(2):637–641. [DOI] [PubMed] [PMC] Defines NolA as a MerR-type regulator of genotype-specific nodulation; repressor of nodD2.
R13 Baev N, Schultze M, Barlier I, Ha DC, Virelizier H, Kondorosi E, Kondorosi A. (1992). Rhizobium nodM and nodN genes are common nod genes: nodM encodes functions for efficiency of Nod signal production and bacteroid maturation. Journal of Bacteriology 174(23):7555–7565. [DOI] [PubMed] [PMC] NodM glucosamine synthase function; NodN role in Nod signal production.
R14 Mergaert P, D'Haeze W, Fernández-López M, Geelen D, Goethals K, et al. (1996). Fucosylation and arabinosylation of Nod factors in Azorhizobium caulinodans: involvement of nolK, nodZ as well as noeC and/or downstream genes. Molecular Microbiology 21(2):409–419. [DOI] [PubMed] nolK role in GDP-fucose biosynthesis; noeC accessory function.
R15 Corvera A, Promé D, Promé J-C, Martínez-Romero E, Romero D. (1999). The nolL gene from Rhizobium etli determines nodulation efficiency by mediating the acetylation of the fucosyl residue in the nodulation factor. Molecular Plant-Microbe Interactions 12(3):236–246. [DOI] [PubMed] nolL O-acetyltransferase activity on fucosyl residue; host specificity.
R16 Geelen D, Mergaert P, Geremia RA, Goormachtig S, Van Montagu M, Holsters M. (1993). Identification of nodSUIJ genes in Nod locus 1 of Azorhizobium caulinodans: evidence that nodS encodes a methyltransferase involved in Nod factor modification. Molecular Microbiology 9(1):145–154. [DOI] [PubMed] nodS N-methyltransferase function in Nod factor modification.
R17 Roche P, Debellé F, Maillet F, Lerouge P, Faucher C, et al. (1991). Molecular basis of symbiotic host specificity in Rhizobium meliloti: nodH and nodPQ genes encode the sulfation of lipo-oligosaccharide signals. Cell 67(6):1131–1143. [DOI] [PubMed] nodH sulfotransferase and nodPQ sulfate activation; absent in most Bradyrhizobium.
R18 Sanjuan J, Carlson RW, Spaink HP, Bhat UR, Barbour WM, Glushka J, Stacey G. (1992). A 2-O-methylfucose moiety is present in the lipo-oligosaccharide nodulation signal of Bradyrhizobium japonicum. PNAS 89(18):8789–8793. [DOI] [PubMed] [PMC] Identifies 2-O-methylfucose on B. japonicum Nod factors; noeI methyltransferase context.
R19 Loh J, Stacey G. (2003). Nodulation gene regulation in Bradyrhizobium japonicum: a unique integration of global regulatory circuits. Applied and Environmental Microbiology 69(1):10–17. [DOI] [PubMed] [PMC] Review of all B. japonicum nod/nol/noe gene regulation; NodD, NodW, NolA circuits.

