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Review

Molecular Basis of Symbiotic Promiscuity

Xavier Perret, Christian Staehelin, William J. Broughton
Xavier Perret
Laboratoire de Biologie Moléculaire des Plantes Supérieures, Université de Genève, 1292 Chambésy/Geneva, and
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Christian Staehelin
Botanisches Institut der Universität, 4056 Basel, Switzerland
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William J. Broughton
Laboratoire de Biologie Moléculaire des Plantes Supérieures, Université de Genève, 1292 Chambésy/Geneva, and
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DOI: 10.1128/MMBR.64.1.180-201.2000
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  • Fig. 1.
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    Fig. 1.

    Invasion of legume root hairs by Rhizobium. (A) Rhizobia (rh) colonize the rhizosphere and attach to the root hairs (r). (B) Opening the “outer door.” Nod factors induce root hair curling and permit bacterial penetration at the center of infection (ci). The plant nucleus (n) precedes the growing infection thread(s) (it). (C) Crossing the inner doors. Still accompanied by the nucleus (n) an elongating infection thread (it) reaches the base of the root hair cell. (D) A developing infection thread ramifies (rit) near the nodule primordia formed by dividing cortical cells. (E) Bacteroids (b) are released from the infection thread (it) and form symbiosomes (s) in nodule cells. Granules of poly-β-hydroxybutarate (phb) accumulate in bacteroids surrounded by the peribacteroid membrane (pb). Other abbreviations:c, cortex; d, digestive vacuole; ep, epidermis; ed, endodermis.

  • Fig. 2.
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    Fig. 2.

    Early steps in nodulation of legumes showing that continued development of infection threads is under the control of thenodD1 gene in Rhizobium sp. NGR234. (A) Fluorescent image of a Vigna unguiculata root hair inoculated with a mutant incapable of producing NodNGR factors (NGRΔnodABC) and concomitantly treated with 10−7 M NodNGR(S) factors. Arrows point to rhizobia (rh). (B) Commencement of curling of a root hair stained with methylene blue. Extreme curling leads to the formation of a bright spot (bs), where rhizobia are often entrapped (same treatment as in panel A). (C) A bright-field image of a root hair inoculated with NGRΔnodABC::GUS3, treated with 10−7M NodNGR(S) factors, and stained for β-glucuronidase activity. Arrows point to the entrapped rhizobia within the curl. (D) Fluorescent image of a root hair curled in the shape of a shepherd's crook, showing the center of infection (ci). (E) Experiment in which the nodABCmutant was replaced with NGRΔnodD1::GUS3, but incubated with 10−7 M NodNGR(S) factors, and stained for β-glucuronidase activity. Apparently, the nodD1 mutant lacks a factor(s) that is necessary for the continued development of infection threads (it). In its absence, infection threads abort (ait), forming a structure that resembles a cerebellum (cb). (F) Photomicrograph of root hairs inoculated with wild-type NGR234 marked with GUS3. Infection threads develop along the length of the root hair (dit). B. Relić and W. J. Broughton (unpublished results; see reference 215 for further details).

  • Fig. 3.
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    Fig. 3.

    Examples of the five classes of rhizobial polysaccharides. (A) Structure of cyclic β-(1,6)-β-(1,3)-glucans common to B. japonicum. Redrawn from reference26. (B) Acidic EPS of Rhizobium sp. strain NGR234 (60). EPS I (succinoglycan) of R. meliloti resembles the EPS of strain NGR234. (C) KPS of R. leguminosarum bv. trifolii (98). (D) The somatic K antigen of R. fredii USDA257 (83). (E) Core structure of the LPS of R. etli (84). Abbreviations: Gal, galactose; GalA, galacturonic acid; Glc, glucose; GlcA, glucoronic acid; Man, mannose; Kdo, 3-deoxy-d-manno-2-octulosonic acid; OAc, acetate group; Pyr, pyridine.

Tables

  • Figures
  • Table 1.

