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Comparative Study
. 2019 Feb;5(2):e000254.
doi: 10.1099/mgen.0.000254. Epub 2019 Feb 19.

Transcriptomic Analysis of Rhizobium Leguminosarum Bacteroids in Determinate and Indeterminate Nodules

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Free PMC article
Comparative Study

Transcriptomic Analysis of Rhizobium Leguminosarum Bacteroids in Determinate and Indeterminate Nodules

R T Green et al. Microb Genom. .
Free PMC article

Abstract

Two common classes of nitrogen-fixing legume root nodules are those that have determinate or indeterminate meristems, as in Phaseolus bean and pea, respectively. In indeterminate nodules, rhizobia terminally differentiate into bacteroids with endoreduplicated genomes, whereas bacteroids from determinate nodules are less differentiated and can regrow. We used RNA sequencing to compare bacteroid gene expression in determinate and indeterminate nodules using two Rhizobium leguminosarum strains whose genomes differ due to replacement of the symbiosis (Sym) plasmid pRP2 (strain Rlp4292) with pRL1 (strain RlvA34), thereby switching symbiosis hosts from Phaseolus bean (determinate nodules) to pea (indeterminate nodules). Both bacteroid types have gene expression patterns typical of a stringent response, a stressful environment and catabolism of dicarboxylates, formate, amino acids and quaternary amines. Gene expression patterns were indicative that bean bacteroids were more limited for phosphate, sulphate and iron than pea bacteroids. Bean bacteroids had higher levels of expression of genes whose products are predicted to be associated with metabolite detoxification or export. Pea bacteroids had increased expression of genes associated with DNA replication, membrane synthesis and the TCA (tricarboxylic acid) cycle. Analysis of bacteroid-specific transporter genes was indicative of distinct differences in sugars and other compounds in the two nodule environments. Cell division genes were down-regulated in pea but not bean bacteroids, while DNA synthesis was increased in pea bacteroids. This is consistent with endoreduplication of pea bacteroids and their failure to regrow once nodules senesce.

Keywords: RNA- Seq; Rhizobium leguminosarum; bacteroids; determinate nodules; indeterminate nodules; transcriptomics.

Conflict of interest statement

The authors declare that there are no conflicts of interest.

Figures

Fig. 1.
Fig. 1.
Scale genetic maps of Sym plasmids pRP2 [Rlp4292, 433 genes (RHLp67647197)] and pRL1 [RlvA34, 223 genes (RHLv8000–8223)]. Genes are coloured according to differential expression in bean and pea bacteroids. Genes up-regulated >10-fold in bacteroids are red; >2-fold up-regulated, orange; between 2-fold up-regulated and 2-fold down-regulated, yellow; >2-fold down-regulated, light blue; >10-fold down-regulated, dark blue. Exploded regions show the names of genes discussed in the text. The prefix for each gene name is shown in brackets within each replicon and the numbers printed inside the outer ring indicate the gene (e.g. on pRP2: RHLp7097, nifB). Data for this figure is given in Tables S6 and S8.
Fig. 2.
Fig. 2.
Summary of Sym plasmid genes differentially regulated in bacteroids. Expression data of Sym plasmid genes of pRP2 (433 genes) in bean bacteroids are given in Table S6 and for those of pRL1 (223 genes) in pea bacteroids in Table S8. Data for genes that are common (>80 % id) to both pRP2 and pRL1 (45 genes) are given in Table S9.
Fig. 3.
Fig. 3.
Summary of genes on the shared genome differentially regulated in bacteroids. Genes up-regulated >5-fold in both bean and pea bacteroids (89 genes) are listed in Table S10. Genes up-regulated >5-fold in bean and <2-fold in pea bacteroids (150 genes) are listed in Table S13. Genes up-regulated >5-fold in pea and <2-fold in bean bacteroids (116 genes) are listed in Table S15. Genes down-regulated >5-fold in both bean and pea bacteroids (17 genes) are listed in Table S18. Genes down-regulated >5-fold in bean and >1-fold pea bacteroids (14 genes) are listed in Table S19. Genes down-regulated >5-fold in pea and >1-fold bean bacteroids (18 genes) are listed in Table S20.
Fig. 4.
Fig. 4.
Transporter systems whose genes are up-regulated in Rlp4292 and RlvA34 bacteroids. Common nodule-specific transporters (up-regulated >5-fold in nodules of both strains) are shown in black, those specific to bean (up-regulated >5-fold in bean bacteroids and <5-fold in pea bacteroids) are shown in purple and those specific to pea (up-regulated >5-fold in pea bacteroids and <5-fold in bean bacteroids) are shown in green. In addition to being up-regulated in bacteroids, all genes are also highly expressed (>200 000 reads). Data for this figure is given in Table S12.
Fig. 5.
Fig. 5.
TCA cycle and associated metabolic pathways. Enzymes whose genes are up-regulated >10-fold in RlvA34 pea bacteroids are shown in green. Data for this figure are given in Table S17.

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