Signals in Root Nodule Organogenesis and Endocytosis of Rhizobium.

The rhizobia comprise a diverse group of organisms that elicit hypertrophic growth on the roots of legume plants to form a new organ, the root nodule, which they inhabit to fix nitrogen. This endosymbiotic association makes legume plants autotrophic for external nitrogen, an essential nutrient for plant growth. Because the interaction with rhizobia is highly beneficial, legume plants have evolved a set of genes encoding nodulekpecific proteins (nodulins; Legocki and Verma, 1980); expression of these genes is required for the development and function of root nodules. A cascade of events controlling the expression of these genes allows for the development of infection, nodule organogenesis, the release of rhizobia from the infection thread, and the establishment of a symbiotic state. Although the root nodule structure can develop without bacteria1 infection (see below), infection and organogenesis normally proceed simultaneously. Furthermore, neither nodule organogenesis nor endocytosis of rhizobia depends on the ability of the bacteria to fix nitrogen. lntensive study over the past two decades has led to an understanding of many of the molecular events in early plant-Rhizobium communication leading to nodule organogenesis. It is now clear that nodule development is under the control of specific nodulation (nod) signal(s) produced by rhizobia in response to the host, although hypertrophic growth can also occur autonomously on roots of certain legumes (Truchet et al., 1989; CaetanoAnolles and Gresshoff, 1991). Nod signals have recently been purified from severa1 rhizobia, and their structures have been determined (see below); these may allow elucidation of the molecular basis for host specificity. The application of purified nod factors triggers nodule ontogeny, and these signals can be modified chemically or by mutagenesis of bacteria, providing an excellent system to study the development of this plant organ. Because generation of the nodule requires new cell division in root cortical cells, nod factors may control events leading to the initiation and/or regulation of cell division. Uncoupling of nodule organogenesis from endocytosis of bacteria may allow identification of the signal(s) that operate once the nodule developmental program is triggered. Understanding the signal transduction pathways that control the expression of host genes required for the initiation of nodule primordia may reveal how the development of a plant organ can be regulated by interna1 or external factors and how bacteria have acquired the ability to trigger this organogenesis program. Meristems are generally refractive to bacterial infection; however, rhizobia invade the newly divided cells of the nodule primordium. lnvasion of legume roots occurs through a highly orchestrated infection process that does not provoke host defense reactions, and the bacteria are released via the infection thread into the “target cell.” Little is known about the endocytosis of bacteria in plant cells, the nature of the subcellular compartment that harbors the bacteria, and the biogenesis of this compartment. The formation of such a compartment is essential to all endosymbioses; the failure to form this compartment may evoke pathogenic responses in the host. Rhizobium has evolved a mechanism to counter the host defense response (Verma and Nadler, 1984), but it elicits a pathogenic response in certain ineffective conditions (werner et al., 1985; Djordjevic et al., 1987). Current interest in extending symbiosis to other crop plants requires understanding of host specificity, organogenesis of nodule structure, invasion and endocytosis of bacteria, and formation of a new subcellular compartment able to sustain a foreign organism endosymbiotically. Some of the key issues yet to be understood in our efforts to uncover molecular events in the control of nodule development and endocytosis of rhizobia are discussed here.