    Nodulation capacities of symbiotic members of the bacterial family Rhizobiaceaea

    SpeciesTypical host(s)Host rangeExamples of nonhostsReference(s)
    Azorhizobium caulinodansRobinieae (P),Sesbania spp.Compatible only with Sesbania punctata and S. rostrataMIMOSOIDEAE, PAPILIONOIDEAE (except Sesbania)M. Holsters, personal communication
    Bradyrhizobium spp.Genisteae (P),Lupinus spp.Acacieae (M), Mimoseae (M), Desmodieae (P), Loteae (P), Psoraleeae (P), Phaseoleae (P), Aeschynomeneae (P)Vicieae (P), Cicereae (P), Trifolieae (P)C. E. Pankhurst and C. W. Ronson, personal communication; H. Meyer z. A. and W. J. Broughton, unpublished data
     Lupinus isolates
    Vigna isolates
    Phaseoleae (P), Macroptilium, Vignaspp.
    Bradyrhizobium elkaniiPhaseoleae (P),Glycine spp.Phaseoleae (P), Macroptilium,Vigna spp.Vicieae (P), Cicereae (P), Trifolieae (P)G. Stacey, personal communication
    Bradyrhizobium japonicumPhaseoleae (P), Glycine spp.Aeschynomeneae (P), Arachis spp., Phaseoleae (P), Macroptilium,Vigna spp.Vicieae (P), Cicereae (P), Trifolieae (P)G. Stacey, personal communication
    Mesorhizobium huakuiiAstragalus sinicusGalegeae (P),Astragalus spp.MIMOSOIDEAE, PAPILIONOIDEAE282
    Mesorhizobium lotiLoteae (P), Lotus spp., Genisteae (P),Lupinus spp.Mimoseae (M), Mimosa pudica,Leuceana leucocephala; Phaseoleae (P), Macroptilium atropurpureumVicieae (P), Cicereae (P), Trifolieae (P)G. Stacey, personal communication
    Rhizobium sp. strain NGR234Phaseoleae (P), Desmodieae (P)Mimoseae (M), Acacieae (M), Ingeae (M), Sophoreae (P), Dalbergieae (P), Amorpheae (P), Millettieae (P), Robinieae (P), Indigofereae (P), Loteae (P), Galegeae (P), Bossiaeae (P), Mirbelieae (P), Podalyrieae (P), Crotalarieae (P), Thermopsideae (P), Genisteae (P), Psoraleeae (P)Vicieae (P), Cicereae (P), Trifolieae (P)207
    Rhizobium etliPhaseoleae (P), Phaseolus spp.Ingeae (M), Crotalarieae (P), Galegeae (P), Mimoseae (M), Desmodieae (P), Robinieae (P)Robinieae (P)122; E. Martínez-Romero, personal communication
    Rhizobium frediiPhaseoleae (P), Desmodieae (P)Mimoseae (M), Ingeae (M), Sophoreae (P), Amorpheae (P), Millettieae (P), Robinieae (P), Indigofereae (P), Loteae (P)Vicieae (P), Cicereae (P), Trifolieae (P)207
    Rhizobium galegaeGalegeae (P), Galega spp.Compatible only with Galegaspp.MIMOSOIDEAE, PAPILIONOIDEAE (except Galega)K. Lindström, personal communication
    Rhizobium leguminosarum bv. phaseoliPhaseoleae (P), Phaseolusspp.Phaseoleae (P)MIMOSOIDEAE, Trifolieae (P)E. Martínez-Romero, personal communication
    Rhizobium leguminosarum bv. trifoliiTrifolieae (P), Trifoliumspp.Phaseoleae (P), Desmodieae (P), Trifolieae (P),Medicago spp.MIMOSOIDEAE, Phaseoleae (P)H. P. Spaink, personal communication
    Rhizobium leguminosarumbv. viciaeVicieae (P), Pisum sativum, Viciaspp.Lathyrus spp. (e.g., L. sativa)MIMOSOIDEAE, Phaseoleae (P), Desmodieae (P)J. A. Downie, personal communication
    Rhizobium melilotiTrifolieae (P), Medicago spp.,Melilotus spp., Trigonellaspp.Acacieae (M), Desmodieae (P), Mimoseae (M), Phaseoleae (P), Vicieae (P)J. Dénarié, personal communication
    Rhizobium saheliRobinieae (P),Sesbania spp.Acacieae (M), Mimoseae (M)165; C. Boivin, personal communication
    Rhizobium teranga bv. acaciaeAcacieae (M),Acacia spp.Mimoseae (M), Leucaena leucocephala, Prosopis julifloraRobinieae (P),Sesbania spp.165; C. Boivin, personal communication
    Rhizobium teranga bv. sesbaniaeRobinieae (P), Sesbania spp.Acacieae (M), Mimoseae (M)165; C. Boivin, personal communication
    Rhizobium tropiciPhaseoleae (P),Phaseolus spp.Galegeae (P), Crotalarieae (P), Desmodieae (P), Mimoseae (M), Robinieae (P), Loteae (P)Vicieae (P), Cicereae (P), Trifolieae (P)E. Martinez-Romero, personal communication
    • ↵a Plants are listed by their subfamilies, tribes, genera, and species. Associations are listed only where fully effective nodulation (i.e., Fix+) has been reported. Subfamily names are listed in capital letters (Caesalpinioideae [C], Mimosoideae [M], and Papilionoideae [P]) (201).

