Regulators and regulation of legume root nodule development.

Nitrogen is the nutrient plants require in the highest amount, and in agriculture nitrogen availability has a major influence on both yield and product quality. In nature plants acquire nitrogen by assimilation of nitrate and ammonium or from dinitrogen through association with nitrogen-fixing bacteria. Symbiotic nitrogen fixation, where the plant supplies the carbon source for the energy-dependent reduction of dinitrogen and protects the oxygen-sensitive nitrogenase enzyme, is among the most effective fixation systems. To establish a symbiosis, the bacterial microsymbionts gain access to single plant cells and install themselves in compartments surrounded by a plant membrane. In Gunnera sp. the cyanobacterium Nostoc sp. invades pre-existing stem glands and forms nitrogen-fixing heterocysts in infected cells. In most other symbiotic interactions, a specialized plant organ, the root nodule, is developed to provide optimal conditions for the nitrogen-fixing bacteria. Among woody plant species belonging to eight different families, an interaction with the gram-positive genus Frankia leads to the development of actinorhizal root nodules. In legumes, gram-negative soil bacteria belonging to the family Rhizobiaceae (here collectively called Rhizobium) infect root tissue and induce the formation of the nitrogen fixing nodules. Why certain plants are able to develop root nodules is unclear, but recent phylogenetic studies based on DNA sequence analysis place all plants involved in rhizobial or actinorhizal symbiosis in the same lineage and suggest that the predisposition for nodulation evolved only once (Soltis et al., 1995; Doyle, 1998). The relationship between Rhizobium and legume plants is selective. Individual species of rhizobia have a distinct host range allowing nodulation of a particular set of legume plants. For example, Rhizobium leguminosarum bv viciae nodulates pea and vetch, whereas Bradyrhizobium japonicum nodulates soybean. At the other extreme, the exceptionally broad host-range Rhizobium sp. NGR234 nodulates 353 legume species representing 122 genera (Pueppke and Broughton, 1999). Differences in both infection processes and organogenic programs are reflected in variations in root nodule morphology (Doyle, 1998), but overall there are pronounced developmental similarities as would be expected from a common ancestry. To cover most aspects of this unusual plant-prokaryote symbiosis, the study of nodulation is a multifaceted research area aiming to understand this plant-microbe interaction in a framework of physiological and developmental processes underlying infection and organogenesis. With this perspective, this Update draws on observations from different Rhizobium-legume interactions. The following sections focus on plant control of root nodule organ formation and sketch the way plant genetics and functional genomics are changing our thinking. The early signal exchange as well as the biosynthesis and properties of the bacterial Nod factor signal molecules have been reviewed extensively (Dénarié et al., 1996; Spaink, 1996; Downie and Walker, 1999, and refs. therein) and will be presented only briefly.