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Vernie, T.

Publications and source records attributed to Vernie, T..

8 recordsLinked to original sources

A single genetic innovation at the origin of plant terrestrialization

How the functional innovations that enabled plants to first colonize land 450 million years ago evolved remains puzzling. Here, we show that the gain of a single family of enzymes was pivotal in the evolution of two of these innovations, the cuticle that protect plants from dehydration and UV light, and the Arbuscular Mycorrhizal symbiosis promoting water and nutrient uptake. We show that functional phosphatase domain Glycerol-3-Phosphate Acyl Transferase (p-GPATs) evolved in the first land plants, concomitantly with the cuticle and symbiosis. Mutation of two p-GPATs from the liverwort Marchantia paleacea is sufficient to abolish both cuticle formation and AM symbiosis, leading to major developmental defects. We propose that the evolution of p-GPATs in land plants acted as a two birds-one stone innovation, diverting intracellular lipids to the extracellular space and providing a simple path to the evolution of two traits essential for the colonization of land.

plant biology↗

EPP1 is an ancestral component of the plant Common SymbiosisPathway

The success of plants on land has been enabled by mutualistic intracellular associations with microbes for 450 million years (Delaux and Schornack 2021). Because of their intracellular nature, the establishment of these interactions requires tight regulation by the host plants. In particular, three genes - SYMRK, CCaMK and CYCLOPS - form the core of an ancestral common symbiosis pathway (CSP) for intracellular symbioses, and are conserved since the most recent common ancestor of land plants (Radhakrishnan et al. 2020; Delaux et al. 2015; Wang et al. 2010; Parniske 2008). Here, we describe EPP1 as a fourth gene committed to the CSP. Among land plants, EPP1 is conserved only in species able to associate with at least one type of intracellular symbiont. We found that loss-of-function epp1 mutants or EPP1 knock-down lines in four clades of land plants - legumes, Solanaceae, monocots and bryophytes - are all impaired in their ability to associate with arbuscular mycorrhizal fungi. We discovered that the plasma membrane-localized receptor-like SYMRK phosphorylates EPP1 on a conserved serine residue and that this phosphorylation is essential for symbiosis. Using a gain-of-function approach, we demonstrate that EPP1 is upstream of the nuclear kinase CCaMK. We propose that EPP1 is an ancestral component of the essential pathway that has regulated plant symbiosis for half a billion years.

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↗

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↗

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↗

RPG acts as a central determinant for infectosome formation and cellular polarization during intracellular rhizobial infections

Host-controlled intracellular accommodation of nitrogen-fixing bacteria is essential for the establishment of a functional Root Nodule Symbiosis (RNS). In many host plants, this occurs via transcellular tubular-structures (infection threads - ITs) that extend across cell layers via polar tip- growth. Comparative phylogenomic studies have identified RPG (RHIZOBIUM-DIRECTED POLAR GROWTH) among the critical genetic determinants for bacterial infection. In Medicago truncatula, RPG is required for effective IT progression within root hairs but the cellular and molecular function of the encoded protein remain elusive. Here, we show that RPG resides in the protein complex formed by the core endosymbiotic components VAPYRIN (VPY) and LUMPY INFECTION (LIN) required for IT polar growth, co- localizes with both VPY and LIN in IT tip- and perinuclear-associated puncta of M. truncatula root hairs undergoing infection and is necessary for VPY recruitment to puncta. Fluorescence Lifetime Imaging Microscopy (FLIM) of phosphoinositide species during bacterial infection revealed that functional RPG is required to sustain strong membrane polarization at the advancing tip of the IT. In addition, loss of RPG functionality alters the cytoskeleton-mediated connectivity between the IT tip and the nucleus and affects polar secretion of the cell wall modifying enzyme NODULE PECTATE LYASE (NPL). Our results integrate RPG into a core host machinery required to support symbiont accommodation, suggesting that its occurrence in plant host genomes is essential to co-opt a multimeric protein module committed to endosymbiosis to sustain IT-mediated bacterial infection.

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↗