  • Table 2.

    Nodulation capacities of some broad-host-range rhizobia isolated from various legumes

    Plant nodulatedaNodulationa, bby rhizobia isolated from:
    Mucuna(P10)cAlbizia(M5)Desmodium (P11)Glycine(P10)Lablab (P10) NGR234Sesbania (P8)
    Amorpheae (P6)
     Amorphaspp.++++++
    Mirbelieae (P24)
     Chorizemaspp.+++−++
    Phaseoleae (P10)
     Centrosema spp.+++−++
     Phaseolus spp.++++++
    Robinieae (P8)
     Robiniaspp.++++++
     Sesbaniaspp.++++++
    • ↵a Letters in brackets represent the subfamily to which the legume belongs (M, Mimosoideae; P, Papilionoideae), and the numbers represent the tribe (201).

    • ↵b +, effective (Fix+) nodulation; −, failure to nodulate (Nod−). Data forMucuna, Albizia, Desmodium, andSesbania rhizobia from reference 279; data for Glycine (rhizobial strain USDA257) andLablab (rhizobial strain NGR234) rhizobia from reference207.

    • ↵c We assigned this rhizobial isolate toBradyrhizobium because of its slow growth.

  • Table 3.

    Responses of known promiscuous legumes to diverse rhizobia

    LegumeaGeographical originb% Nod+Reference
    Mimosoideae (M3)I
     Leucaena leucocephalaTropical America44157
    Amorpheae (P6)I
     Amorpha fruticosaNorth America91279
    Mirbelieae (P24)I
     Chorizema ilicifoliumSoutheast Australia91279
    Phaseoleae (P10)D
     Centrosema virgininianumWarm America91279
     Lablab purpureusTropical Africa50157
     Macroptilium atropurpureumTropical America41H. Meyer z. A. and W. J. Broughton, unpublished
     Phaseolus coccineusTropical and warm America91279
     Vigna unguiculataOld World Tropical56157
    Robinieae (P8)I
     Robinia pseudoacaciaTropical and warm America94279
     Sesbania drummondiiOld World Tropical94279
    • ↵a Letters in parentheses represent the subfamily to which the legume belongs (M, Mimosoideae; P, Papilionoideae), and the numbers represent the tribe (201). D = determinate nodules; I, indeterminate nodules.

    • ↵b Data from reference 166. The data were taken from the reports of Wilson (279), who tested the nodulation capacity of 32 rhizobial isolates (from 31 legume genera) on the nodulation capacities of 160 species (78 genera), and Meyer z. A. and Broughton (see reference 157), who assayed the ability of 50 rhizobial isolates to nodulate 16 species (13 genera) of legumes.

  • Table 4.

