The Rhizobium-legume symbiosis involves the formation of a novel plant organ, the nodule, in which intracellular bacteria reduce molecular dinitrogen in exchange for plant photosynthates. Nodule development requires a bacterial signal referred to as Nod factor, which in Sinorhizobium meliloti is a -(1,4)-linked tetramer of N-acetylglucosamine containing N-acyl and O-acetyl modifications at the nonreducing end and a critical 6-O-sulfate at the reducing end. This sulfate modification requires the action of three gene products: nodH, which catalyzes the sulfonyl transfer, and nodPQ, which produce the activated form of sulfate, 3-phosphoadenosine-5-phosphosulfate. It was previously reported that S. meliloti cell surface polysaccharides are also covalently modified by sulfate in a reaction dependent on NodPQ. We have further characterized this unique form of bacterial carbohydrate modification. Our studies have determined that one of the nodPQ mutant strains used in the initial study of sulfation of cell surface harbored a second unlinked mutation. We cloned the gene affected by this mutation (referred to as lps-212) and found it to be an allele of lpsL, a gene previously predicted to encode a UDP-glucuronic acid epimerase. We demonstrated that lpsL encoded a UDP-glucuronic acid epimerase activity that was reduced in the lps-212 mutant. The lps-212 mutation resulted in an altered lipopolysaccharide structure that was reduced in sulfate modification in vitro and in vivo. Finally, we determined that the lps-212 mutation resulted in a reduced ability to elicit the formation of plant nodules and by altered infection thread structures that aborted prematurely.In order to acquire reduced nitrogen, many leguminous plants enter into symbiotic associations with bacteria, culminating in the formation of a novel plant organ, the nodule, in which intracellular bacteria reduce molecular dinitrogen to ammonia. In a compatible symbiotic interaction, the bacteria trigger an alteration in the growth of the plant root hairs, resulting in a curled structure that entraps a microcolony of the bacteria. This curled root hair is the site for a plant cell wallencapsulated ingrowth of the root hair, referred to as an infection thread. The infection thread, filled with proliferating bacteria, extends to the base of the root hair cell and then penetrates the root, allowing bacterial entry into the plant. Concurrent with the development of the infection thread, the cells in the root cortex dedifferentiate, leading to new cell division and the consequent formation of the nodule. The infection thread branches and penetrates the developing nodule, delivering the bacteria, which are then released into the plant cytoplasm. These intracellular bacteria undergo a series of developmental changes and signal transduction events to induce the expression of nitrogenase, which catalyzes the reduction of molecular dinitrogen to ammonia (4,5,18,20,31,41).Symbiotic nitrogen-fixing relationships between legumes and the genera Rhizobium, Bradyrhizobium, Mesorhi...