nodD2, and nodD3) affect the rate at which this bacterium nodulates different host
plants. For example, trigonelline and stachydrine, major components in seed exudates of M. sativa L., induce nod gene transcription in R. meliloti by activating
the regulatory protein NodD2, but not the homologous NodDl protein [92].
2.4
Nod Factors, Surface Polysaccharides, and Secreted Proteins
as Rhizobial Determinants of Host Specificity
2.4.1 Nod Factors
The products of rhizobial nod genes are involved in synthesis and secretion of
specific lipochitooligosaccharidic molecules called Nod factors. Nod factors serve
as signaling molecules that are essential for bacterial invasion and initiation of
the nodule formation in the root cortex [7, 21, 93, 94]. Nod factors are the most
important signals in the symbiotic development; without them rhizobia cannot enter
legume roots [19]. Nod factors are oligomers that consist of usually four or five
β-(1,4)-linked N-acetyl-glucosamine residues, to which a fatty acyl chain with
varying length and varying degrees of unsaturation is attached at the nonreducing
terminus [20, 22]. Within rhizobia, Nod factors are structurally diverse and specific
for individual rhizobial strains [11, 18, 86, 87, 90, 91]. Different rhizobial species
produce various Nod factors, which have chemical substitutions on the reducing
and nonreducing monosaccharides in the backbone chain and variations in the
structure of the acyl chain. The broad range of Nod factors produced by rhizobia
appears to be important for the selection of host range and specific nodulation. For
example, each species of Rhizobium has a certain set of nod genes that determine the
length of the lipochitooligosaccharide skeleton and make the Nod factors specific to
the host plant [19].
Rhizobia have common and specific nod genes. The first groups of nod genes
(nodABC) encode the core Nod structure that is common to all rhizobia species [22,
67]. NodA gene encodes an acyltransferase that binds an acyl chain to the
nonreducing end of the oligosaccharides; nodB encodes a deacetylase, which
removes the N-acetyl moiety from the nonreducing terminus of these oligosaccharides; and nodC encodes N-acetyl-glucosaminyltransferase that polymerizes
UDP-N-acetyl-D-glucosamine into oligosaccharide chains [67]. The second group
of nod genes (e.g., nodPQ, nodH, nodEF, nodX) has a strong species specificity
[71]. They control the modification of chemical structure of Nod factors by changing
the size and saturation of the acyl chain or adding to the terminal sugar units with
acetyl, methyl, carbamoyl, sulfuryl, or glycosyl groups [12].
Nod genes were shown to be highly conserved even between distantly related
lineages of rhizobia, suggesting that they might have a monophyletic origin and
could have been transmitted to different groups of nonsymbiotic bacteria by horizontal transfer [22]. Genes encoding enzymes involved in the Nod factor synthesis
and genes of symbiotic nitrogen fixation (nif and fix genes) are either located on one
of the megaplasmids, called a symbiotic plasmid (pSym) (e.g., in R. leguminosarum,
13 Legume-Rhizobium Symbiosis: Secondary Metabolites, Free Radical Processes. . .
299
plants. For example, trigonelline and stachydrine, major components in seed exudates of M. sativa L., induce nod gene transcription in R. meliloti by activating
the regulatory protein NodD2, but not the homologous NodDl protein [92].
2.4
Nod Factors, Surface Polysaccharides, and Secreted Proteins
as Rhizobial Determinants of Host Specificity
2.4.1 Nod Factors
The products of rhizobial nod genes are involved in synthesis and secretion of
specific lipochitooligosaccharidic molecules called Nod factors. Nod factors serve
as signaling molecules that are essential for bacterial invasion and initiation of
the nodule formation in the root cortex [7, 21, 93, 94]. Nod factors are the most
important signals in the symbiotic development; without them rhizobia cannot enter
legume roots [19]. Nod factors are oligomers that consist of usually four or five
β-(1,4)-linked N-acetyl-glucosamine residues, to which a fatty acyl chain with
varying length and varying degrees of unsaturation is attached at the nonreducing
terminus [20, 22]. Within rhizobia, Nod factors are structurally diverse and specific
for individual rhizobial strains [11, 18, 86, 87, 90, 91]. Different rhizobial species
produce various Nod factors, which have chemical substitutions on the reducing
and nonreducing monosaccharides in the backbone chain and variations in the
structure of the acyl chain. The broad range of Nod factors produced by rhizobia
appears to be important for the selection of host range and specific nodulation. For
example, each species of Rhizobium has a certain set of nod genes that determine the
length of the lipochitooligosaccharide skeleton and make the Nod factors specific to
the host plant [19].
Rhizobia have common and specific nod genes. The first groups of nod genes
(nodABC) encode the core Nod structure that is common to all rhizobia species [22,
67]. NodA gene encodes an acyltransferase that binds an acyl chain to the
nonreducing end of the oligosaccharides; nodB encodes a deacetylase, which
removes the N-acetyl moiety from the nonreducing terminus of these oligosaccharides; and nodC encodes N-acetyl-glucosaminyltransferase that polymerizes
UDP-N-acetyl-D-glucosamine into oligosaccharide chains [67]. The second group
of nod genes (e.g., nodPQ, nodH, nodEF, nodX) has a strong species specificity
[71]. They control the modification of chemical structure of Nod factors by changing
the size and saturation of the acyl chain or adding to the terminal sugar units with
acetyl, methyl, carbamoyl, sulfuryl, or glycosyl groups [12].
Nod genes were shown to be highly conserved even between distantly related
lineages of rhizobia, suggesting that they might have a monophyletic origin and
could have been transmitted to different groups of nonsymbiotic bacteria by horizontal transfer [22]. Genes encoding enzymes involved in the Nod factor synthesis
and genes of symbiotic nitrogen fixation (nif and fix genes) are either located on one
of the megaplasmids, called a symbiotic plasmid (pSym) (e.g., in R. leguminosarum,
13 Legume-Rhizobium Symbiosis: Secondary Metabolites, Free Radical Processes. . .
299