Terminal bacteroid differentiation in the<i>Medicago–Rhizobium</i>interaction – a tug of war between plant and bacteria

Haag, Andreas F.; Mergaert, Peter

doi:10.1002/9781119409144.ch75

Cited by 8 publications

(4 citation statements)

References 115 publications

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“…Within nodules of legumes of the inverted-repeat lacking clade (IRLC) and Dalbergioid clade, rhizobia undergo a process called terminal bacteroid differentiation (TBD) prior to fixing nitrogen (4,5) This involves bacterial cell enlargement, genome endoreduplication, increased membrane permeability, and major changes in gene expression and cellular metabolism (6)(7)(8). TBD is essential for SNF in these legumes and is driven by a family of small, plant-encoded proteins known as nodulespecific cysteine-rich (NCR) peptides, which target the intracellular symbiotic bacteria to promote TBD (9,10).…”

Section: Introductionmentioning

confidence: 99%

Taxonomic distribution of SbmA/BacA and BacA-like antimicrobial peptide transporters suggests independent recruitment and convergent evolution in host-microbe interactions

Smith,

Boukherissa,

Antaya

et al. 2024

Preprint

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Small, antimicrobial peptides are often produced by eukaryotes to control bacterial populations in both pathogenic and mutualistic symbioses. These include proline-rich mammalian immune peptides and cysteine-rich peptides produced by legume plants in symbiosis with rhizobia. The fitness of the bacterial partner is dependent upon their ability to persist in the presence of these antimicrobial peptides. In the case ofEscherichia coliandMycobacterium tuberculosispathogens and nitrogen-fixing legume symbionts (rhizobia), the ability to survive exposure to these peptides depends on peptide transporters called SbmA (also known as BacA) or BclA (for BacA-like). However, how broadly these transporters are distributed amongst bacteria, and their evolutionary history, is poorly understood. Here, we used hidden Markov models, phylogenetic analysis, and sequence similarity networks to examine the distribution of SbmA/BacA and BclA proteins across a representative set of 1,255 species from across the domainBacteria. We identified a total of 71 and 177 SbmA/BacA and BclA proteins, respectively. Phylogenetic and sequence similarity analyses suggest that these protein families likely did not evolve from a common ancestor and that their functional similarity is instead a result of convergent evolution.In vitrosensitivity assays using the legume peptide NCR247 and several of the newly-identified BclA proteins confirmed that transport of antimicrobial peptides is a common feature of this protein family. Analysis of the taxonomic distribution of these proteins showed that SbmA/BacA orthologs were encoded only by species in the phylumPseudomonadotaand that they were primarily identified in just two orders:Hyphomicrobiales(classAlphaproteobacteria) andEnterobacterales(classGammaproteobacteria). BclA orthologs were somewhat more broadly distributed and were found in clusters across four phyla. These included several orders of the phylaPseudomonadotaandCyanobacteriota, as well as the orderMycobacteriales(phylumActinomycetota) and the classNegativicutes(phylumBacillota). Notably, many of the clades enriched for species encoding BacA or BclA orthologs also include many species known to interact with eukaryotic hosts in mutualistic or pathogenic interactions. Collectively, these observations suggest that SbmA/BacA and BclA proteins have been repeatedly co-opted to facilitate both mutualistic and pathogenic associations with eukaryotic hosts by allowing bacteria to cope with host-encoded antimicrobial peptides.

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Section: Introductionmentioning

confidence: 99%

Taxonomic distribution of SbmA/BacA and BacA-like antimicrobial peptide transporters suggests independent recruitment and convergent evolution in host-microbe interactions

Smith,

Boukherissa,

Antaya

et al. 2024

Preprint

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“…In some legumes, such as those belonging to the Inverted Repeat Lacking Clade (IRLC), the rhizobia undergo an irreversible hostinduced process known as terminal differentiation that is largely driven by a unique class of legume proteins known as nodule-specific cysteine-rich (NCR) peptides (Van de Velde et al, 2010). Terminal differentiation involves cell enlargement, genome endoreplication, and increased membrane permeability and is thought to increase the efficiency of N 2 -fixation (Haag & Mergaert, 2019;Lamouche et al, 2019;Mergaert et al, 2006). Not all rhizobium/legume pairings are compatible (Pueppke & Broughton, 1999;Wilson, 1939).…”

Section: Introductionmentioning

confidence: 99%

Reference nodule transcriptomes for Melilotus officinalis and Medicago sativa cv. Algonquin

