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Pervent, M.

Publications and source records attributed to Pervent, M..

7 recordsLinked to original sources

The free-living wellspring of symbiotic nitrogen fixation in Bradyrhizobium

The evolutionary origin of nitrogen-fixing symbiosis has been a long-standing question. To address this, we focused on Bradyrhizobium, a globally abundant bacterial genus that includes classic symbiotic lineages, which rely on the common Nod factor signaling pathway to form nodules, and close relatives capable of fixing nitrogen in a free-living state. We isolated 88 strains carrying the key genes for nitrogen fixation (nif) from non-legume environments and analyzed them alongside 586 public Bradyrhizobium genomes harboring these genes to reconstruct a robust phylogeny of nif genes. Analysis reveals that the earliest-diverging nif lineages are members capable of free-living nitrogen fixation, establishing this as the ancestral state. The Nod factor-dependent symbiotic lineages are polyphyletic, demonstrating at least three independent origins via horizontal acquisition of symbiosis islands. This evolutionary history is reflected in a genomic dichotomy: lineages capable of free-living nitrogen fixation possess a conserved nif island architecture that consistently includes the oxygen-protective gene glbO, whereas the symbiotic nif-associated regions are highly variable and universally lack glbO. Using both loss-of-function and gain-of-function genetic approaches, we show that glbO contributes significantly to nitrogenase activity under free-living conditions, whereas it is dispensable within the protected nodule environment. This work establishes a new framework for the evolution of symbiosis, identifying free-living ancestors as the source from which nitrogen-fixing symbiosis repeatedly and independently evolved in Bradyrhizobium. SignificanceFor over a century, nitrogen-fixing bacteria called rhizobia have been celebrated for their symbiotic partnership with legumes like soybeans and peas. This study overturns the view that this symbiotic lifestyle was the original, advanced state. By discovering and analyzing diverse Bradyrhizobium bacteria from ordinary soils and non-legume plants, we show that the ancestor was capable of free-living nitrogen fixation. Root nodule nitrogen fixation evolved multiple independent times from free-living ancestors. We identify glbO, an oxygen-protective gene located immediately next to the nitrogen fixing genes, as critical for nitrogen fixation in variable soil conditions but dispensable and lost in Bradyrhizobium specialized inside nodules. This repositions free-living Bradyrhizobium as a major potential nitrogen source beyond legumes, with promise for sustainable agriculture.

microbiology↗

A novel pathosystem between Aeschynomene evenia and Aphanomyces euteiches reveals new immune components in quantitative legume root-rot resistance.

Legumes are pivotal for sustainable agriculture, yet their productivity is hindered by soilborne pathogens such as Aphanomyces euteiches. This study introduces Aeschynomene evenia as a novel model to investigate legume immunity and its interplay with Nod factor-independent symbiosis (NFIS). Inoculation of A. evenia accessions with A. euteiches strains revealed a range of quantitative resistance levels. Phenotypic and cytological analyses showed a compatible interaction, including root browning, intracellular colonisation, and oospore production; along with partial resistance traits such as phenolic accumulation at the endodermal barrier. Transcriptomic analyses at 1 and 3 dpi identified 3,403 differentially expressed genes (DEGs), with upregulated genes associated with pathogen perception, immune signalling and specialised metabolite biosynthesis. Kinase-mediated signalling, ROS homeostasis, and WRKY transcription factors were among the most enriched functional categories. Comparative transcriptomics with Medicago truncatula confirmed conserved immune responses, while A. evenia displayed broader transcriptional repression. Integration with symbiotic transcriptomic data revealed overlapping gene signatures, including AeRLCK2 and AeCRK, previously found to be NFIS-specific, as putative dual-function kinases. Aerlck2 and Aecrk mutants exhibited enhanced resistance to A. euteiches, supporting their roles in immune regulation. This work positions A. evenia-A. euteiches as a valuable system to dissect legume quantitative resistance and its intersection with symbiosis.

plant biology↗

A Receptor Like Cytoplasmic Kinase evolved in Aeschynomene legumes to mediate Nod-independent rhizobial symbiosis

Many plants interact symbiotically with arbuscular mycorrhizal (AM) fungi to enhance inorganic phosphorus uptake, and legumes also develop a nodule symbiosis with rhizobia for nitrogen acquisition. Establishment and functioning of both symbioses rely on a common plant signaling pathway activated by structurally related Myc- and Nod-factors. Recently, a SPARK Receptor-like-Kinase (RLK)/Receptor-like Cytoplasmic Kinase (RLCK) complex was shown to be essential for AM in both monocot and dicot plants. Here, we show that in Aeschynomene legumes the RLCK component of this receptor complex has evolved following a gene duplication event and mediates a unique nodule symbiosis that is independent of rhizobial Nod factors. In Aeschynomene evenia, AeRLCK2 is crucial for nodule initiation but not for AM. Additionally, AeRLCK2 physically interacts with and is phosphorylated by the Cysteine-rich RLK, AeCRK, also required for nodulation. This work reveals a novel evolutionary origin of this Nod-independent symbiosis from AM.

