The <i>Rhizobium</i> trap: root hair curling in root–nodule symbiosis

Kijne, Jan W.; Bakhuizen, R.; Brussel, A. A. N. Van; Cremers, H.C.J. Canter; Diaz, C. L.; Páter, Béla; Smit, Gerrit; Spaink, H. P.; Swart, S. H.; Wijffelman, C. A.; Lugtenberg, Ben

doi:10.1017/cbo9780511565243.015

Cited by 9 publications

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“…The infection thread is occupied by the bacteria, allowing their entry into the plant interior. Finally, the rhizobia are released from the infection thread into the plant cytoplasm, where they differentiate into nitrogenfixing bacteroids (7,8,24,30,54,63).…”

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Sinorhizobium meliloti SyrA Mediates the Transcriptional Regulation of Genes Involved in Lipopolysaccharide Sulfation and Exopolysaccharide Biosynthesis

Keating

2007

J Bacteriol

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Sinorhizobium meliloti is a gram-negative soil bacterium found either in free-living form or as a nitrogenfixing endosymbiont of leguminous plants such as Medicago sativa (alfalfa). S. meliloti synthesizes an unusual sulfate-modified form of lipopolysaccharide (LPS). A recent study reported the identification of a gene, lpsS, which encodes an LPS sulfotransferase activity in S. meliloti. Mutants bearing a disrupted version of lpsS exhibit an altered symbiosis, in that they elicit more nodules than wild type. However, under free-living conditions, the lpsS mutant displayed no change in LPS sulfation. These data suggest that the expression of lpsS is differentially regulated, such that it is transcriptionally repressed during free-living conditions but upregulated during symbiosis. Here, I show that the expression of lpsS is upregulated in strains that constitutively express the symbiotic regulator SyrA. SyrA is a small protein that lacks an apparent DNA binding domain and is predicted to be located in the cytoplasmic membrane yet is sufficient to upregulate lpsS transcription. Furthermore, SyrA can mediate the transcriptional upregulation of exo genes involved in the biosynthesis of the symbiotic exopolysaccharide succinoglycan. The SyrA-mediated transcriptional upregulation of lpsS and exo transcription is blocked in mutants harboring a mutation in chvI, which encodes the response regulator of a conserved two-component system. Thus, SyrA likely acts indirectly to promote transcriptional upregulation of lpsS and exo genes through a mechanism that requires the ExoS/ChvI twocomponent system.When nitrogen is limiting, leguminous plants enter into symbioses with members of the genera Rhizobium, Bradyrhizobium, Mesorhizobium, Azorhizobium, and Sinorhizobium (collectively called rhizobia) resulting in the formation of nodules. Within the nodule, differentiated cytoplasmic rhizobia called bacteroids reduce molecular dinitrogen to ammonia. Bacterial colonization of the nodule requires morphological alteration of epidermal cells called root hairs, resulting in the formation of a curled structure referred to as a shepherd's crook. Shepherd's crook formation is followed developmentally by the formation of an infection thread, a tubular ingrowth of the root hair that penetrates the plant. The infection thread is occupied by the bacteria, allowing their entry into the plant interior.

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Sinorhizobium meliloti SyrA Mediates the Transcriptional Regulation of Genes Involved in Lipopolysaccharide Sulfation and Exopolysaccharide Biosynthesis

Keating

2007

J Bacteriol

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“…The infection thread is occupied by rhizobia and penetrates into the root, allowing bacterial entry into the plant. The bacteria within the infection thread are then released into the plant cytoplasm where they develop into nitrogen-fixing bacteroids (3,4,16,20,32,43 …”

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Sinorhizobium meliloti Sulfotransferase That Modifies Lipopolysaccharide

Cronan

Keating

2004

J Bacteriol

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Sinorhizobium meliloti is a gram-negative soil bacterium found either in free-living form or as a nitrogenfixing endosymbiont of a plant structure called the nodule. Symbiosis between S. meliloti and its plant host alfalfa is dependent on bacterial transcription of nod genes, which encode the enzymes responsible for synthesis of Nod factor. S. meliloti Nod factor is a lipochitooligosaccharide that undergoes a sulfate modification essential for its biological activity. Sulfate also modifies the carbohydrate substituents of the bacterial cell surface, including lipopolysaccharide (LPS) and capsular polysaccharide (K-antigen) (R. A. Cedergren, J. Lee, K. L. Ross, and R. I. Hollingsworth, Biochemistry 34:4467-4477, 1995). We utilized the genomic sequence of S. meliloti to identify an open reading frame, SMc04267 (which we now propose to name lpsS), which encodes an LPS sulfotransferase activity. We expressed LpsS in Escherichia coli and demonstrated that the purified protein functions as an LPS sulfotransferase. Mutants lacking LpsS displayed an 89% reduction in LPS sulfotransferase activity in vitro. However, lpsS mutants retain approximately wild-type levels of sulfated LPS when assayed in vivo, indicating the presence of an additional LPS sulfotransferase activity(ies) in S. meliloti that can compensate for the loss of LpsS. The lpsS mutant did show reduced LPS sulfation, compared to that of the wild type, under conditions that promote nod gene expression, and it elicited a greater number of nodules than did the wild type during symbiosis with alfalfa. These results suggest that sulfation of cell surface polysaccharides and Nod factor may compete for a limiting pool of intracellular sulfate and that LpsS is required for optimal LPS sulfation under these conditions. Symbioses between leguminous plants and the genera Rhizobium, Bradyrhizobium, Mesorhizobium, Azorhizobium, and Sinorhizobium (collectively called rhizobia) result in the formation of a novel plant organ, referred to as the nodule. Within the nodule, differentiated intracellular forms of rhizobia called bacteroids reduce molecular dinitrogen to ammonia. To gain entry into the plant, the bacteria induce morphological alterations of epidermal cells called root hairs, eliciting the formation of a curled structure referred to as a shepherd's crook. Shepherd's crook formation is followed developmentally by the formation of a tubular ingrowth of the root hair, called an infection thread. The infection thread is occupied by rhizobia and penetrates into the root, allowing bacterial entry into the plant. The bacteria within the infection thread are then released into the plant cytoplasm where they develop into nitrogen-fixing bacteroids (3,4,16,20,32,43

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“…scribed 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. scribed 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.…”

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confidence: 99%