    Nod factors and their baroque decorationsa  

    Embedded Image
    A. caulinodansORS571C18:1, C16:0MeOHCb, HFuc, HAra, HOH1, 2172
    B. elkaniiUSDA61C18:1Me, HCb, HAc, HMeFucHOH1, 235
    B. japonicum USDA110C16:0, C16:1, C18:1HOHHMeFucHOH2229
    Rhizobium sp. strain GRH2C16:0, C18:0, C18:1, C20:1Me, HOHHS, HHOH1, 2, 3160
    Rhizobium sp. strain ORS1645C18:0, C18:1MeCbcCbcS, HHOH2164
    Rhizobium sp. strain NGR234C16:1, C18:0, C18:1MeCb, OHCb, HMeFuc, AcMeFuc, SMeFucHOH2206
    R. etliCFN42C18:1MeCb, OHHAcFucHOH233
    R. etli CE3C18:0, C18:1MeCb, OHHAcFucHOH2203
    R. fredii USDA191bC18:1, C18:0, C16:1HHHFuc, MeFucHH0, 1, 27
    R. frediiUSDA257C18:1HOHHFuc, MeFucHOH0, 1, 26
    R. galegaeC18:1, C18:2, C18:3, C20:2, C20:3HOHCbHHAc1282
    R. huakuiidC18:4HOHHSHOH2282
    R. leguminosarum
     bv. trifolii ANU843C16:0, C16:1, C18:0, C18:1, C18:2, C20:3HOHH, AcHHOH0, 1, 2188
     bv. trifolii LPR5045C18:0, C18:1, C20:3, C20:4HOHAcHHOH2269b
     bv. viciae RBL5560C18:1, C18:4HOHAcHHOH1, 2252
     bv. viciae TOMC18:1, C18:4HOHAcAcHOH1, 280
    R. lotiNZP2213C16:0, C16:1, C18:0, C18:1, C20:0, C20:1, C22:1HCbHFuc, AcFucHFuc−1, 0, 1, 2187
    R. lotiNZP2037C18:0, C18:1MeCbCbAcFucHOH2161
    R. meliloti RCR2011C16:1, C16:2, C16:3HOHH, AcSHOH1, 22, 154
    R. tropiciCFN299C18:1MeOHHS, HHOH2202
    S. saheliORS611C16:0, C18:1MeCbcCbcFuc, HAra, HOH2163
    S. terangabv. acaciae ORS1602C16:0, C18:0, C18:1MeCbcCbcS, HHOH2164
    • ↵a Abbreviations: Ac, acetyl; Ara, arabinosyl; Cb, carbamoyl; Fuc, fucosyl; H, hydrogen; Me, methyl; S, sulfate; MeFuc, methylfucose; AcMeFuc, acetylated methylfucose; SMeFuc, sulfated methylfucose.

    • ↵b In USDA191, a minor fraction of theN-acetylglucosamine marked in brown is replaced by a glucose.

    • ↵c Carbamoyl group is either on R2 or R3.

    • ↵d R. huakuii Nod factors are partially glycolylated at the C-2 position of the reducing terminus.

  • Table 5.

    Effects of apigenin, nodD1, andnodSU on Nod factor production and nodulation of L. leucocephala by strains NGR234 and USDA257

    StrainaNod factor productionbNodulation of L. leucocephala
    − Apigenin+ Apigenin
    NGR2340.4 ± 0.261.8 ± 9.7Nod+Fix+
    NGRΔnodD10.4 ± 0.30.3 ± 0.2Nod−
    NGRΔnodSU0.3 ± 0.35.7 ± 2.5Nod−
    USDA2570.2 ± 0.21.5 ± 1.1Nod−
    USDA257(nodSU)0.1 ± 0.138.3 ± 9.8Nod+Fix+
    • ↵a NGRΔnodD1,nodD1 mutant of Rhizobium sp. strain NGR234; NGRΔnodSU, nodSU mutant of strain NGR234; USDA257 (nodSU), R. fredii USDA257 transconjugant containing the functional nodSU genes of NGR234.

    • ↵b Nod factors were quantified using the tomato cell suspension assay (259). The results are expressed in nanomoles per milliliter of culture corrected to an absorbance at 700 nm of 1 and were taken from references 144, 158, and214.

  • Table 6.