nif Genes — Nitrogenase Structure and Biosynthesis

R20 Fischer H-M. (1994). Genetic regulation of nitrogen fixation in rhizobia. Microbiological Reviews 58(3):352–386. [DOI] [PubMed] [PMC] Comprehensive review of all nif and fix gene regulation in B. japonicum, S. meliloti, A. caulinodans; nifA, FixLJ, FixK cascades.
R21 Howard JB, Rees DC. (1996). Structural basis of biological nitrogen fixation. Chemical Reviews 96(7):2965–2982. [DOI] [PubMed] Defines NifH, NifD, NifK structural roles; Mo-nitrogenase mechanism.
R22 Rubio LM, Ludden PW. (2008). Biosynthesis of the iron-molybdenum cofactor of nitrogenase. Annual Review of Microbiology 62:93–111. [DOI] [PubMed] Detailed review of nifB, nifE, nifN, nifX, nifS, nifU, nifV, nifW, nifY, nifZ, nifQ cofactor assembly pathway.
R23 Morett E, Fischer H-M, Hennecke H. (1991). Influence of oxygen on DNA binding, positive control, and stability of the Bradyrhizobium japonicum NifA regulatory protein. Journal of Bacteriology 173(10):3478–3487. [DOI] [PubMed] [PMC] Characterises NifA oxygen sensitivity and σ⁵⁴-dependent activation in B. japonicum.
R24 Nukui N, Minamisawa K, Ayabe S, Aoki T. (2006). Expression of the 1-aminocyclopropane-1-carboxylic acid deaminase gene requires symbiotic nitrogen-fixing regulator gene nifA2 in Mesorhizobium loti MAFF303099. Applied and Environmental Microbiology 72(7):4774–4779. [DOI] [PubMed] [PMC] Demonstrates two nifA copies (nifA1/nifA2) in M. loti and their functional divergence.
R25 Kullik I, Fritsche S, Knobel H, Sanjuan J, Hennecke H, Fischer H-M. (1991). Bradyrhizobium japonicum has two differentially regulated, functional homologs of the σ54 gene (rpoN). Journal of Bacteriology 173(5):1125–1138. [DOI] [PubMed] [PMC] Defines rpoN1/rpoN2 two-copy arrangement in B. japonicum and their roles in nif gene activation.
R53 Hauser F, Pessi G, Friberg M, Weber C, Rusca N, Lindemann A, Fischer H-M, Hennecke H. (2007). Dissection of the Bradyrhizobium japonicum NifA+σ⁵⁴ regulon, and identification of a ferredoxin gene (fdxN) for symbiotic nitrogen fixation. Molecular Genetics and Genomics 278(3):255–271. [DOI] [PubMed] [Full Text] Genome-wide characterisation of the B. japonicum NifA+σ⁵⁴ regulon; identifies fdxN as a NifA-regulated ferredoxin required for efficient symbiotic N₂ fixation and candidate direct electron donor to nitrogenase.
R54 Klipp W, Reiländer H, Schlüter A, Krey R, Pühler A. (1989). The Rhizobium meliloti fdxN gene encoding a ferredoxin-like protein is necessary for nitrogen fixation and is cotranscribed with nifA and nifB. Molecular and General Genetics 216(2–3):293–302. [DOI] [PubMed] Establishes that fdxN is absolutely required for symbiotic N₂ fixation in S. meliloti; defines the nifA-nifB-fdxN operon; functional cysteine motifs characterised.
R55 Ebeling S, Noti JD, Hennecke H. (1988). Identification of a new Bradyrhizobium japonicum gene (frxA) encoding a ferredoxin-like protein. Journal of Bacteriology 170(4):1999–2001. [DOI] [PubMed] [PMC] Original identification of frxA (fdxA) as a novel ferredoxin-like protein gene in B. japonicum; distinct from fdxN.
R56 Weidenhaupt M, Rossi P, Beck C, Fischer H-M, Hennecke H. (1996). Bradyrhizobium japonicum possesses two discrete sets of electron transfer flavoprotein genes: fixA, fixB and etfS, etfL. Archives of Microbiology 165(3):169–178. [DOI] [PubMed] Identifies and characterises etfS and etfL as bona fide housekeeping ETF genes (Group I), distinct from the symbiosis-specific fixA/fixB (Group II); aerobically expressed; provides the two-ETF-family framework for B. japonicum.

fix Genes — Microaerobic Respiration and Regulatory Cascades

R26 Preisig O, Zufferey R, Thöny-Meyer L, Appleby CA, Hennecke H. (1996). A high-affinity cbb3-type cytochrome oxidase terminates the symbiosis-specific respiratory chain of Bradyrhizobium japonicum. Journal of Bacteriology 178(6):1532–1538. [DOI] [PubMed] [PMC] Defines fixNOQP-encoded cbb3 oxidase biochemical properties; key fix gene reference.
R27 Preisig O, Zufferey R, Hennecke H. (1996). The Bradyrhizobium japonicum fixGHIS genes are required for the formation of the high-affinity cbb3-type cytochrome oxidase. Archives of Microbiology 165(5):297–305. [DOI] [PubMed] Defines fixGHIS role in cbb3 oxidase assembly; copper chaperone function of FixG/FixI.
R28 Preisig O, Anthamatten D, Hennecke H. (1993). Genes for a microaerobically induced oxidase complex in Bradyrhizobium japonicum are essential for a nitrogen-fixing endosymbiosis. PNAS 90(8):3309–3313. [DOI] [PubMed] [PMC] First demonstration that fixNOQP mutations abolish symbiotic N₂ fixation; discovery paper.
R29 Bauer E, Kaspar T, Fischer H-M, Hennecke H. (1998). Expression of the fixR-nifA operon in Bradyrhizobium japonicum depends on a new response regulator, RegR. Journal of Bacteriology 180(15):3853–3863. [DOI] [PubMed] [PMC] Defines the fixR-nifA operon and RegSR (RegR) two-component system as primary O₂-sensing cascade in B. japonicum (replaces FixLJ).
R30 Mesa S, Bedmar EJ, Chanfon A, Hennecke H, Fischer H-M. (2003). Bradyrhizobium japonicum NifA is a target for FixK2-mediated repression. Journal of Bacteriology 185(21):6392–6396. [DOI] [PubMed] [PMC] Defines FixK2 as main transcriptional activator of fixNOQP; describes 2 fixK copies in B. japonicum.
R31 Gubler M, Hennecke H. (1986). fixA, fixB and fixC genes are essential for symbiotic and free-living microaerobic nitrogen fixation. FEBS Letters 200(1):186–192. [DOI] [PubMed] Defines fixABCX operon essentiality in B. japonicum.
R32 Earl CD, Ronson CW, Ausubel FM. (1987). Genetic and structural analysis of the Rhizobium meliloti fixA, fixB, fixC, and fixX genes. Journal of Bacteriology 169(3):1127–1136. [DOI] [PubMed] [PMC] Original description and structural analysis of the fixABCX operon.
R33 Lindström K, Mousavi SA. (2020). Effectiveness of nitrogen fixation in rhizobia. Microbial Biotechnology 13(5):1314–1335. [DOI] [PubMed] [PMC] Comprehensive modern review; covers nosZ, fixLJ, fnrN, regSR, hup, and all major gene families across rhizobia.