plant biology↗

Stem nodulation: diversity and occurrence in Aeschynomene and Sesbania legumes from wetlands of Madagascar

As an adaptation to flooding, few legume species have the original ability to develop nitrogen-fixing nodules on the stem. By surveying wetlands of Madagascar, we found a large occurrence and diversity of stem nodulation in Aeschynomene and Sesbania legumes. They represent opportunities to investigate different modalities of the nitrogen-fixing symbiosis in legumes.

plant biology↗

ORM-mediated regulation of sphingolipid biosynthesis is essential for nodule formation in Aeschynomene evenia

Legumes are able to establish symbiotic interactions with nitrogen-fixing rhizobia that are accomodated in root-derived organs, the nodules. Rhizobia recognition triggers a plant symbiotic signalling pathway activating two coordinated processes: infection and nodule organogenesis. How these are orchestrated in legumes species utilizing intercellular infection and lateral root-base nodulation remain elusive. Here, we show that Aeschynomene evenia OROSOMUCOID PROTEIN 1 (AeORM1), a key regulator of sphingolipid biosynthesis, is required for nodule formation in this legume species. Using A. evenia orm1 mutants, we demonstrate that alterations in AeORM1 function result in numerous early aborted nodules, exhibiting defense-like reactions, and shortened lateral roots. Consistantly, AeORM1 was expressed during lateral root initiation and elongation, including at lateral root bases where nodule primordia form in the presence of symbiotic bradyrhizobia. Sphingolipidomics revealed that mutations in AeORM1 leaded to sphingolipid overaccumulation in roots, in particular the very-long-chain-fatty-acid (VLCFA)-containing ceramids relative to the wild-type plants. Taken together, our findings reveal that AeORM1-regulated sphingolipid homeostasis is essential for rhizobial infection and nodule organogenesis, and indicate a shared requirement for nodule formation and lateral root development in A. evenia.

plant biology↗

Autoregulation dependent and independent mechanisms are responsible for the systemic control of nodule formation by the plant N demand

In legumes interacting with rhizobia the formation of symbiotic organs responsible for the acquisition of atmospheric nitrogen is depending of the plant nitrogen (N) demand. We discriminated between local and systemic impact of nitrogen on nodule formation using Medicago truncatula plants cultivated in split-root systems. We obtained evidence of the control of nodule formation by whole plant systemic N-satisfaction signaling but obtained little evidence of a local control by mineral nitrogen. We characterized the impact of systemic N signaling on the root transcriptome reprogramming associated to nodule formation. We identified, large genes clusters displaying common expression profiles in response to systemic N signaling enriched in particular fonctions required during these biological processes. We found evidence of a strong effect of SUNN in the control by systemic N signaling of many genes involved in the early interaction with rhizobium as well as organogenesis supporting a role of autoregulation pathway in systemic N signaling. However, we also found evidence that major SUNN independent systemic N signaling controls were maintained in the mutant. This study shed light on the unexpected high complexity of the control of nodule formation by systemic N signaling, that probably involves multiple pathways.

plant biology↗

Genetics of nodulation in Aeschynomene evenia uncovers new mechanisms of the rhizobium-legume symbiosis

Among legumes (Fabaceae) capable of nitrogen-fixing nodulation, several Aeschynomene spp. use a unique symbiotic process that is independent of Nod factors and infection threads. They are also distinctive in developing root and stem nodules with photosynthetic bradyrhizobia. Despite the significance of these symbiotic features, their understanding remains limited. To overcome such limitations, we conducted genetic studies of nodulation in Aeschynomene evenia, supported by the development of a genome sequence for A. evenia and transcriptomic resources for 10 additional Aeschynomene spp. Comparative analysis of symbiotic genes substantiated singular mechanisms in the early and late nodulation steps. A forward genetic screen also showed that AeCRK, coding a novel receptor-like kinase, and the symbiotic signaling genes AePOLLUX, AeCCamK, AeCYCLOPS, AeNSP2 and AeNIN, are required to trigger both root and stem nodulation. This work demonstrates the utility of the A. evenia model and provides a cornerstone to unravel new mechanisms underlying the rhizobium-legume symbiosis.

plant biology↗