    Hydrolysis of Nod factors by chitinases and related enzymesa

    EnzymePlant isozymesbNod factors used as substratesb, cAcylated products in hydrolysateb, dReference(s)
    Chitinase class IMs, Pv,Vs,NtNodRm-V(C16:2, S)III241, 258
    Ms,VsNodRm-V(C16:2)IV, III258
    Ms,Pv, Vs,NtNodRm-IV(C16:2, S)None241, 258
    Ms, Pv, Vs,NtNodRm-IV(C16:2)III241, 258
    VuNodNGR-V(AcMeFuc)Unknown structures259
    VuNodNGR-V(SMeFuc)Unknown structures259
    Ps, Pv,VuNodNGR-V(MeFuc)Unknown structures259
    NtNodRm-IV(Ac, C16:2)None241
    NtNodRlv-V(Ac, C18:4)AcIV, AcIIIOvtsyna et al., submitted
    NtNodRlv-V(Ac, C18:4, Fuc)AcIIIOvtsyna et al., submitted
    NtNodRlv-IV(Ac, C18:4)NoneOvtsyna et al., submitted
    NtNodRlv-IV(Ac, C18:4, Fuc)NoneOvtsyna et al., submitted
    Chitinase class IINtNodRm-V(C16:2, S)III241
    NtNodRm-IV(C16:2, S)None241
    NtNodRm-IV(C16:2)III241
    Chitinase class IIICa, Bv,NtNodRm-V(C16:2, S)III, II241
    Ca, Bv,NtNodRm-IV(C16:2, S)II241
    Ca, Bv,NtNodRm-IV(C16:2)III, II241
    SrNodAc factorsUnknown structures103
    NtNodRm-IV(Ac, C16:2, S)None241
    NtNodRm-V(Ac, C16:2, S)AcIII241
    NtNodRlv-V(Ac, C18:4)AcIV, AcIIIOvtsyna et al., submitted
    NtNodRlv-V(Ac, C18:4, Fuc)AcIIIOvtsyna et al., submitted
    NtNodRlv-IV(Ac, C18:4)AcIIIOvtsyna et al., submitted
    NtNodRlv-IV(Ac, C18:4, Fuc)NoneOvtsyna et al., submitted
    Chitinase class IVBv,DcNodRm-V(C16:2, S)III241
    Bv,DcNodRm-IV(C16:2, S)None241
    Bv,DcNodRm-IV(C16:2)III241
    Chitinase class VNtNodRm-V(C16:2, S)III241
    NtNodRm-IV(C16:2, S)None241
    NtNodRm-IV(C16:2)III241
    Chitinase class VINtNodRm-V(C16:2, S)III241
    NtNodRm-IV(C16:2, S)None241
    NtNodRm-IV(C16:2)III241
    Novel chitinase/lysozymeMsNodRm-V(C16:2, S)III179
    MsNodRm-IV(C16:2, S)III179
    MsNodRm-IV(C16:2)III179
    MsNodRm-IV(Ac, C16:2, S)AcIII179
    Nod factor hydrolaseMsNodRm-V(C16:2, S)II258, 260
    MsNodRm-V(C16:2)II258
    MsNodRm-IV(C16:2, S)II258, 260
    MsNodRm-IV(C16:2)II258, 260
    MsNodRm-IV(Ac, C16:2, S)AcII260
    MsNodRm-V(Ac, C16:2, S)AcII260
    RootsMs,VsNodRm-V(C16:2, S)III, II258, 260
    Ms,VsNodRm-V(C16:2)IV, III, II258
    Ms,VsNodRm-IV(C16:2, S)II258, 260
    Ms,VsNodRm-IV(C16:2)III, II258
    MsNodRm-IV(C16:0, S)II258
    Ms, Ps,VsNodRlv-V(Ac, C18:4)AcIV, AcIII, AcII97, 118
    VsNodRlv-IV(Ac, C18:4)AcIII, AcII118
    VsNodRlv-V(Ac, C18:0)AcIV, AcIII, AcII118
    SrNodAc factorsUnknown structures103
    • ↵a Purified enzymes (as well as whole roots) of both legumes (bold) and nonlegumes were incubated with Nod factors, and the reaction products were examined for the presence of acylated chitin fragments.

    • ↵b Abbreviations are as follows. Hydrolases were isolated from the following legumes: Cicer arietinum(Ca), Medicago sativa (Ms),Phaseolus vulgaris (Pv), Pisum sativum(Ps), Sesbania rostrata (Sr),Vicia sativa (Vs), and Vigna unguiculata (Vu) and the nonlegumes Beta vulgaris (Bv), Daucus carota(Dc), and Nicotiana tabacum (Nt). Chemical groups are abbreviated as follows: acetyl (Ac), fucosyl (Fuc), methyl (Me), sulfate (S), methylfucose (MeFuc), acetylated methylfucose (AcMeFuc), sulfated methylfucose (SMeFuc).

    • ↵c Nod factors were purified from A. caulinodans (NodAc), R. leguminosarum bv. viciae (NodRlv), Rhizobium sp. strain NGR234 (NodNGR), and R. meliloti (NodRm). Details of their structure, such as the presence of certain baroque decorations (for abbreviations, see footnote b), the length of the acyl chain, and the number of double bonds, are shown in brackets. Tetramers and pentamers of N-acetylglucosamine are marked as IV and V, respectively. The nonsulfated NodRm factors and fucosylated NodRlv factors are derivatives of the wild type obtained by desulfation and fucosylation with NodZ, respectively. NodRm-IV(C16:0, S) was prepared from NodRm-IV(C16:2, S) by catalytic reduction.

    • ↵d Acylated products were separated from the substrate by reverse-phase high-pressure liquid chromatography (179, 241, 258, 260; A. O. Ovtsyna, M. Schultze, I. A. Tikhonovich, H. P. Spaink, É. Kondorosi, Á. Kondorosi, and C. Staehelin, submitted for publication) and thin-layer chromatography (97, 103, 118, 258). Abbreviations: lipotetrasaccharide (IV); lipotrisaccharide (III); lipodisaccharide (II); O-acetylated lipotetrasaccharide (AcIV); O-acetylated lipotrisaccharide (AcIII); O-acetylated lipodisaccharide (AcII); Nod factors resistant to hydrolysis by the given enzyme (None).

