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Libourel, C.

Publications and source records attributed to Libourel, C..

16 recordsLinked to original sources

The demonstration of a single origin for nodule evolution, with nodule engineering in a non-nodulating species

The nitrogen-fixing root-nodule symbiosis provides a sustainable source of nitrogen for plants within the Nitrogen (N)-fixing clade (NFC). A debate has raged over whether nodulation evolved once, with many losses or multiple times following a predisposition event. Here we demonstrate that nodule-organogenesis is fully conserved between an actinorhizal nodulator Datisca glomerata and the legume Medicago truncatula, showing entirely conserved programmes for Nodule INception (NIN)-controlled development leading to nodule emergence. Convergent losses of N-fixation within the NFC is associated with loss of NIN and we show the engineering of nodule-like development into strawberry, a non-nodulating member of the NFC, through the repair of NIN-functionality. Similar NIN-engineering resulted in altered-root developmental responses in barley. Our work is consistent with the single-gain hypothesis, where repair of NIN can recapitulate nodules in species within the NFC, demonstrating that understanding the ancestral state of nodulation facilitates its engineering.

plant biology↗

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↗

An Arabidopsis receptor-like kinase mediates competitive plant-plant interactions

While competition among plant species is recognized as a major factor affecting crop yield and plant community dynamics, the genetic and molecular mechanisms underlying natural variation of such biotic interactions remain poorly characterized. Here, we report the cloning of a Quantitative Trait Locus previously detected in a Genome-Wide Association Study investigating the competitive response of Arabidopsis thaliana to the presence of the annual bluegrass weed species Poa annua. Using mutant and complementation strategies, we identified ESCAPE 1 (ESC1) as the gene responsible for the natural variation of an escape strategy of A. thaliana in response to the presence of P. annua. ESC1 encodes a proline-rich, extensin-like receptor kinase, also known as PERK13. An RNA-seq experiment revealed that PERK13 functions through different pathways in leaves and roots involving genes associated with responses to biotic and abiotic stresses. Using these RNA-seq together with yeast two-hybrid (Y2H) data, protein-protein interaction network reconstruction revealed two distinct decentralized protein networks in leaves and roots. These findings support the notion of an active response mechanism involved in neighbor detection. The functional validation of ESC1 underlying natural variation in response to competition opens new avenues for a better understanding of the molecular dialogue involved in plant-plant interactions. HighlightIn this study, we identify a receptor-like kinase enabling Arabidopsis thaliana to detect neighboring species through the activation of specific genetic pathways.

plant biology↗

Nissolia brasiliensis as a non-nodulating model legume

The nitrogen-fixing root nodule symbiosis (RNS) is specifically formed by four orders of angiosperms. The largest of these four orders include the legume family, the Fabaceae. Among legumes, historical model species have emerged, such as the RNS-forming Medicago truncatula and Lotus japonicus, or, more recently, Aeschynomene aevenia. By contrast, legume species that have lost RNS have been largely ignored. Here, we describe the first chromosome-level assembly for a non-RNS-forming legume, the tropical papilionoid Nissolia brasiliensis. We compared its genome to closely related legumes and identified genes associated with RNS. Finally, we developed a stable transformation protocol that can be deployed in the future to re-evolve RNS in legumes, a first step toward the goal of engineering RNS in non-legume crops.

plant biology↗

Leafy liverwort genomes shed light on the evolution of ericoid symbiosis

Symbioses have been fundamental to colonization of terrestrial ecosystems by plants and their evolution. Emergence of the ancient arbuscular mycorrhizal symbiosis was followed by the diversification of alternative intracellular symbioses, such as the ericoid mycorrhizae (ErM). We aimed at understanding how these diversifications occurred. We sequenced the genomes of ErM-forming liverworts, and reconstituted symbiosis under laboratory conditions. We demonstrated the existence of a nutrient-regulated symbiotic state that enables ErM and underlies intracellular colonization of plant tissues. Comparative transcriptomic analyses identified an ancestral gene module associated with intracellular symbiosis beyond ErM. Genetic manipulations in the liverwort Marchantia paleacea, phylogenetics and transactivation assays demonstrated its essential function for intracellular symbiosis. We conclude that plant have maintained, and convergently recruited, an ancestral gene module for intracellular symbioses.

plant biology↗

Horizontal gene transfers and terpene metabolism drive plant-fungal interaction in Marchantia polymorpha

