Rhizobium-legume nodulation: life together in the underground.

The MerR family is a group of transcriptional activators with similar N-terminal helix-turn-helix DNA binding regions and C-terminal effector binding regions that are specific to the effector recognised. The signature of the family is amino acid similarity in the first 100 amino acids, including a helix-turn-helix motif followed by a coiled-coil region. With increasing recognition of members of this class over the last decade, particularly with the advent of rapid bacterial genome sequencing, MerR-like regulators have been found in a wide range of bacterial genera, but not yet in archaea or eukaryotes. The few MerR-like regulators that have been studied experimentally have been shown to activate suboptimal σ70-dependent promoters, in which the spacing between the −35 and −10 elements recognised by the σ factor is greater than the optimal 17±1 bp. Activation of transcription is through protein-dependent DNA distortion. The majority of regulators in the family respond to environmental stimuli, such as oxidative stress, heavy metals or antibiotics. A subgroup of the family activates transcription in response to metal ions. This subgroup shows sequence similarity in the C-terminal effector binding region as well as in the N-terminal region, but it is not yet clear how metal discrimination occurs. This subgroup of MerR family regulators includes MerR itself and may have evolved to generate a variety of specific metal-responsive regulators by fine-tuning the sites of metal recognition.

The MerR family of transcriptional regulators

Initial stages in the Rhizobium–legume symbiosis can be thought of as a reciprocal molecular conversation: transmission of a gene inducer from legume host to bacterium, with ensuing bacterial synthesis of a morphogen that is transmitted to the plant, switching the developmental fate of the legume root. These signal molecules have a key role in determining bacterium–host specificity and the purified Nod factor compounds provide useful new tools to probe plant cell function.

Rhizobium-plant signal exchange

The Rhizobium-plant symbiosis.

Symbiosis between rhizobia and leguminous plants leads to the formation of N2-fixing root nodules. The interaction of rhizobia and plants shows a high degree of host specificity based on the exchange of chemical signals between the symbiotic partners. The plant signals, flavonoids exuded by the roots, activate the expression of nodulation genes, resulting in the production of the rhizobial lipochitooligosaccharide signals (Nod factors). Nod factors act as morphogens that, under conditions of nitrogen limitation, induce cells within the root cortex to divide and to develop into nodule primordia. This review focuses on how the production of Nod factors is regulated, how these signals are perceived and transduced by the plant root, and the physiological conditions and plant factors that control the early events leading to root nodule development.

Regulation of symbiotic root nodule development

Several soybean genotypes have been identified which specifically exclude nodulation by members of Bradyrhizobium japonicum serocluster 123. We have identified and sequenced a DNA region from B. japonicum strain USDA 110 which is involved in genotype-specific nodulation of soybeans. This 2.3-kilobase region, cloned in pMJS12, allows B. japonicum serocluster 123 isolates to form nodules on plants of serogroup 123-restricting genotypes. The nodules, however, were ineffective for symbiotic nitrogen fixation. The nodulation-complementing region is located approximately 590 base pairs transcriptionally downstream from nodD2. The 5' end of pMJS12 contains a putative open reading frame (ORF) of 710 base pairs, termed nolA. Transposon Tn3-HoHo mutations only within the ORF abolished nodulation complementation. The N terminus of the predicted nolA gene product has strong similarity with the N terminus of MerR, the regulator of mercury resistance genes. Translational lacZ fusion experiments indicated that nolA was moderately induced by soybean seed extract and the isoflavone genistein. Restriction fragments that hybridize to pMJS12 were detected in genomic DNAs from both nodulation-restricted and -unrestricted strains.

The Bradyrhizobium japonicum nolA gene and its involvement in the genotype-specific nodulation of soybeans.

At least two nodD genes are necessary for efficient nodulation of alfalfa by Rhizobium meliloti.

Recent advances in our understanding of the molecular genetics of legume-Rhizobium symbioses have indicated that relatively few bacterial genes are required for nodulation. While some of these genes are functionally similar and shared among microsymbionts nodulating genetically diverse legumes, others appear to encode host-specific nodulation (hsn) functions which allow for nodulation of plants within a given legume genus. More recently, genotype-specific nodulation (GSN) determinants have been identified in R. leguminosarum bv. viceae strain TOM and in B. japonicum strain USDA 110. GSN determinants refer to those bacterial sequences that allow for nodulation of specific plant genotypes within a given legume species. In contrast to the avr loci of several plant pathogens, rhizobial host-range determinants (hsn and GSN) have been shown to positively affect nodulation. That is, the introduction of exogenous hsn and GSN loci extends host-range. Since GSN loci have been reported to interact with single host plant alleles, it suggests that gene-for-gene interactions occur in rhizobial-legume symbioses and contribute to nodulation specificity at the host genotype level.

Francisco Rodriguez-Quinones

Papers

The Bradyrhizobium japonicum nolA gene and its involvement in the genotype-specific nodulation of soybeans.

At least two nodD genes are necessary for efficient nodulation of alfalfa by Rhizobium meliloti.

Microbial influence on gene-for-gene interactions in legume-Rhizobium symbioses