  • Table 7.

    Sites of hydrolytic cleavage of Nod factors ofRhizobium meliloti by enzymes isolated from the roots ofMedicago sativaa  

    Embedded Image
    Hydrolase (reference)No. of N-acetylglucosamine residuesR1R2Cleavage site(s)
    Intact roots (258, 260)IVSulfatylHa
    IVHHa, b
    IVSulfatylO-Acetyla
    VSulfatylHc, d
    VHHc, d, e
    Chitinase class I (241, 258)IVSulfatylHNone
    IVHHb
    IVSulfatylO-AcetylNone
    VSulfatylHd
    VHHd, e
    Novel chitinase/lysozyme (179)IVSulfatylHb
    IVHHb
    IVSulfatylO-Acetylb
    VSulfatylHd
    Nod factor hydrolase (258, 260)IVSulfatylHa
    IVHHa
    IVSulfatylO-Acetyla
    VSulfatylHc
    VHHc
    VSulfatylO-Acetylc
    • ↵a Distinct cleavage site preferences exist toward tetrameric (IV) and pentameric (V) Nod factors of R. meliloti as well as their desulfated and deacetylated derivatives, respectively.

  • Table 8.

    Effects of mutations in nonnodulation genes on Fix phenotypes in various legumes

    RhizobiumstrainLocus or gene(s)ProductaRegulatorPhenotypeaPlantReference(s)
    A. caulinodansORS571dTDP-d-gluc. synth.Deoxy sugarsFix−Sesbania rostrata56
    B. japonicum USDA110exoPEPS exportFix−Glycine max10
    ndvCCyclic β-glucansFix−Glycine max19
    ndvBCyclic β-glucansFix−Glycine max65
    M. lotiNZP2037EPSFix−Leucaena leucocephala127
    Fix+Lotus pedunculatus
    NGR234exoYEPSFix−Leucaena leucocephala106
    fixFRhamnose-rich SPSnodD1Fix−Vigna unguiculata130
    R. etliCFN42lpsβLPSFix−Phaseolus vulgaris92
    R. leguminosarum strain 300lpsLPSFix−Pisum sativum136
     bv. trifolii AR5LPSFix−Trifolium pratense100
     bv. trifolii 24.1EPSFix−Trifolium pratense247
     bv. trifolii LPR5pssDEPSFix−Trifolium repens270, 271
     bv. trifolii TA1pssDEPSInf+Fix−Trifolium pratense147
    R. meliloti 2011exoAMONPEPS 1Fix−Medicago sativa8
    exoUVWTIEPS 1Fix−Medicago sativa9
    R. meliloti1021exoYSGexoS,chv1Inf+ Fix−Medicago sativa40, 41
    ndvAβ-(1→2)GlucanFix−Medicago sativa262
    R. melilotiAK631rkpKKPSFix+Medicago sativa138
    rkpK1KPSexoB(galE)Fix−Medicago sativa31
    R. tropiciCIAT899::Tn5EPSExo−Fix+Macroptilium atropurpureum176
    • ↵a Abbreviations: SPS, surface polysaccharide; SG, succinoglycans; Inf, formation of infection threads; Fix, nitrogen fixation; Exo, EPS synthesis.

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Molecular Basis of Symbiotic Promiscuity
Xavier Perret, Christian Staehelin, William J. Broughton
Microbiology and Molecular Biology Reviews Mar 2000, 64 (1) 180-201; DOI: 10.1128/MMBR.64.1.180-201.2000

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Molecular Basis of Symbiotic Promiscuity
Xavier Perret, Christian Staehelin, William J. Broughton
Microbiology and Molecular Biology Reviews Mar 2000, 64 (1) 180-201; DOI: 10.1128/MMBR.64.1.180-201.2000
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  • Top
  • Article
    • SUMMARY
    • BACTERIAL PROMISCUITY
    • LEGUME FIDELITY
    • MOLECULAR BASES
    • NOD FACTORS OPEN THE LEGUME OUTER DOOR
    • DO INFECTION THREADS HAVE AN INNER DOOR?
    • EVOLUTION OF HOST SPECIFICITY
    • ACKNOWLEDGMENTS
    • REFERENCES
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KEYWORDS

Fabaceae
Plants, Medicinal
Symbiosis

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