The liverwort Marchantia polymorpha has emerged as a model for studying plant immunity in bryophytes, providing unique insights into conserved defense mechanisms across land plants. By contrast, Marchantia-specific immune mechanisms have not been explored. In this study, we investigated the genetic basis of quantitative resistance in M. polymorpha against the fungal pathogen Colletotrichum nymphaeae, a naturally occurring compatible parasite. Through a combination of phenotypic, cytological and transcriptomic approaches, combined with genome-wide association studies (GWAS), we identified key defense-related genes and pathways. Transcriptomic analyses performed on two lines with contrasting suceptibilities to the pathogen revealed a strong overlap in immune responses between M. polymorpha and angiosperms, including the upregulation of PR proteins, transcription factors typically associated with biotic stresses, and enzymes involved in specialized metabolism. Leveraging the biological and genetic variability present in a collection of natural M. polymorpha accessions, highlight the role of horizontally transferred microbial-like terpene synthase (MTPSL) genes, which may contribute to the exceptional terpene diversity in liverworts and play a role in pathogen resistance. GWAS uncovered candidate loci associated with resistance traits, implicating both core immune components and specialized metabolic pathways. These results provide new insights into the specific molecular underpinnings of bryophyte immunity and underscore the evolutionary significance of horizontal gene transfer and specialized metabolites in shaping plant-pathogen interactions.

plant biology↗

Ectomycorrhizal symbiosis evolved independently and by convergent gene duplication in rosid lineages

Many land plants rely on mutualistic symbiotic associations to thrive, starting with their common ancestor associating with arbuscular mycorrhizal (AM) fungi. Similar to AM symbiosis, multiple other intracellular symbiotic interactions have evolved in a variety of land plants. Ectomycorrhizal (ECM) symbiosis contrasts with these relationships as there is no intracellular accommodation of the symbiont inside the plant cell, but only intercellular colonization. This symbiotic relationship is common in a variety of seed plants, mostly trees and shrubs such as pines, willows and oaks. Although it is known which plant lineages are involved in ECM symbiosis, there has been little investigation into the evolutionary origin of ECM symbiosis in these lineages. Furthermore, the genetic innovations and transcriptomic response related to this symbiosis have been studied largely in a genus or species-specific context, which hinders the study of their evolutionary origins. In this study, we reconstruct the origin of ECM in the rosid clade, showing at least 16 independent origins, resulting in the 17 known extant ECM rosid lineages. Moreover, comparative genomics of these lineages highlight genes involved in cell wall remodeling which underwent duplications in a convergent manner across ectomycorrhizal lineages.

plant biology↗

Conservation of symbiotic signalling across 450 million years of plant evolution

HighlightO_LIThe common symbiotic pathway is activated during arbuscular mycorrhizal symbiosis in Marchantia paleacea C_LIO_LIThe three core members of the common symbiotic pathway are essential for symbiosis in Marchantia paleacea C_LIO_LIThe molecular function of the CCaMK/CYCLOPS module is conserved across land plants C_LIO_LISymbiotic signalling has been conserved in plants for 450 million years C_LI The colonization of land by plants 450 million years ago revolutionized life on Earth1. The fossil record2 and genetic evidence in extant species3 suggest that this transition was facilitated by interactions with symbiotic arbuscular mycorrhizal (AM) fungi4. This ancestral symbiosis relied on the biosynthesis of chemicals by the host plant, both as signals5 and as nutrients3. In angiosperms, a signalling pathway involving the receptor-like kinase SYMRK/DMI26,7, the Calcium and Calmodulin-dependent protein kinase CCaMK/DMI38 and the transcription factor CYCLOPS/IPD39,10 has been described as the common symbiosis pathway (CSP), essential for the establishment of the AM symbiosis and the root-nodule symbiosis11. Phylogenetic and comparative phylogenomic analyses indicated an ancient origin of the CSP, present in all extant land plants forming intracellular symbioses12-15. Trans-complementation assays of the angiosperm mutants with orthologs from diverse species further indicated the conservation of the molecular function of the CSP across the embryophytes9,12,14-16. However, this correlative evidence did not allow testing the ancestral biological function of the CSP. In this study we demonstrate that SYMRK, CCaMK and CYCLOPS are essential for the colonization by AM fungi in bryophytes, indicating that plants have maintained a dedicated signalling pathway to support symbiotic interactions for 450 million years.