2022

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Host/symbiont compatibility is a hallmark of the symbiotic nitrogen-fixing interaction between rhizobia and legumes, mediated in part by plant-produced nodule-specific cysteine-rich (NCR) peptides and the bacterial BacA membrane protein that can act as a NCR peptide transporter. In addition, the genetic and metabolic properties supporting symbiotic nitrogen fixation often differ between compatible partners, including those sharing a common partner, highlighting the need for multiple study systems. Here, we report high-quality nodule transcriptome assemblies for Medicago sativa cv. Algonquin and Melilotus officinalis, two legumes able to form compatible symbioses with Sinorhizobium meliloti. The compressed M. sativa and M. officinalis assemblies consisted of 79,978 and 64,593 contigs, respectively, of which 33,341 and 28,278 were assigned putative annotations, respectively. As expected, the two transcriptomes showed broad similarity at a global level. We were particularly interested in the NCR peptide profiles of these plants, as these peptides drive bacterial differentiation during the symbiosis. A total of 412 and 308 NCR peptides were predicted from the M. sativa and M. officinalis transcriptomes, respectively, with approximately 9% of the transcriptome of both species consisting of NCR transcripts.Notably, transcripts encoding highly cationic NCR peptides (isoelectric point > 9.5), which are known to have antimicrobial properties, were $2-fold more abundant in M. sativa than in M. officinalis, and $27-fold more abundant when considering only NCR peptides in the six-cysteine class. We hypothesize that the difference in abundance of highly cationic NCR peptides explains our previous observation that some rhizobial bacA alleles which can support symbiosis with M. officinalis are unable to support symbiosis with M. sativa.

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“…In some legumes, such as those belonging to the Inverted Repeat Lacking Clade (IRLC), the rhizobia undergo an irreversible host-induced process known as terminal differentiation that is largely driven by a unique class of legume proteins known as nodule-specific cysteine-rich (NCR) peptides (3). Terminal differentiation involves cell enlargement, genome endoreplication, and increased membrane permeability, and is thought to increase the efficiency of N2-fixation (4)(5)(6). Not all rhizobium/legume pairings are compatible (7,8).…”

Section: Introductionmentioning

confidence: 99%

Reference nodule transcriptomes for Melilotus officinalis and Medicago sativa cv. Algonquin

Huang

Snedden

diCenzo

2022

Preprint

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Host/symbiont compatibility is a hallmark of the symbiotic nitrogen-fixing interaction between rhizobia and legumes, mediated in part by plant produced nodule-specific cysteine-rich (NCR) peptides and the bacterial BacA membrane protein that can act as a NCR peptide transporter. In addition, the genetic and metabolic properties supporting symbiotic nitrogen fixation often differ between compatible partners, including those sharing a common partner, highlighting the need for multiple study systems. Here, we report high quality nodule transcriptome assemblies for Medicago sativa cv. Algonquin and Melilotus officinalis, two legumes able to form compatible symbioses with Sinorhizobium meliloti. The compressed M. sativa and M. officinalis assemblies consisted of 79,978 and 64,593 contigs, respectively, of which 33,341 and 28,278 were assigned putative annotations, respectively. As expected, the two transcriptomes showed broad similarity at a global level. We were particularly interested in the NCR peptide profiles of these plants, as these peptides drive bacterial differentiation during the symbiosis. A total of 412 and 308 NCR peptides were predicted from the M. sativa and M. officinalis transcriptomes, respectively, with approximately 9% of the transcriptome of both species consisting of NCR transcripts. Notably, transcripts encoding highly-cationic NCR peptides (isoelectric point > 9.5), which are known to have antimicrobial properties, were ~2-fold more abundant in M. sativa than in M. officinalis, and ~27-fold more abundant when considering only NCR peptides in the six-cysteine class. We hypothesize that the difference in abundance of highly-cationic NCR peptides explains our previous observation that some rhizobial bacA alleles which can support symbiosis with M. officinalis are unable to support symbiosis with M. sativa.

show abstract

Terminal bacteroid differentiation in theMedicago–Rhizobiuminteraction – a tug of war between plant and bacteria

Cited by 8 publications

References 115 publications

Taxonomic distribution of SbmA/BacA and BacA-like antimicrobial peptide transporters suggests independent recruitment and convergent evolution in host-microbe interactions

Taxonomic distribution of SbmA/BacA and BacA-like antimicrobial peptide transporters suggests independent recruitment and convergent evolution in host-microbe interactions

Reference nodule transcriptomes for Melilotus officinalis and Medicago sativa cv. Algonquin

Reference nodule transcriptomes for Melilotus officinalis and Medicago sativa cv. Algonquin

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