Symbiotic Nitrogen Fixation.

Biosphere nitrogen is subjected to rapid turnover, and because it is eventually lost as nitrogen into the atmosphere, its maintenance requires continuous replenishment with reduced nitrogen from atmospheric nitrogen. Biological reduction of nitrogen to ammonia can be performed only by some prokaryotes and is a highly oxygen-sensitive process. The most efficient nitrogen fixers establish a symbiosis with higher plants in which the energy for nitrogen fixation and, in general, the oxygen protection system are provided by the plant partner. In two groups of symbiotic interactions, the prokaryotic partners are soil bacteria (rhizobia in legume symbioses and Frankia bacteria in actinorhizal symbioses), whereas in the case of symbiosis of Gunnera, nitrogen is fixed by the cyanobacterium Nostoc. In Gunnera, the symbionts reside in already existing stem glands, whereas in legumes and actinorhizal plants, new organs, the root nodules, are formed by the plant upon infection with the symbiont. In all three systems, the prokaryotes fix nitrogen inside the cells of their host, but they are separated from the plant cytoplasm by membranes derived from the plant plasmalemma (Figure 1). Because research on legume symbiosis is the most advanced of these three symbiotic systems, in this article we concentrate mainly on this system. The interaction of rhizobia and legumes begins with signal exchange and recognition of the symbiotic partners, followed by attachment of the rhizobia to the plant root hairs. The root hair deforms, and the bacteria invade the plant by a newly formed infection thread growing through it. Simultaneously, cortical cells are mitotically activated, giving rise to the nodule primordium. lnfection threads grow toward the primordium, and the bacteria are then released into the cytoplasm of the host cells, surrounded by a plantderived peribacteroid membrane (PBM). The nodule primordium thereupon develops into a mature nodule, while the bacteria differentiate into their endosymbiotic form, which is known as the bacteroid (Figure 1A). Bacteroids, together with the surrounding PBMs, are called symbiosomes. At this stage, bacteria synthesize nitrogenase, which catalyzes the reduction of nitrogen. The product of nitrogen fixation, ammonia, is then exported to the plant. All of the steps of nodule development involve the expression of nodule-specific plant genes, the socalled nodulin genes (van Kammen, 1984). The early nodulin genes encode products