plant biology↗

The Marchantia pangenome reveals ancient mechanisms of plant adaptation to the environment

Plant adaptation to a terrestrial life 450 million years ago played a major role in the evolution of life on Earth. This shift from an aquatic environment has been mostly studied by focusing on flowering plants. Here, we gathered a collection of 133 accessions of the non-vascular plants Marchantia polymorpha and studied its intraspecific diversity using selection signature analyses, genome-environment association study and a gene-centered pangenome. We identified adaptive features shared with flowering plants, such as peroxidases or nucleotide-binding and leucine-rich repeat (NLR), which likely played a role in the adaptation of the first land plants to the terrestrial habitat. The M. polymorpha pangenome also harbored lineage-specific accessory genes absent from seed plants. We conclude that different land plants lineages still share many elements from the genetic toolkit evolved by their most recent common ancestor to adapt to the terrestrial habitat, refined by lineage specific polymorphisms and gene family evolutions.

plant biology↗

Comparative phylotranscriptomics reveals a 110 million years-old symbiotic program

Symbiotic interactions have structured past and present ecosystems and shaped the evolution of life. As any trait, the symbiotic state observed in extant species builds on ancestral and conserved features, and lineage-specific innovations. From these mixed origins, defining the ancestral state of symbiotic associations is challenging although it is instrumental for understanding how symbiotic abilities emerge from non-symbiotic states. Here we aimed at reconstructing the intermediate steps leading to the root-nodule nitrogen-fixing symbiosis (RNS) observed in some extant flowering plants. For this, we compared the transcriptomic responses of nine host plants in response to symbiotic bacteria. We included the mimosoid legume Mimosa pudica for which we assembled a chromosome-level genome and generated the transcriptomic response to experimentally evolved bacterial symbionts. With this dataset, we reconstructed the ancestral RNS transcriptome, composed of most already described symbiotic genes together with hundreds of novel candidates. We found that the response to the chemical signals produced by the symbiont, nodule organogenesis and nitrogen-fixation are predominantly linked to ancestral responses, although these traits have diversified in the different nitrogen-fixing lineages. We detected a clear signature of recent and convergent evolution for the ability to release intracellular symbiosomes in two legume lineages, exemplified by the expression of different classes of small proteins in each group, potentially leading to the convergent gain of symbiotic evolutionary stability. Our findings demonstrate that most of the novelties for RNS were mostly in place in the most recent common ancestor of the RNS-forming species that lived on Earth 110 million years ago. Graphical abstractA little graphical/nice phylogeny with nodes of interest HighlightsO_LIWe sequenced a high-quality genome of the Mimosoideae Mimosa pudica C_LIO_LIThe nitrogen-fixing root-nodule symbiosis relies on an ancestral transcriptomic response C_LIO_LIAll symbiotic traits involve genes of the ancestral symbiotic program C_LIO_LISymbiont perception, nodule organogenesis and nitrogen-fixation are essentially ancestral processes C_LIO_LIConvergent evolution of intracellular accommodation of symbionts additionally involves lineage-specific genes C_LI

plant biology↗

Remorin proteins serve as membrane topology scaffolds in plants

Organization of membrane topologies in plants has so far been mainly attributed to the cell wall and the cytoskeleton. Taking rhizobial infections of legume root cells, where plasma membranes undergo dynamic and large-scale topology changes, as an initial model, we challenged this paradigm and tested whether additional scaffolds such as plant-specific remorins that accumulate on highly curved and often wall-less plasma membrane domains, control local membrane dynamics. Indeed, loss-of-function mutants of the remorin protein SYMREM1 failed to develop stabilized membrane tubes as found in colonized cells in wild-type plants, but released empty membrane spheres instead. Expression of this and other remorins in wall-less protoplasts allowed engineering different membrane topologies ranging from membrane blebs to long membrane tubes. Reciprocally, mechanically induced membrane indentations were equally stabilized by SYMREM1. This function is likely supported by remorin oligomerization into antiparallel dimers and the formation of higher order membrane scaffolding structures. Taken together we describe an evolutionary confined mechanism that allows the stabilization of large-scale membrane conformations and curvatures in plants. One-sentence summaryThe remorin SYMREM1 evolved as structural membrane scaffold that stabilizes membrane tubulation and curvature during symbiotic intracellular infections.

plant biology↗

Phylogenomics reveals the evolutionary origin of lichenization in chlorophyte algae

