Plant genetic suppression of the non-nodulation phenotype of Rhizobium meliloti host-range nodH mutants: gene-for-gene interaction in the alfalfa-Rhizobium symbiosis?

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Abstract
Rhizobium nodulation genes can produce active extracellular signals for legume nodulation. The R. meliloti host-range nodH gene has been postulated to mediate the transfer of a sulfate to a modified lipo-oligosaccharide, which in its sulfated form is a specific nodulation factor for alfalfa (Medicago sativa L.). We found that alfalfa was capable of effective nodulation with signal-defective and non-nodulating nodH mutants (Nnr) defining a novel gene-for-gene interaction that conditions nodulation. Bacteria-free nodules that formed spontaneously at about a 3–5% rate in unselected seed populations of alfalfa cv ‘Vernal’ in the total absence of Rhizobium (Nar) exhibited all the histological, regulatory and ontogenetic characteristics of alfalfa nodules. Inoculation of such populations with nodH mutants, but not with nodA or nodC mutants, produced a four- to five-fold increase in the percentage of nodulated plants. Some 10–25% of these nodulated plants formed normal pink nitrogen-fixing nodules instead of white empty nodules. About 70% of the S1 progeny of such Nnr+ plants retained the parental phenotype; these plants were also able to form nodules in the absence of Rhizobium. If selected Nar+ plants were self-pollinated almost the entire progeny exhibited the parental Nar+ phenotype. Segregation analysis of S1 and S2 progeny from selected Nar+ plants suggests that the Nar character is monogenic dominant and that the nodulation phenotype is controlled by a gene dose effect. The inoculation of different S1 Nar+ progeny with nodH mutant bacteria gave only empty non-fixing nodules. Our results indicate that certain alfalfa genotypes can be selected for suppression of the non-nodulation phenotype of nodH mutants. The fact that the Nnr plant phenotype behaved as a dominant genetic trait and that it directly correlated with the ability of the selected plants to form nodules in the absence of Rhizobium suggests that the interaction of plant and bacterial alleles occurs early during signal transduction through the alteration of a signal reception component of the plant so that it responds to putative signal precursors.