hup / hyp Genes — Hydrogenase and Maturation

R34 Baginsky C, Brito B, Imperial J, Ruiz-Argüeso T, Palacios JM. (2002). Diversity and evolution of hydrogenase systems in rhizobia. Applied and Environmental Microbiology 68(10):4915–4924. [DOI] [PubMed] [Full Text] Comprehensive survey of hup/hyp gene distribution, organisation, and evolution across rhizobia.
R35 Sayavedra-Soto LA, Powell GK, Evans HJ, Morris RO. (1988). Nucleotide sequence of the genetic loci encoding subunits of Bradyrhizobium japonicum uptake hydrogenase. PNAS 85(23):8395–8399. [DOI] [PubMed] [PMC] Original sequencing and characterisation of hupS and hupL structural genes.
R36 Fu C, Maier RJ. (1994). Organization of the hydrogenase gene cluster from Bradyrhizobium japonicum: sequences and analysis of five more hydrogenase-related genes (hupGHIJK). Gene 145(1):91–96. [DOI] [PubMed] Defines hupG, hupH, hupI, hupJ, hupK accessory protein functions in hydrogenase assembly.
R37 Black LK, Fu C, Maier RJ. (1994). Sequences and characterization of hupU and hupV genes of Bradyrhizobium japonicum encoding a possible nickel-sensing complex involved in hydrogenase expression. Journal of Bacteriology 176(22):7102–7106. [DOI] [PubMed] [PMC] Defines HupUV regulatory hydrogenase as a Ni/H₂-sensing complex.
R38 Van Soom C, Lerouge I, Vanderleyden J, Ruiz-Argüeso T, Palacios JM. (1999). Identification and characterization of hupT, a gene involved in negative regulation of hydrogen oxidation in Bradyrhizobium japonicum. Journal of Bacteriology 181(15):5085–5089. [DOI] [PubMed] [PMC] Defines HupT histidine kinase role in repression of hupSL transcription in absence of H₂.
R39 Tsukada S, Inoue S, Okubo T, Itakura M, Minamisawa K, et al. (2015). Identification of the hydrogen uptake gene cluster for chemolithoautotrophic growth and symbiosis hydrogen uptake in Bradyrhizobium diazoefficiens. Frontiers in Microbiology 6:1034. [DOI] [PubMed] [PMC] Documents two hupSL copies (hupS1L1 and hupS2L2) in B. diazoefficiens USDA110; dual-cluster organisation.
R40 Albrecht SL, Maier RJ, Hanus FJ, Russell SA, Emerich DW, Evans HJ. (1979). Hydrogenase in Rhizobium japonicum increases nitrogen fixation by nodulated soybeans. Science 203(4384):1255–1257. [DOI] [PubMed] Landmark demonstration that Hup⁺ strains improve symbiotic N₂ fixation efficiency by recycling H₂.