Mutualistic symbioses have contributed to major transitions in the evolution of life. Here, we investigate the evolutionary history and the molecular innovations at the origin of lichens, which are a symbiosis established between fungi and green algae or cyanobacteria. We de novo sequence the genomes or transcriptomes of 12 lichen algal symbiont (LAS) and closely related non-symbiotic algae (NSA) to improve the genomic coverage of Chlorophyte algae. We then perform ancestral state reconstruction and comparative phylogenomics. We identify at least three independent gains of the ability to engage in the lichen symbiosis, one in Trebouxiophyceae and two in Ulvophyceae, confirming the convergent evolution of the lichen symbioses. A carbohydrate-active enzyme from the glycoside hydrolase 8 (GH8) family was identified as a top candidate for the molecular-mechanism underlying lichen symbiosis in Trebouxiophyceae. This GH8 was acquired in lichenizing Trebouxiophyceae by horizontal gene transfer, concomitantly with the ability to associate with lichens fungal symbionts (LFS) and is able to degrade polysaccharides found in the cell wall of LFS. These findings indicate that a combination of gene family expansion and horizontal gene transfer provided the basis for lichenization to evolve in chlorophyte algae.

plant biology↗

An ancestral function of strigolactones as symbiotic rhizosphere signals

In flowering plants, carotenoid-derived strigolactones (SLs) have dual functions as hormones that regulate growth and development, and as rhizosphere signaling molecules that induce symbiosis with arbuscular mycorrhizal (AM) fungi. Here, we report the identification of bryosymbiol (BSB), a previously unidentified SL from the bryophyte Marchantia paleacea. BSB is also found in vascular plants, indicating that it is ancestral in land plants. BSB synthesis is enhanced at AM symbiosis permissive conditions and BSB deficient mutants are impaired in AM symbiosis. In contrast, the absence of BSB synthesis has little effect on the growth and gene expression. We show that the introduction of the SL receptor of Arabidopsis renders M. paleacea cells BSB-responsive. These results suggest that BSB is not perceived by M. paleacea cells due to the lack of cognate SL receptors. We propose that SLs originated as AM symbiosis-inducing rhizosphere signaling molecules and were later recruited as plant hormone.

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↗

An ancestral signalling pathway is conserved in plant lineages forming intracellular symbioses

Plants are the foundation of terrestrial ecosystems and their colonization of land was facilitated by mutualistic associations with arbuscular mycorrhizal fungi. Following that founding event, plant diversification has led to the emergence of a tremendous diversity of mutualistic symbioses with microorganisms, ranging from extracellular associations to the most intimate intracellular associations, where fungal or bacterial symbionts are hosted inside plant cells. Through analysis of 271 transcriptomes and 122 plant genomes, we demonstrate that the common symbiosis signalling pathway controlling the association with arbuscular mycorrhizal fungi and with nitrogen-fixing bacteria specifically co-evolved with intracellular endosymbioses, including ericoid and orchid mycorrhizae in angiosperms and ericoid-like associations of bryophytes. In contrast, species forming exclusively extracellular symbioses like ectomycorrhizae or associations with cyanobacteria have lost this signalling pathway. This work unifies intracellular symbioses, revealing conservation in their evolution across 450 million years of plant diversification.

plant biology↗

The genomic architecture of competitive response of Arabidopsis thaliana is highly flexible between monospecific and plurispecific neighborhoods.

Although plants simultaneously interact with multiple neighboring species throughout their life cycle, there is still very limited information about the genetics of the competitive response in the context of plurispecific interactions. Using a local mapping population of Arabidopsis thaliana, we set up a Genome Wide Association study to estimate the extent of genetic variation of the competitive response in presence of 12 plant species assemblages, and to compare the genetic architecture of the competitive response between monospecific and plurispecific neighborhoods. Based on four phenotypic traits, we detected strong crossing reaction norms not only among the three monospecific neighborhoods, but also among the different plant assemblages. Accordingly, the genetic architecture of the competitive response was highly dependent on the identity and the relative abundance of the neighboring species. In addition, enriched biological processes underlying the competitive response largely differ between monospecific and plurispecific neighborhoods. In particular, receptor-like kinases and transporters were significantly enriched in plurispecific neighborhoods. Our results suggest that plants can integrate and respond to different species assemblages depending on the identity and number of each neighboring species, through a large range of genes associated mainly with perception and signaling processes leading to developmental and stress responses.

genetics↗