Rhizobium symbiosis: nod factors in perspective.

Rhizobium and its allies (Azorhizobium, Bradyrhizobium, and Sinorhizobium) are Gram-negative bacteria that cause the development of root (and sometimes stem) nodules on plant hosts, which the bacteria inhabit as nitrogen-fixing endosymbionts. The early stages of this process, including gene expression in the bacterium and cell growth, division, and differentiation in the host, are mediated by signal exchange between the eukaryotic host and the prokaryotic symbiont (Figure l A , left). The plant produces a signal, usually aflavonoid, that induces gene expression in the bacterium; the bacterium subsequently synthesizes a signal that triggers early nodule development on the plant. The developmental time line for nodulation has been described in several reviews and essays (Sprent, 1989; Truchet et al., 1989; Brewin, 1991; Brewin et al., 1992; Hirsch, 1992; Kijne et al., 1992; Ridge, 1992; Vijn et al., 1993) and is only considered briefly here. Nodules can take on several patterns during development, the form of the nodule being determined by the plant, not the bacterium. One major form is the indeterminate (also called meristematic or cylindrical) type, which develops on alfalfa, clover, and pea roots. A second major type is the spherical or determinate nodule, which is formed by soybean, Phaseolus, and Lofus. A comparison of these symbiotic nodules with those of nonlegumes is presented elsewhere in this issue (see Pawlowski and Bisseling, 1996). The twin hallmarks of early nodulation are its developmental complexity and its specificity. The developmental process in the plant involves architectural changes at the cell and organ levels (for example, root hair morphogenesis, cortical cell enlargement, and vascular patterning) as well as interna1 cellular differentiation that includes cytoplasmic activation, cell division, and new gene expression. Structural and developmental studies of nodule formation remain an important part of the overall Rhizobium research picture. Indeed, new views of infection thread formation, cell wall modifications, and intracellular rearrangements in root hairs and elsewhere have recently appeared (Kijne et al., 1992; van Brussel et al., 1992; van Spronsen et al., 1994; DeBoer and Djordjevic, 1995; Ridge, 1995). The exciting tools of video microscopy and image analysis are making it possible to obtain dynamic views of early plant reactions to Rhizobium signals (Allen et al., 1994; Sanchez et al., 1996). Thus, in addition to its inherent interest as a model for understanding plant-microbe interactions, the specificity and timing of early nodulation events make the Rhizobium-plant symbiosis an attractive model system for general plant cell biology studies. The specificity of nodulation is likewise remarkable: with one known exception, the Rhizobium nodulation habit is restricted to a single plant taxon, the Fabaceae, or legume family. Within this family, individual species, strains, or biovars of bacteria nodulate a restricted set of host plants that are usually but not always related. The signal model (Figure 1) provides an explanation for the species-leve1 pattern of host specificity. But we cannot yet answer the larger mechanistic and evolutionary question: Why only legumes? Because a short review cannot catalog complete lists of referentes, even recent ones, the focus of this article is to put selected papers in context: Why is it important for plant biologists to be concerned with bacterial genes, their regulation, and activities? Where do the questions lie in the study of the plant response? What new genetic and cellular methods are needed for their resolution?