T3SS / nop Genes — Type III Secretion and Effectors

R41 Krause A, Doerfel A, Göttfert M. (2002). Mutational and transcriptional analysis of the type III secretion system of Bradyrhizobium japonicum. Molecular Plant-Microbe Interactions 15(12):1228–1235. [DOI] [PubMed] [Full Text] First comprehensive characterisation of B. japonicum T3SS; ttsI regulation via nod box and NodW; nopB, rhcV defined.
R42 Zehner S, Schober G, Wenzel M, Lang K, Göttfert M. (2008). Expression of the Bradyrhizobium japonicum type III secretion system in legume nodules and analysis of the associated tts box promoter. Molecular Plant-Microbe Interactions 21(8):1087–1093. [DOI] [PubMed] [Full Text] Defines tts box promoter element; T3SS activity confirmed in mature nodules; rhcV, nopL, nopB expression.
R43 Wenzel M, Friedrich L, Göttfert M, Zehner S. (2010). The type III-secreted protein NopE1 affects symbiosis and exhibits a calcium-dependent autocleavage activity. Molecular Plant-Microbe Interactions 23(1):112–117. [DOI] [PubMed] Defines NopE1 Ca²⁺-dependent autocleavage; nopE1/nopE2 two-paralog discovery in B. japonicum USDA110.
R44 Ausmees N, Kobayashi H, Bhalerao RP, et al. (2004). Characterization of NopP, a type III secreted effector of Rhizobium sp. NGR234. Journal of Bacteriology 186(14):4774–4780. [DOI] [PubMed] [PMC] Defines NopP effector; phosphorylation-based interaction with plant defence signalling.
R45 Dai W-J, Zeng Y, Xie Z-P, Staehelin C. (2008). Symbiosis-promoting and deleterious effects of NopT, a novel type 3 effector of Rhizobium sp. NGR234. Journal of Bacteriology 190(14):5101–5110. [DOI] [PubMed] [PMC] Characterises NopT YopT-family cysteine protease effector; host-range effects both positive and negative.
R46 Fauvart M, Michiels J. (2008). Rhizobial secreted proteins as determinants of host specificity in the rhizobium-legume symbiosis. FEMS Microbiology Letters 285(1):1–9. [DOI] [PubMed] Review of all rhizobial nop effectors (nopB, nopC, nopL, nopM, nopP, nopT, nopX) and their host specificity roles.
R47 Tampakaki AP. (2014). Commonalities and differences of T3SSs in rhizobia and plant pathogenic bacteria. Frontiers in Plant Science 5:114. [DOI] [PubMed] [PMC] Comparative overview of rhcC, rhcJ, rhcN, rhcQ–rhcV structural genes; T3SS apparatus across rhizobia.
R48 Marie C, Deakin WJ, Viprey V, Kopcinska J, Golinowski W, et al. (2003). Characterization of Nops, nodulation outer proteins, secreted via the type III secretion system of NGR234. Molecular Plant-Microbe Interactions 16(9):743–751. [DOI] [PubMed] Defines NopM (IpaH-type E3 ubiquitin ligase effector) and multiple nop effector proteins; two nopM copies in B. elkanii context.

Regulatory Genes and Other Symbiotic Support

R49 Oldroyd GED, Murray JD, Poole PS, Downie JA. (2011). The rules of engagement in the legume-rhizobial symbiosis. Annual Review of Genetics 45:119–144. [DOI] [PubMed] Broad review covering regulatory cascades, NodD, NifA, FixLJ, rpoN, and signal exchange in legume symbiosis.
R50 Giraud E, Moulin L, Vallenet D, Barbe V, Cytryn E, et al. (2007). Legumes symbioses: absence of Nod genes in photosynthetic bradyrhizobia. Science 316(5829):1307–1312. [DOI] [PubMed] Landmark paper; nod-independent bradyrhizobia BTAi1/ORS278; nifV requirement for Aeschynomene strains; nosZ distribution.
R51 Masson-Boivin C, Giraud E, Perret X, Batut J. (2009). Establishing nitrogen-fixing symbiosis with legumes: how many rhizobium recipes? Trends in Microbiology 17(10):458–466. [DOI] [PubMed] Evolutionary perspective on rhizobial symbiotic gene acquisition; covers regSR, fnrN, and regulatory diversity across genera.
R52 Tian C-F, Zhou Y-J, Zhang Y-M, Li Q-Q, Zhang Y-Z, et al. (2012). Comparative genomics of rhizobia nodulating soybean suggests extensive recruitment of lineage-specific genes in adaptations. Molecular Biology and Evolution 29(11):2658–2676. [DOI] [PubMed] [PMC] Comparative genomics of soybean-nodulating rhizobia; context for rpoN, regSR and fnrN copy numbers and regulatory diversity.

📚 Literature References

Genome Sequences — Bradyrhizobium

nod / nol / noe Genes — Nodulation and Nod Factor Biosynthesis

nif Genes — Nitrogenase Structure and Biosynthesis

fix Genes — Microaerobic Respiration and Regulatory Cascades

hup / hyp Genes — Hydrogenase and Maturation

T3SS / nop Genes — Type III Secretion and Effectors

Regulatory Genes and Other Symbiotic Support