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Discovery of a rhizobial RNA that is essential for symbiotic root nodule development.

ABSTRACT: All of the Azorhizobium, Bradyrhizobium, and Rhizobium genes known to be involved in the development of nitrogen-fixing legume root nodules are genes that code for proteins. Here we report the first exception to this rule: the sra gene; it was discovered during the genetic analysis of a Bradyrhizobium japonicum Tn5 mutant (strain 259) which had a severe deficiency in colonizing soybean nodules. A DNA region as small as 0.56 kb cloned from the parental wild type restored a wild-type phenotype in strain 259 by genetic complementation. The sra gene was located on this fragment, sequenced, and shown to be transcribed into a 213-nucleotide RNA. Results obtained with critical point mutations in the sra gene proved that the transcript was not translated into protein; rather, it appeared to function as an RNA molecule with a certain stem-and-loop secondary structure. We also detected an sra homolog in Rhizobium meliloti which, when cloned and transferred to B. japonicum mutant 259, fully restored symbiotic effectiveness in that strain. We propose several alternative functions for the sra gene product, of which that as a regulatory RNA for gene expression may be the most probable one.

SUBMITTER: Ebeling S

PROVIDER: S-EPMC208969 | biostudies-other | 1991 Oct

REPOSITORIES: biostudies-other

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Discovery of a rhizobial RNA that is essential for symbiotic root nodule development.

Ebeling S S Kündig C C Hennecke H H

Journal of bacteriology 19911001 20

All of the Azorhizobium, Bradyrhizobium, and Rhizobium genes known to be involved in the development of nitrogen-fixing legume root nodules are genes that code for proteins. Here we report the first exception to this rule: the sra gene; it was discovered during the genetic analysis of a Bradyrhizobium japonicum Tn5 mutant (strain 259) which had a severe deficiency in colonizing soybean nodules. A DNA region as small as 0.56 kb cloned from the parental wild type restored a wild-type phenotype in ...[more]

PMID: 1717438

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Project description:Soybean root nodules are known to contain a high diversity of both rhizobial endophytes and nonrhizobial endophytes (NREs). Nevertheless, the variation of these bacteria among different root nodules within single plants has not been reported. So far, it is unclear whether the selection of NREs among different root nodules within single plants is a random process or is strictly controlled by the host plant to favor a few specific NREs based on their beneficial influence on plant growth. As well, it is also unknown if the relative frequency of NREs within different root nodules is consistent or if it varies based on the location or size of a root nodule. We assessed the microbiomes of 193 individual soybean root nodules from nine plants using high-throughput DNA sequencing. Bradyrhizobium japonicum strains occurred in high abundance in all root nodules despite the presence of other soybean-compatible rhizobia, such as Ensifer, Mesorhizobium, and other species of Bradyrhizobium in soil. Nitrobacter and Tardiphaga were the two nonrhizobial genera that were uniformly detected within almost all root nodules, though they were in low abundance. DNA sequences related to other NREs that have frequently been reported, such as Bacillus, Pseudomonas, Flavobacterium, and Variovorax species, were detected in a few nodules. Unlike for Bradyrhizobium, the low abundance and inconsistent occurrence of previously reported NREs among different root nodules within single plants suggest that these microbes are not preferentially selected as endophytes by host plants and most likely play a limited part in plant growth as endophytes.IMPORTANCE Soybean (Glycine max L.) is a valuable food crop that also contributes significantly to soil nitrogen by developing a symbiotic association with nitrogen-fixing rhizobia. Bacterial endophytes (both rhizobial and nonrhizobial) are considered critical for the growth and resilience of the legume host. In the past, several studies have suggested that the selection of bacterial endophytes within root nodules can be influenced by factors such as soil pH, nutrient availability, host plant genotype, and bacterial diversity in soil. However, the influence of size or location of root nodules on the selection of bacterial endophytes within soybean roots is unknown. It is also unclear whether the selection of nonrhizobial endophytes within different root nodules of a single plant is a random process or is strictly regulated by the host. This information can be useful in identifying potential bacterial species for developing bioinoculants that can enhance plant growth and soil nitrogen.

Project description:The interactions of legumes with symbiotic nitrogen-fixing bacteria cause the formation of specialized lateral root organs called root nodules. It has been postulated that this root nodule symbiosis system has recruited factors that act in early signaling pathways (common SYM genes) partly from the ancestral mycorrhizal symbiosis. However, the origins of factors needed for root nodule organogenesis are largely unknown. NODULE INCEPTION (NIN) is a nodulation-specific gene that encodes a putative transcription factor and acts downstream of the common SYM genes. Here, we identified two Nuclear Factor-Y (NF-Y) subunit genes, LjNF-YA1 and LjNF-YB1, as transcriptional targets of NIN in Lotus japonicus. These genes are expressed in root nodule primordia and their translational products interact in plant cells, indicating that they form an NF-Y complex in root nodule primordia. The knockdown of LjNF-YA1 inhibited root nodule organogenesis, as did the loss of function of NIN. Furthermore, we found that NIN overexpression induced root nodule primordium-like structures that originated from cortical cells in the absence of bacterial symbionts. Thus, NIN is a crucial factor responsible for initiating nodulation-specific symbiotic processes. In addition, ectopic expression of either NIN or the NF-Y subunit genes caused abnormal cell division during lateral root development. This indicated that the Lotus NF-Y subunits can function to stimulate cell division. Thus, transcriptional regulation by NIN, including the activation of the NF-Y subunit genes, induces cortical cell division, which is an initial step in root nodule organogenesis. Unlike the legume-specific NIN protein, NF-Y is a major CCAAT box binding protein complex that is widespread among eukaryotes. We propose that the evolution of root nodules in legume plants was associated with changes in the function of NIN. NIN has acquired functions that allow it to divert pathways involved in the regulation of cell division to root nodule organogenesis.

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Discovery of a rhizobial RNA that is essential for symbiotic root nodule development.

Publications

Discovery of a rhizobial RNA that is essential for symbiotic root nodule development.

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